NEIL C. HULING Proceedings of the

First International

Conference on Meiofauna

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY NUMBER 76
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SMITHSONIAN CONTRIBUTIONS TO

ZOOLOGY

NUMBER 76

EDITOR

Neil c. Huimgs Proceedings of the

First International

Conference on Meiofauna

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International Conference on Meiofauna

1-11 July 1969, Tunis, Tunisia

ORGANIZATION

Neil C. Hulings, convener

J. S. Gray, co-convener

R. P. Higgins, co-convener

PARTICIPANTS

Dr. C. Clausen

Zoological Laboratory

University of Bergen

Bergen, Norway

Dr. M. T. Gomoiu

"Traian Savelescu" Institute of Biology

Department of Marine Biology

Constantza, Romania

Dr. J. S. Gray

Wellcome Marine Laboratory

Robin Hood's Bay

Yorkshire, England

Dr. R. R. Hessler

Scripps Institution of Oceanography

La Jolla, California 92037

Dr. R. P. Higgins

Office of Oceanography and Limnology

Smithsonian Institution

Washington, D.C. 20560

Dr. W. D. Hope

Department of Invertebrate Zoology

National Museum of Natural History

Smithsonian Institution

Washington, D.C. 20560

Dr. N. C. Hulings

Office of Oceanography and Limnology

Smithsonian Institution

Washington, D.C. 20560

Dr. W. D. Hummon

Department of Zoology

Ohio University

Athens, Ohio 45701

Dr. S. Husmann

Limnologische Flusstation

Max-Planck-Instituts fur Limnologie

Schlitz, West Germany

Dr. B. O. Jansson

Askolaboratoriet

Trosa, Sweden

Dr. C. Jouin

Laboratoire de Zoologie

Faculte" des Sciences

7, Quai St. Bernard

Paris, France

Dr. E. Kirsteuer

Department of Living Invertebrates

American Museum of Natural History

New York, New York 10024

Dr. H. Kiihl

Institut fur Kiisten- und Binnenfischerei

Laboratorium Cuxhaven

Cuxhaven, West Germany

Dr. P. Lasserre

Institut de Biologie Marine

University de Bordeaux

33 Arcachon, France

Mr. A. D. Mclntyre

Marine Laboratory

Aberdeen, Scotland

Dr. F. Monniot

Museum National d'Histoire Naturelle

Laboratoire de Biologie des Inverte'bre's Marins

Paris, France
Dr. I. M. Newell

Department of Life Sciences

University of California

Riverside, California 92502

Dr. W. Noodt

Zoologisches Institut der Universitat

Hegewischstrasse 3

Kiel, West Germany

Dr. O. H. Pilkey

Department of Geology

Duke University

Durham, North Carolina 27708

Dr. L. W. Pollock

Systematics-Ecology Program

Marine Biological Laboratory

Woods Hole, Massachusetts 02543

Dr. J. Renaud-Mornant

Museum National d'Histoire Naturelle

43, rue Cuvier

Paris, France

Dr. F. Riemann

Institut fiir Meeresforschung

Bremerhaven, West Germany

Dr. W. Sterrer

Bermuda Biological Station

St. Georges West, Bermuda

Dr. B. Swedmark

Kristinebergs Zoological Station

Fiskebackskil, Sweden

Dr. G. Uhlig

Biologisches Anstalt Helgoland

Helgoland, West Germany

Dr. J. B. J. Wells

Department of Zoology

University of Aberdeen

Aberdeen, Scotland

Dr. W. Westheide

II Zoologisches Institut der Universitat

Gottingen, West Germany

Dr. R. Williams

Oceanographic Laboratory (S.M.B.A.)

Edinburgh, Scotland
Foreword

The First International Conference on Meiofauna was held in Tunis, Tunisia,

1-11 July, 1969. Twenty-eight invited participants from seven countries assembled

to review the status of the systematic^ and ecology of meiofaunal taxa, the ecology

of meiobenthic communities, and techniques of faunal and environmental analyses. Of the 30 papers presented at the conference, 27 are included in this

volume.

The convening of the conference was stimulated by the increasing emphasis

on and need for investigations of the systematics and ecology of meiofauna and

for a means to provide an exchange of ideds between systematists and ecologists.

Also it was felt that there was a need to standardize techniques of collecting and

reporting data so that results from one area of investigation could be compared

with those from another area. Toward this end, all participants contributed to

"A Manual for the Study of Meiofauna" (Neil C. Hulings and John S. Gray, 1971,

Smithsonian Contributions to Zoology, Number 78).

There remains much to be done in the sphere of meiofauna investigations.

One of the most pressing problems is the need for more attention to the problem

of sampling. Statistical evaluation of various techniques of sampling and statistical

treatment of the sampling efforts are imperative. Not only must there be concern

for individual species but also for the community as a whole. There must be

continuous dialogue between systematists and ecologists to advance properly our

knowledge of meiofaunal species and communities. Ultimately, the ecologist

must consider all specimens to the species level. By the same token, the systematist must take into consideration taxa other than those of his particular interest.

In this way he can provide taxa that are properly preserved for study by other

systematists. It is through such consideration and cooperation that our knowledge

of meiofauna will be increased greatly. These approaches assume an even greater

significance when considering the effects of pollution on meiofauna.

Other pressing problems exist in the area of the physiology of meiofauna. In

terms of collecting and properly preserving specimens for study, what are the

effects of various preservatives and anesthetizing agents now available? In the

past, only the traditional agents have been used. New agents need to be evaluated,

for it may be that these give better results than the traditional ones. To what

degree do taxa, from the polar regions to the tropics, react differently to prepreservation storage and various extraction techniques? Preliminary evidence

indicates the reaction is considerably different, and further evaluation of this

aspect may result in greater extraction efficiency. This emphasizes the need for

taking the local environmental conditions of the organism into consideration.

Investigations in the area of culture of meiofaunal taxa must be accelerated to

determine the degree of rsponse to various environmental parameters.

Such needs represent some of the more pressing problems in the study of

meiofauna. These and other problems in the study of meiofuna are apparent in

this volume and in the "Manual for the Study of Meiofauna." It is hoped that

the papers presented in both publications will stimulate research along these and

other lines.
I am indebted to many persons for assistance in organizing the conference and

in editing the papers of this volume. John S. Gray and Robert P. Higgins were

of invaluable assistance in organizing and convening the conference. The personnel of the Mediterranean Marine Sorting Center, Salammbo, Tunisia—especially

Dr. Hedia Baccar, Mrs. Genevieve Dargouth, and Mr. Mohammed Shili—freely

provided assistance prior to and during the conference. The Tunisian government—especially the National Scientific and Technical Institute for Oceanography and Fisheries, the Department of Higher Education and Scientific Research, and the Ministry of Foreign Affairs—endorsed the conference and assisted

in many ways. The American Embassy, Tunis, was most helpful on numerous

occasions. Funding for the conference was made possible through the Office of

International Activities of the Smithsonian Institution. The assistance of Dr.

Ray Manning and his staff of the Department of Invertebrate Zoology, Smithsonian Institution, is gratefully acknowledged. And lastly, sincere appreciation is

expressed to the authors of the papers in this volume for their patience and

cooperation.

NEIL C. HULINGS

Department of Biology

American University of Beirut

Beirut, Lebanon
Contents

SYSTEMATICS AND ECOLOGY OF MEIOFAUNA TAXA

Page

CLAUS CLAUSEN: Interstitial Cnidaria: Present Status of Their Systematics

and Ecology 1

WOLFGANG STERRER: Gnathostomulida: Problems and Procedures 9

ERNST KIRSTEUER: The Interstitial Nemertean Fauna of Marine Sand .. 17

WILLIAM D. HUMMON: The Marine and Brackish-Water Gastrotricha in

Perspective 21

ROBERT P. HIGGINS: A Historical Overview of Kinorhynch Research .. . 25

W. DUANE HOPE: The Current Status of the Systematics of Marine

Nematodes 33

JOHN S. GRAY: The Meiobenthic Bryozoa 37

BERTIL SWEDMARK: A Review of Gastropoda, Brachiopoda, and Echinodermata in Marine Meiobenthos 41

CLAUDE JOUIN: Status of the Knowledge of the Systematics and Ecology

of Archiannelida 47

WILFRIED WESTHEIDE: Interstitial Polychaeta (Excluding Archiannelida) 57

PIERRE LASSERRE: Oligochaeta from the Marine Meiobenthos: Taxonomy

and Ecology 71

ROBERT R. HESSLER: Biology of the Mystacocarida: A Prospectus 87

NEIL C. HULINGS: Summary and Current Status of the Taxonomy and

Ecology of Benthic Ostracoda Including Interstitial Forms 91

WOLFRAM NOODT: Ecology of the Copepoda 97

IRWIN M. NEWELL: Problems in the Study of Subtidal Halacaridae (Acari) 103

JEANNE RENAUD-MORNANT AND LELAND W. POLLOCK: A Review of the

Systematics and Ecology of Marine Tardigrada 109

F. MONNIOT: Les Ascidies littorales et profondes des sediments meubles 119

ECOLOGY OF MEIOFAUNA

BENGT-OWE JANSSON: The "Umwelt" of the Interstitial Fauna 129

LELAND W. POLLOCK: Ecology of Intertidal Meiobenthos 141

A. D. MCINTYRE: Observations on the Status of Subtidal Meiofauna

Research 149

M. T. GOMOIU: Ecology of Subtidal Meiobenthos 155

SIEGFRIED HUSMANN: Ecological Studies on Freshwater Meiobenthon in

Layers of Sand and Gravel 161

H. KUHL: On Changes of the Interstitial Water after Decomposition of

Organic Matter 171
SAMPLING FOR MEIOFAUNA

J. B. J. WELLS: A Brief Review of Methods of Sampling the Meiobenthos 183

ROBERT R. HESSLER: Problems of Meiobenthic Sampling in the Deep Sea 187

JOHN S. GRAY: Sample Size and Sample Frequency in Relation to the

Quantitative Sampling of Sand Meiofauna 191

R. WILLIAMS: A Technique for Measuring the Interstitial Voids of a

Sediment Based on Epoxy Resin Impregnation 199

Vll l
SYSTEMATICS AND ECOLOGY OF MEIOFAUNA TAXA

ciaus Clausen Interstitial Gnidaria:

Present Status of Their

Systematics and Ecology

ABSTRACT

A synopsis is given of the interstitial Cnidaria

(Hydrozoa: Protohydra, Psammohydra, Siphonohydra, Armorhydra, Halammohydra, Otohydra;

Scyphozoa: Stylocoronella; Anthozoa: Sphenotrochus). Systematics, ecology, adaptive morphological characters, and geographic distribution are

discussed.

The number of cnidarian species inhabiting interstitial environments is small, both in proportion to

other Cnidaria and when compared with the number of interstitial species of many other invertebrate phyla. Only twelve cnidarians are known

from this milieu, There are seven recognized genera, of which five belong to the class Hydrozoa and

one to each of the classes Scyphozoa and Anthozoa.

Despite this small number, the group shows many

interesting features, some of which exhibit remarkable adaptations to the habitat.

Class HYDROZOA

Genus Protohydra Greeff

Protohydra leuckarti Greeff is a small (1.5 mm),

solitary polyp that is shaped like Hydra and lacks

tentacles. It was discovered by Greeff in 1868 in an

oysterpark near Ostende, Belgium, where it occurred in muddy substrate rich in diatoms. The

polyp may fasten itself with a basal disk, or it may

move like a caterpillar larva. The sexes are separate. Gonads, however, are only rarely present; reClaus Clausen, Zoological Laboratory, University of Bergen,

Bergen, Norway.

production is mostly asexual, the polyp dividing

transversely.

Protohydra leuckarti has a very wide distribution. In Europe it has been found in England,

near Plymouth, in brackish water (Baker, 1913),

at Tvarminne (Luther, 1923), along the coasts of

Sweden and Norway (Westblad, 1929, 1954), in

the North Sea at Amrum (Schulz, 1950a), in the

British Channel at Roscoff (Teissier, 1950), in the

Biskaia at Arcachon, in the Mediterranean at

Canet and Banyuls (Nyholm, 1951); and in the

Black Sea (Valkanov, 1947).

Outside of Europe Protohydra leuckarti has

been reported from a lake in Kamtschatka

(Abonyi, 1929), along the east coast of the United

States (Ruebush, 1939), and in Puget Sound

(Wieser, 1958). In addition, Remane claims to

have found a specimen of Protohydra leuckarti or

closely related species in samples from South-West

Africa (Schulz, 1950a); Omer-Cooper (1957) reported a species of Protohydra from South Africa;

and Dawydoff (1930) described Protohydra caullery from the coast of Indo-China.

Protohydra leuckarti is a shallow-water form occurring from just a few centimeters below the water

surface (Westblad, 1929) down to at least 13 m

(Schulz, 1950a). The salinity range is wide, from 4

ppt in the Baltic (Schulz, 1950a) to 36 ppt at

Canet Plage (Delamare Deboutteville, 1960). This

species has a preference for sheltered places, being

absent in the zone of Otoplana (Schulz, 1950a);

otherwise, it appears that the biotopes are quite

varied. A frequent bottom type is mud, with a

layer of diatoms and detritus; but sand—fine or

coarse, pure or mixed with mud—as well as algal

vegetation also are frequent biotopes. Protohydra

leuckarti has been found in coastal subsoil water
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

(as noted by Delamare Deboutteville, 1960), and

it is the only cnidarian known from that particular

habitat. As for food, Schulz (1950a) found nematodes, larvae of mosquitos, copepods, ostracods,

and parts of gastrotrichs and oligochaetes. Thiel

(1962, after Naumov) maintains the classification

of Protohydra in a separate family, Protohydridae,

within the order Hydrida, that is equivalent to the

suborder Hydrina of Werner (1965b).

Genus Psammohydra Schulz

Psammohydra is the smallest known polyp, reaching a length of 250 to 400 p. A little above the

middle of the slender, cylindrical body are three to

five (usually four) short tentacles. A swollen proboscis terminates in a distensible mouth. At the

base of the polyp are small papillae by which the

animal adheres to a sand grain. Gonads seem to be

absent. Sexual reproduction by binary fission, as in

Protohydra, has been observed. The locomotion is

like that of Protohydra; the proboscis adheres to

the substrate, and the hind end is loosened from

the grain and fastened again near the proboscis.

According to Schulz (1950b) Psammohydra belongs to the Turbanella hyalina coenose. As to nutrition, Schulz (1950b) observed that copepod nauplii were ingested.

Psammohydra nanna Schulz (Figure 1) was

described by Schulz (1950b) from the Baltic, north

of Kiel, where he found it in fine sand at a depth

of 2 m. Currently, there are only two other reports

of Psammohydra nanna. Swedmark (1956) found

it in fine sand at Roscoff together with another interstitial cnidarian, Halammohydra octopodides.

Another finding was made by Salvini Plawen

(1966) in the Adriatic Sea near Rovigne where it

was found at depths of 4 to 8 m, mostly in medium-fine to medium-coarse sand, together with six

other cnidarians Halammohydra octopodides, H.

schulzei, Otohydra vagans, Armorhydra janowiczi,

Siphonohydra adriatica, and Styolcoronella riedli.

Like Protohydra leuckarti, Psammohydra nanna

must be characterized as being euryhaline.

Regarding the taxonomy, Schulz (1950b) left

Psammohydra nanna incertae sedis, whereas Salvini

Plawen (1966) thought it should be placed within

the Athecata in the family Tubulariidae.

FIGURE 1.—Psammohydra nanna from life. (Redrawn from

Schulz, 1950b.)

Genus Siphonohydra Salvini Plawen

In 1965 Salvini Plawen found a new interstitial

polyp, Siphonohydra adriatica Salvini Plawen, in

coarse sand at a depth of 6 m near Rovigne. He

found two specimens whose lengths were 0.75 mm

and 1.2 mm. The body is composed of a lengthened, saclike hydranth, emerging from a hydrocaulus, that comprises little more than a third of the

total length. The hydranth bears two widely separated whorls of alternating tentacles, four tentacles

in each whorl. Four processes, each covering a gonophore, are located at the base of the hydranth, in

the axis of the oral tentacles.
NUMBER 76

The gonophores consist of reduced but elongate

medusoids. Asexual reproduction appears predominant, and buds develop on the hydranth and later

detach to form new individuals. The buds may

possess secondary buds or tentacles before their detachment.

At the type-locality, Siphonohydra adriatica was

associated with Psammohydra nanna, Halammohydra schulzei, Armorhydra janowiczi, and Stylocoronella riedli.

Salvini Plawen (1966) placed the new genus

within the family Tubulariidae because of the similarities with the already existing genera of the

family. Chief similarities include shape and arrangement of the tentacles, absence of rhizoids,

and sexual reproduction by medusoids.

Genus Armorhydra Swedmark and Teissiex

Armorhydra janowiczi Swedmark and Teissier resembles both a craspedote medusa and an ovoid

polyp. There is a single whorl of tentacles inserted

near the oral end and the tentacles are differentiated into catching and adhesive tentacles. The

latter have distal thickenings provided with small

mobile papillae (Lacassagne, 1968c). Whereas nematocysts are plentiful in the defensive tentacles,

they are wanting in the adhesive tentacles. This

high degree of specialization of the tentacles is a

noticeable adaptation to the interstitial mode of life.

The sexes are separate and the gonads are arranged in longitudinal fields at the surface of the

manubrium. The manubrium is connected with

the umbrella through a system of longitudinal, mesogleal septa, radiating across the subumbrellar

cavity. There is no form of adhesive structure at

the aboral end.

The life cycle of Armorhydra is unknown. In

1966, however, F. Monniot discovered, in Morlaix

Bay near Roscoff, a new interstitial polyp, only 1

mm long, that had a cnidome quite similar to that

of Armorhydra janowiczi (Lacassagne, 1968c) . The

polyp reproduces by podocysts and also by shedding a tentacle which may grow into a new polyp

(Lacassagne, 1968c). Lacassagne also noted a close

resemblance to the limnomedusa Ostroumovia

horii (Uchida and Uchida) with respect to the

asexual reproduction. Since medusa buds have not

been observed in the new polyp, it would be only

a hypothesis to regard this polyp as the asexual

form of Armorhydra; however, if such could be

shown, the classification of Armorhydra within the

Limnohydrina would seem justified.

Apart from the findings at Roscoff, there have

been two other findings of Armorhydra janowiczi

in the Mediterranean, one at Rovigne by Salvini

Plawen (1966) and the other at Ischia by the author (unpublished). Armorhydra janowiczi is one

of the largest of the interstitial cnidarians, reaching a length of 2 mm. At all three localities it was

found in coarse sand.

Genus Halammohydra Remane

The curious hydrozoan Halammohydra (Figure 2)

was discovered by Remane in Kiel Bay in 1924

(Remane, 1927) and was the first cnidarian known

to inhabit interstitial environments. It reaches a

size of 0.3 to 1.3 mm and has the characters of

both polyp and medusa.

The body, which is entirely ciliated (or flagellated) , consists of two main parts: a lengthened

gastric tube and a small, conical-shaped aboral

cone. The two parts are joined by a neck-like part.

FIGURE 2.—Halammohydra schulzei. (From Clausen, 1967.)
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Two whorls of long, slender tentacles arise from

the aboral cone. Alternating with the oral tentacles

are statocysts of the lithostyle type, which are innervated from a nerve ring in the aboral cone. An

urn-shaped depression in the point of the aboral

cone serves as an adhesvie organ. The sexes are

separate, and the gonads lie between the epidermis

and the gastrodermis of the gastric tube.

Swedmark and Teissier (1950, 1957a,b) have

studied the development of two of the species. The

eggs are shed through the mouth before they are

fertilized. The fertilized egg develops directly via

an actinula-like stage into a young animal basically like the adult but having only four statocysts

and four tentacles in each whorl. This is called the

halhydrula stage.

Despite its simple structure, Halammohydra

shows a great variation in character, both quantitatively and qualitatively, and six species have been

described: Halammohydra octopodides Remane,

H. schulzei Remane, H. vermiformis Swedmark

and Teissier, H. adherens Swedmark and Teissier,

H. intermedia Clausen, and H. coronata Clausen.

Populations of the same species frequently differ,

especially with respect to the cnidome; the rhopaloids (penetrants) are present in either of two size

categories.

Locomotion is by flagella. Like a medusa, Halammohydra swims in the direction of the aboral

pole, but the body is kept horizontal. Halammohydra octopodides and H. vermiformis are very active animals; H. adherens is characteristically semisessile. The food seems to consist of nematodes and

small crustaceans.

While the group as a whole inhabits different

kinds of sediment—from fine sand to coarse shell

gravel—a given form, as Swedmark (1957) first noticed, usually is found in the same type of sediment over wide geographic areas. This isolation of

the populations obviously promotes the pronounced raciation. Halammohydra prefers wellaerated sediments and is more frequent in euhaline

than in oligohaline water—in the Baltic, only Halammohydra octopodides and H. schulzei are observed, and in small numbers (Remane, 1927;

Schulz, 1952). It has been found from the tidal

zone (H. vermiformis) down to 60 m (H. adherens).

In Europe the distribution, in addition to the

western Baltic, includes Great Britan and from the

Barents Sea (Mamkaev, 1962) to the Adriatic Sea

(Salvini Plawen, 1966). Outside Europe, Halammohydra has been reported from Indian waters

(Rao and Ganapati, 1966), and it also occurs on

the east coast of North America (W. Sterrer, personal communication).

Genus Otohydra Swedmark and Teissier

Otohydra vagans Swedmark and Teissier was discqvered in 1957 at Roscoff, where it was found in

coarse shell gravel together with Halammohydra

adherens and Armorhydra janowiczi. Salvini

Plawen (1966) has reported Otohydra vagans from

Rovigne.

The structure of Otohydra is polypoid. One

whorl of 12 to 24 tentacles surrounds a short hypostome which terminates in a very distensible

mouth. Between the tentacle bases are up to twelve

statocysts of the lithostyle type. The body reaches a

length of 350 ft; the tentacles are a little longer. By

means of flagellae, which cover the entire surface,

the animal swims actively through the interstices

with the aboral pole in front.

Otohydra is hermaphroditic. Fertilization is internal, and the development of the larva, which is

direct, occurs in an incubatory chamber in the gastral region between the epidermis and gastrodermis. The young have eight tentacles when set free.

Two or three embryos of different developmental

stages may be present at the same time in the

chamber.

When considering the taxonomic position of

Otohydra, Swedmark and Teissier (1958) pointed

to its similarities with Halammohydra. Egg cleavage and gastrulation are of the same type in both

genera and there is no planula stage. Both genera

possess flagella and have statocysts of the same

type; and the young animal of either genus, apart

from the statocysts, has the organization of an actinula. Yet, there are great differences between the

two genera; for example, Otohydra lacks an adhesive organ, has only one whorl of tentacle, and is

hermaphroditic and viviparous. Despite the differences, Swedmark and Teissier (1958, 1966) saw a

clear relationship and denied the interpretation of

either genus as a medusa or a polyp. As neither

genus could be placed satisfactorily in any of the

existing orders—Hydroida, Trachylida, and Siphon-
NUMBER 76

ophora—they felt justified in creating a new order,

which they called Actinulida, to include the families Halammohydridae and Otohydridae. In sup

port of this action, they pointed to the fact that

the once-advanced actinula theory (Bohm, 1878;

Brooks, 1886) had been defended by Hyman

(1940), Rees (1957), and others as the only one

that gives a satisfactory explanation of the phylogeny of the Hydrozoa.

While Kramp (1961) and others adopted the

order Actinulida, other writers had objections to

it. Werner (1965a) could not accept the Actinulida (nor the earlier interpretation of Halammohydra) as a narcomedusa and claimed that Halammohydra should be placed within the Hydroida.

One of Werner's arguments was that he could

prove that flagellae are common among adult hydromedusae. Further, in the anthomedusa Margelopsis haeckeli Hartlaub and in the limnomedusa

Gonionemus vertens A. Agassiz a reduction of the

umbrella may occur under certain circumstances,

giving these species an appearance rather similar to

that of Halammohydra. A third argument was that

the combination of nematocysts in Halammohydra

differs from that in the Trachylida, while it is

found in the Hydroida and Siphonophora.

Recent discoveries regarding the cnidome of

Halammohydra and Otohydra have provided additional information. In an undescribed species of

Otohydra, Lacassagne (1968a) described a new

type of nematocyst, the spirotele euryteloid, which

shares the characteristics of both desmonemes and

euryteles. The new type can be referred to the

group astomocnida. Lacassagne (1968a) also observed euryteloids, the aspiroteles, in a population

of Halammohydra. The findings are circumstantial

evidence of the relationship between the two

genera.

Lacassagne (1968b) discovered in Halammohydra still another type of nematocyst, the atrichous

anisorhizas. The number of categories of nematocysts in Halammohydra and Otohydra, viewed

together, is now up to seven, of which three are

known only from these two genera. It is clear that

FIGURE S.—Stylocoronella riedli: a, segmentation of buds; b, free planuloid; c, longitudinal

section through the planuloid; k, bud; p, proboscis; s, pedal disk. (From Salvini Plawen, 1966.)
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

1 mm

FIGURE 4.—Sphenotrochus sp. (Redrawn from Swedmark, 1964.)

the concept of Actinulida has a more substantial

foundation because of these findings.

Class SCYPHOZOA

Genus Stylocoronella Salvini Plawen

Monniot (1962) reported the occurrence of an interstitial scyphozoan, about 1 mm long, in "Amphioxus sand" from Banyuls. The first description

of an interstitial scyphozoan, however, was by Salvini Plawen in 1966 when he described Stylocoronella riedli from Rovigne. Salvini Plawen found

several specimens that were very similar to the

form from Banyuls. He stated that the maximum

size is 400 p, of which the stalk makes up 150 M.

There are up to 24 tentacles surrounding a prominent proboscis. Each tentacle has an ocellus at the

subumbrellar base (Figure 3). Stylocoronella riedli

is semisessile. It may creep with the aid of the tentacles, the ends of which are haptic because of a

local concentration of sticky isorhizes.

Only asexual reproduction is known. Interradial

stolonial buds grow out just basad to the tentacles.

The buds are shed as unciliated planuloids which

fasten after some days and grow into new polyps.

Strobilation was not observed.

Because of the lack of knowledge of sexual reproduction, the grouping of the new genus within

the Scyphozoa is difficult; the ocelli and the planuloids are characters shared with the Stauromedusae, while the number of tentacles is more in

agreement with the conditions in the Semaestomae.

Class ANTHOZOA

Genus Sphenotrochus Milne-Edwards and Haime

The first interstitial anthozoan was recorded from

the Mediterranean, near Marseilles, where the madreporarian Sphenotrochus sp. (Figure 4) was

found at a depth of 15 to 20 m (Rossi, 1961). It

belongs to the family Caryophylliidae (subfamily

Turbinolinae), and, according to Rossi (1961), is

probably conspecific with Sphenotrochus wrighti

described by Gosse (1859) from the Irish Sea.

Sphenotrochus sp. later was found also in the shell

dunes at Roscoff (Swedmark, 1964).

The organization of this small madreporarian,

which attains a length of only 2 mm, is bipolar,

with both the upper and lower extremity, in some

cases, having a mouth and a tentacle crown. The

lower extremity generates a new polyp opposite to

the upper extremity. Rossi (1961) stressed the peculiar adaptation to life on sandy bottom as shown

by the bipolarity and asexual mode of reproduction.

Summary

Even though the interstitial cnidarians are few,

their discovery has raised several ecological and

phylogenetic questions. Wide geographic areas still

are uninvestigated, however. Discoveries of new
NUMBER 76

forms and a better knowledge of the distribution

of known forms may provide answers to some of

these questions.

Literature Cited

Abonyi, A.

1929. Ober Protohydra leuckarti Greeff und ihre geographische Verbreitung. Proceedings of the 10th

International Congress of Zoology, Budapest,

8:1452-1460.

Baker, R. J.

1913. Protohydra leuckarti, Tidal Pools River Tavy.

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Bohm, R.

1878. Helgola'nder Leptomedusen. Jenaische Zeitschrift

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Brooks, W. K.

1886. The Life-History of the Hydromedusae: A Discussion of the Origin of the Medusae and the Significance of Metagenesis. Memoirs of the Boston Society of Natural History, 3(14):359-430.

Clausen, C.

1967. Morphological Studies of Halammohydra Remane

(Hydrozoa). Sarsia, 29:349-370.

Dawydoff, C. N.

1930. Protohydra caulleryi n. sp. des eaux indochinoises.

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Delamare Deboutteville, C.

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Gosse, P. H.

1859. On Sphenotrochus wrightii,z New Irish Madrepore.

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Hyman, L. H.

1940. The Invertebrates: Protozoa through Ctenophora.

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Kramp, P. L.

1961. Synopsis of the Medusae of the World. Journal of

the Marine Biological Association of the United

Kingdom, 40:1-469.

Lacassagne, M.

1968a. Deux nouveaux types de nematocystes astomocnides

chez les Actinulides (Hydrozoaires): les euryteloides

spiroteles et aspiroteles. Comptes Rendus de I'Academic des Sciences, 266:892-894.

1968b. Les anisorhizes atriches, nouveau type de nematocystes stomocnides presents chez deux formes d'Halammohydra (Hydrozoaires, Actinulides). Comptes

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1968c. Anatomie et histologie de l'Hydromeduse benthique

Armorhydra janowiczi Swedmark et Teissier, 1958.

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Luther, A.

1923. Ueber das Vorkommen von Protohydra leuckarti

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Societatis pro Fauna et Flora Fennica, 52:1-23.

Mamkaev, J. V.

1962. Records of Interstitial Fauna from the Barents Sea.

Vestnik Lcningradskogo Universiteta, 9(2): 193-224.

Monniot, F.

1962. Recherches sur les graviers a Amphioxus de la

region de Banyuls-sur-Mer. Vie et Milieu, 13:231-

322.

Nyholm, K. G.

1951. A Contribution to the Study of the Sexual Phase

of Protohydra leuckarti Greeff. Arkiv for Zoologi,

2:529-530.

Omer-Cooper, J.

1957. Protohydra and Kinorhyncha in Africa. Nature,

179(4557):486.

Rao, G. C, and P. N. Ganapati

1966. A Report on the Occurrence of an Aberrant Cnidarian, Halammohydra octopodides Remane, in

Indian Waters. Current Science, 35:129-130.

Rees, W. J.

1957. Evolutionary Trends in the Classification of Capitate Hydroids and Medusae. Bulletin of the Brit~

ish Museum (Natural History), Zoology, 4(9):455-

534.

Remane, A.

1927. Halammohydra, ein eigenartiges Hydrozoon der

Nord- und Ostsee. Zeitschrift fur Morphologic und

Okologie der Tiere, 7:643-678.

Rossi, L.

1961. Morfologia e riproduzione vegetativa di un Madreporario nuovo per il Mediterraneo. Bolktino di

Zoologia, 28:261-272.

Ruebush, T. K.

1939. The Occurrence of the Two Rare Genera, Protohydra and Protodrilus, on the East Coast of North

America. Science, 90(2348):617-618.

Salvini Plawen, L.

1966. Zur Kenntnis der Cnidaria des nordadriatischen

Mesopsammon. Veroffentlichungen des Instituts

fiir Meeresforschung in Bremerhaven, Sonderband

2:165-186.

Schulz, E.

1950a. Zur Oekologie von Protohydra leuckarti Greeff

(studien an Hydrozoa, I). Kieler Meeresforschungen, 8(l):53-57.

1950b. Psam mo hydra nanna, ein neues solitares Hydrozoon

in der westlichen Beltsee (studien an Hydrozoa, II).

Kieler Meeresforschungen, 8(2): 122-137.

1952. Halammohydra schulzei Remane in der westlichen

Ostsee. Faunistische Mitteilungen arts Norddeutschland, 2:6-7.
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Swedmark, B.

1956. Nouveau Gastrotriches Macrodasyoides de la region

de Roscoff. Archives de Zoologie Expe'rimentale et

Generate, Notes et Revue, 94:43-57.

1957. Variation morphologique des differentes populations regionales d'Halammohydra. Annie Biologique, 44(3/4):183-189.

1964. The Interstitial Fauna of Marine Sand. Biological

Reviews, 39:1-42.

Swedmark, B., and G. Teissier

1950. Developpement d'un Hydrozoaire aberrant Halammohydra schuhei Remane. Comptes Rendus de

I'Academie des Sciences, 231:173-174.

1957a. Organisation et developpement des Halammohydra

(Hydrozoaires). Comptes Rendus de I'Academie des

Sciences, 244:501-504.

1957b. Halammohydra vermiformis n. sp. et la famille des

Halammohydridae Remane. Bulletin de la Sociite

Zoologique de France, 82:38-49.

1958. Otohydra vagans n.g., n. sp., Hydrozoaire des sables,

apparante aus Halammohydridees. Comptes Rendus de I'Academie des Sciences, 247:238-240.

1966. The Actinulida and Their Evolutionary Significance. Symposium of the Zoological Society of

London, 16:119-133.

Teissier, G.

1950. Notes sur quelques Hydrozaires de Roscoff. Archives de Zoologie Experimental et Generate, Notes

et Revue, 87:1-10.

Thiel, M. E.

1962. Bestimmungstabellen der Polypen und Medusen

der russischen Gewasser. Mitteilungen aus dem

Hamburgischen Zoologischen Museum und Institut,

60:285-324.

Valkanov, A.

1947. Protohydra leuckarti Greeff vom Schwarzen Meer.

Arbeiten aus der Biologischen Meeresstation in

Varna, 13:31-35.

Werner, B.

1965a. Halammohydra Remane, Medusennatur und Stellung im System. Zoologischer Anieiger, Supplementband 28:163-168.

1965b. Die Nesselkapseln der Cnidaria, mil besonderer

Beriicksichtigung der Hydroida. 1. Klassifikation

und Bedeutung fiir die Systematik und Evolution.

Helgoldnder wissenschaftliche Meeresuntersuchungen, 12(1-2): 1-39.

Westblad, E.

1929. Protohydra leuckarti Greeff, an der schwedischen

Kuste entdeckt. Archiv for Zoologie, 21(4): 1-4.

1954. Some Hydroidea and Turlx'llaria from Western

Norway with Descriptions of Three New Species

of Turbellaria. Universitetet i Bergen, Arbok,

Naturvitenskapelig rekke, 10:1-22.

Wieser, W.

1958. Occurrence of Protohydra leuckarti in Puget Sound.

Pacific Science, 12:106-108.
Wolfgang Sterrer Gnathostomulida:

Problems and Procedures

ABSTRACT

Procedures of sampling and extracting Gnathostomulida from sediments are evaluated. Distribution,

ecology, and taxonomy are discussed. Statisticalmetrical data are emphasized.

The Gnathostomulida, today a well-established

group of marine meiofauna, have rapidly expanded in terms of knowledge of forms and distribution since their original description (Ax, 1956).

More than 80 species and 18 genera are known to

the present author, and a first approach to their

systematics and evolution soon will be published

(Sterrer, in press.b).

The question as to why such an abundant and

cosmopolitan constituent of marine meiofauna was

discovered so late is only one in a series of problems that arises when dealing with this group. Others are connected with sampling and extracting,

ecology and distribution, and biology and systematics. The purpose of this paper is to give a brief

synopsis of current problems as they emerge during

the different procedures of investigation. More detailed technical recommendations are given in Hulings and Gray (1971), whereas a complete bibliography of the class will be found in Sterrer (in

press,b).

Sampling and Extracting

Sampling and extracting procedures have to take

into account the ecophysiological particularities of

the group and can, in fact, take advantage of

them.

Wolfgang Sterrer, Bermuda Biological Station, St. Georges

West, Bermuda.

Sampling can be effected with almost any device

that penetrates deeply enough to get to the "black

layer." A spade usually is sufficient in the intertidal,

and any dredge provided with a hovel-knife to

secure depth can be used in the subtidal. Small

sand patches ("Austrognathia sand"), however,

can be sampled only with skin diving methods (a

smaller triangular net is pushed through the

sand). For quantitative sampling, any corer can be

used. The slow locomotion of gnathostomulids

makes a secondary displacement in the corer during or after sampling quite improbable.

Qualitative samples, at least 1 liter in volume

(but usually 10 liters), are kept in the laboratory

in covered buckets for at least five days before first

extraction takes place. Deterioration of climate

which occurs in the sample gradually forces the vagile fauna towards the surface layers, from which

they can be extracted. Gnathostomulids, however,

appear very late at the surface, the density peak

usually being reached in the second week. At that

time the sample shows black spots at the surface

due to growth of iron bacteria, and it emits a

heavy H2S smell. Hence, one more reason for the

late discovery of the group: such samples were

usually discarded long before gnathostomulids

emerged.

For the extraction of gnathostomulids, two effective methods have been found: the seawater-ice

method (Uhlig, 1964, 1968) and the magnesium

chloride method (Sterrer, 1968). The author has

had no personal experience with Uhlig's method,

but he has found that the MgClj method is very

simple and produces high specimen numbers. Portions of surface sand from the deteriorated sample

("primary sample," about 250 ml) are placed in

an Erlenmeyer flask (2 liters), and isotonic MgCl^

solution is added. After mixing gently, the flask is

left for 10 minutes. Then it is vigorously shaken

and, when the sand has settled, the suspension is
10

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

filtered through a 62-/i nylon monofilament sieve

mounted on a plexi ring. This procedure is repeated once with MgCl, and once with seawater.

After a short rinse with seawater (to get rid of the

MgCls), filter and deposit are placed in a Petri

dish with a little seawater. To avoid evaporation,

the dish should be covered and kept in a cool

place. Animals tend to move through the meshes

of the filter to the bottom of the dish, where they

can be collected free from sediment. This process

starts immediately after extraction and may go on

for several days. These "secondary samples" can be

checked periodically, during which time the filter

is placed in an alternate dish. Obviously based on

a combination of taxes (negative phototaxis and

positive geotaxis and thigmotaxis), this method

works equally well for other groups of the mesopsammon (especially Gastrotricha and Turbellaria).

The spaces between the meshes as well as between

the filter and the bottom of the dish apparently

represent equivalents of the natural interstitial

habitat. This method is especially useful where

large quantities of detritus make it impossible to

mechanically separate larger numbers of animals.

For quantitative purposes, the same filter can be

used upside down, and the deposit is washed into

a dish where the animals can be sorted and

counted. Otherwise, quantitative samples of

usually 100 ml are treated the same way as qualitative ones, but without deterioration.

The efficiency of these extracting methods, although considered high, has not been tested as yet

for Gnathostomulida, since the emphasis during

the initial period of investigation was simply to obtain as much material for systematic studies as possible. It is obvious that the taxon's slow locomotory ability and its retarded response to environmental pressure make most quantitative methods

rather questionable.

Ecology

The main reason for the late discovery of Gnathostomulida probably is that they have not been

looked for in the right biotope. Classical research

on interstitial fauna tended to concentrate on

clean, well-aerated sand, and that is exactly where

gnathostomulids do not occur. The typical biotope,

instead, is sand with a large amount of organic detritus. (This characterization is still as vague as it

sounds, since at present about 50 percent of the

author's samples taken specifically for gnathostomulids do not yield a single specimen.) This type

of sediment invariably occurs in sheltered positions

such as (intertidally) on sand flats in sounds, or

(subtidally) on small sand patches surrounded by

rocks, larger plants, or coral. Such sand flats are

determined by a moderate but steady rhythm of

water movement and, therefore, have a rather narrow granulometrical spectrum, often with a medium grain size of 150 p (which was thought uninhabitable for metazoa). Such a spectrum is

different in the small subtidal basins. Sediment

there is often extremely heterogeneous, typically

composed of large shell fragments together with

medium-size sand and flocculent detritus. This

seems to indicate that, hydrodynamically, small

subtidal basins act as more or less stagnant niches

which, under a water body of varying movement

and speed, collect any suspended sediment that

comes under their influence. As far as the gnathostomulids are concerned, these heterogenous sands

are typically inhabited by representatives of Austrognathiidae. This type of sediment should not be

confused with what is known as "Amphioxus sand."

The latter, composed of a coarse sand fraction

with a high content of "mud," probably represents

the only true intermediate biotope between sand

and mud. "Austrognathia sand," however, seems to

have only a very negligible fraction of silt and clay

or none at all.

Another reason why gnathostomulids were so

long unknown is that they prefer deeper and

mostly H2S-rich sand layers. It had been taken for

granted that, except in high-energy beaches, only

the uppermost sand layer was inhabited by an interstitial fauna. Recent investigations (Riedl,

1969) showed that the maximum density of the

gnathostomulid population is at the discontinuity

layer, i.e., often considerably below the sand surface. Recently, even living embryos, still in the egg

capsule, have been found in these deep layers

(Riedl and Sterrer, unpublished). Whether this

means that gnathostomulids have anaerobic metabolism or that their distribution is determined by

that of another organism (bacteria as food) is yet

undecided.

A further interesting feature about the occur-
NUMBER 76 11

rence of the group is that a "typical" biotope almost invariably yields several species. Up to 13 species can be extracted from one sample of about 10

liters of sand. This points to a very high degree of

specialization in a biotope whose characteristics we

still ignore. This particular organism-biotope interrelationship should be studied from two sides: detailed analysis of the structural, chemical, and biological (including bacterial growth) properties of

several "typical" substrata, and preference experiments.

Whereas the above-mentioned ecological requirements are very much the same for most gnathostomulids, the genus Gnathostomula Ax differs in

several respects. First of all, it is rather eurytopic:

species of this genus can be found on "typical"

substrata as well as on pure sand, on seagrass roots,

or even on mud. This unselective behavior probably also accounts for the fact that Gnathostomula

species—contrary to the usual occurrence of several

species per sample—are, in many samples, the only

representatives of the class. True mass occurrence,

furthermore, has been noted only in Gnathostomula so far, with densities so high as to outnumber even the nematodes in the sample. As to the

vertical distribution in the substratum, Gnathostomula seems to prefer the surface layers. This agrees

very well with the observation that, in a deteriorating sample, Gnathostomula is among the first gnathostomulids to migrate to the surface (Sterrer,

1965; Riedl, 1969). Finally, the genus Gnathostomula is known from all geographic regions where

gnathostomulids have been found, again probably

due to its eurytopic occurrence. This leads to questions of distribution and zoogeography.

Distribution

World-wide distribution of gnathostomulids was to

be expected after the first descriptions had been

published, and such distribution has since been

well documented. The best known faunas so far

are those of the North Sea (Ax, 1965; Sterrer,

1966a,b, 1968, and in press.a), the Adriatic (Sterrer, 1965), and the east coast of the United States

(Reidl, 1969, 1970a,b, and in press; Sterrer, 1970,

and in press.c). The author has extensive collections

from the Mediterranean, Florida, and Panama. On

the other hand, in the Pacific and adjacent areas

the gnathostomulids are poorly known, with only a

few scattered finds in the Red Sea (Riedl, 1966b),

the Maldives (Gerlach, 1958), the Sea of Japan

(Mamkaev, in Ax, 1965), and California (T. G.

Karling, personal communication).

On the basis of the present material, an interesting zoogeographical aspect seems to emerge. As in

many other taxa of the interstitial fauna (see

Schopfer-Sterrer, 1969, for Gastrotricha), the differences, for example, between the European and the

American Atlantic faunas seem to be on the species level, i.e., the same genera are present on both

sides of the Atlantic.

In certain species, differences may be so minute

that they can be detected only by applying the statistical metric method (see under Taxonomy,

below). This leads to the question of dispersal of

the interstitial fauna. Since it is a common fact

that most members of the interstitial fauna have

no planktonic larvae, the paradox of the high similarity in geographically distant faunas becomes

more and more obvious. A striking example is the

gnathostomulid genus Gnathostomaria Ax. The

first (and so far the only) described species, G.

lutheri Ax, was found in a coastal pond ("e"tang")

on the south coast of France (Ax, 1956). The biotope is wet sand above high water level. During

the author's investigations of the North Carolina

beaches, a second Gnathostomaria species was

found in an almost identical biotope: wet sand

above high water mark at a sound near Wilmington. There is no doubt about a close relation of

these two species within the genus Gnathostomaria.

A very similar case seems to be that of the Mystacocarida. The latter, however, occur on exposed

beaches and have larval stages, which may present

more opportunity for passive dispersal than is the

case in Gnathostomulida. An investigation of such

dispersal would obviously also have a bearing on

the question of the relative age of the biotopes (is

sand, in particular anaerobic sand, the most ancient biotope?) as well as of the origin of oceans

and continents (e.g., continental drift).

It is hoped that with increasing knowledge of the

distribution oi the interstitial fauna it will be possible, in time, to reconstruct the mechanism of

their worldwide dispersal. The possibility exists of

tracing the gradual spreading of a systematic group
12

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

during evolution by carefully comparing the morphological differences between species with the actual geographic distances of their distribution (see

Riedl, 1966a, "Lebensorttyp").

Biology

Very few data on the biology of the Gnathostomulida are available so far (Sterrer, in press, a; Riedl,

1969). There are two reasons for this. First, the initial period of gnathostomulid research mainly was

devoted to morphological studies, and biological

observations were rather fragmentary. Second, it

still is a difficult problem to keep animals alive in

the laboratory.

Whereas some species of Austrognatharia Sterrer are able to form a mucous cyst in which they

may survive for several days, most other gnathostomulids begin to disintegrate within hours after

they have been extracted from the sediment (Sterrer, in press,a). It is not clear yet whether this is

due to the extraction method (mostly with

MgCl2), to the lack of sediment, or to the presence

of oxygen or some other unknown component of

the artificial environment.

Taxonomy

Taxonomy often has to rely on minute characters

which, in some cases, can be detected only by careful measurements of many members of a population. With this statement of a "splitter," for reasons of taxonomical accuracy—as well as zoogeographical information (see "Distribution")—a concept that permits one to find differences rather than

similarities in a new locality is preferable to "finding the same old European species in the South

Pacific." The same species may occur in the new

locality but this would have to be proved (see

Hulings and Gray, 1971).

Differences have to be expressed in metrical

data, a method applied regularly to the macrofauna and "hard" meiofauna (Arthropoda, Nematoda) but used very little in the taxonomy of the

"soft" meiofauna. As long as the criteria (such as

degree of contraction and squeezing,"" or points of

reference) remain the same, however, such measurements prove extremely valuable even in soft organisms (Sterrer, 1968). Furthermore, most "soft"

taxa have at least some hard structures (such as

mouthparts, stylets, scales, spines, etc.) that can

easily be measured. For better comparison of relative dimensions (length-width ratio, or ratio and

situation of organs) it is advisable to take the

body length of a specimen as 100 units (U 0 to U

100); e.g., "ovary from U 60 to U 72," or "maximal width 33 fi (=7 U) at U 65" (Rieger and

Sterrer, 1968).

One of the major problems in gnathostomulid

taxonomy concerns size. This is particularly true

for the most important character, the jaws. Gnathostomula seems to be the most difficult genus in this

respect. Known from all over the world, it already

comprises a considerable number of species (about

20 so far) that differ only slightly, although in a

number of characters. With regard to the jaws, this

means counting teeth in the dimension of one

third of a micron, which coincides with the absolute limitation of the optical microscope (Figure la).

Another difficulty is that of poor delimitation between cuticular parts and surrounding tissue. This

is especially true for the basal plate. In the Filospermoidea and lower Scleroperalia it often is difficult to determine whether a basal plate is present

at all, and even in Gnathostomula the outline of

the plate can be difficult to define. Cuticular parts

are best studied in squeeze preparation, with increasing pressure being applied to the coverslip

(Hulings and Gray, 1971). If a specimen is well

oriented dorsoventrally, pictures of squeezed jaws

may be obtained that allow exact counts of teeth

(Figure la). It is hoped, however, that the scanning microscope will furnish a better method for

the study of these structures.

A further character of high taxonomic value is

the sensory organs (Figure \b). Numbers, arrangement, and length of sensory cilia and bristles are

important in phylogenetical considerations. But it

often is extremely difficult to obtain such data, one

reason being that the sensory bristles often join the

ciliary beat, making them difficult to locate; furthermore, these structures disintegrate readily

when the animal starts feeling uncomfortable. Recording of the above data, therefore, should be the

first step in the series of observations.

Among the characters that seem to be of high

taxonomic value is the pattern of the epidermal
NUMBER 76 13

10 jjm

FIGURE 1.—Gnathostomula paradoxa: a, ideally squeezed preparation of basal plate and jaws, showing the three rows of teeth on

each jaw (bp, basal plate; dr, dorsal row; mr, middle row; vr,

ventral row of teeth) ; b, head, slightly squeezed, demonstrating

the arrangement of sensory organs (d, dorsalia; f, frontalia; 1,

lateralia; r, rostralia; ph, pharynx; v, ventralia).

cells. In higher Scleroperalia as well as in the Conophoralia the cells are usually arranged in rows

that converge rostrally in the ventral median line

and caudally in the dorsal median line, thus forming inclined rhomb-like stripes around the body.

Sperm morphology is one of the most puzzling

features in gnathostomulid research. It is, in fact,

the most heterogeneous morphological character

throughout the class. Known so far are three major

types of sperm (filiform, dwarf, and conulus; see

Sterrer, in press, b), each of which is structurally

quite different from the others. It is hoped that a

better knowledge of spermatogenesis, as well as

special staining and ultrastructural techniques, will

clarify the homology of the sperm types. An interesting aspect relevant to the clarification of gnathostomulids as a whole will be the possible homology of one of the types with sperm known from

other classes: the "filiform" type of Gastrotricha

and some Turbellaria, and the aberrant "conulus"-like type of Catenulida (Turbellaria).

Going into histological methods, finally, a striking contrast becomes apparent: small dimension,

low level of general organization, and poor tissue

differentiation on one side and the extremely complicated muscular pharynx on the other. A method

of serial, ultrathin sections with subsequent threedimensional reconstruction of electron micrographs

hopefully will contribute to a better understanding

of this paradox.

Taxonomic difficulties related to biology are

those of life cycles. For instance, all specimens of

Gnathostomaria lutheri collected at the type-locality in October 1966 were anterior fragments, and a

study of the genital organs was impossible. Similar

fragmentation seems to occur in many Filospermoidea. Another biological phenomenon occurs in

Gnathostomulidae: sexual stages seem to alternate

with feeding stages (Riedl, 1969), the latter being

characterized by a reduction of sexual organs. All

of these phenomena make taxonomy rather difficult, and they emphasize once more the necessity

of getting the most out of the few available characters.

Finally, the systematic position of the taxon is
14

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

far from being solved. Many features both in organization and biology are similar to those of widely

distant taxa—features such as the cuticular mouthparts of Rotataria and Turbellaria, the general organization of lower Turbellaria, the sperm of Gastrotricha and Turbellaria, the quasi-lack of a

parenchyma in the whole of the Aschelminthes,

and the monociliary epithelium of larvae of echinoderms. This means, on the other hand, that all

of these features need to be studied much more

thoroughly, preferably with electron microscopy

techniques. A possible relationship with the extinct

Conodontophorida has been discussed recently by

paleontologists (Durden et al., 1969). Careful evaluation of the available data leads the author to

consider the Gnathostomulida as a class within the

Platyhelminthes, with possible relationships to

Turbellaria via the turbellarian order Catenulida

(Sterrer, in press.b).

Summary

The problems connected with the study of Gnathostomulida (Platyhelminthes) have been briefly

evaluated. Procedures of sampling (spade, corer,

diver-operated net or dredge) and extracting

(modified anesthetization, or Uhlig method) have

been followed by remarks of distribution (worldwide) , zoogeography (relation between morphological differences and geographical distances), and

ecology ("black layer," hence probability of anaerobic metabolism, "typical" substratum with high

species diversity). Biology is poorly known (difficulty of keeping and rearing in the laboratory).

Taxonomy should rely on statistical-metrical data;

the main problems are small size, as opposed to

complex, frail, or poorly delimited structures, and

gaps in comparability within (e.g., sperm) and

without (e.g., cuticular mouthparts) the class.

Literature Cited

Ax, P.

1956. Die Gnathostomulida, eine ratselhafte Wurmgruppe

aus dem Meeressand. Abhandlungen der Akademie der Wissenschaften und der Literatur, Mathematischnaturwissenschaftliche Klasse, Mainz, 8:1-32.

1965. Zur Morphologie und Systematik der Gnathostomulida. Untersuchungen an Gnathostomula paradoxa

Ax. Zeitschrift fiir Zoologische Systematik und Evolutionforschung, 3:259-276.

Durden, C; J. Rodgers; E. Yochelson; and R. Riedl

1969. Gnathostomulida: Is there a Fossil Record? Science, 164:855-856.

Gerlach, S. A.

1958. Ein neuer Vertreter der Gnathostomulida (Turbellaria?) aus dem Meeressand der Malediven. Kieler

Meeresforschungen, 14:175-176.

Hulings, N. C., and J. S. Gray

1971. A Manual for the Study of Meiofauna. Smithsonian Contributions to Zoology, 78:1-8S.

Riedl, R.

1966a. Biologic der Meereshohlen. Topographic, Faunistik

und dkologie eines unterseeischen Lebensraumes.

636 pages. Hamburg and Vienna: P. Parey.

1966b. Faunistische Studien am Roten Meer im Winter

1961/62, III. Die Aufsammlungen in Suez und AlGhardaqa, nebst einigen Bemerkungen tiber Gnathostomulida. Zoologische Jahrbiicher, Systematik,

93:139-157.

1969. Gnathostomulida from America. Science, 163:445-

452.

1970a. Semaeognathia, a New Genus of Gnathostomulida

from the North American Coast. Internationale

Revue der gesamten Hydrobiologie, 55:359-370.

1970b. On Labidognathia Longicollis nov. gen., nov. spec,

from the West Atlantic Coast (Gnathostomulida).

Internationale Revue der gesamten Hydrobiologie,

55:227-244.

In press. On Onychognathia, a New Genus of Gnathostomulida from the Tropical and Subtropical West

Atlantic. Bulletin of Marine Science.

Rieger, R., and W. Sterrer

1968. Megamorion brevicauda gen. nov., spec, nov., ein

Vertreter der Turbellarienordnung Macrostomida

aus dem Tiefenschlamm eines norwegischen Fjords.

Sarsia, 31:75-100.

Schopfer-Sterrer, C.

1969. Chordodasys riedli gen. nov., spec, nov., a Macrodasyoid Gastrotrich with a Chordoid Organ. Cahiers de Biologic Marine, 10:391-404.

Sterrer, W.

1965. Gnathostomula axi Kirsteuer und Austrognathia

(ein weiteres Gnathostomuliden-Genus) aus der

Nordadria. Zeitschrift fur Morphologie und Okologie der Tiere, 55:783-795.

1966a. Gnathostomula paradoxa Ax und Vertreter von

Pterognathia (Ein neues Gnathostomuliden-Genus)

von der schwedischen Westkiiste. Arkiv for Zoologi,

18:405-412.
NUMBER 76 15

1966b. Neue Gnathostomulida. Veroffentlichungen des

Instituts fiir Meeresforschung in Bremerhaven, sonderband 2:201-207.

1968. Beitrage zur Kenntnis der Gnathostomulida. I. Anatomie und Morphologie des Genus Pterognathia

Sterrer. Arkiv for Zoologi, 22:1-125.

1970. On some Species of Austrognatharia, Pterognathia

and Haplognathia nov. gen. from the North Carolina Coast (Gnathostomulida). Internationale Revue

der gesamten Hydrobiologie, 55:371-385.

In press,a. On the Biology of Gnathostomulida. In Proceedings of the Third European Marine Biology

Symposium. Vie et Milieu, supplement 22.

In press.b. Systematic and Evolution within the Gnathostomulida. Systematic Zoology.

In press.c. Agnathiella backeri nov. gen., nov. spec, from

Southern Florida: The First Gnathostomulid without Jaws. Internationale Revue der gesamten

Hydrobiologie.

Uhlig, G.

1964. Eine einfache Methode zur Extraktion der vagilen,

mesopsammalen Mikrofauna. Helgolander wissenschaftliche Meeresuntersuchungen, 11:178-185.

1968. Quantitative Methods in the Study of Interstitial

Fauna. Transactions of the American Microscopical Society, 87(2):226-232.

Ernst Kirsteuer The Interstitial

Nemertean Fauna

of Marine Sand

ABSTRACT

Lists of the interstitial nemerteans and their geographic distribution are given. The general biology,

including morphology, development, and ecology,

is discussed.

The acoelomate phylum Nemertina comprises

about 850 species of worms with a body length between 1 mm and 30 m. Nemerteans are known

from land and fresh water, from all oceans, all

depths, and all major marine habitats. As far as

the marine sediment bottoms are concerned, it is

possible to distinguish between a mud fauna and a

sand fauna. The present review, however, deals

mainly with the nemerteans inhabiting the interstices of marine sand. Nemerteans living in or on

mud are not characterized by small size and are

generally well above the 1 to 2 mm body length

limit usually applied for meiobenthic forms. Furthermore, they have, with the exception of some

statocyst-bearing palaeonemerteans, no developed

morphological features which would make them

quite distinct from species occurring in other marine habitats such as the phytal, coral reefs, submarine caves, etc. In mud fauna, representatives of

all three free-living nemertean orders are included,

and when the composition of die fauna is compared with that from other biotopes it becomes evident that the Palaeonemertina have their highest

frequency on mud bottoms whereas the Heteronemertina occupy an intermediate position and the

Ernst Kirsteuer, American Museum of Natural History, New

York, New York 10004. Study supported in part by National

Science Foundation grant GB-7952.

Hoplonemertina are the poorest represented order

(Kirsteuer, 1963).

The marine interstitial nemertean fauna, on the

other hand, is systematically less diverse but the

species clearly show morphological adaptation to

the life in the interstitial environment. Twentyseven species of interstitial nemerteans have been

described, seven of which are palaeonemerteans:

Carinina arenaria Hylbom. Atlantic: Gullmar Fjord.

Cephalothrix arenaria Hylbom. Atlantic: Gullmar Fjord.

Cephalothrix atlantica Gerner. Atlantic: Arcachon.

Cephalothrix germanica Gerner. Atlantic: Sylt.

Cephalothrix mediterranea Gerner. Mediterranean Sea: Canet

Plage.

Cephalothrix paciftca Gerner. Pacific: Washington.

Procephalothrix kiliensis Friedrich. Baltic Sea: Kiel.

The remaining species, belonging to the order

Hoplonemertina and the suborder Monostilifera,

are as follows:

Arenonemertes microps Friedrich. Baltic Sea: Kiel.

Arenonemertes minutus Friedrich. Baltic Sea: Fehmarn.

Prostomatella arenicola Friedrich. Baltic Sea: Kiel.

Otonemertes marcusi Corr£a. Atlantic: Brazil.

Ototyphlonemertes pallida (Keferstein). Atlantic: St. Vaast,

Hornum, Amrum. Black Sea: Suchumi, Constantza, Agigea.

Ototyphlonemertes aurita (Uljanin). Black Sea: Sevastopol,

Suchumi.

Ototyphlonemertes aurantiaca (Du Plessis). Mediterranean

Sea: Nice, Banyuls sur Mer, Canet Plage.

Ototyphlonemertes macintoshi Burger. Mediterranean Sea:

Naples, Villefranche sur Mer.

Ototyphlonemertes brunnea Burger. Mediterranean Sea: Naples, Villefranche sur Mer.

Ototyphlonemertes duplex Burger. Mediterranean Sea: Naples, Villefranche sur Mer.

Ototyphlonemertes spiralis Coe. Pacific: California.

Ototyphlonemertes pellucida Coe. Atlantic: Massachusetts,

Florida.

Ototyphlonemertes evelinae Correa. Atlantic: Brazil, Florida.

Ototyphlonemertes brevis Correa. Atlantic: Brazil.

Ototyphlonemertes erneba Correa. Atlantic: Brazil.

17
18

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Ototyphlonemertes parmula Correa. Atlantic: Brazil.

Ototyphlonemertes fila Correa. Atlantic: Brazil, Florida.

Ototyphlonemertes lactea Correa. Atlantic: Brazil, Florida.

Ototyphlonemertes antipai Miiller. Black Sea: Agigea, Costinesti, Vama Veche, Solotyie, Pesski, Kaba Kum.

Ototyphlonemertes americana Gerner. Pacific: Washington.

Like many other invertebrate groups the nemerteans also have their smallest representatives in the

interstitial fauna. Arenonemertes tninutus, which

reaches a length of only 1 mm, is the smallest described nemertean. Several of the other species are

between 2 and 10 mm long, and some, such as

Ototyphlonemertes macintoshi, O. spiralis, and O.

evelinae, measure from 30 to 50 mm in length.

The body, however, is always extremely slender

with a diameter of not more than 500 p, thus enabling the animals to move through the interstitial

system without actively replacing the sand grains;

all the listed species, therefore, are considered to

be mesopsammon forms sensu Boaden (1962).

Interstitial nemerteans are white, orange or

brownish, yellowish white or greenish white, and

they lack the elaborate color patterns so often

found in other species. Generally, locomotion is effected by ciliary gliding. Locomotion by writhing,

similar to that of nematodes, was described by

Friedrich (1935) for Prostomatella arenicola, but

this is an exception and atypical for nemerteans.

In some species of Ototyphlonemertes Diesing conspicuously long tactile cirri are arranged along the

anterior and posterior body margins, and near the

posterior end of the body adhesive plates are

formed by aggregation of epidermal gland cells.

Large adhesive gland cells distributed over the

whole body surface also were found in Arenonemertes minutus and A. microps by Friedrich

(1949). A chordoid tissue, considered by Ax (1966)

to be typical "Lebensform" characteristic of the

mesopsammon, was observed in Ototyphlonemertes

antipai by Miiller (1968b), who compared the

vacuolized epithelium with that in the turbellarian

Cystiplex axi Karling.

Static organs are developed in Carinina arenaria,

Otonemertes marcusi, and in all species of the

genus Ototyphlonemertes, where either one or two

pairs of statocysts are present. Ocelli, on the other

hand, are lacking in most of the species of interstitial nemerteans.

In the stenoecious genera Ototyphlonemertes

(recently reviewed by Miiller, 1968a) and Arenonemertes Friedrich there is a tendency for reduction,

in various degrees, of the organs otherwise typical

for nemerteans. Within the Ototyphlonemertes, the

proboscis sheath extends over the entire length of

the body in O. aurita, whereas in the majority of

the other species it reaches only for half or one

third of the body length; and in O. brevis and O.

lactea it is restricted to 10 percent of the body

length. In the same genus the chemoreceptive cerebral sense organs also show different stages of reduction, from normal organization to the complete

loss of the organ (Miiller, 1968a).

Correlated with the reduction of body size, the

midgut diverticula are generally less developed and

are lacking in the species of Arenonemertes and in

the smaller species of Ototyphlonemertes. For one

of the latter, O. brevis, Correa (1950) was able to

show that the loss of diverticula is compensated for

by intensified enzymatic processes. Further reduction occurs in the gonads which, in accordance

with observations in other mesopsammic invertebrates, are limited in number. In Arenonemertes

minutus only six gonads, each containing just one

ripe oocyte, were found (Friedrich, 1949).

The development of interstitial nemerteans is

still unknown, but as only species of the orders Palaeonemertina and Hoplonemertina are present in

this fauna it can be assumed that the development

is of the direct type, thus omitting a pelagic larval

phase, which is known only from heteronemerteans.

Interstitial nemerteans, found in the intertidal

zone and in the subtidal region to a depth of 15

m, seem to prefer rather clean sand. More detailed

ecological data are available for some species of

Ototyphlonemertes (Muller, 1968a). Ototyphlonemertes aurita lives on sand under stones, occupying

ecologically a transient position between sand epifauna and mesopsammon; interestingly, this is also

the species with the unreduced proboscis sheath and

normal cerebral organs. Ototyphlonemertes pallida

occurs from the upper intertidal to 10 m. Muller

(1968a) found O. pallida 20 mm long in fine sand

only and specimens of O. antipai 4 to 7 mm long

in coarse sand (1.2-mm grain size) only. Correa

(1948) observed during experiments that the 30-mm
NUMBER 76 19

specimens of O. evelinae and the 10-mm specimens

of O. brevis showed no preference for either fine

sand of 0.5-mm to 2-mm grain size or coarse sand of

2-mm to 5-mm grain size. Correa (1961) also collected O. evelinae (30 mm long), O. fila (20 mm

long), O. pellucida (12 mm long) and O. lactea (4.5

mm long) from the same area of a coarse-sand

beach near Miami, Florida. The present data do

not indicate a specialized substratum selection for

the Ototyphlonemertes, and obviously there is no

correlation between the size of the animals and the

grain size of the sand they inhabit.

The quantitative distribution of Ototyphlonemertes evelinae and O. brevis was studied by

Correa (1949) along a transect from the line of

mean high tide to that of mean low tide on a Brazilian beach. Under normal weather conditions the

worms occurred mainly in the upper 10 cm of

sand. The largest number of specimens was registered in samples taken from the middle part of the

transect, and in this region animals also were

found 20 cm deep in the substratum. No migration

patterns in connection with the changing tides

were observed, and only when the beach was

struck occasionally by heavy waves did the animals

go deeper into the sediment. The maximum number of specimens recorded for the two species combined was 555 in 1,000 cm3

 of sand. Correa (1949),

however, pointed out that this extremely high population density presumably was due to the fact

that garbage from a nearby hotel was disposed in

the collecting area, thus providing a rich food supply—either directly or by attracting other interstitial animals like polychaetes and crustaceans upon

which nemerteans prey.

Literature Cited

Ax, P.

1966.

Boaden

1962.

Correa,

1948.

1949.

1950.

1961.

Friedrich, H.

1935. Beobachtungen iiber eigenartige Bewegungsweisen

bei Nemertinen. Biologisches Zentralblatt, 55:84-86.

1949. tJber zwei bemerkenswerte neue Nemertinen der

Sandfauna. Kieler Meeresforschungen, 6:68-72.

Kirsteuer, E.

1963. Zur Okologie systematischer Einheiten bei Nemertinen. Zoologischer Anzeiger, 170:343—354..

Miiller, G. J.

1968a. Betrachtungen iiber die Gattung Ototyphlonemertes

Diesing 1863 nebst Bestimmungsschliissel der validen Arten (Hoplonemertini). Senckenbergiana Biologica, 49:461-168.

1968b. Ototyphlonemertes antipai n. sp., ein neues Mitglied des mediolitoralen Mesopsammals des Schwarzen Meeres. Travaux du Museum d'Histoire Naturelle "Grigore Antipa," 8:343-348.

Die Bedeutung der interstitiellen Sandfauna fiir

allgemeine Probleme der Systematik, Okologie und

Biologic Veroffentlichungen des Instituts fiir

Meeresforschung in Bremerhaven, Son der band

2:15-^5.

, P. J. S.

Grazing in the Interstitial Habitat: A Review.

British Ecological Society Symposium Number 4,

pages 299-303.

D. D.

Ototyphlonemertes from the Brazilian Coast. Comunicaciones Zoologicas del Museo de Historic

Natural de Montevideo, 2(49): 1-12.

Ecological Study of Brazilian Ototyphlonemertes.

Comunicaciones Zoologicas del Museo de Historia

Natural de Montevideo, 3(55): 1-7.

Sobre Ototyphlonemertes do Brasil. Boletins da

Faculdade de Filosofia, Ciencias e Letras, Universidade de Sao Paulo, Zoologia, 15:203-233.

Nemerteans from Florida and Virgin Islands. Bulletin of Marine Science of the Gulf and Caribbean,

William D. Hummon The Marine and

Brackish-Water

Gastrotricha

in Perspective

ABSTRACT

The Gastrotricha are reviewed in terms of taxonomy, with generic and species criteria emphasized. The ecology of gastrotrichs, including the

sampling problem, also is discussed.

Gastrotrichs are recognizable even at low magnification by their morphology and movement. Adult

specimens seldom exceed 1 mm, although those of

a few species reach 2 to 4 mm. They range from

strap-shaped animals showing lateral and posterior

adhesive tubes to bottle-shaped animals possessing

a prominent caudal furca. Gastrotrichs typically

move by means of ventral cilia, and they rarely, if

ever, reverse direction. They are most likely to be

confused with Turbellaria or Gnathostomulida,

but they are easily distinguished at higher magnifications since they have a terminal mouth, an anterior pharynx, and an anus but lack both lateral

and dorsal locomotor cilia and a statocyst. Densities of individuals in a single species reach as high

as 2,307 in 6 cm3 (384.5/cm3) of substratum

(Hummon, unpublished) but vary considerably

and generally average less than 2/cm3 of substratum.

The phylum, as presently defined, generally is

divided into two orders, the Macrodasyida and the

Chaetonotida. Macrodasyida comprises about a

third of the 340 species described as of mid-1969 and

William D. Hummon, Department of Zoology, Ohio University, Athens, Ohio 45701.

is confined almost exclusively to marine or brackish-water habitats, though a few species are known

to have invaded waters with salinity as low as 1 ppt.

Chaetonotida includes the remaining species. Two

of the six chaetonotid families are restricted to marine and brackish-water habitats; members of two

additional families occur in similar habitats.

A major trend in gastrotrich systematics began

during the 1930s with a shift from fresh-water to

marine species. The latter forms continue to receive the most attention, their proportion currently

making up about 50 percent of the described species. Published species descriptions often lack information beyond that needed to distinguish proposed

species from those which preceded them. In many

cases important characters have been overlooked,

resulting in a need to redescribe or more fully

document generic and species descriptions. Typespecimens often have been poorly preserved, or,

more often, have been entirely lacking. Drawings

are rarely suitable, though some very good illustrations are on record. Ecological work is generally

absent or is based on cursory observations. And, far

too often, the more recent reports fail to make

morphological comparisons with data found in

either the original description or subsequent accounts.

Several recently described forms tend to blur established distinctions between genera and even

between families. As a result, criteria on which

these taxa are based will have to be revised. The

combined need for descriptions of new forms in

neglected localities and biotopes, along with redescriptions of previously described species based

on a broader spectrum of specific characters, im21
22

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

poses an important obligation on future taxonomic

research. Few persons who enter into the study of

gastrotrich biology can avoid the inclusion of some

serious taxonomy in their work.

With this in mind, it is important that taxonomic work be approached with the same care and

preparation as needed for an experimental problem. Species descriptions should be sufficiently detailed as to provide a basis against which future

species can be compared. Minimally, this means

more complete descriptions based, where possible,

on data derived from populations of animals. It

means noting and quantifying both genetic and

ontogenetic variability among specimens. It also

means working with relaxed and extended specimens, and making detailed and representative

drawings and supplementing them with photomicrographs and well-preserved permanent specimen

mounts.

Taxonomic work on gastrotrichs, often diffuse

and ill-defined, has been most valuable when based

on multiple characters—metric, meristic, and what

might be termed eidostic (Greek eidos: form,

figure, thing seen). It would be helpful if, in future work, a sequence of metric-meristic-eidostic

portraits could be constructed for each species. Ideally such a sequence of measured, counted, and visualized characters would be drawn from the population living in the type-locality of a species. In

practice it could come from any location at which

a species is sufficiently abundant as to provide adequate material with which to work. The procedure

is simply to relate all metric and meristic characters

to total body length of extended specimens for

each of several developmental length classes, ranging from juveniles to adults. Several such length

classes, including the smallest and largest, should

be illustrated in detail so as to allow visualization

of proportions and placement of parts (for a preliminary study of this type see Hummon, 1966).

Though time-consuming, this procedure allows

separation of genetic from ontogenetic variability

and provides a base line against which specimens

from other localities or biotopes can be compared.

It also enables one to more accurately assess geographical and ecological variability and to analyze

precisely cases of suspected character displacement

or interspecific hybridization.

Generic characters in gastrotrichs usually involve

one or more of the following: general body conformation; presence or absence of lobes, palps, or tentacles; presence or absence of entire groups of adhesive tubes; pattern of ventral cilia; type of

cuticular ornamentation, if present; type and location of pharyngeal pores, if present; and the components and positions of reproductive structures.

Specific characters often are related to the further

definition of generic characters, but nearly as often

the"y involve nongeneric characters which show consistent differences from population to population.

Some characters develop rather fully in the

embryo prior to its hatching, whereas other characters tend to emerge in the juvenile almost as rudiments and to undergo subsequent development in

the free-swimming animal throughout life. In

terms of energy conservation, it is an efficient

strategy for a minute animal, living within benthic

sediments, to reproduce by means of a few relatively large eggs which can be attached to the substratum and from which emerge "miniatures" of

the adult. Those features most necessary for survival of the newly hatched juvenile are favored by

selection and hence are well developed. All systems

except the reproductive are functional, though

they often add numbers or increments as the juvenile matures. It is this latter group of features

which provides data for the ontogenetic growth sequence, through characters such as tubule or bristle number, size, and locations; scale size; intestine

length; and body proportions.

Gastrotrichs have been little studied ecologically.

Of the work that has been done, most has centered

on marine and brackish-water forms living in

sandy intertidal or shallow subtidal substrata. Such

work should be continued, and should be closely

correlated with systematic studies to enhance our

knowledge of gastrotrich biogeography and of the

role played by various species of gastrotrichs in differing ecosystems. These studies should be broadened to include those forms living in other habitats, such as in mud bottoms, on algae or

barnacles, among eelgrass roots or ascidian colonies, in estuaries, salt ponds or tidal marshes, and

in benthic zones of the continental shelf or the

abyssal plain.

In making intensive ecological studies, it often is

productive to determine the extent of the habitat
NUMBER 76 23

to be studied, to select a two-dimensional transect

plane which lies perpendicular to the greatest

number or "most important" environmental gradients, and to determine the maximum number of

samples and subsamples which can be processed

per collection. The samples, with their clustered

subsamples, can then be allocated along the study

plane. Sample and subsample size, interval between

collections, duration of the study, and other features also must be considered. When possible, both

biotic and physicochemical factors should be assessed in determining local distribution patterns.

These should be related to laboratory determinations of species tolerances and preferences as well

as to field conditions. Consideration should be

given to obtaining data that will provide maximum information for use in studies of biogeography, species diversity, and population dynamics. Finally, all such ecological work should be done at

the species level of identification (see Hummon,

1969; Schmidt and Teuchert, 1969).

References to the Gastrotricha are widely scattered in the literature. Rather than include an extended list of recent papers, only four additional

references are cited here. Remane (1936) has provided the most comprehensive review of the entire

group. The most recent reviews are those of

Hyman (1951, 1959), in English; Voigt, (1958), in

German; Beauchamp (1965), in French. A complete bibliography of marine and brackish-water

gastrotrichs is available from the author on request.

Literature Cited

Beauchamp, P.

1965. Classe des Gastrotriches. In P. P. Grasse, editor,

TraitS de Zoologie, 4(3): 1381-1430.

Hummon, W. D.

1966. Morphology, Life History, and Significance of the

Marine Gastrotrich, Chaetonotus testiculophorus n,

sp. Transactions of the American Microscopical

Society, 85:450-457.

1969. Distributional Ecology of Marine Interstitial Gastrotricha from Woods Hole, Massachusetts, with

Taxonomic Comments on Previously Described Species. Unpublished Ph.D. dissertation, University of

Massachusetts.

Hyman, L. H.

1951. The Invertebrates: Acanthocephala, Aschelminthes,

and Entoprocta. Volume 3, pages 53-59, 151-170.

New York: McGraw-Hill.

1959. The Invertebrates: Smaller Coelomate Groups. Volume 5, pages 697-766. New York: McGraw-Hill.

Remane, A.

1936. Gastrotricha und Kinorhyncha. In H. G. Bronns,

editor, Klassen und Ordnungen des Tierreichs,

4(2): 1-242.

Schmidt, P., and G. Teuchert

1969. Quantitative Untersuchungen zur Okologie der

Gastrotrichen im Gezeiten-Sandstrand der Insel

Sylt. Marine Biology, 4:4-23.

Voigt, M.

1958. Gastrotricha. Tierwelt Mitteleuropas, 1 (4a): 1-74.

Robert P. Higgins A Historical Overview

of Kinorhynch Research

ABSTRACT

The historical development of the systematics of

the Kinorhyncha from the phylum to the species

level is reviewed. Procedures for collecting, extracting, study, and curating are discussed.

Considering the relative abundance of the Kinorhyncha as a constituent of the meiobenthos in

marine sediments, it is difficult to understand why

these invertebrates have received so little attention.

Indeed, the present status of kinorhynch research

seems to be as restrictive as it was more than a

hundred years ago when the first kinorhynch was

discovered.

While observing the meiofauna washed from

algae collected along the Normandy coast in 1841,

Dujardin discovered a remarkable invertebrate, less

than a half millimeter in length, which he called

"l'echinodere" some ten years later when he published his only paper on this subject (Dujardin,

1851). Dujardin's "l'echinodere," so named because of the animal's recurved spines on its eversible head (which Dujardin apparently considered

its neck), became Echinoderes dujardini when Claparede (1863) described the first species. As in the

case of Dujardin's short-lived interest in the new

taxon, this was Claparede's only contribution to kinorhynch research. Many investigators have repeated Claparede's disinterest in continuing research on the Kinorhyncha, and this has

contributed to the relative obscurity of one of the

most interesting and challenging phyla of meiobenthic invertebrates.

Robert P. Higgins, Office of Oceanography and Limnology,

Smithsonian Institution, Washington, D. C. 20560.

Dujardin (1851) did not assign his newly discovered taxon to a particular group of invertebrates

but suggested that "l'echinodere" was probably an

intermediate between the "Worms" and the Crustacea. Prior to the publication of the nominal species by Claparede (1863), kinorhynchs were "rediscovered" by Leuchart (1854), who mistakenly

assumed his specimen to be dipteran larval stage.

Nonetheless, from the initial description of the

first known kinorhynch until the present time, Dujardin's peculiar invertebrates have had a rather

simple nomenclatorial history.

Biitschli (1876) erected the family Echinoderidae for the single species of Echinoderes known at

that time. Soon afterwards, Greeff (1869a,b), Metschnikoff (1869), and Pagenstecher (1875) established several new species and the fact that these

were, indeed, adults and not unknown larval stages

of an already known invertebrate. The name Kinorhyncha was introduced by Reinhard (1881,

1887), who tried to avoid confusing this new taxon

with the many other taxa whose names began with

the prefix "echino-." Later authors were to use

widely the name Echinodera or Echinoderida—certainly an acceptable synonym—and, more recently,

the inevitable mistake "Echinorhyncha" has appeared as the phylum name (Russell-Hunter, 1968).

Although it is apparent that Reinhard recognized

that the Kinorhyncha constituted a major taxonomic category of invertebrates, he carefully

avoided designating a level for his new name.

Not long after the first few kinorhynch papers

appeared, Carl Zelinka became interested in this

challenging invertebrate. Zelinka had finished his

monograph on another meiofaunal taxon, the Gastrotricha (Zelinka, 1889), when he accepted the

challenge offered by Dujardin's discovery. Certainly no other scientist of that time was better

prepared to recognize the phylogenetic significance

25
26

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

of the Kinorhyncha. Thus, Zelinka began his studies of a new invertebrate taxon. Between 1894 and

1913 he published seven preliminary papers, including a description of a new species. By 1919 Zelinka's

monograph was ready for publication, but events

following World War I delayed publication until

his 78th year, 1928. Zelinka's Monographic der

Echinodera still remains the most singularly important work on Kinorhyncha.

By 1908, the Kinorhyncha (Echinodera) occupied

an ordinal level within Grobben's class Aschelminthes (phylum Protostomia). Twenty years later

Zelinka (1928) elevated the Echinodera to a class of

the phylum Aschelminthes. This classification remains satisfactory, although Pearse (1936) elected to

use Reinhard's name Kinorhyncha, the name preferred by most present-day invertebrate zoologists.

While Zelinka was working on his monograph

several other scientists published short papers on

various aspects of kinorhynch biology. These include the papers by Haeckel (1896), Hartog

(1896), and Schepotieff (1907a,b, 1908a,b). A single paper by Southern (1914) was the first to utilize Zelinka's (1896) classification in a species description.

Following the appearance of Zelinka's monograph, Remane (1928, 1929, 1936) published

several summaries of the former author's work,

adding some original material. Between 1922 and

1947 five papers, primarily taxonomic, appeared.

Abe's (1930) description of Echinodere masudai

from Japan was the first for a kinorhynch from the

Pacific. Blake (1930) described three species from

the coast of Maine (these recently were redescribed

by Higgins, 1964, 1965). In 1943 Lou reported a

new species, Echinoderes tchefouensis from Chefou

(Yellow Sea); however, this species, like the one

reported by Abe, remains a nomen dubium. In

keeping with a series of carefully rendered descriptions on other taxa, Lang (1935) published a short

paper on kinorhynchs from the Swedish coast. In

later years Lang (1949, 1953) made additional noteworthy contributions, both in additional new

species and phylogenetic discussion. The two other

papers of the post-World War II era were those of

Johnston (1938), who described a new species found

by the Australian Antarctic Expedition 1911-1914,

and Zaneveld (1938), who reported finding a kinorhynch on the coast of the Netherlands.

Although Zelinka and others had considerable

information on the postembryonic stages of many

kinorhynch taxa, the first report on the embryonic

("nonmotile") stages was made by Nyholm

(1947a,b). Since 1947, very little effort has been directed toward the embryonic or postembryonic life

history of the kinorhynchs. Most papers on this

taxon have remained descriptive. Zelinka's introduction of larval generic names (Higgins, 1968)

and the problem of recognition of the adult of certain taxa offer difficult challenges in kinorhynch research.

Despite several important new taxonomic additions to the phylum, the Kinorhyncha possess the

same basic taxonomic constructs as were established by Zelinka in 1896 (Figure 1). The first of

the two orders, Cyclorhagida, includes the majority

of lesser taxonomic components on all levels and

includes three suborders. The second order, Homalorhagida, has a much simpler taxonomic make-up.

Generally speaking, the cyclorhagids are the

smallest and most difficult kinorhynchs to study,

despite the fact that they are the most commonly

encountered taxon. The suborder Cyclorhagae is

the most common of all suborders. Within it, the

monotypic family Echinoderidae, composed of 26

described species of Echinoderes, has only 19 species that can be properly recognized. Echinoderes,

the most commonly encountered kinorhynch genus,

often is mistaken for a copepod in preserved material.

Most closely related to the Echinoderidae is the

family Centroderidae. Its nominal genus, Centroderes Zelinka, has two species. A second genus,

Campyloderes Zelinka, has three species; and the

third and final genus, Condyloderes Higgins, has

two species. Species of the genus Centroderes

are known only from the Black Sea, Mediterranean

Sea, Bermuda waters, and Buzzards Bay, Massachusetts (Higgins, unpublished). Campyloderes,

until it appeared in samples of meiofauna collected in New Caledonia, was considered to be bipolar temperate to boreal. Condyloderes Higgins,

recently described (Higgins, 1969a,b) from material the author obtained in India, is distinctly neotenic and includes Mclntyre's (1962) Centroderes

miiltispinosus, found along the coast of Scotland.

Conchorhagae, a second suborder of Cyclorhagida, now contains two genera. Semnoderes Zelinka,
NUMBER 76 27

KINORHYNCHA

CYCLORHAGIDA

CYCLORHAQAE

ECHINODERIDAE CENTRODERIDAE

HOMALORHAGIDA

i

CONCHORHAGAE CRYPTORHAGAE HOMALORHAGAE

SEMNODERIDAE CATERHDAE NEOCENTROPHYIDAE PYCNOPHYIOAE

Echinoderes Campyloderes Condyhderes Cenlroderes Semnoderes Sphenoderes Catena Neocentrophyes Pycnophyes Tnchydamus

P\

A

rm

FIGURE 1.—Schematic representation of the phylum Kinorhyncha showing ventral (top row) and

lateral (bottom row) aspects of adult representatives of the known genera. (Illustrations are

diagrammatic and are not drawn to the same scale.)

the original conchorhagid, consists of three species.

Sphenoderes Higgins is a monotypic genus which

the author recently described from India (Higgins,

1969a). It would appear, from what little evidence

is available, that the Conchorhagae more commonly are inhabitants of muddy sands as opposed

to the finer marine sediment. No conclusions can

be reached regarding their distribution or ecology.

The third and final cyclorhagid suborder, Cryptorhagae, is known from a single genus, Catena

Gerlach, discovered in the interstitial zone of a marine beach near Macae, Brazil (Gerlach, 1956).

Gerlach's species has been reported from the Angolan coast by Delamare Deboutteville (1957) and

from the east coast of India by Rao and Ganapati

(1966); and a second species, Cateria gerlachi Higgins, occurs in the latter locality as well (Higgins,

1968).

Until recently (Higgins, 1969a), the second and

only other order, Homalorhagida, consisted of a

single suborder, Homalohagae, a single family, Pycnophyidae, and two genera. The nominal genus,

Pycnophyes Zelinka, consists of 20 described species,

16 of which are recognizable by their published de-
28

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

scriptions. Pycnophyes species are among the largest known kinorhynchs and may approach 1 mm

in length.

The genus Trachydemus Zelinka consists of

seven easily recognized species, most of which,

from evidence the author has accumulated, appear

to prefer very fine sediments.

A second family of homalorhagids has been described (Higgins, 1969b) from material collected

by the author in the Indian Ocean in 1964. Neocentrophyidae is a neotenic taxon made up of a

single genus, Neocentrophyes Higgins, and two

species. Phylogenetically speaking, this is an important taxon, for many of its characteristics suggest a position intermediate between the two established orders of Kinorhyncha.

The most singularly difficult problem in kinorhynch research has been the collection of sufficient

material. The Kinorhyncha of marine beaches require no special technique different than that used

in other studies. The great majority of kinorhynch

taxa associate with subtidal sediments, particularly

soft sediments—mud or mud mixed with sand with

a relatively high organic content. Kinorhynchs are

eurybathic, intertidal to 5,000 m or more; are euryhaline, occurring at salinities as low as 7 ppt and as

high as 60 ppt; and are eurythermic, from — 2° to

40°C. They usually are found within the upper

few centimeters or even the upper few millimeters

of marine sediments.

Qualitative collecting is best accomplished by a

dredge designed to skim off the upper layer of sediment. Techniques which collect large quantities of

sediment deeper than the surface layer are less

likely to yield sufficient numbers of organisms for

study.

Quantitative collecting is best accomplished by

coring techniques. The Smith-Mclntyre grab seems

to be an effective sampler and can be subsampled

with reasonable accuracy. The most important

problem to avoid is a shock wave which dissipates

the kinorhynch's habitat—the light, flocculent interface layer of soft sediments.

Removal of kinorhynchs from sediment is facilitated by introducing fine bubbles of air into a sediment sample diluted with seawater. The bubbles

cause the kinorhynchs to rise to surface film where

they are trapped. After the sediment is allowed to

settle slightly, the kinorhynchs and several other

meiofaunal taxa can be blotted off the surface by

gently allowing a piece of mimeograph paper to

come in momentary contact with the surface film.

By washing the adhering organisms into a small

dish one can immediately determine the success of

the procedure. In most cases, if kinorhynchs are

present in the sample they will appear after the

first few times the blotting and washing procedure

is followed.

Meiofauna obtained in the above-described manner can be concentrated, by repeated bubbling,

blotting, and washing, into a conical-shaped, finemesh (62 /A) net. The accumulated material may

then be washed into a bish or directly into a suitable fixative, such as 4 to 7 percent formalin or 70

percent ethanol or isopropynol.

According to the author's best estimates, which

are based on several tests, this technique extracts

over 80 percent of the kinorhynchs in a large sample. It does not, however, substitute for the accuracy of meticulous sorting of the sediment, sieved

through a 62-fi mesh net. The author has found

that a coring tube with a cross-sectional area of

about 100 cm3 will provide reasonably accurate

quantification. In a core 10 cm deep, 99 percent of

the kinorhynchs occur within the upper 2 cm.

Rose Bengal, liberally applied to the sample, helps

in the sorting procedure, but one must be cautious

since not all specimens will be penetrated by the

stain. Irwin loops are most helpful in handling individual specimens.

In order to properly identify a specimen, it

should be slowly transferred from alcohol or formalin to glycerin. Although glycerin mounts are

satisfactory for some taxa, not all of the intricate

cuticular morphology can be seen. It is necessary,

therefore, to mount each animal in Hoyer's medium which contains enough Lugol's iodine to give

it an amber color. Hoyer's mounted specimens

clear very well for observation under oil immersion phase optics, and especially for Nomarski interference contrast optics.

The most satisfactory mounts are double coverglass preparations attached to Cobb aluminumslide frames, an important tool of the nematologist.

Such a mount with the animal positioned in a

dorsal (or ventral) perspective will allow the observer to reverse the slide and view it from the

opposite perspective.
NUMBER 76 29

Since Dujardin's discovery of the first kinorhynch almost 130 years ago, some 21 authors have

been responsible for the description of the 71 species now established in the literature. Seventeen of

the 21 taxonomic authors, approximately 75 percent, have published only a single paper on this

subject, while two others have published two papers each. The remaining 37 species descriptions

are shared by Zelinka and the author.

The preponderance of single-attempt publications, aside from having a potentially demoralizing

effect on aspirant students of the taxon, often has

created considerable technical problems in taxonomy. The problems do not reflect, necessarily, the

qualifications of the author as a systematist; rather,

they substantiate the well-known fact that extensive experience is necessary before any taxonomist

can be effective in his area of specialization. Consequently, many species descriptions—most of which

reflect a short-lived active interest in the kinorhynchs—are inaccurate. Few type-specimens have

been established or properly curated. This necessitates re-collection from the type-locality if, indeed, that locality was noted in the original publication. In several instances the known type-localities

have succumbed to the effects of pollution or other

destructive forces associated with our modern world

and its population expansion.

Few attempts have been made to collect sufficient quantities of kinorhynchs for proper study.

Most kinorhynchs are described from only a few

specimens—sometimes not by choice, but far too

often more specimens could have been collected.

Furthermore, few attempts have been made to

study carefully the ontogeny of taxonomic characters. Which ones are stable? Which ones are reliable? Which ones are subject to environmental influences?

Similarly, there has been little interest in

kinorhynch ecology. The kinorhynchs have been

included with the more commonly discussed taxa

of a marine sediment community by Wieser

(1960) and by Mclntyre (1962, 1964, 1969). Few

other investigators have been concerned with the

role of Kinorhyncha as a component of meiobenthos. No study has been conducted on the autecology of any species, nor has any study been made

on the kinorhynch population dynamics of any

meiobenthic community.

Summary

Most kinorhynch research has been in basic systematics, although Zelinka's monograph provides a

considerable foundation for other disciplines. The

kinorhynchs offer an interesting challenge among

the taxa which remain "lesser known." Unless

more researchers can be recruited to the ranks of

those willing to accept such challenges, Kinorhyncha literature may continue to be as cryptic as the

environment in which these animals dwell.

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Abe, Y.

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Blake, C. H.

1930. Three New Species of Worms Belonging to the

Order Echinodera. Biological Survey of the Mount

Desert Region, 4:3-10.

Butschli, O.

1876. Untersuchungen iiber freilebende Nematoden und

die Cattung Chaetonotus. Zeitschrift fur wissenschaftliche Zoologie, 26:363-413.

Claparede, E.

1863. Beobachtungen iiber Anatomie und Entwicklungsgeschichte wirbelloser Tiere und der Kiiste der

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Delamare Deboutteville, C.

1957. Sur la presence des Echinoderes de la famille des

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Dujardin, F.

1851. Sur un petit animal marin, l'Echinodere, formant

un type intermediare entre les Crustaces et les Vers.

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15:158-160.

Gerlach, S. A.

1956. Uber einen aberranten Vertreter der Kinorhynchen

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Greeff, R.

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SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Grobben, K.

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Haeckel, E.

1896. Systematische Phylogenie. Entwurf eines natiirlichen Systems der Organismen auf Grund ihrer

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Hartog, M.

1896. Rotifera, Gastrotricha and Kinorhyncha. Cambridge

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Higgins, R. P.

1964. Redescription of the Kinorhynch Echinoderes

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1965. The Homalorhagid Kinorhyncha of Northeastern

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1967. The Kinorhyncha of New Caledonia. In Expedition Frangaise sur les Recifs coralliens de la Nouvelle-Cale'donie, volume 2, pages 75-90.

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1969b. Indian Ocean Kinorhyncha. 2. Neocentrophyidae,

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Biological Society of Washington, 82:113-128.

Johnston, T. H.

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Lang, K.

1935. Undersokningar over Oresund. Untersuchungen aus

dem Oresund XXI. Einige Kleintiere aus dem

Oresund. Lunds Universitets Arsskrift, 31(10):l-8.

1949. Echinoderida. In J. H. Odhner, editor, Further

Zoological Results of the Swedish Antarctic Expedition, 1901-1903, volume 4, part 2, pages 1-22.

1953. Reports of the Lund University Chile Expedition

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Leuckart, R.

1854. Bericht iiber die Leistungen in der Naturgeschichte

der niederen Thiere wahrend der Jahre 1848-1853.

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Lou, T. H.

1934. Sur la presence dun nouveau Kinorhynque a

Tchefou: Echinoderes tchefouensis sp. nov. Contributions du Laboraloire de Zoologie, Academic

Nationale de Piping, l(4):l-9.

Mclntyre, A. D.

1962. The Class Kinorhyncha (Echinoderida) in British

Waters. Journal of the Marine Biological Association of the United Kingdom, 42:503-509.

1964. Meiobenthos of Sub-Littoral Muds. Journal of the

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1969. Ecology of Marine Meiobenthos. Biological Reviews, 44:245-290.

Metschnikoff, E.

1869. Bermerkungen iiber Echinoderes. Melanges biologiques 7. Bulletin de I'Academie des Sciences de

Saint Petersbourg, 4:190-194.

Nyholm, K. G.

1947a. Contributions to the Knowledge of the Postembryonic Development in Echinoderida Cyclorhagae.

Zoologiska bidrag fran Uppsala, 25:423-428.

1947b. Campyloderes—An "Antarctic" Genus of Echinoderida off the West Coast of Sweden. Arkiv fur

Zoologi, 39(13): 1-6.

1947c. Studies in the Echinoderida. Arkiv fur Zoologi,

39(14): 1-36.

Pagenstecher, H. A.

1875. Echinoderes Sieboldii. Zeitschrift fur wissenschaftliche Zoologie, supplement, 25(S): 117-123.

Pearse, A. S.

1936. Zoological Names. A List of Phyla, Classes, and

Orders. 24 pages. Durham, North Carolina: American Association for the Advancement of Science.

Rao, G. C, and P. N. Ganapati

1966. Occurrence of an Aberrant Kinorhynch Cateria styx

Gerlach, in Waltair Beach Sands. Current Science,

35(8):212-213.

Reinhard, W.

1881. Ober Echinoderes und Desmoscolex der Umgegend

von Odessa. Zoologischer Anzeiger, 4(97):588-591.

1887. Kinorhyncha (Echinoderes), ihr anatomischer Bau

und ihre Stellung im System. Zeitschrift fur wissenschaftliche Zoologie, 45:401-467.

Remane, A.

1928. Kinorhyncha. In G.Grimpe and E. Wagler, editors,

Die Tierwelt der Nord- und Ostsee, 7(d2):57-84.

1929. Kinorhyncha. In W. Kiikenthal and T. Krumbach,

editors, Handbuch der Zoologie, volume 2, part 1,

pages 187-248.

1936. Gastrotricha and Kinorhyncha. In G. G. Bronns,

editor, Klassen und Ordnungen des Tierreichs, volume 4, part 2, pages 1-385.

Russell Hunter, W. D.

1968. Biology of Lower Invertebrates. 181 pages. New

York: Macmillan.

Schepotieff, A.

1907a. Zur Systematic der Nematoideen. Zoologischer Anzeiger, 31(5/6): 132-161.

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1908a. Zur Kenntnis der Echinoderiden. Zoologischer Anzeiger, 32(20/21):585-589.

1908b. Das Exkretionssytem der Echinorhynchen. Zoologisches Jahrbiicher, Abteilung fur Anatomie und

Ontogenie der Tiere, 26:291-304.

Southern, R.

1914. Nemathelmia, Kinorhyncha and Chaetognatha.

Clare Island Survey. Proceedings of the Royal Irish

Academy, 31(54)69-72.

Wieser, W.

1960. Benthic Studies in Buzzards Bay. II. The Meiofauna.

Limnology and Oceanography, 5:121-137.

Zaneveld, J. S.

1938. Marine Gastrotricha and Kinorhyncha from Scheveningen. Zoologische Mededeelingen, Leiden,

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Zelinka, C.

1889. Die Gastrotrichen.Eine monographische Darstellung

ihrer Anatomie, Biologie und Systematik. Zeitschrift fur wissenschaftliche Zoologie, 49:209-384.

1896. Demonstration von Tafeln der Echinoderes—Monographie. Verhandlungen der Deutschen Zoologischen Gesellschaft, 6:197-199.

1928. Monographic der Echinodera. 396 pages. Leipzig:

Wilhelm Engelmann.

w. Duane Hope The Current Status

of the Systematics

of Marine Nematodes

ABSTRACT

The systematics of marine nematodes is discussed

in terms of the need for proper study, including the

necessity for adequate specimens, the designation

of type specimens, and the description, measurement, illustration and diagnosis of species. The

need for more detailed studies of species using new

techniques is emphasized.

Perhaps there is no taxon of metazoans so commonly obtained in sediment samples as marine nematodes. Nearly every sample of sediment will

yield appreciable quantities of nematodes regardless of whether from abyssal depths, intertidal

zones, estuaries, or tropical or polar seas. Their

great abundance, adaptation to a wide diversity of

habitats, and diverse morphology suggest that nematodes play a complex and significant role in the

ecology of the marine environment. Yet, few major

taxa have received the attention of so few taxonomists, and few taxa have been so consistently

ignored by ecologists.

The reasons for this disparity are manifold and

complex. For example, until recently there has not

been a great deal of interest in benthic ecology;

most undergraduate biology courses fail to properly introduce the student to free-living nematodes;

study of marine nematodes has not been spurred

by economic pressures; the animals are cryptic because of their small size and sediment-inhabitating

nature; and time-consuming and laborious techW. Duane Hope, Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution,

Washington, D. C. 20560.

niques must be employed to extract nematodes

from sediment and prepare them for study. But

probably the most important single reason is the

difficult nature of marine nematode systematics,

the difficulties having resulted from less than adequate practices in taxonomy.

In order to appreciate the magnitude of these

problems, a consideration of the plight of the

novice taxonomist or ecologist who for the first

time attempts the identification of a collection of

marine nematodes is in order. If such a person has

had an adequate introduction to the anatomy of

marine nematodes, he probably will be able to

identify the specimens to the subfamily level by

using the chapter on the systematics of the infraclass Adenophorea by de Coninck (1965). By using

the extensive collection of keys in Wieser's (1953,

1954, 1956) study of the marine nematodes of the

coast of Chile or the keys to the species of the suborder Oncholaimina by Kreis (1943), one may be

able to assign specimens to the proper genus.

But even if the novice taxonomist does make a

correct generic identification, the identification at

the specific level will be much more difficult—if at

all possible—since so many of the keys are now

obsolete. It is true that there has been some effort

to keep some of these keys up to date and prepare

new ones where needed, but for the almost 400

valid nominal genera, only 68 keys to species have

been published in the last ten years. And, of course,

many of these are now out of date because of additional new species descriptions.

Consequently, to find the correct specific name

for a specimen at hand, assuming it has been described, a search must be made through various abstracting periodicals such as Biological Abstracts,

Helminthological Abstracts, and Zoological Record
34

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

in hopes of obtaining references to all work on

species of the genus in question. This, of course, is

a very time-consuming task and leads to problems

of obtaining literature which may be scattered

through 50 or more journals. But assuming this is

accomplished and descriptions of all species are at

hand, there is a good chance the descriptions will

be incomplete or in other ways inadequate, and

the illustrations may be so diagramatic that at best

the identification can be narrowed only to two or

three possible species. The final step then becomes

an effort to borrow type material of the two or

three species still in question, and in this final effort there is once more little chance of success, as a

considerable number of marine nematologists have

not saved specimens upon which descriptions of

new taxa were based—a practice that has occurred

as recently as the late 1950s and may well persist

today. Or, when specimens have been set aside at

the conclusion of a study, they may not have been

clearly marked as types or they may have been

mounted in formalin, which inevitably evaporates,

leaving the specimens in poor condition. Therefore, without the benefit of large collections of correctly identified specimens to work from, an up-todate index to the species of marine nematodes—of

which there are few in the world today—and an

extensive collection of literature, it is no wonder

that the novice taxonomist or ecologist will turn

his interests to less-exasperating taxa.

Such, then, is the plight of the novice who engages in the systematics of marine nematodes, and

it depicts the status of marine nematode systematics today. Because these difficulties partially stem

from less-than-adequate practices in descriptive taxonomy, it seems that a review of some of the preferred practices is appropriate and justified. These

practices are considered below in approximately

the same sequence as employed when describing a

new taxon.

ADEQUATE MATERIAL—The first step is to judge

whether specimens at hand are of sufficient quality

and quantity to serve as the basis for a new species

description. As a general rule, specimens fixed in

alcohol are shrunken and distorted to the point

where they are of doubtful value for such descriptions. Measurements of specimens fixed in such a

manner are not likely to be representative of the

species. Usually males must be available, for in

most species they possess diagnostic characters not

shared by females or juveniles. Diagnostic descriptions should be based on females in only those few

genera in which species are known only from females. Never should new species of free-living marine nematodes be described and named from

collections of juvenile specimens alone. Juvenile

specimens lack secondary sexual characters, which

are imperative for proper identification. Juveniles

of a new species may be described and assigned to

a genus for any of several reasons, but they should

not be given a specific name. In fact, editors of

journals should be discouraged from accepting for

publication manuscripts that contain new species

named and described on the basis of juveniles

alone.

The number of specimens to be employed in a

type series is rather arbitrary. New species descriptions based on single specimens, regardless of sex,

are to be discouraged, however; 10 to 20 specimens

of each sex would be more appropriate.

TYPE-SPECIMENS.—At some point in the preparation of a new species description, a holotype specimen must be selected. For the same reason stated

above, the holotype should, in most cases, be a

male. It should be the best specimen available;

that is, it should display to best advantage the

greatest number of diagnostic characters.

In most instances the holotype should be

mounted individually in anhydrous glycerin and

the coverslips sealed with some durable ringing

compound such as Murrayite or Zut. Preferably,

the specimen should be mounted on Cobb aluminum slides so that the specimens may be observed

from either side and so the slide will not break so

easily if dropped. Supports should be used to prevent the specimens from being crushed or distorted

by the weight of the coverslip. This is especially

important, for if such support is not used it will

be impossible at later dates to accurately measure

the diameter of the body and other structures. The

slide should be clearly labeled with the name of the

species, sex of the specimen, name of author, date

of publication, collection data, identity of the

mounting medium, registration or catalog number

assigned by the institution in which it is to be deposited for safe keeping, and the word "holotype."

A similar slide, with appropriate labeling, also
NUMBER 76 35

should be prepared for the allotype and for each

paratype.

If structures such as the spicula, gubernacula, or

stomatal armature cannot be properly studied in situ

from whole-mount preparations, then dissections

and serial sections should be made from paratype

material to obtain the best possible understanding

of structural detail; also body parts should be specially oriented in glycerin jelly or other special

preparations. These should be preserved with the

rest of the type series. It is also advisable, if sufficient material is available, to preserve additional

paratype material in small bottles containing anhydrous glycerin. These specimens may be used later

for special preparations should the need arise.

DESCRIPTIONS.—Accurate and complete descriptions should be made of all structures known to

have, or suspected of having, taxonomic value.

While unnecessarily lengthy descriptions are to be

avoided, it is even more important to avoid incomplete descriptions, often prepared under the pretenses of reducing publication costs. Such descriptions frequenly prove to be inadequate and

necessitate subsequent redescriptions at greater cost

and loss of time.

The characters to be included in descriptions are

best determined through experience, but when

description of a particular taxon is attempted

for the first time it is well to compile first a list

of taxonomic characters that have been used in

previous descriptions of other species of the same

genus. Some of the characters obtained for such

a list might be of doubtful value and may be

discarded, but one should also be alert to useful

characters that may have been overlooked by earlier workers. While descriptions of new species

should basically be of the holotype, structural variation found among the paratypes also should be

given. Incidentally, it is convenient for the purpose

of comparing descriptions if the same structures

are consistently described in the same sequence for

each species.

MEASUREMENTS.—If dimensions of structures are

of taxonomic importance they should be determined and expressed in absolute units of measure

(microns or millimeters). It is not sufficiently

accurate to express dimensions only as fractions

or multiples of the dimensions of other structures; i.e., "tail length equal to 3 anal-body

diameters." Further, measurements should be given

separately for the holotype and allotype, and at

least the range of values, if no other statistic, for

the paratypes. If new or unusual structures are

being measured, the precise points between which

the measurements are made should be clearly understood. A scale should be included with each illustration and photograph so that measurements

given in the text may be checked against the illustration.

ILLUSTRATIONS.—Anatomical structure can almost

always be represented graphically with greater accuracy and more clarity than by verbal descriptions. Consequently, descriptions of all important

characters should be accompanied by accurate illustrations or photographs. Drawings should not

be made free-hand, but rather with the aid of a

camera lucida or other device that will provide at

least comparable accuracy.

Illustrations should not be so diagrammatic that

important taxonomic detail is lost, and structures

should be studied until they are well understood

before attempting to illustrate them, even if this

necessitates special specimen preparations. Photographs are preferred to drawings, but they have

limited application because of problems with

depth of focus.

DIAGNOSIS.—A diagnosis should follow the description of each new species. The character or

characters by which the new species differs from

those to which it is judged to be most closely related must be stated precisely. Preparation of a key

to the species of a genus may be useful in determining the closest affinities of a new species if they

are not otherwise evident.

No doubt there are additional ways in which the

general quality of the alpha taxonomy of marine

nematodes can be improved, but the preceding recommendations cover some of the major problems.

In addition to the problems that exist at the

level of alpha taxonomy, there is a continuing

need for easier inroads into the taxonomy and systematics of marine nematodes. Here, reference is

made to the need for keys, checklists, bibliographies, revisions, and monographs. Contributions of

this nature are the responsibility of those working

in institutions where all or most of the marine nematode literature, large collections of specimens,

and species indices are available. There are few
36

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

such institutions in the world today, and those

that exist should encourage work in these directions.

A final trouble area to be mentioned is the

higher classification of marine nematodes. For the

most part, the classification used today is the same

as that proposed by Filipjev (1916, 1918, 1921,

1927, 1934), with minor modifications by several

ensuing nematologists. But this classification is

based largely on light microscope studies of wholemount specimens. As a result, the evolution and

systematic importance of amphids, the male copulatory complex, stomatal armature, esophagus, and

other features are not adequately known. Further,

so little is known about other anatomical features

whose detailed structure is beyond the resolution

of the light microscope—such as the cuticle, muscle,

and nervous system—that they may be regarded as

untapped sources of taxonomic data. The electron

microscope now makes these sources available.

Also, the stereoscan electron microscope will provide valuable data regarding surface features of the

cuticle, structure of the amphids, lips, cephalic

setae, stoma, and ventromedian copulatory supplements of the male. Indeed, it is predictable that

during the next several years there will be dramatic changes in the means by which nematode

anatomy may be recorded for taxonomic studies,

and with unprecedented accuracy.

Summary

An attempt has been made to provide an impression of the current status of marine nematode taxonomy and to identify some of the underlying

problems. The approximately 6,000 nominal species known today probably represents much less

than half of the species that exist. If taxonomists

of marine nematodes are to move ahead in the task

that lies before them, and not become mired in

problems created by taxonomists themselves, they

must set and attain high standards, keeping in

mind that the new species and other taxa described today must be distinguished not only from

those previously described but from the many that

are yet to be described.

Literature Cited

de Conick, L.

1965. Syste"matique des Wmatodes. In P. P. Grasse", editor, Traite de Zoologie, 4:586-726.

Filipjev, I. N.

1916. Lcs Nematodes libres contenus dans les collections

du Miirft Zoologique de 1'Acade'mie Impe'riale des

Sciences de Petrograd. Extrait de Vannuarie du

Muste zoologique de 1'Acade'mie Impe'riale des

Sciences, 21:59-116.

1918. Free-Living Marine Nematodes of the Sevastopol

Area. Trudy Osoboi Zoologischeskoi Laboratorii 1

Sevastopol 'Skoi Biologischeshoi Stantsii Rossiiskoi

Akademii Nauk, 2(4): 1-350.

1921. Free-Living Marine Nematodes of the Sevastopol

Area. Trudy Osoboi Zoologischeskoi Laboratorii I

Sevastopol 'Skoi Biologischeskoi Stantsii Rossiiskoi

Akademii Nauk, 2(4):353-614.

1927. Les N£matodes libres des mers septentrionales appartenant a la Famille des Enoplidae. Archiv fur

Naturgeschichte, 91:1-216.

1934. The Classification of the Free-Living Nematodes

and Their Relation to the Parasitic Nematodes.

Smithsonian Miscellaneous Collections, 89(6): 1-63.

Kreis, H. A.

1934. Oncholaiminae Filipjev 1916 eine Monographische

Studie. Capita Zoologica, 4(5): 1-271.

Wieser, W.

1953. Reports of the Lund University Chile Expedition

1948-1949. 10. Free-Living Marine Nematodes. I.

Enoploidea. Lunds Universitets Arsskrift, 49(6):

1-155.

1954. Reports of the Lund University Chile Expedition

1948-1949. 10. Free-Living Marine Nematodes.

II. Chromadoroidea. Lunds Universitets Arsskrift,

50(16):l-148.

1956. Reports of the Lund University Chile Expedition

1948-1949. 10. Free-Living Marine Nematodes. III.

Axonolaimoidea and Monhysteroidea. Lunds Universitets Arsskrift, 52(13):1-115.
John s. Gray The Meiobenthic Bryozoa

ABSTRACT

The morphology, ecology, and techniques for study

of Monobryozoon ambulans and Monobryozoon

limicola are discussed. The lunulitiform Bryozoa

are considered briefly.

The Bryozoa constitute a relatively insignificant

part of the meiobenthos. Like the Tunicata, however, the modifications of sedentary organisms to a

relatively unstable habitat are interesting. Two

groups of meiobenthic Bryozoa are known, the

truly interstitial genus Monobryozoon Remane and

the epibenthis lunulitiform species. Knowledge of

both groups is scarce. Monobryozoon is known

from Helgoland, Germany (Remane, 1936, 1938),

the Gullmar Fjord, Sweden (Franzen, I960),

Robin Hood's Bay, England (Gray, in press) and

Roscoff, France (Monniot, unpublished). The lunulitiform species are not well known but they appear to have a widespread distribution (Cook,

1963, 1965a-c, 1966; Lagaaij, 1963a,b; and Marcus

and Marcus, 1962).

As the author is familiar only with Monobryozoon, the remarks are concerned mainly with this

genus. Only two species are known, Monobryozoon

ambulans Remane and M. limicola Franzen. Neither species is abundant. Monobryozoon ambulans

is described from seven specimens (Remane, 1936,

1938). More recently, Gray (in press) reported the

finding of 15 specimens in England. Monobryozoon

limicola has been found at Gullmar Fjord, Sweden, in larger numbers (240 specimens) by Franzen (1960); at Roscoff, France, by F. Monniot (unpublished) , and at Robin Hood's Bay, England, by

Gray (unpublished). No quantitative sampling

methods have been used.

John S. Gray, Wellcome Marine Laboratory, Robin Hood's

Bay, England.

Monobryozoon ambulans, when alive, is yellowbrown, the same color as the substratum it inhabits. Further, the "locomotion" exhibited is slow

and cumbersome and does not aid location of specimens in a dish, as do the movements of many interstitial species. The animals are robust and are

not likely to be easily damaged.

Monobryozoon ambulans lives in coarse shellgravel whereas M. limicola lives in soft mud. The

morphological differences between the species reflect the habitat differences. Figure 1 shows diagrammatically the differences between the two species.

Monobryozoon ambulans is small (up to 2 mm

tall) and has up to 15 short, thick stolons, each

less than half the width of the animal. Monobryozoon limicola is larger (up to 2.5 mm tall) but

thinner, and has two or three long, thin stolons,

each greater than the width of the animal. The

collar in M. ambulans is short, whereas in M. limocola it is much longer.

Since Monobryozoon ambulans occurs sublittorally, samples of coarse shell-gravel can be taken

with a grab or dredge The sediment samples are

then placed in large polyethylene bags which are

kept in running seawater. The animals survive well

within the substratum, and oxygen diffuses

through the bag walls. Monobryozoon limicola inhabits the rich detrital layer covering mud at

depths down to 55 m. Samples are best taken with

an epibenthic sledge.

For extraction of both species, the traditional

method of anaesthetization, with MgCl2 (73.2

g/liter isotonic to 34 ppt seawater) for 10 minutes,

followed by filtration of the supernatant liquid

through a fine-mesh plankton net after vigorous

agitation, is successful. The net is inverted in a

Petri dish and the animals and substratum are

washed off with normal seawater. The dish must

be examined with extreme care under low-power

microscope. Once extracted, both species survive

well in dishes containing substratum and seawater

37
M . AMBULANS M.LIMICOLA

FIGURE 1.—Diagram of the two known species of Monobryozoon, showing morphological

differences.

FIGURE 2.—Photomicrographs of living Monobryozoon ambulans. a, Individual with contracted

lophophore; note egg and asexually produced bud produced from a stolon; b, mature, asexually

produced individual still attached to parent.
NUMBER 76 39

kept at 8° to 10° C. It is difficult, however, to induce the animals to extend the lophophore, even

under anaesthetics. For anatomical studies, relaxed

animals are essential. Six percent formalin or 1.5

percent propylene phenoxetol have been used as

preservatives.

As there are only two known species, keys are

not necessary. Specimens of the Robin Hood's Bay

population of Monobryozaon ambulans have been

examined by the author. Figure 2 shows examples

of M. ambulans with a ripe egg (Figure 2a) and

with a mature asexually produced bud (Figure

26). Specimens of M. limicola are deposited in the

museum of the zoology department, University of

Uppsala, Sweden.

The genus Monobryozoon is suspected of having a

much wider sublittoral distribution pattern than is

known at present. The extreme difficulty of locating nonmotile specimens of a color similar to the

substratum in a dish is probably the reason for our

lack of knowledge of this group.

The lunulitiform Bryozoa inhabit a variety of

substrata from shell-gravel to mud. They show

modifications of typically sedentary species in having discoidal or conical shapes, and they may be

free-living or be attached to the substratum by

rootlets. Typically, the lunulitiform Bryozoa have

small numbers of zoecia in each colony, and the

colonies themselves are small. Specimens have been

recorded from depths of 10 to 805 m. The works

of Cook (1963, 1964a,b, 1965a-c, 1966), Lagaaij

(1963a,b), and Marcus and Marcus (1962) should

be consulted for detailed information on the lunulitiform Bryozoa.

Literature Cited

Cook, P. L.

1963. Observations on Live Lunulitiform Zoaria of Polyzoa. Cahiers de Biologic Marine, 4:407-413.

1964a. Polyzoa from West Africa. 1. Notes on the Steganoporellidae, Thalamoporellidae and Onychocellidae

(Anasca, Coilostega). Annales de I'Institut Oceanographique, (Calypso, VI), 41:43-78.

1964b. Polyzoa from West Africa. Notes on the Genera

Hipporina Neviana, Hippoporella Canu, Cleidochasma Harmer and Hippoporidra Canu and Bassler (Cheilostomata, Ascophora). Bulletin of the

British Museum (Natural History), Zoology, 12:1-35.

1965a. Notes on the Cupuladriidae (Polyzoa, Anasca), Bulletin of the British Museum (Natural History),

Zoology, 13:151-187.

1965b. Polyzoa from West Africa. The Cupuladriidae

(Cheilostomata, Anasca). Bulletin of the British

Museum (Natural History), Zoology, 13:189-227.

1965c. Notes on Some Polyzoa with Conical Zoaria. Cahiers de Biologie Marine, 6:435-454.

1966. Some "Sand Fauna" Polyzoa (Bryozoa) from Eastern

Africa and the Northern Indian Ocean. Cahiers

de Biologie Marine, 7:207-223.

Franzen, A.

1960. Monobryoioan limicola n. sp., a Ctenostomatous

Bryozoan from the Detritus Layer on Soft Sediments. Zoologiska bidrag (ran Uppsala, 33:135-148.

Gray, J. S.

In press. Occurrence of the Aberrant Bryozoan Monobryozoan ambulans Remane off the Yorkshire Coast.

Journal of Natural History.

Lagaaij, R.

1963a. Culpuladria canariensis (Busk)—Portrait of a Bryozoan. Paleontology, 6:172-217.

1963b. New Additions to the Bryozoan Fauna of the Gulf

of Mexico. Publications of the Institute of Marine

Science, 9:162-236.

Marcus, Eveline, and Ernesto Marcus

1962. On Some Lunulitiform Bryozoa. Boletim de Faculdade de Filosofia, Ciencias e Letras de Universidade

de Sao Paulo, Zoologia, 24:281-324.

Remane, A.

1936. Monobryozoon ambulans n.g. n.sp., ein eigenartiges

Bryozoon des Meeresandes. Zoologischer Anzeiger,

113:161-167.

1938. Erganzende Mitteilungen iiber Monobryozoon ambulans Remane. Kieler Meeresforschungen, 2:356-

358.

Bertil Swedmark A Review of Gastropoda,

Brachiopoda,

and Echinodermata

in Marine Meiobenthos

ABSTRACT

The morphological and reproductive adaptations

of the meiobenthic Gastropoda, Brachiopoda, and

Echinodermata are discussed. Keys for the Pseudovermidae and the marine species of Acochlidiacea (Gastropoda, Opisthobranchia) are given.

Since small body size is unusual in gastropods,

brachiopods, and echinoderms, these systematic

units are minor constituents of the meiofauna.

This does not mean, however, that they are unimportant for the meiobenthologist. Of general biological interest are the adaptations that these taxa

have made to the ecological demands of the environment. They have a reduced or modified anatomy which may cause problems for the phylogenist

and systematist who study relationships between

these aberrant forms and the more-typical members

of their taxa.

Up to the present time, most of the work concerning these animals has been devoted to morphology and general biology, and little is known about

population densities and the particular role that

these animals may play in food chains and the general dynamics of the meiobenthos. Brachiopods

and echinoderms are represented in the meiobenthos by very few permanent members; the gastropods are relatively more important.

Bertil Swedmark, Kristinebergs Zoological Station, Fiskebackskil, Sweden.

Gastropoda

Best known among the prosobranchs is the genus

Caecum Fleming (Figure la), with two European

species which are characteristic members of the interstitial fauna of the so-called "Amphioxus sand."

The slightly curved shell of this 1-mm-long animal

is an effective adaptation to living conditions in

the interstitial environment. The anatomy, which

presents features of reduction, is well known from

the studies of Gotze (1938). Caecum belongs to

the important group of interstitial animals that

feed on diatoms.

The opisthobranchs are represented in the

meiobenthos by the following groups: the order

Acochlidiacea with eleven species, the order Philinoglossacea with three species, and the Aeolid family Pseudovermidae with eight species.

The Acochlidiacea (Figure Ib) were first studied by Kowalevsky (1901) in sublittoral sand and

shell debris in the eastern Mediterranean. The systematics has been studied by Thiele (1931),

Odhner (1937, 1952), Marcus (1953), Challis

(1968), and Swedmark (1968). Odhner derives the

Acochlidiacea from the primitive family Diaphanidae, but there is no generally accepted opinion on

the natural systematic position of these shell-less

opisthobranchs. The small body size (0.8 to 3

mm) and the consequently small number of cells

available for anatomical differentiation resulted in

regressions in structure in the evolution of the

Acochlidiacea. Regression is observed in several

organ systems: there are no ctenidia, there is only

one tubular digestive gland, the radula is simplified, the sexual apparatus is much less differentiated than is usual in opisthobranchs. The regres41
42

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

sive characters often are combined with morphological specialization. One such character is

the differentiation of spicules in certain species. In

Hedylopsis loricata Swedmark, a species living in

sublittoral shell dunes, the large epidermal spicules

cover the entire surface of the visceral sac, giving it

a shell-like rigidity. This secondary "shell" undoubtedly is of importance for the mechanical protection of this animal, which lives in a particularly

dynamic biotope where the sediment particules are

continuously displaced by the action of currents.

The Acochlidiacea also present interesting adaptations in their reproductive biology. Such

adaptations are necessary for the maintenance of

populations, because the animals produce very few

gametes. In the Acochlidiacea, fertilization is cutaneous without copulation. The animals produce

spermatophores which become attached to the epidermis of the animal to be fertilized, and the spermatozoa penetrate the mucuous base of the spermatophore and the epidermis. This type of

fertilization is not known to occur in other molluscs, but it has been studied in certain Turbellaria and Archiannelida.

It is the regressive character, combined with specializations in the anatomy of the Acochlidiacea,

which makes this order systematically isolated.

More detailed knowledge of the anatomy is needed

in order to learn the evolutionary pathways which

have led to the organization of the Acochlidiacea.

We can expect that more species will be discovered

in the coming years and may help us in the analysis

of the systematic position of these opisthobranchs.

The key for the identification of genera and species, given below, differs considerably from the one

given by Odhner (1952).

Philinoglossa helgolandica Hertling (Figure \c)

and Pluscula cuica Marcus form another group of

Key to the Marine Acochlidiacea

A. Family Microhedylidae: labial tentacles of same shape or slightly larger than rhinophores;

the latter may be reduced or absent; posterior region of digestive gland (liver) bent forward or looped; sexes separate; no vas deferens.

1. Radula: n{2.\2).

a. Digestive gland without loop Microhedyle Hertling

(1) With rhinophores.

(a), n = 34 to 35 M. glandulijera (Kowalevsky)

(b). n = 39 to 44 M. lactea Hertling

(2) Without rhinophores M. milaschewitchii (Kowalevsky)

b. Digestive gland with loop Parhedyle Thiele; P. tyrtowii (Kowalevsky)

2. Radula: n(l.l.l).

a. With rhinophores Vnela Marcus

(1) No spicules; no eyes V. remanei Marcus

(2) With spicules; with eyes 17. odhneri (Delamare Deboutteville)

b. Without rhinophores Ganitus Marcus; G. evelinae Marcus

3. Radula: n(O.l.O) Paraganitus Challis

Digestive gland looped, male intraepidermal duct present P. ellynae Challis

B. Family Hedylopsidae: labial tentacles usually larger than rhinophores; digestive gland

forms a straight tube; external male duct (ciliated groove from genital pore to right

rhinophore); hermaphroditic; one genus, Hedylopsis Thiele.

1. Radula: n(l.l.l).

a. With eyes.

From 3 to 4 mm long; white, opaque H. spiculifera (Kowalevsky)

(H. suecica Odhner = local form)

b. Without eyes.

From 0.8 to 1 mm long; dense epidermal spicules make the wall of visceral

sac a "secondary shell" H. loricata Swedmark

2. Radula: n(2.1). Without eyes H.brambelli Swedmark

NOTE: In the radula formula, n is the number of radular series. The three numbers signify

elements of radular series: (2.1.2) = one median and one lateral plate at each side of the central tooth; (1.1.1) = one lateral plate at each side of the central tooth; (0.1.0) = central tooth,

plates absent.
NUMBER 76 43

opisthobranchs belonging to the interstitial fauna

of sand (Herding, 1932; Marcus, 1953). The

group, named Philinoglossacea, was erected as a distinct order by Hoffmann (1933). Both Odhner

(1952) and Bottger (1955) derive Philinoglossacea

from the primitive Notodiaphanidae, but here,

too, regression in structure and a modified organization considerably hamper a systematic evaluation.

The eight known species belonging to the family

Pseudovermidae are aeolid opisthobranchs with a

peculiar, elongated shape of body. All belong to

the interstitial fauna of sand. The head of Pseudovermis Periaslavzewa (F gure Id) is acorn-like

in shape and is without appendages.

All species have liver papillae, though these are

more or less reduced in some species. The papillae

sometimes contain nematocysts, indicating that

Pseudovermis may prey on interstitial cnidarians

such as Psammohydra Schulz and Halammohydra

Remane, which usually live in the same habitat.

The biology of reproduction is of the same type

as in Acochlidiacea and Philinoglossacea. In Pseudovermis, which is hermaphroditic, fertilization is

believed to occur after copulation. The veliger larvae develop in adhesive cocoons attached to sand

grains. The hatched veliger larvae swim slowly and

lack photic reaction. This is evidence for a sessile

development, counteracting dispersion of the larvae and keeping them within the territory of the

FIGURE 1.—Gastropoda, Brachiopoda, Echinodermata. a, Caecum glabrum (Montagu); b, Hedylopsis brambelli Swedmark; c, Philinoglossa helgolandica Hertling; d, Pseudovermis papillifer

(Kowalevsky); e, Gwynia capsula Jeffreys; /, Labidoplax buskii (M'Intosh).
44

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

population. This can be considered a necessary adaptation in these animals, which produce few gametes (Swedmark, 1968a).

The family Pseudovermidae consists of one

genus, Pseudovermis. The species are from 1 to 6

mm long. The head is acorn-shaped and without

appendices. The pedal epidermis is ciliated and

there is no distinct foot. The papillae occur in

lateral rows. The pharynx has one pair of jaws.

The radula formula is n (1.1.1), where N = 26-36.

The median plate has one median denticle and

from four to seven lateral denticles. The lateral

plates have one or two points. The salivary gland

is paired and there is one digestive gland. The

genital pore is located on the right side in front

of the anus. (Description from Salvini Plawen and

Sterrer, 1968).

A key for the identification of seven species of

the Pseudovermidae has been published by Salvini

Plawen and Sterrer (1968). That key, with the addition of an eighth species, P. setensis Fize, is given

below.

Key to Species of Pseudovermis, Family Pseudovermidae

1. Without eyes 2

With eyes 3

2. Long, finger-like papillae, median radular plate with nine denticles, lateral plates with one

point P. salamandrops Marcus

Papillae very small, median radial plates with 11-15 denticles, lateral plates with two

points P. axi Marcus and Marcus

3. Papillae very small, retractile, visible on contracted animal only; anterior margin of jaws

dentated 4

Long, nonretractile, finger-like papillae, distinct even on extended animals; anterior margins

of jaws smooth P. papillifer Kowalevsky

4. More than 10 pairs of papillae (13 pairs) P. kowalevskyi Salvini Plawen and Sterrer

Fewer than 10 pairs of papillae 5

5. Not more than five papillae in total, lateral radular plates with two points

P. schulxi Marcus and Marcus

Seven or eight papillae at each side 6

Five papillae at each side 7

6. Papillae paired (symmetrically), lateral radular plates with one point

P. paradoxus Periaslavzewa

Papillae in asymmetrical arrangement, lateral radular plates with two points

P. boadem Salvini Plawen and Sterrer

7. Papillae in asymmetrical arrangement, lateral radular plates with one point....P. setensis Fize

BRACHIOPODA

As far as we know, there is only one brachiopod

that belongs to the meiofauna. Gwynia capsula Jeffreys (Figure \e), with a shell diameter of only 1

mm, was described as early as 1859 by Jeffreys.

Until recently, it was considered a doubtful species

and perhaps the juvenile form of some larger species. The author has found mature specimens (at

Bangor, North Wales) and has been able to study

part of their development; therefore, it can be concluded that Gwynia capsula is a distinct species

(Swedmark, 1967).

Gwynia Jeffreys is an articulate brachiopod and

is the smallest known genus within the group. As

in many other small forms in various systematic

groups, the anatomy of Gwynia has peculiar features that perhaps are the result of a small number

of cells. The lophophore is trocholophous, the simplest type in any brachiopod.

Originally, Gwynia was found under stones and

pebbles in the littoral zone. Later it became

known as a permanent member of the interstitial

fauna of sand and shell debris (Menai Strait, Anglesey, North Wales). Along with some Foraminifera and coelenterates, it is one of the rare sedentary animals of this fauna.

For a brachiopod, the reproductive biology of

Gwynia is peculiar. The eggs, 2 to 6 in number,

develop in a kind of maternal pouch up to a stage

when three segments are well differentiated, before

the larvae are liberated.
NUMBER 76 45

ECHINODERMATA

In sublittoral sand and mud, juvenile ophiuroids

are seasonally frequent, but other echinoderms are

rare in the meiofauna. The most important echinoderms which are permanent members of the

meiobenthos are apodous holothurians. Three of

these synaptids are common in European waters:

Rhabdomolgus ruber Keferstein, Leptosynapta minuta Becher, and Labidoplax buskii M'Intosh (see

Becher, 1906; Nyholm, 1952). A fourth form,

Psammothuria ganapatii, recently has been described from the Waltair coast in India (Rao,

1968). All are vermiform, and 2 to 8 mm long. Labidoplax buskii (Figure If) is a characteristic member of the fauna of sublittoral mud, the other three

species belong to the interstitial fauna of sand.

The tentacles, digitate in Labidoplax Oerstergren and Psammothuria Rao and simple in the

other two species, are of importance not only for

the ingestion of food but also for locomotion.

All species are provided with statocysts, each of

which contain one or more statoliths. The positive geotaxis, manifested by the synaptids of the

meiofauna, is believed to be mediated by the statocysts, but these organs also serve for orientation in

the interstitial environment. It is well known from

the works of Remane (1952) that the interstitial

fauna contains a notable fraction of species with

static organs.

The animals are hermaphroditic, and the development has been studied by Becher (1906) for

Leptosynapta minuta and by Nyholm (1952) for

Labidoplax buskii. They produce a small number

of eggs. Coelomic incubation occurs in Leptosynapta minuta and from 2 to 4 embryos at a time

develop in the coelomic cavity of the mother.

Literature Cited

Becher, S.

1906. t)ber Synapta minuta n. sp., eine brutpflegende

Synaptide der Nordsee, und iiber die contractilen

Rosetten der Holothurien. Zoologischer Anzeiger,

30(ll/12):505-509.

Bottger, C. R.

1955. Die Systematik der euthyneuren Schnecken. Zoologischer Anzeiger, Supplementband 18:253-280.

Challis, D. A.

1968. A New Genus and Species of the Order Acochlidiacea (Mollusca: Opisthobranchia) from Melanesia.

Transactions of the Royal Society of New Zealand,

Zoology, 10(20):191-197.

Gotze, E.

1938. Bau und Leben von Caecum glabrum (Montagu).

Zoologische Jahrbucher, Abteilung fur Systematik,

Okologie und Geographic der Tiere, 71:55-122.

Herding, H.

1932. Philinoglossa helgolandica, n.g., n.sp.( ein neuer

Opisthobranchier aus der Nordsee bei Helgoland.

Wissenschaftliche Meeresuntersuchungen, 19(l):l-9.

Hoffman, H.

1933. Opisthobranchia. In G. C. Bronns, editor, Klassen

und Ordnungen des Tierreichs, 3(2): 1-1247.

Jeffreys, J. G.

1859. Additional Gleanings in British Conchology. Annals

and Magazine of Natural History, series 3,4:189-201.

Kowalevsky, A.

1901. Les Hexlylides, £tude anatomique. Me'moires de

I'Acadimie Imperiale des Sciences de St. Pitersbourg, 12(6): 1-32.

Marcus, Ernesto

1953. Three Brazilian Sand-Opistobranchia. Boletim de

Faculdade de Filosofia, Ciencias e Letras de Universidade de Sao Paulo, Zoologica, 18:165-203.

Nyholm, K.-G.

1952. The Development and Larval Form of Labidoplax

buskii. Zoologiska Bidrag fran Uppsala, 29:239-254.

Odhner, N. Hj.

1937. Hedylopsis suecica n. sp. und die Nacktschneckengruppe Acochlidiacea (Hedylacea). Zoologischer

Anzeiger, 120:51-64.

1952. Petits Opisthobranches peu connus de la cote

m^diterrane^nne de France. Vie et Milieu, 3:136-

147.

Rao, G. C.

1968. On Psammothuria ganapatii n. gen. n. sp., an

Interstitial Holothurian from the Beach Sands of

Waltair Coast and Its Autoecology. Proceedings

of the Indian Academy of Sciences, 67(5):2O1-2O6.

Remane, A.

1952. Die Besiedelung des Sandbodens im Meere und die

Bedeutung der Lebensformtypen fur die Okologie.

Zoologischer Anzeiger, Supplementband 16:327-339.

Salvini Plawen, L., and W. Sterrer

1968. Zur Kenntnis der mesopsammalen Gattung Pseudovermis (Gastropoda, Nudibranchia) . Helgoldnder

wissenschaftliche Meeresuntersuchungen, 18:69-77.

Swedrnark, B.

1967. Gwynia capsula (Jeffreys), an Articulate Brachiopod

with Brood Protection. Nature, 213:1151-1152.

1968a. The Biology of Interstitial Mollusca. Symposia of

the Zoological Society of London, 22:135-149.

1968b. Deux especes nouvelles d'Acochlidiacees (Mollusques Opisthobranches) de la faune interstitielle

marine. Cahiers de Biologie Marine, 9:175-186.

Thiele, J.

1931. Handbuch der systematischen Weichtierkunde,

I—III. Jena: Gustav Fischer.

Claude jouin Status of the Knowledge

of the Systematics

and Ecology

of Archiannelida

ABSTRACT

The systematics and ecology of the marine Archiannelida are reviewed. Keys to the species of Saccocirrus and to the genera of the family Nerillidae are

given.

The Archiannelida form a heterogeneous group of

annelids and should be considered an order of Polychaeta (Hermans, 1969). This order is composed

of five families that have few affinities with each

other or with other families within the Polychaeta.

From the aspect of morphology (see Figure 1), archiannelids are aberrant, some being without parapodia and setae (Polygordiidae, Protodrilidae, Dinophilidae) and others very reduced in size

(Dinophilidae, Nerillidae). Formerly, archiannelids were regarded as primitive annelids, but, according to modern views, they are either regressive,

secondarily altered annelids (Remane, 1932) or

annelids primarily adapted for interstitial life

(Hermans, 1969).

Since several of the Archiannelida can be collected in great numbers, they form suitable and interesting objects for experimental studies of ecology. These aberrant annelids have been exciting

study material for morphologists and taxonomists

—especially during recent years, since many new

archiannelids have been discovered.

Nearly all archiannelids live in marine sediments, and most of them are small. In the DinoClaude Jouin, Laboratoire de Zoologie, Faculte des Sciences,

7 Quai Saint Bernard, Paris Ve, France.

philidae and Nerillidae, most species are less than

1 mm long. The species in the other three families

are, as a rule, elongated. Species of Polygordius

may become 80 mm long and 1 mm broad; consequently, they should be assigned to the macrobenthos.

Generally speaking, the larger archiannelids

(Polygordius) are endopsammic and the smaller

ones are mesopsammic except for Paranerilla,

which is known from subtidal mud. Nerilla and

Dinophilus seem to be less dependent than the

others on the nature of the sediment and they live

in various biotopes.

Most Protodrilidae are exclusively marine, but

some species occur in brackish water and two even

occur in fresh water (Pierantoni, 1908). Troglochaetus, which is closely related to the marine Nerillidum and Thalassochaetus, is a hypogeal form,

occurring in continental fresh water.

Family POLYGORDIIDAE

Genus Polygordius Schneider

Twelve species of Polygordius are known. The specific characteristics are mainly the size of the body,

the shape of the pygidium and its adhesive papillae, the nuchal organs, circulatory apparatus, and

sperm. Polygordius lives in infralittoral sediments

("Amphioxus sand") or, less often, in the intertidal zone. Its geographical distribution includes the

Mediterranean Sea, Adriatic Sea, Black Sea, North

Sea, English Channel, Atlantic Ocean, and IndoPacific waters.

A key to the species has been published by Marcus (1948) but it is incomplete; other important

47
48 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

works are those of Aiyar and Alikunhi (1944) and

Marcus (1955).

Family PROTODRILIDAE

The family Protodrilidae is composed of two genera, Protodrilus Hatschek with twenty species and

Protodriloides Jouin, with two species. Half of the

species of Protodrilus are described in older works

and are included in Pierantoni's (1908) monograph.

Jagersten (1952) has published an excellent

work on the anatomy of four species from Gullmar

Fjord, Sweden, in which he shows that some characteristics of the males are of great taxonomic

value. When determining species of Protodrilus, it

is always important to have sexually mature individuals available, and it is quite necessary to have

such specimens at hand if new species are to be described. The following anatomic characteristics are

important from the aspect of taxonomy: position

of the salivary glands and the front limit of the

fertile region of the body, shape and size of the lateral organs of the males, and position and number

of the spermducts.

FIGURE 1.—Diagrams of typical Archiannelida. a, Polygordius; b, Saccocirrus; c, Protodrilus;

d, Protodriloides; e, Mesonerilla; f, Nerillidium; g, Diurodrilus; h, Mesonerilla intermedia; i,

Paranerilla limicola; j , Nerillidum simplex; k, Diurodrilus; I, Trilobodrilus.
NUMBER 76 49

Pierantoni's (1908) monograph includes the

general morphological characteristics but since that

work contains some errors and is incomplete in

some respects there has been a need for a revision

of Protrodrilus. In a revision by the present author

(Jouin, in preparation) eleven species will be

studied; among these, three will appear as new.

Figure 2 shows the most important characters of

the males in four species revised by the author and

in four species studied by Jagersten (1952).

The genus Protodriloides includes only two

known species (Jouin, 1966): P. chaetifer (Remane) , which has small setae, and P. symbioticus

(Giard), which is without setae but which has, instead, segmental adhesive organs.

Protodriloides has yellowish green inclusions in

the epidermis. The tentacles, which point forward,

are without the tentacle channel characteristic of

Protodrilus and Saccocirrus. Both salivary glands

and lateral organs are lacking; the sperm are without flagella (Jouin, 1966). The females have large,

yolk-rich eggs that are deposited in a cocoon in

which fertilization takes place. Development is direct (Swedmark, 1954; Jouin, 1962).

The geographic distribution of Protodrilus includes the Mediterranean Sea; Black Sea; North

Sea; English Channel; the Skagerrak; Atlantic

Ocean including Europe, Brazil, and east coast of

the United States; Indo-Pacific waters, including

India, South Africa (collected by C. Berrisford and

3 4 5 6 7 8 9 10 11 12 13 14 15 16

FIGURE 2.—Diagram of the male characters for eight species of Protodrilus (lateral view of

segments 3 to 17) showing salivary glands in the anterior segments, fertile part of the body

(shading) with spermaducts and lateral organs (open grooves).
50 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

determined by the author), and New Caledonia;

and Pacific coast of North America. The species

are cosmopolitan on the European coasts, and the

same species occur in the Mediterranean Sea and

Gullmar Fjord.

Protodriloides chaetifer is known from the European coasts, the Pacific coast of North America

(Puget Sound, Wieser, 1957), and the east coast of

South Africa (collected by C. Berrisford and determined by the author). This distribution, which

implies cosmopolitanism, is interesting because the

species is without a pelagic larval stage.

The Protodrilidae occur in both the intertidal

zone and in infralittoral sediment. In the Mediterranean, Protodriloides symbioticus (A. Fize, personal communication) and Protodrilus adhearens

Jagersten are found in coastal subsoil water ("kustengrundwasser"). In the neighborhood of Banyuls, Protodrilus adhaerens is found together with

P. leuckarti Hatschek in brackish water ("etang

de Salses").

Renaud-Debyser (1963) studied the vertical and

horizontal distribution of Protodrilus in Arcachon

over a period of several months. In these studies a

cprer was used to obtain cores of sediment 0.8 to 1

m long from various levels in the tidal area. Figure

3 shows the migrations observed. Boaden (1962)

studied the significance of grain sizes for the distribution of meiofauna within the tidal area by inserting tubes containing sifted sand, representing a

specific fraction into the beach sand. He was able

to show that Protodrilus adhaerens prefers grain

sizes between 500 and 1400 p., while the preferred

range for P. chaetifer was between 162 and 211 fi.

FIGURE 3.—Seasonal evolution of a population of Protodrilus at Arcachon, intertidal of Eyrac

beach, HM, high-water mark; B-E, sampling sites; broken line, level of interstitial water. (After

Renaud-Debyser, 1963.)
NUMBER 76 51

Gray (1965, 1966a-d, 1967a,b) experimentally

investigated the preference of several species of

Protodrilidae for such ecological factors as light,

grain size, oxygen content, salinity, and current velocity. A hundred or so individuals were exposed

to gradients of light, temperature etc., and the resulting distribution of the experimental animals

was analyzed. In this way, Gray was able to determine the optimal demands made by a certain species on these ecological factors.

Jagersten (1940a,b) was the first to draw attention to the fact that larvae of Protodrilus rubropharyngeus Jagersten are dependent for their

metamorphosis on grains of sand but he did not

describe the nature of the metamorphosis-enhancing factor. Gray (1966c, I967a,b) investigated the

attractiveness of sand for three species of Protodrilidae and found that it is influenced by the thin

film produced on the sand grains by certain favorable bacteria. Chemically or mechanically, the attraction to the grains of sand was reduced, but it

returned successively as new films of bacteria were

formed after inoculation (Figure 4).

The species of Saccocirrus Bobretzky are large

forms, usually about 20 mm long. The largest species is 80 mm long and the smallest is 4 mm long.

Saccocirrus has cephalic tentacles and adhesive pyU

z

>

U 0 6

gidial lobes; therefore, it is somewhat similar to

Protodrilus, but it has retractile parapodia and

setae and the ventral band of cilia is absent from

all species except one, Saccocirrus eroticus Gray.

The setae are important from the aspect of taxonomy, as are the general morphological characters

of adult animals. Saccocirrus is dioecious and the

gonads are in pairs in some animals and single in

others.

The males have organs of copulation on each

fertile segment, and these organs also are in pairs

or single, according to the species. The females of

all species, with one exception (Saccocirrus pussicus Marcus), have spermathecae.

The occurrence of a pharyngeal bulb in certain

species is another important taxonomic feature.

The existence of a pharyngeal muscular bulb was

first noted by Goodrich (1901) for specimens of

Saccocirrus papillocercus Bobretzky from Naples

but, later, other authors denied the existence of

such a bulb in this species. Jagersten (1947), who

did not investigate the species himself, agrees with

Goodrich on the existence of a muscular pharyngeal apparatus.

During a search for archiannelids at Naples, the

author found two species of Saccocirrus in the

same sediment: S. papillocercus without pharyn2 3 4

TIME IN DAYS

FIGURE 4.—Increase of the attractiveness index of autoclaved gravel to

Protodrilus hypoleucus on inoculating with a culture of natural gravel

bacteria: •, number of bacteria; A,

attractiveness index; •, sterile controls.

(After Gray, 1967a.)
52

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

geal muscular apparatus and S. krusadensis Alikunhi with a pharyngeal muscular pad. The specimens of S. krusadensis were immature and their

provisory identification is based only on the setae.

It is possible, therefore, that Goodrich mixed these

two species, working with S. krusadensis for the

pharyngeal apparatus and with S. papillocercus for

the genital organs.

The following key to the species of Saccocirrus

includes eleven known species. A twelfth species,

Saccocirrus maculatus Tenerelli, is, in the opinion

of the author, invalid, having been described from

one sterile specimen having only 26 segments. Pigment granules in the epidermis very often are

found in juvenile specimens in archiannelids.

There is much evidence that Saccocirrus is carnivorous. Marcus (1948) collected Saccocirrus with

fish as bait, and she found remains of fish tissue in

the digestive organs. In other cases, remains of copepods have been found in the intestine of Saccocirrus; Rao and Ganapati (1968) state that S.

minor Aiyar and Alikunhi is carnivorous and that

the intestine often contains microfauna.

Species of Saccocirrus have been found in the

Mediterranean Sea, Black Sea, English Channel,

Atlantic (Europe and Brazil), Indo-Pacific (India),

and North Pacific (Japan, United States). The biotope, most often, is coarse-grained sediment in the

intertidal or infralittoral zones. Saccocirrus parvus

Gerlach lives in coastal waters. Two species, S.

papillocercus and S. major, occur on the shores of

the Mediterranean in the upper littoral zone.

Key to the Species of Saccocirrus

1. With pharyngeal muscular pad 2

Without pharyngeal muscular pad 7

2. Pygidium bifurcate, with two cirri and without adhesive papillae

S. cirratus Aiyar and Alikunhi

Pygidium bifurcate but without cirri and with numerous adhesive glands forming papillae,

or else with only a few adhesive glands S

3. Each parapodium with three types of setae: long capillary, medium with broad tip, and

short 4

Each parapodium with only two types of setae (no long capillary setae) S. pussicus Marcus

4. Long setae slender and smooth at tip; only a few adhesive glands on pygidium

S. archboldi Kirsteuer

Long setae furcate at tip; adhesive papillae on pygidium 5

5. Bifid tip of the long setae symmetrical 6

Bifid tip of the long setae asymmetrical S. krusadensis Alikunhi

6. Tip of the medium setae unequally forked; band of epidermal ventral cilia on setigerous

segments 1 to 7 S. eroticus Gray

Tip of the medium setae with a deep median notch; no band of epidermal ventral cilia

S. gabriellae Marcus

7. Pygidium without bifurcation, with two adhesive pads S. minor Aiyar and Alikunhi

Pygidium bifurcate g

8. No pygidial adhesive papillae; very few adhesive glands S. parvus Gerlach

Pygidial adhesive papillae well developed 9

9. Long setae with an asymetrical, notched tip; medium setae with a broad chanelled tip

S. papillocercus Bobretzky

Long setae with a smooth tip 10

10. Medium setae with triangular section and three teeth at tip S. major Pierantoni

Medium setae with a smooth tip $. orientalis Alikunhi

Family DINOPHILIDAE

The family Dinophilidae includes three genera:

Dinophilus Schmidt, Diurodrilus Remane, and

Trilobodrilus Remane. Each is very small, with a

ventral band of cilia and without parapodia, setae,

and cephalic tentacles.

The genus Dinophilus consists of two groups

having a total of eight species. One group comprises species that are without sexual dimorphism
NUMBER 76 53

and usually are orange colored (designated as Erythrodinophilidae by Shearer); the other group is

made up of species with pronounced sexual dimorphism and usually without pigmentation (designated as Leucodinophilidae by Shearer). The females are known best in the latter group, as the

males are very small (Jones and Ferguson, 1957).

Jagersten (1944), in a study of a monomorphic Dinophilus, revealed that it spends half its life in an

encysted state.

Most species live in the intertidal zone, usually

among algae or on the surface of the sediment,

more seldom interstitially. Dinophilus gyrociliatus

Schmidt, however, has been found at a depth of 20

cm in sediment in the lower part of the intertidal

zone (Rao and Ganapati, 1968). This species has a

wide geographical distribution (Mediterranean

Sea, Europen coasts of the Atlantic, and Indian

Ocean).

Diurodilus, which includes five species, is among

the smallest (250 to 500 p. long) of the archiannelids. The taxonomy is based on the shape of the

pygidium. Diurodrilus moves very rapidly because

of powerful ventral ciliation. The organization of

the cilia grouping in cirri and membranella on the

ventral side of the body is reminiscent of the arrangement in hypotrichous Ciliata.

Most species live in the intertidal zone or the littoral zone, but some are found also in submerged

sand and several species inhabit coastal subsoil

water. As far as known, Diurodrilus minimus Remane has the widest geographical distribution:

North Sea, Baltic Sea, Gullmar Fjord, English

Channel, Atlantic Ocean (Europe), Mediterranean

B

PY

FIGURE 5.—A, Trilobodrilus axi: a, habitus; b, ventral view of head. B, Diurodrilus ankeli: oe,

oesophagal gland; h, epidermal gland; pr, prostomium; m, metastomium (pharyngeal segment);

ri_5, trunk segments; py, pygidium. (After Westheide, 1967, and Ax, 1967.)
54

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Sea, and Indian Ocean. The species is pronouncedly euryhaline. It has been found in abundance from 12 to 34 cm in the sediment (Frenchel,

Jansson, and von Thun, 1967). Diurodrilus benazzi

Gerlach is known from the Mediterranean Sea and

the Indian Ocean (Rao and Ganapati, 1968). The

genus Diurodrilus is now known from the North

American coast of the Pacific, where the largest

(500 ft long) known species, D. ankeli (Figure

5B) , was found by Ax (1967).

The genus Trilobodrilus (Figure 5A) comprises

three species, two of which, T. heideri Remane

and T. axi Westheide, occur on the coasts of Europe. A third species, T. nipponicus Uchida and

Okuda, which is very similar to Trilobodrilus heideri, has been found in Japan, the Bay of Bengal,

and on the North American coast of the Pacific

Ocean (Wieser, 1957).

Boaden (1963) has shown in laboratory experiments and field studies that Trilobodrilus heideri

avoids light, and that it can tolerate low salinity

better than high salinity. The species has tendencies towards gregariousness, with signs of a characteristic rhythm. In the course of 24 hours four

periods of dispersion and four periods of concentration occur. This rhythm probably is related to

that of the tides.

Family NERILLIDAE

The Nerillidae is a homogeneous family. Presently

known are 10 genera and 25 species, which are distinguished taxonomically by such features as number of metameres, type of setae (capillary or composed) , number of cephalic tentacles, and presence

of a pharyngeal bulb with or without stilettes.

The larger species have nine metameres and the

body lengths vary from 0.6 mm to 1.2 mm. Among

these larger species are those of the genera Nerilla

Schmidt, Mesonerilla Remane, and Meganerilla

Boaden. Five genera have eight metameres and

body lengths between 350 p and 600 p: Nerillidium Remane, Nerillidopsis Jouin, Troglochaetus

Delachaux, Thalassochaetus Ax, and a new genus

(see footnote in key to the Nerillidae) . Two genera, Psammoriedlia Kirsteuer and Paranerilla

Jouin and Swedmark, have only seven metameres.

Key to Genera of the Family Nerillidae

1. Body with nine segments, including the pharyngeal segment (SI) 2

Body with less than nine segments 4

2. Simple capillary setae 3

Compound setae Mesonerila Remane

3. Three antennae, two palps Nerilla Schmidt

One antennae or none, two large palps Meganerilla Boaden

4. Eight segments, including the pharyngeal segment (SI) 5

Seven segments, including the pharyngeal segment 9

5. All segments of the body bearing the same type of setae 6

All segments of the body not bearing the same type of setae; simple and capillary setae (SI,

S5 to S8), compound setae (S2 to S4) Nerillidopsis Jouin

6. Compound setae 7

Simple, capillary setae 8

7. No parapodial cirri; no antennae, two palps Thalassochaetus Ax

Parapodial cirri well developed, often double; three antennae, two palps New genus i

8. Pharyngeal segment setigerous; two antennae or none, two palps Nerillidium Remane

Pharyngeal segment achaetous; no antennae, two palps; fresh water and hypogeous form

Troglochaetus Delachaux

9. Compound setae; no antennae, no palps, no parapodial cirri; external ciliation well developed; limicolous form Paranerilla Jouin and Swedmark

Capillary setae; no antennae, two palps, parapodial cirri present except on last segment;

mesopsammic form Psammoriedlia Kirsteuer

i With Dr. B. Swedmark's agreement, Mesonerilla minuta Swedmark will be placed in a new

genus and species by the author (Jouin, in preparation).
NUMBER 76 55

FIGURE 6.—Photomicrograph of spermatophores of

Nerilla antennata.

The Nerillidae have colonized biotopes of

widely different types. Most species are mesopsammic and marine, and are found mainly in infralittoral sediments, although some species are

found in the intertidal or in the splash zone of seashores. The mesopsammic species are browsers living on diatoms and bacteria on grains of sand.

The genus Troglochaetus is hypogeal, and is found

in continental subterranean waters in Europe. The

only species is closely related to Nerillidium, and

it may be assumed that Troglochaetus is of marine

origin.

Paranerilla Jouin and Swedmark is known in

subtidal mud; it was described from the Gullmar

Fjord and was found later near Bergen, Norway,

on the Atlantic coast (Sterrer, 1968) and in the

Atlantic Ocean (Renaud-Mornant, personal communication) .

The genera Nerilla, Nerillidium, and Mesonerilla are cosmopolitan. Nerilla antennata Schmidt

and Nerillidium mediterraneum Remane, described

from European waters, have been found in the Indian Ocean (Rao and Ganapati, 1968). Nerilla is

very euryoecious and depends little on the substratum. It breeds easily in aquaria. The period of

egg-laying is long, and fertilization is by spermatophores (Jouin, 1968); see Figure 6. Development

is direct and rapid.

Literature Cited

Aiyar, R. G., and K. H. Alikunhi

1944. On Some Archiannelids of the Madras Coast. Proceedings of the National Institute of Sciences of

India, 10(1): 113-140.

Ax, P.

1967. Diurodhilus ankeli nov. spec. (Archiannelida) von

der Nordamerikanischen Pazifikkiiste. ZeitschriU

fur Morphologic und Okologie der Tiere, 60:5-16.

Boaden, P. J. S.

1962. Colonization of Graded Sand by an Interstitial

Fauna. Cahiers de Biologic Marine, 3:245-248.

1963. Behaviour and Distribution of the Archiannelid

Trilobodrilus heideri. Journal of the Marine Biological Association of the United Kingdom, 43:239-

250.

Fenchel, T.; B. O. Jansson; and W. von Thun

1967. Vertical and Horizontal Distribution of the Metazoan Microfauna and of some Physical Factors in

a Sandy Beach in the Northern Part of the

0resund. Ophelia, 4:227-243.

Goodrich, E. S.

1901. On the Structure and Affinities of Saccocirrus. The

Quarterly Journal of Microscopical Science, 44:413-

428.

Gray, J. S.

1965. The Behaviour of Protodrilus symbioticus (Giard)

in Temperature Gradients. Journal of Animal

Ecology, 34:455-461.

1966a. The Response of Protodrilus symbioticus (Giard)

(Archiannelida) to Light. Journal of Animal Ecology, 35:55-64.

1966b. Selection of Sands by Protodrilus symbioticus

(Giard). Veroffentlichungen des Instituts fur

Meeresforschung in Bremerhaven, Sonderband,

2:105-116.

1966c. The Attractive Factor of Intertidal Sands to Protodrilus symbioticus. Journal of the Marine Biological Association of the United Kingdom, 46:627-645.

1966d. Factors Controlling the Localisations of Populations

of Protodrilus symbioticus (Giard). Journal of Animal Ecology, 35:435-442.
56

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

1967a. Substrate Selection by the Archiannelid Protodrilus

hypoleucus Armenante. Journal of Experimental

Marine Biology and Ecology, 1:47-54.

1967b. Substrate Selection by the Archiannelid Protodrilus

rubropharyngeus. Helgoldnder wissenchafliche

Meeresuntersuchungen, 15:253-269.

Hermane, C. O.

1969. The Systematic Position of the Archiannelida.

Systematic Zoology, 18(l):85-102.

Jagersten, G.

1940a. Die Abhangigkeit der Metamorphose vom Substrat

des Biotops bei Protodrilus. Arkiv for Zoologi,

1940b. Zur Kenntnis der ausseren Morphologic Entwicklung und Okologie von Protodrilus rubropharyngeus n.sp. Arkiv for Zoologi, 32(16):1-19.

1944. Zur Kenntnis der Morphologic, Enzystierung und

Taxonomie von Dinophilus. Kungliga Svenska

Vetenskapsakademiens Handlingar, 21(2): 1-90.

1947. On the Structure of the Pharynx of the Archiannelida with Special Reference to There-occurring

Muscle Cells of Aberrant Type. Zoologiska bidrag

fr&n Uppsala, 25:551-570.

1952. Studies on the Morphology, Larval Development

and Biology of Protodrilus. Zoologiska bidrag fr&n

Uppsala, 29:425-512.

Jones, E. R., and F. F. Ferguson

1957. The Genus Dinophilus (Archiannelida) in the

United States. American Midland Naturalist,

57:440-449.

Jouin, C.

1962. Le Developpement larvaire de Protodrilus chaetifer

Remane (Archiannelides). Comptes Rendus de

VAcademie des Sciences, series D, 255:3065-3067.

1966. Morphologic et anatomie comparee de Protodrilus

chaetifer Remane et Protodrilus symbioticus Giard;

creation du noveau genre Protodrilotdes (Archiannelides). Cahiers de Biologie Marine, 7:139-155.

1968. Scxualite et biologie de la reproduction chez

Mesonerilla Remane et Meganerilla Boaden (Archiannelides Nerillidae). Cahiers de Biologie Marine,

9:31-52.

Marcus, E. du B.-R.

1948. Further Archiannelids from Brazil. Communicaciones Zoologicas del Museo de Historia Natural de

Montevideo, 2(48): 1-77.

1955. On Turbellaria and Polygordius from the Brazilian

Coast. Boletim da Faculdade de Filosofia, CiSncias

e Letras, Universidade de Sao Paulo, Zoologia,

20(207): 19-65.

Pierantoni, U.

1908. Protodrilus. Fauna und Flora des Golfes von

Neapel und der angrenzenden Meeresabschnitte,

Monographic 31, 226 pages. Zoologische Station,

Naples.

Rao, C. G., and P. N. Ganapati

1968. On some Archiannelids from the Beach Sands of

Waltair Coast. The Proceedings of the Indian

Academy of Sciences, 67(l):24-30.

Remane, A.

1932. Archiannelida. Tierwelt der Nord- und Ostsee,

6(22, Via): 1-36.

Renaud-Debyser, J.

1963. Recherches ecologiques sur la faune interstitielle

des sables. (Bassin d'Arcachon, lie de Bimini,

Bahamas.) Vie et Milieu, supplement 15:1-157.

Sterrer, W.

1968. Paranerilla limicola Jouin und Swedmark (Archiannelida) von der Norwegischen und Adriatischen

Kiiste. Santa, 36:65-68.

Swedmark, B.

1954. £tudc du developpement larvaire et remarques

sur la Morphologie de Protodrilus symbioticus

Giard (Archiannelides). Arkiv for Zoologi, 6(25):

511-522.

Westheide, W.

1967. Die Gattung Trilobodrilus (Archiannelida, Polychaeta) von der deutschen Nordseekuste. Helgoldnder wissenchaftliche Meeresuntersuchungen, 16:

207-215.

Wieser, W.

1957. Archiannelids from the Intertidal of Puget Sound.

Transactions of the American Microscopical Society,

76(3):275-285.
Wilfried Westheide Interstitial Polychaeta

(Excluding

Archiannelida)

ABSTRACT

Systematics, distribution, eidonomical and anatomical organization, and reproductive biology of

interstitial polychaetes as represented in 16 families

are discussed. Adaptations to interstitial life in

Pisione, Hesionides, Microphthalmus, Petitia,

Psammodrilus, and other genera are emphasized.

The class Polychaeta is a rather heterogeneous

group. It includes nearly 10,000 species whose

lengths range from three meters to only a few

more millimeters. Many of these animals belong to

the meiofauna but no real distinction can be made

between the larger benthic forms and the smaller

meiofaunal ones.

Only the "interstitial" polychaetes, inhabitants

of sandy and sandy-muddy sediment, form a small,

more or less homogeneous ecological group. More

precisely, only those animals which are able to live

in the interstices of sediments because of their

small body dimensions, and especially because of

their small diameters, are considered "interstitial."

Well-known interstitial species include Hesionides

arenaria Friedrich (length 2 mm, diameter 0.1

mm; Figure la,b), Microphthalmus listensis

Westheide (length 2.5 mm, diameter 0.15 mm, Figure 16), Petitia amphophthalma Siewing (length

1.5 mm, diameter 0.14 mm; Figure Id), Stygocapitella subterranea Knollner (length 3.5 mm, diameter 0.4 mm; Figure 2b), and Psammodriloides fauveli Swedmark (length 1 mm, diameter 0.12 mm).

Many of the larger polychaetes of sandy biotopes,

Wilfried Westheide, II Zoologisches Institut der Universitdt,

Gottingen, West Germany.

however, also are considered to be interstitial animals. Among these are some representatives in the

families Pisionidae, Syllidae, and Glyceridae with

body dimensions greater than the pore spaces of

coarse sandy sediments—for example, Pisione remota (Southern), length 7 to 15 mm, diameter 1

mm (see Figure 2a) —and by pushing aside the

sand grains they make space in which to move.

Numerous characteristics, however, of organization

and biology that have been recognized as adaptations to the sand biotope correspond to those of

the smaller inhabitants of sandy environments.

Thus, it is justifiable to extend the definition of

the term "interstitial polychaetes" to a series of

larger forms.

Accordingly, interstitial polychaetes are represented in at least 16 families (Hartmann-Schroder,

1964; Laubier, 1967a): Pisionidae (Alikunhi, 1947,

1949, 1951; Akesson, 1961; Laubier, 1967c; Siewing,

1953, 1954, 1955a; Stecher, 1968; Storch, 1966; Tenerelli, 1965), Phyllodocidae (Hartmann-Schroder,

1963; Laubier, 1961, 1965), Hesionidae (Alikunhi,

1948; Bobretzky, 1880; Friedrich, 1937, 1956; La

Greca, 1950; Westheide and Ax, 1965; Westheide,

1967, 1969; Zunarelli-Vandini, 1968), Syllidae

(Cognetti, 1961, 1962, 1965; Gidholm, 1962; Hartmann-Schroder, 1956; Rao and Ganapati, 1966;

Siewing, 1955b), Sphaerodoridae (Reimers, 1933),

Nereidae, Nephtyidae (Marinov, 1963), Glyceridae, Goniadidae, Dorvillaeidae (Levi, 1954; Dohle,

1967), Orbiniidae (Laubier, 1962), Paraonidae,

Cirratulidae, Ctenodrilidae, Stygocapitellidae (Karling, 1958; Knollner, 1934), and Psammodrilidae

(Swedmark, 1952, 1955, 1959). Only the important

literature dealing with interstitial polychaetes is

cited above.

Two families, the Psammodrilidae and probably

the Pisionidae (Figure 3), consisting of only a few

57
58

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

species, are restricted to the microfauna of sandy

biotopes. Altogether, approximately 75 to 100 species that can be considered "interstitial" are

known. This estimate, which is not even 1 percent

of all known polychaetes, does not include those

species which spend their juvenile stages in the mesopsammal, for example the younger stages of some

Nereidae and Opheliidae.

Most of the interstitial species are motile forms.

Many move very quickly and some, like chilopods,

run by means of leg-shaped neuropodia; for example, the species of the genus Hesionides (Friedrich,

1937; Westheide, 1967). Ciliary gliding and swimming in the pore spaces are known to occur in the

juvenile stages of some species. Sessile polychaetes

are almost lacking in the mesopsammal; only

Psammodrilus balanoglossoides Swedmark is semisessile and lives in mucous tubes between the sand

grains (Swedmark, 1955).

Interstitial polychaetes occur in sandy and sandymuddy shores in the eulittoral region as well as

sandy sediments in sublittoral zones. Many mesopsammic forms (such as Hesionides gohari Hartmann-Schroder and Petitia amphophthalma) are

found in both habitats. According to Tenerelli

(1966a,b), a few species seem to be limited to the

eulittoral shores (e.g., Stygocapitella subterranea)

or to sublittoral regions only (e.g., Plakosyllis

brevipes Hartmann-Schroder).

There probably are no polychaetes which characterize the "coastal subsoil water," or "Kiistengrundwasser" (inter alia, Hartmann-Schroder, 1964). Like

most other organisms, the polychaetes avoid that

region, as has been demonstrated by many investigations on tidal as well as atidal beaches (Ax,

1969; Schmidt, 1968; Westheide, 1967). Thus, Stygocapitella Knoller, still regarded as a typical subsoil water animal, is not found in this region

throughout most of the year, but it is found almost

always in the wet sand of the upper eulittoral

beach slopes. The overemphasis of the role of subsoil water in meiobenthology can be traced back to

the inaccuracy of quantitative sampling techniques. Nevertheless, for limited periods the subsoil water is important for a few species. The

whole population of Hesionides arenaria of the

North Sea coast hibernates in very deep regions of

subsoil water, deep enough not to be reached by

the usual sampling techniques (Westheide, 1967).

Suitable habitats for most of the interstitial polychaetes are known all over the world. The distribution of six well-known, typical species of littoral

sandy biotopes is shown in Figures 3-5. For the localities of these species consult the literature given

above and the following: Aiyar and Alikunhi

(1940), Day (1967), Delamare Deboutteville

(1954, 1956, 1960), Delamare Deboutteville, Gerlach, and Siewing (1954), Fize (1963), Gerlach

(1955), Hartmann-Schroder (1958, 1959, 1960a,b,

1962), Hartmann-Schroder and Hartmann (1962),

Laubier (1964, 1967b, 1968), Laubier and Paris

(1962), Rao and Ganapati (1967), Renaud-Debyser

(1963), Renaud-Debyser and Salvat (1963), RenaudMornant and Serene (1967), Storch (1967), Tenerelli (1964), and Valkanov (1954).

It is quite certain that additional localities of

these animals will be discovered during the next

few years through further investigations on other

beaches. It must be considered, however, that some

of these presently recognized species are really

"morphologically similar or identical natural populations that are reproductively isolated" (Mayr,

1965), thus, so-called sibling species.

An example of great external similarity of two

quite different species is found in the family Hesionidae. Microphthalmus sczelkowii Metschnikow

and M. aberrans (Webster and Benedict) often

live in the same biotope. Their external conformity (Figure 6) is so great that it is difficult to separate the two forms, especially in fixed material. Microphthalmus sczelkowii lacks only a specific seta

in notopodia, and its dorsal cirri are relatively

longer than those of M. aberrans; however, its sexual organs, reproductive behavior, development,

and seasonal history are quite different from those

of M. aberrans (Westheide, 1967). There are also

only slight differences between Hesionides arenaria

and H. gohari (Figure 7a-d). The shape of the

anal lobes and the quantitative differences in tentacles and cirri are the external characters by

which these species can be differentiated. In Tunisian beaches these species live in the same littoral region; the two populations usually are separated only by approximately 25 cm of vertical

distance, and individuals of Hesionides gohari and

H. arenaria may be found in the same samples.

There are, however, distinct differences in reproductive biology (Westheide, 1969).
FIGURE 1.—Typical interstitial polychaetes, anterior part: a, Hesionura sp., with proboscis

partly evaginated; b, Microphthalmus listensis; c, Streptosyllis sp. (Photo by P. Schmidt);

d, Petitia atnphophthalma.
60 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

a

\ \

HPra6E

FIGURE 2.—Typical interstitial polychaetes, anterior part; a, Pisione remota (photo by J. Stecher);

b, Stygocapitella subterranea.

The study of interstitial species is especially interesting for by comparison with more typical polychaetes of other biotopes, adaptations to the

environmental factors of mesopsammic habitats—

"Lebensformcharaktere" (Ax, 1963; Remane, 1952)

—can be easily recognized.

In the external organization different kinds of

reduction are found. (1) Regressive evolution in

body size and number of segments and setae: Some

typical mesopsammic species have an average

length of 2 to 3 mm; the average number of segments in Plakosyllis brevipes is 40, in Hesionides

arenaria 20, in Hesionides gohari 12, and in Petitia amphophthalma 12. (2) Modification of body

appendages in number and form: Here, different

types of evolution can be distinguished—increased

function of appendages as sense organs (e.g., Pisione Grube, Hesionides Friedrich, Microphthalmus Mecznikow; Figures 16, 2a, 6, 7,); development of extremely long filiform appendages which

serve, perhaps as adhesive organs (e.g., Microphthalmus listensis Westheide and Dioplosyllis cirrosa Gidholm); reduction to small, often tubercleshaped tentacles and cirri as seen in Plakosyllis

brevipes and other syllids (Hartmann-Schroder,

1964); or, finally, loss of all appendages (e.g., Stygocapitella subterranea, Figure 2b). Certain external characters, such as the shape of the prostomium and ciliation, are considered to be neotenic

in the genera Ophryotrocha Claparede and Mecznikow (inter alia, Dohle, 1967), Psammodrilus (Swedmark, 1955), and Psammodriloides (Swedmark,

1959).

Adhesive organs constitute another group of specific adaptive characters. Epidermal adhesive

glands are distributed all over the body in Pisione
NUMBER 76 61
62

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

3
5.—Distribution of Petitia amphophthalma Slewing and Plakosyllts brevipes Hartmann-Schroder. Syllidae.
64

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

FIGURE 6.—TWO species of the genus Mtcrophttialmus: a, M. sczelkowii; b, M. aberrans.

remota (Stecher, 1968) and in Microphthalmus listensis. In the genera Hesionides and Microphthalmus characteristic caudal adhesive lobes (Figure

7b,d) are found. The loss of light-sensitive organs

as in Sphaerosyllis renaudae Hartmann-Schroder,

and Parapionosyllis subterranea Hartmann-Schroder and the loss of pigments as in Friedericiella pacifica (Friedrich) and Stygocapitella subterranea are

characters considered as examples of degenerative

evolution (Hartmann-Schroder, 1964). In Petitia

amphophthalma (Siewing, 19556) and Hesionides

gohari, eyes are reduced during postembryonic development.

A second group of adaptive features is found

among the psammobiontic polychaetes. There is a

specific epidermis with a chorda-like layer of small

vacuoles as in Hesionides arenaria (Ax, 1966;

Westheide, 1967) or a very thick cuticula serving

for mechanical protection as in Pisione remota

(Stecher, 1968). The remarkable pharyngeal apparatus of Psammodrilus balanoglossoides, formed by

transformation of longitudinal body muscles, serves

as a suction pump for feeding on diatoms and detritus (Swedmark, 1955). Operation of the pharynx

in Hesionides is similar (Westheide, 1967). A low

production of gametes is perhaps the consequence

of the few cells in interstitial animals (Swedmark,

1964). The number of eggs found at the same time

in Pisione remota was 450 to 600, Psammodrilus

balanoglossoides 75, Hesionides arenaria 30 to 80,

Microphthalmus sczelkowii 10 to 14, Microphthalmus listensis 5 to 10, and Psammodriloides fauveli

1.

The Pisionidae (Alikunhi, 1949, 1951; Stecher,

1968) and the genera Hesionides and Microphthalmus (Bobretzky, 1880; Alikunhi, 1948; Westheide,
FIGURE 7.—TWO species of the genus Hesionides: a, H. arenaria, anterior part with a double

spermatophore, fixed on the epidermis; b, H. arenaria, posterior part with adhesive anal lobes;

c, H. gohari, with spermatodesme (sperm bundle without any covering, fixed on the epidermis):

d, H. gohari, posterior part with adhesive anal lobes.
66

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

1967) have complicated reproductive organs almost

unknown in other polychaetes. Their structures are

closely related to the reproductive biology of these

species. The study of transmission of sperm, in particular, has produced new results in the biology of

this class.

The best-known species of the Pisionidae is Pisione remota. The reproductive organs of the

males are located in each parapodium in the middle part of the body (Figure 8a) and they consist

of a copulatory organ and a modified cirrus. Sperm

are transmitted by direct copulation. The male

creeps over the female, and it adheres closely by

means of specific glands that open at the ventral

body wall. The copulatory organs are inserted into

the genital pores of the female. In most cases

nearly all receptacula of the female are filled in 15

minutes (Stecher, 1968).

In Hesionides arenaria the male has testes in the

middle and posterior segments and a pair of peculiar mating organs in the anterior part. There are

two vesiculae, each supplied with a partly glandular duct that opens above the prostomium. In

these organs the formation of 100-JU, double spermatophores takes place (Figure 7a). The spermatophores are pressed out of the ducts and fixed to

the body of the female and the sperm penetrate

the epidermis (Westheide and Ax, 1965; Westheide,

1967).

The male organs of Hesionides gohari are similar to those of H. arenaria. The glandular parts of

the spermducts, however, are much smaller. There

are no real spermatophores—only sperm bundles

("spermatodesma"), without any covering, which

are fixed to the integument of the sexual partner

(Westheide, 1969), as in Figure 7c.

The genus Microphthalmus is hermaphroditic.

Sperm are produced in the anterior half of the

body, eggs in the posterior segments. All species except M. tyrrhenicus (Cognetti) are equipped with

complicated male sexual organs in the second and

third setigerous metameres (Zunarelli-Vandini,

1968). The organs of M. sczelkowii consist of a ciliated funnel, vesicula, ductus ejaculatorius, and a

muscular bulbus that resembles a suctorial organ.

In M. aberrans there is only an unpaired (but similar-appearing) genital organ. The terminal part is

evaginated as a penis (Figure 86). In M. listensis

the mating organs are paired, with ciliated funnel,

vesicula, a large glandular ductus ejaculatorius extending to setigerous segment 7, a cuticular penis,

and a special muscular pump. Mating in M. aberrans takes place by transmission of spermatophores;

in the other species, the development of copulatory

organs suggests a direct mating process (Westheide,

1967).

The polychaetes of the mesopsammal do not

spawn their eggs free into the water. The eggs are

shed individually or in greater numbers in the

pore spaces of the substratum (Pisione remota, Hesionides arenaria) or in a mucous mass

(Microphthalmus aberrans, M. listensis) as seen in

Figure 8c. Microphthalmus sczelkowii forms a cocoon, like an oligochaete, by means of clitellumlike glands of the epidermis (Westheide, 1967). A

primitive type of brood protection has been found

in the genus Ophryotrocha, where the female

guards a cylindrical mass of 30 to 400 eggs (Akesson, 1967). Methods of reproduction in the Syllidae (direct reproduction, viviparity, schizogamy,

gestation, etc.) are summarized by Potts (1913).

Investigations of the Exogoneae have been made

by Haswell (1920).

The development of members of the interstitial

fauna is normally direct, and free-swimming larvae

are suppressed (Swedmark, 1964); see Figure 8d.

Of the polychaetes already investigated, trochophores are found only in Pisione remota (Stecher,

1968; Akesson, 1961; Banse, 1957) and Microphthalmus aberrans (Westheide, 1967).

Little is known about the age of interstitial polychaetes. North Sea populations of Hesionides arenaria, Microphthalmus sczelkowii, and M. aberrans

probably are annual, with only one period of reproduction—in summer, autumn, or winter

(Westheide, 1967). Pisione remota lives several

years and has one reproductive period per year

(Stecher, 1968).

An analysis of interstitial polychaetes shows that

the evolution of particular characters has occurred

in two directions: first, by regression and reduction, especially of external features; second, by formation or development of internal features and,

particularly, of specific new kinds of behavior.

Both groups of characters may coincide in some

species.
NUMBER 76 67

FIGURE 8.—Reproductive biology: a, Pisione remota, male, copulatory organs at several parapodia

(photo by J. Stecher); b, Microphthalmus aberrans, copulatory organ, evaginated; c, Af. listensis, eggs in a mucous mass; d, Af. sczelkowii, young animal which has just left the cocoon,

seven days after spawning.
68

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

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1920. The Exogoneae. Journal of the Linnean Society,

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1958. Zur Kenntnis von Stygocapitella subterranea

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Knollner, F.

1934. Die Tierwelt des Kiistengrundwassers bei Schilksee

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La Greca, M.

1950. Sulla presenza nel Mediterraneo di Lycastoides

pontica (Bobr.), Microphthalmus fragilis Bobr. e

M. similis Bobr. (Annelida Polychaeta). Annuario

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Napoli, 2:1-16.

Laubier, L.

1961. Mystides (Pseudomystides) coineaui n. sp., un Phyllodocien des eaux souterraines littorales de Mediterranee occidentale. Rapports et Proces-Verbaux

des Reunions, Commission Internationale pour

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1962. Schroederella pauliani gen. nov., sp. nov., un

nouvel orbiniide (polychetes sedentaires) de la

faune interstitielle d'Afrique. Annals of the Transvaal Museum, 24:231-238.

1964. Deux polychetes interstitielles des plages de Corse.

Vie et Milieu, 15:813-815.

1965. Sur la presence d'Eteonides augeneri (Friedrich,

1937) dans les sables du Bassin d'Arcachon. Actes

de la Societe Linne'enne de Bordeaux, 102:1-3.

1967a. Adaptations chez les Annelides Polychetes interstitielles. Annie Biologique, 6:1-16.

1967b. Annelides Polychetes interstitielles de NouvelleCaledonie. Expedition Francaise sur les Recifs

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1967c. Presence d'une Annelide Polychete de la famille des

Pisionidae appartenant a un genre nouveau dans

les eaux interstitielles littorales de C6te d'lvoire.

Comptes Rendus de I'Academie des Sciences, series

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1968. Presence au Portugal de deux Annelides Polychetes

interstitielles. Vie et Milieu, 19:426-428.

Laubier, L., and J. Paris

1962. Annelides Polychetes. Faune marine des PyreneesOrientales, 4. Vie et Milieu, 13:1-80.

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1954. Ophryotrocha minuta nov. sp., nouveau Polychete

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Marinov, T.

1963. t)ber die Polychatenfauna der Sandbiozonose vor

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Bulgarian.]

Mayr, E.

1965. Animal Species and Evolution. 797 pages. Cambridge, Massachusetts: Cambridge University Press.

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Rao, G. C, and P. N. Ganapati

1966. On a New Species of Sphaerosyllis (Polychaeta)

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1933. Morphologie der Polychaetengattung Sphaerodorum.

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1952. Die Besiedlung des Sandbodens im Meere und die

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1963. Recherches ecologiques sur la faune interstitielle

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Schmidt, P.

1968. Die quantitative Verteilung und Populationsdynamik des Mesopsammons am Gezeiten Sandstrand

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70 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Siewing, R.

1953. Morphologische Untersuchungen am "Kopf" der

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1966. Drei neue Polychaeten aus dem Litoral des Roten

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1952. Note preliminaire sur un polychete sedentaire aberrant, Psammodrilus balanoglossoides n. gen., n. sp.

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1964. Su una associazione di Policheti mesopsammici del

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1954. Zwei neue Polychaeten fur das Schwarze Meer.

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1967. Monographic der Gattungen Hesionides Friedrich

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Pierre Lasserre Oligochaeta from the

Marine Meiobenthos:

Taxonomy and Ecology

ABSTRACT

The taxonomy of the marine Oligochaeta belonging to the families Aeolosomatidae, Potamodrilidae, Tubificidae, Naididae, and Enchytraeidae is

discussed with emphasis on morphology. Ecology

is discussed in terms of adaptations to the habitat,

locomotion, reproduction, and distribution in intertidal and subtidal habitats. Distribution of intertidal species is interpreted in terms of physiological

ecology.

The class Oligochaeta has both interstitial and

freshwater representatives and some members have

penetrated marine habitats. Certain groups that

occur in estuarine muds are very abundant in

terms of individuals and biomass (Brinkhurst,

1963b, 1964; Dahl, 1960; Lasserre, 1967a,b). Some

groups often are dominant members of the subtidal meiobenthos, others mainly are restricted to

the upper areas of sandy beaches.

It is generally accepted that the term meiofauna

refers to those animals which pass through a

0.5-mm sieve. In general, adult meiobenthic oligochaetes are between 1 and 6 mm in length, with a

diameter not exceeding 300 p. There are, however,

some that are larger as adults but whose juvenile

forms exist as temporary members of the meiobenthos.

Many meiobenthic oligochaetes are cosmopolitan. The same species often are found on the

shores of the Baltic Sea, the North Sea, around the

English coast, and on both the Atlantic and Mediterranean shores of France. Recently, the author

Pierre Laserre, Institut de Biologie Marine, University de

Bordeaux, 33 Arcachon, France.

found on the eastern coast of North America many

species which occur in Europe.

I thank Dr. R. Weevers, University of Bristol

(England), for his linguistic revision of this manuscript.

Taxonomy

The basis for the classification of Oligochaeta is

the arrangement of the genital segments and gonoducts (Avel, 1959; Stephenson, 1930). The Aeolosomatidae, Potamodrilidae, Tubificidae, Naididae,

and Enchytraeidae include species living as marine

meiobenthos. All of these families are plesiopora

(Figure 1), that is, the vasa deferentia open on the

segment posterior to the segment containing the

testes. The plesiothecate plesiopora includes the

Tubificidae and Naididae, in which the spermathecae are found in or near the segment containing

the testes (segment 5 for Naididae, segment 10 for

Tubificidae; see Figure 1). The prosothecate plesiopora includes the Enchytraeidae, in which the

spermathecae are situated in segment 5, far anterior to the genital segments (Figure 1).

The Aeolosomatidae and Potamodrilidae apparently are very primitive in many respects and not

closely related to the other families. Representatives of these families often look more like polychaetes or archiannelids than oligochaetes (Figure 1).

Only partial keys have been published: Bunke

(1967) for Aeolosomatidae and Potamodrilidae;

Sperber (1950) for Naididae; Brinkhurst (1963a)

for Tubificidae; Nielsen and Christensen (1959,

1963a,b), Lasserre (1966, 1967b,c), and Tynen and

Nurminen (1969) for Enchytraeidae. A review of

the marine Enchytraeidae, with keys, is in preparation by the author. In many cases, original de71
72

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Prosothecat e

Plesiopor a

11 12

1jr

ENCHYTRAEIDAE

Plesiothecat e

Plesiopor a

10 11

WTT

T U B I F I C I DA E

5 6

a

NAIDI DAE

POTAMODRIL IDAE

AEOLOSOMATIDAE

FICURE 1.—Diagrammatic views showing arrangement of reproductive organs and setae in

different families of meiobenthic Oligochaeta.
NUMBER 76 73

scriptions have been supplemented, emended, invalidated, and revalidated by later authors

(Michaelsen, 1927; Ude, 1929; Cernosvitov, 1937;

Sperber, 1950; Brinkhurst, 1963a; Nielsen and

Christensen, 1959; Bunke, 1967).

The taxonomy of meiobenthic oligochaetes is

difficult since careful microscopic study of live and

serially sectioned animals is quite essential. Single

characters generally are not diagnostic at either the

generic or specific levels; their importance must be

assessed in each case. The setae are the principal

criteria used for identification. Of the families considered here, the setae are arranged in four bi.ndles—two ventrolateral (termed "ventral") and

two dorsolateral (termed "dorsal"). The first segment is devoid of setae.

The taxonomic difficulties encountered in descriptions of gross morphology may be overcome,

with certain limitations, by the use of chromosome

counts and observations on the course of the first

meiotic division. Cytological investigation seems to

offer a promising approach to the solution of many

confusing problems in oligochaete taxonomy.

Family AEOLOSOMATIDAE

FIGURE 2G-K

The representatives of the family Aeolosomatidae

have an elongated and tactile prostomium which is

ciliated ventrally. Many species have prominent epidermal glands which produce a colored secretion.

The color of this secretory product is an important

diagnostic character which is not present after fixation in formalin or alcohol; therefore, the observation of live specimens is essential. The main colors

are red and yellow-green. In some species the secretion is not colored.

Segmentation is not well marked and the

number of segments is low, usually about 10. The

position of the budding zone is of importance

(Figure 2G) .

Setae are present in the genus Aelosoma Ehrenberg but absent in the genus Rheomorpha Ruttner-Kolisko. Hair setae are dominant, and occur in

both dorsal and ventral bundles. They are slender,

more or less flexible filaments (Figure 2H1-K1) ; a

serration is present on one side in some species,

such as Aeolosoma litorale Bunke (Figure 2H2) .

Smaller sigmoid setae with a proximal serration

are found very often (Figure 2K2).

The shape of the prostomium and the form and

position of ciliated pits are important (Figure

2IJ). Since the sex organs are present only in rare

individuals, they are not used for classification and

do not appear in the existing keys.

Family POTAMODRILIDAE

FIGURE 2L,M

Like the previous family, Potamodrilidae has an

elongated and tactile prostomium which is ciliated

ventrally. Following is a characterization of the

monotypic genus (Potamodrilus).

The external segmentation is hardly visible.

The number of segments (7) is constant, and there

is a prostomium (Figure 2L). The first segment is

devoid of setae, six segments have two hair setae

(distally serrated) in dorsal and ventral bundles

(Figure 2M 1,2). The epidermal glands produce an

adhesive secretion. A male pore and seminal

groove are present in segment 6. The female pore

is at the junction of segments 6 and 7.

Family NAIDIDAE

FIGURE 2A-C

The number, position, and shape of setae are very

important for identification. In many Naididae the

dorsal bundles begin on a more-posterior segment

(e.g., Paranais Czerniavsky). Hair setae are found

in the dorsal bundles; these are more or less slender filaments more common in front of the clitellum. Bifid crotchets are present in dorsal and ventral bundles (Figure 2B,C) . These S-shaped setae

have a distal hook or crotchet composed of two diverging teeth, and the shape and relative length of

these teeth commonly are referred to in the keys.

Genital setae (penial setae), differing in shape

from the ordinary ventral setae, are present only in

fully developed specimens. The occurrence of

penial setae is a generic character, and the shape

of such setae is of specific value.

The differentiation of the alimentary canal and

the form of the vascular system are diagnostic characters. The alimentary canal consists of the mouth
FIGURE 2.—A-C, Paranais litoralis, Naididae: A, brain (dorsal view); B, setae; cl—3, distal ends

of ventral setae; c4, distal end of dorsal setae, D-F, Phallodrilus monospermathecus, Tubificidae:

D, anterior part; E, brain (dorsal view);Fl,2 setae, o-i, Aeolosoma Morale: c, habitus; Hi, setal

bundle; H2, hair setae; i, prostomium (ventral view), j , K, Aeolosoma psammophilum: j , prostomium (dorsal view); KI, setal bundle; K2, sigmoid seta, L, M, Potamodrilus fluviatilis: L, habitus;

Ml, setal bundle; M2, detail of a hair seta.
NUMBER 76 75

cavity, pharynx, esophagus, and intestine. The

pharynx roof and parts of the esophagus are covered by gland cells and the pharyngeal and esophageal glands. In some genera there are septal glands

instead of pharyngeal or esophageal glands. Behind

the esophagus (segments 4-6) a dilatation of the

gut forms a stomach which merges imperceptibly

into the intestine. The gut behind the first three

to five segments is covered by a layer of chloragogen cells that densely cover the intestine. The vascular system is composed of a contractile longitudinal vessel that divides behind the brain and unites

by anastomosis to the noncontractile ventral vessel,

in anterior part, to form a plexus.

The shape of the brain, as described by many

authors, is of limited value (Figure 2A) , and it

varies much with the state of contraction, both in

living and preserved material.

The reproductive organs are present only in rare

individuals; consequently, they are of little use for

classification and do not appear in existing keys.

Immature specimens, however, should never be

used for species description.

Family TUBIFICIDAE

FIGURE 2D-F

As in the previous family, the setae are very important for identification. Hair setae, when present,

are found dorsally. Bifid crotchets are present in

dorsal and ventral bundles (Figure 2F) , and the

upper tooth may be so reduced that the setae appear to be needle-like, sometimes with a trace of

the reduced tooth. Pectinate setae, present in some

genera, are situated in anterior bundles; the intermediate teeth may be as large as the outer teeth.

Genital setae are associated with the penial or

spermathecal pores; they are frequent in tubificids

and their very characteristic shape is useful for

identification at the generic and specific levels.

The genera and species differ chiefly in the form

of the male efferent ducts. Each of these paired organs is composed of a sperm funnel and vas deferens, both of which lie in the posterior part of the

testis segment. The funnel leads into the vas deferens stalk. A true penis, which may or may not be

sheathed in a cuticle, may or may not be present.

The presence or absence of a prostate, the shape

of the atrium, and the form of the penis, when it

is covered with a chitinous sheath, are generic

characters. The main characters used in species diagnosis are the shape of the setae and spermatheca.

Family ENCHYTRAEIDAE

FIGURES 3-7

The genera and species of this family are not easy

to identify even by experienced systematists. The

difficulties encountered in the taxonomy of Enchytraeidae are due to the great intraspecific variability. A standard procedure is necessary in the description of new species. A style conforming to that

of Nielsen and Christensen (1959, 1963a,b) and

Lasserre (1964, 1966, 1967b,c) will facilitate identification.

The following morphological features are diagnostic for the members of this family. The number

of segments remains practically constant in fully

mature specimens. The number, distribution, and

form of the setae furnish important clues. In the

genus Marionia Michaelsen, which includes many

meiobenthic representatives, one group of three

species has ventral bundles only, and one species,

M. achaeta Lasserre, is without setae. The setae

are broad, usually simple-ended, straight or sigmoid, and with or without an ental hook (Figure

4A-C) .

The brain varies widely in size and shape, but

the form of the more-posterior part, more or less

deeply incised or slightly concave, is of limited diagnostic value at the species level (Figures 3, 5A) .

The septal glands, paired roundish organs of unknown function, are usually attached on septa 4/5,

5/6, and 6/7; and they may vary in number and

shape (Figure 5D-F) . The esophagus may have

paired, elongate appendages which communicate

with the pharynx, the peptronephridia (e.g., the

genera Enchytraeus Henle and Grania Southern).

These organs extend backward, floating freely in

the body cavity. They are highly contractile and,

hence, variable in shape. Their presence or absence

is of generic value. For example, the genus Marionia and a new genus to be described by the author have no peptronephridia.
76

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

FIGURE 3.—A, An enchytraeid oligochaeta (genus Marionina).

B, Lateral view of the anterior part of a living specimen

of Marionina showing brain and pharynx.

Other features of taxonomic importance include

the coelomocytes (=lymphocytes) and the chloragogen cells. The former float freely in the body

cavity (Figure 5B1,2) , while the latter are attached

to the gut (Figure 5B2) . The origin of the dorsal

vessel, color of the blood, and form of the anteseptal portion of the nephridia are important. In

Marionina the anteseptal portion contains one or

more loops of the nephridial canal (Figure 5cl,2);

in other genera (e.g., Lumbricillus Orsted) it consists only of the funnel.

The most important features relating to the

identification of Enchytraeidae lie in the morphology of the sex organs. The sperm funnels (Figure

5c) are enlargements of the inner end of the

sperm ducts and, although they float more or less

freely in the body cavity, usually can be found in a

position just anterior to the clitellum. The

length/width ratio of the sperm funnels often is

taxonomically significant. The seminal vesicles,

when present, are situated just anterior to the

sperm funnels, and they are good diagnostic characters at both generic and species levels. The single

pair of spermathecae, situated in segment 5 and

sometimes extending farther back, is a very important character (Figures 5D-F, 6A-C). In mature individuals the ampulla contains sperm, sometimes

arranged in a manner typical of the species. The

ampulla may or may not have an ental duct opening into the esophagus. The opening of the ectal

duct to the exterior, and/or the duct itself, may be

surrounded by glands, the number and form of

which are important.

The principal characters used for the identification of meiobenthic Marionina are shown in Figure 7.

Ecology

Among oligochaetes, Aeolosomatidae and Potamodrilidae are the best adapted to the intertidal

environment. Typically, they live in groundwater.

These primitive oligochaetes have a prostomium

which is ciliated ventrally (Figure 2), as in archiannelids, and have many epidermal glands, either scattered over the body or concentrated in the

pygidium (as in Potamodrilus) .

Meiobenthic oligochaetes other than the aelosomatids and potamodrilids have no real morphological adaptations. The degree of organization and

differentiation in meiobenthic forms generally are

the same as in related, larger forms. Some species

of Marionina have greatly developed glands in

place of the absent dorsal setal bundles or annexed

to the posterior setae (Figure 4D-E). It seems that

these glands function in promoting adhesion to

sediments which often are unstable. When alive,

the worms can be seen adhering to sand grains—

with the middle or posterior part of the body—

very probably by means of secretion(s) from these

glands. Many species of Tubificidae, Naididae, and

Enchytraeidae have developed a tolerance to brackish water and to variable salinities. Such adaptations may explain the very wide distribution of

many species.

Many enchytraeids, mainly of the genus Marion-
FIGURE 4.—Marionina sp.: A, posterior part of living specimen; B, a posterior segment showing

the two ventral setae and cutaneous glands arranged in transverse rows (orcein coloration);

c, an anterior bundle and posterior seta; D, E, adhesive gland annexed to a posterior seta

(transverse section).

NUMBER 76 79

ina, the tubificid Phallodrilus monospermathecus

(Knollner), and the naidid Paranais litoralis are

restricted to the intertidal zone of sandy beaches.

The distribution of seven species of Marionina

were studied by Lasserre (1967a) over a period of

three years in the Bassin d'Arcachon.

In Marionina, hermaphroditism with cross-fertilization is the rule. Usually one egg is deposited in

a cocoon (Figure 8c) secreted by the clitellar

glands of the parent. The entire life span is

benthic. The young emerge only 10 to 15 days

after the laying (Lasserre, 1967a), and there are

two or three generations per year. In temperate palearctic regions, the species living in the foreshores

reach their maximum density in spring and autumn. Reproduction almost ceases during cold

winters. No doubt a certain mortality occurs, but

it seems to be moderate. As a consequence of the

position of these maximum and minimum values it

follows that the curves depicting the seasonal

trends are asymmetrical and show a slow decrease

during winter and summer and a rapid increase to

maximum density in spring and autumn (Figure 9).

The populations of Marionina achaeta Lasserre,

M. preclitellochaeta Nielsen and Christensen, M.

elongata Lasserre, and M. spicula Leuckart live in

the upper shore with Achaeta littoralis Lasserre

and Enchytraeus capitatus Bulow. Marionina subterranea (Knollner), M. precilitellochaetta, and M.

achaeta live from the middle to the lower shore,

where low salinities may occur, together with the

tubificid Phallodrilus monospermathecus (Figure

10). Such distribution is in agreement with the observations of Jansson (1968) at Swedish beaches.

In each of the middle- and upper-shore populations, 85 to 90 percent of the animals live at

depths between 10 and 70 cm from the surface

(Figure 11). During the period of maximum population the greatest density occurs at 30 cm depth

(noted in September). The density at 50 to 70 cm

depth remains quantitatively constant year round

(Figure 11). The populations migrate neither

daily nor seasonally. Temperature and food are

tentatively concluded to be the most important factors governing the density of Enchytraeidae (Lasserre, 1967a).

Jansson (1962, 1966, 1968) has demonstrated

that, on Swedish coasts, there is a clear reaction to

temperature and salinity gradients for some species

referred to the genus Marionina; however, "the preference for a certain salinity is certainly a less fixed

characteristic of an animal than its tolerance"

(Jansson, 1968). In some experiments the preference is outside the tolerance zone: Marionina preclitellochaeta tolerated 2.5 to 10 ppt salinity but

preferred 0.2 to 3 ppt salinity (Jansson, 1962).

Marionina southerni (Cernosvitov) has a great tolerance with a range of more than 15 ppt, but M.

preclitellochaeta and M. subterranea have a more

restricted range. The Swedish beaches studied by

Jansson have salinities from 7 to 22 ppt (Jansson,

1967b).

In Marionina, locomotion is effected by writhing

or more-coordinated burrowing. The animals force

their way through the substratum. Marionina subterranea shows a preference for a grain size between 125 and 500 /* (Jansson, 1966). The animals

are incapable of moving in sand with particle size

between 1,000 and 2,000 p and lie wriggling in the

large interstices where they are initially deposited

(Jansson, 1967a). The animal can cover a distance

of 3 cm/minute in a thin layer of fine sand.

Marionina subterranea and many other species

investigated on Atlantic coasts of France (Lasserre,

1967a,c) and eastern North America (Lasserre, in

preparation) showed very great tolerance both to

salinity and to temperature, with minimum ranges

of more than 15 ppt and 25°C. These populations

normally are subject to great fluctuations in salinity and temperature (Lasserre, 1967a,b, 1970, and in

FIGURE 5.—A, Marionina sp., brain; BI, Marionina sp., coelomocyte; B2, Marionina achaeta, coelomocyte and chloragogen cells; cl, Marionina sp., nephridia; c2, Af. achaeta, nephridia; D, Af.

achaeta, dorsal view of septal glands and spermathecae (segments 4-6); E, Af. spicula, dorsal

view of septal glands and spermathecae (segments 4-6); F, Af. elongata, dorsal view of septal

glands and spermathecae (segments 4-6).
80 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

press) and need wider physiological tolerance than

the Swedish species. The interstitial salinities in the

Atlantic sandy beaches are influenced mostly by

salt concentration of the sea, evaporation from the

sand, and rain.

Oligochaeta also live as subtidal meiobenthos,

mainly tubificids (Cook, 1969) and naidids. The

enchytraeids of the genus Grania and a new genus

to be described by the author are characteristic of

coarse sediments such as "Amphioxus sand" (Lasserre, 1966, 1967b).

The differences in the distribution of two species, Marionina achaeta and M. spicula, cannot be

explained properly by a difference between the commonly advocated granulometric and climatic factors

(Lasserre, 1967a). Therefore, the physiological preferences of each species were investigated experimentally (Lasserre, 1970 and in press). Marionina

achaeta lives predominantly in the upper shore but

sometimes in the lower part when the salinity is

low (Figure 10). Marionina spicula is found more

or less throughout the shore, though the upper

FIGURE 6.—A, Marionina elongata, dorsal view of septal glands and spermathecae; B, Af. spicula,

dorsal view of septal glands and spermathecae; c, Lumbricillus sp., lateral view of septal glands

and spermathecae. All living.
FIGURE 7.—Diagrammatic views of the genus Marionina.

oo
82

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

FIGURE 8.—A, Spermatids (Marionina), X 1200; B, transverse section through the clitellum, ovary,

intestine, and sperm duct (Marionina sp.); c, cocoon and newly hatched worm (genus Marionina).

limit is slightly below that of M. achaeta (Figure

10). Oxygen consumption was utilized as an indication of the homeostatic capabilities of these organisms. It was found that Marionina achaeta could

tolerate salinities somewhat above 25 ppt. but only

with the expenditure of considerable metabolic energy; therefore, the animal would be at a disadvantage on the lower shore where the salinity is normally above that level. Marionina spicula, on the

other hand, could tolerate salinities above 25 ppt

without the expenditure of metabolic energy, but

it was unable to survive at the high temperatures

(above 30°C) which have been recorded during

summer in the upper part of the range of M.

achaeta. These last two observations, taken together, explain the relative abundance of M. spicula at all except the highest levels. The overall

consumption of oxygen in both species is statistically constant over a range of salinities spanning

those normally encountered; this phenomenon is

termed an "adaptive plateau." At both very low

and high salinity oxygen consumption is considerably elevated.

Further experiments (Lasserre, 1969) on Marionina achaeta, relating to the cellular mechanisms

involved, have shown that this elevation occurs

only when sodium and, to a lesser extent, potassium are present in the medium only at very low

or very high ionic strengths. Chloride concentration changes have no effect on oxygen uptake. Very
NUMBER 76 83

M .preclitellochoeta

M .elongata

M . spicula

M.subterranea

M.weilli

M.mesopsamma

M .achaeta

100 %

50 %

N D J FMAM J J ASO N D j

FIGURE 9.—Seasonal variations of mature animals (in percent) and deposition of cocoons (c).

high concentrations ot sodium lower the metabolic

rate to a standard level which is the same as the

level obtained from treatment with a metabolic inhibitor specific for sodium transport (ouabain

10-3M). The depression by ouabain reaches the

same level regardless of the concentration of sodium.

The tentative conclusion is that the elevated

metabolic rate in media with less or more saline

than the range covered by the adaptative plateau is

the result of extreme activition of a Na-K-ATPase

pump system, working either inward or outward

depending on the conditions. The decrease of oxygen consumption in high-salinity media is attributed to a breakdown of the ion pumps, thus producing the same depression as ouabain.
84

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

level s

in meters

tida l

level s

—0.09-

—1.09—

—1.33—

—2.10—

—2.58—

— 2.91—

—4.66—

—4.72—

—4.94-

MLWST

H CWR

MLWNT

F M T L

HHWNT

HHWST

A EHWST

400 300 200 100

 5 0

 0 5 0 100 200 300 400

- • M.achaeta

-# M.spicula

A -A M. weill i

A -A M.preclitellochaeta

#- ® M. elongate

0 Q M.mesopsamma

• • M. subterranea

FIGURE 10.—Horizontal distribution of seven species of Marionina in the intertidal zone of the

Bassin d'Arcachon, Atlantic coast of France (autumn 1965, Camp Americain, 30 cm depth).

Tidal levels are indicated by combination of letters: E, equinoctial; M, mean; HW, high water;

LW, low water; NT, neap tides; ST, spring tides; MTL, midtidc level; CWR, continental water

resurgence.
NUMBER 76 85

WINTE R

Jan . 1965

AUTUM N

sept. 1965

30 30 300

M. achaeta

M. spicula

M. weilli

300

A M.precli tellochaeta

• M. elongate

FIGURE 11.—Vertical distribution of five species of Marionina in the intertidal zone of the

Bassin d'Arcachon: A, in winter (January, 1965); B, in autumn (September, 1965). Mean

high-water/neap-tide level.

Literature Cited

Avel, M.

1959. Classe de Ann&ides Oligochetes. In P. P. Grasse,

editor, Traite de Zoologie, 5(l):224-470.

Brinkhurst, R. O.

1963a. Taxonomical Studies on the Tubificidae (Annelida,

Oligochaeta). Internationale Revue der gesamten

Hydrobiologie, Systematische Beihefte, 2:1-89.

1963b. Notes on the Brackish-Water and Marine Species

of Tubificidae (Annelida, Oligochaeta). Journal of

the Marine Biological Association of the United

Kingdom, 43:709-715.

1964. Observations on the Biology of the Marine Oligochaete Tubifex costatus. Journal of the Marine

Biological Association of the United Kingdom,

44:11-16.

1966. A Contribution to the Systematics of the Marine

Tubificidae (Annelida, Oligochaeta). Biological

Bulletin, 30:297-303.

Bunke, D.

1967. Zur Morphologie und Systematik der Aeolosomatidae Beddard, 1895, und Potamodrilidae nov. fam.

(Oligochaeta). Zoologische Jahrbiicher, Systematik

Oekologie und Geographic der Tiere, 94:187-368.

Cernosvitov, L.

1937. System der Enchytraeiden. Bulletin de L'Association Russe pour les Recherches Scientifiques, Prague,

5:263-295.

Cook, D. G.

1969. The Tubificidae (Annelida, Oligochaeta) of Cape

Cod with a Taxonomic Revision of the Genera

Phallodrilus Picrantoni, 1902, Limnodriloides

Pierantoni, 1903, and Spiridion Knollner, 1935.

Biological Bulletin. 136:9-27.

Dahl, I. O.

1960. The Oligochaete Fauna ot 3 Danish Water Areas

(Taxonomic and Biological Observations). Meddelelser fra Danmarks Fiskeri-og Havunderspgelser,

2:1-20.
86

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Jansson, B. O.

1962. Salinity Resistance and Salinity Preference of Two

Oligochaetes, Aktedrilus monospermatecus Knollner

and Marionina preclitellochaeta n. sp., from the

Interstitial Fauna of Marine Sandy Beaches. Oikos,

13:293-305.

1966. Microdistribution of Factors and Fauna in Marine

Sandy Beaches. Veroffentlichungen des Instituts

fur Meeresforschung in Bremerhaven, Sonderband

2:77-86.

1967a. The Significance of Grain Size and Pore Water

Content for the Interstitial Fauna of Sandy Beaches.

Oikos, 18:311-322.

1967b. Diurnal and Annual Variations of Temperature

and Salinity of Interstitial Water in Sandy Beaches.

Ophelia, 4:173-201.

1968. Quantitative and Experimental Studies of the Interstitial Fauna in Four Swedish Sandy Beaches.

Ophelia, 5:1-71.

Knollner, F. H.

1935. Okologische und systematische Untersuchungen

uber litorale und marine Oligochaten der Kieler

Bucht. Zoologische Jahrbiicher Systematik, 66:425-

563.

Lasserre, P.

1964. Note sur quelques oligochetes Enchytraeidae presents dans les plages du bassin d'Arcachon. ProcesVerbaux de la SociiU Linnienne de Bordeaux, 101:

87-91.

1966. Oligochetes marins des c6tes de France. I. Bassin

d'Arachon: Systematique. Cahiers de Biologie Marine, 7:295-317.

1967a. Contribution a l'etude des Oligochetes marins du

Bassin d'Arcachon. These de Biologie, Universite

de Bordeaux. 126 pages.

1967b. Oligochetes marins des cotes de France. II. Roscoff,

Penpoull, etangs saumatres de Concarneau: Systematique, £cologie. Cahiers de Biologie Marine,

8:273-293.

1967c. Presence du genre Achaeta Vejdovsky, 1887 (Oligochaeta, Enchytraeidae) dans des plages sableuses

marines. Description de Achaeta littoralis n. sp.

Bulletin du Museum d'Histoire Naturelle, series 2,

39:979-983.

1969. Relations £nergetiques entre le m^tabolisme respiratoire et la regulation ionique chez une Annelide

Oligochete euryhaline, Marionina achaeta (Hagen).

Comptes Rendus de I'Academie des Sciences, series

D, 268:1541-1544.

1970. Action des variations de salinite, sur le metabolisme

respiratoire d'Oligochetes euryhalins de genre

Marionina Michaelsen, 1889. Journal of Experimental Marine Biology and Ecology, 4:150-155.

In Press. Donnees ecophysiologiques sur la repartition des

Oligochetes marins meiobenthiques. Proceedings of

the Third European Marine Biology Symposium.

Vie et Milieu, supplement 20.

Michaelsen, W.

1927. Oligochaeta. Tierwelt der Nord- und Ostsee, 6(9):

1-86.

Nielsen, C. O., and B. Christensen

1959. The Enchytraeidae, Critical Revision and Taxonomy of European Species. Natura Jutlandica,

8-9:1-160.

1963a. The Enchytraeidae, Critical Revision and Taxonomy of European Species. Supplement 1. Natura

Jutlandica, 10:1-23.

1963b. The Enchytraeidae, Critical Revision and Taxonomy of European Species. Supplement 2. Natura

Jutlandica, 10:1-20.

Sperber, C.

1948. A Taxonomical Study of European Naididae. Zoologiska bidrag frdn Uppsala, 28:1-296.

1950. A Guide for the Determination of European

Naididae. Zoologiska bidrag fr&n Uppsala, 29:45-78.

Stephenson, J.

1930. The Oligochaeta. 978 pages. Oxford: Clarendon

Press.

Tynen, M. J., and M. Nurminen

1969. A Key to the European Littoral Enchytraeidae

(Oligochaeta). Annales Zoologici Fennici, 6:150-

155.

Ude, H.

1929. Oligochaeta. Die Tierwelt Deutschlands und der

angrenzenden Meeresteile, 15:1-132.

Udekem, J. d'

1855. Nouvelle classification des Annelides s^tigeres

abranches. Bulletins de I'Academie Royale des

Lettres des Beaux-Arts de Belgique, Classe des

Sciences, 22:533-555.
Robert R. Hessler Biology of

the Mystacocarida:

A Prospectus

ABSTRACT

The general biology of the Mystacocarida, including systematics, biogeography, ecology, functional

morphology and life cycles, is reviewed. Many of

the details of the biology remain unknown and

there is a paucity of seasonal studies.

This report is a superficial review of the present

knowledge of the crustacean subclass Mystacocarida. Much of what is known is summarized in Delamare Deboutteville's (1960) book on the interstitial fauna. The emphasis here is on what is not

known about the Mystacocarida.

It now is generally agreed that the Mystacocarida is a distinct subclass with possible affinities

with the Copepoda (Pennak and Zinn, 1943; Dahl,

1956a,b, 1963; Tiegs and Manton, 1958; Sanders,

1963; Hessler, 1964, 1969a). Some authors unite

the Mystacocarida with the Copepoda, Branchiura,

Cirripedia, and perhaps the Ostracoda in a single

higher taxon, Maxillopoda (Dahl, 1956a, 1963;

Ax, 1960; Siewing, 1963; Newman, Zullo, and

Withers, 1969). Many aspects of mystacocarid anatomy are regarded as primitive, but the possible importance of neoteny in the evolution of this subclass has not been determined. The precise

relationship with the other subclasses remains extremely inferential.

In the field of biogeography, Mystacocarida

occur along the Pacific coast of Chile (Dahl, 1952;

Noodt, 1961), the Atlantic coast of the United

States (Hessler and Sanders, 1966; Hessler, 1969b)

Robert R. Hessler, Scripps Institution of Oceanography,

La Jolla, California 92037.

and southern Europe (Delamare Deboutteville,

1953c, 1954b, 1957; Delamare Deboutteville, Gerlach, and Siewing, 1954; Wells and Clark, 1965),

the Mediterranean (summary in Delamare Deboutteville, 1960; also, Fize, 1963, and Grimaldi,

1963), the Atlantic coast of Africa (Delamare Deboutteville, 1953c; Delamare Deboutteville and

Barros Machado, 1954; Delamare Deboutteville

and Chappuis, 1957; Noodt, 1954), and the tip of

Africa on the Indian Ocean side (Noodt, 1954),

and the tip of Africa on the Indian Ocean side

(Noodt, 1954). Many other portions of the world's

coastlines have been searched with varying intensities but without success. This negative evidence is

not published. Therefore, the presence of Mystacocarida in the rest of the world must be regarded as

mostly unknown. It cannot even be guaranteed

that many of the promising beaches which have

been searched without success truly lacked this

group, because the distribution of mystacocarids

within a beach is so patchy.

Mystacocarida were thought to be absent from

the cold, more-northern coastlines of the continents

(Buchholz, 1953; Noodt, 1954; Delamare Deboutteville, 1960; Hessler and Sanders, 1966), but the recent discovery of Derocheilocaris ingens from the

coast of Maine (Hessler, 1969b) raises the possibility that Mystacocarida might even occur along the

coast of Canada. It also shows that each mystacocarid species does not necessarily have exclusive

control of entire continental coastlines, as previous

knowledge indicated (Delamare Deboutteville,

1960; Hessler, 1969b). Derocheilocaris ingens is

separated by only 260 km from the nearest known

population of D. typicus Pennak and Zinn, and

there are no apparent climatological or physiographic barriers between them. The case of D. remanei Delamare Deboutteville and Chappuis along

87
88

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

the Atlantic coast of Africa is an example of the

general concept of the wide distribution of mystacocarid species. Only four African localities (Kayar,

Senegal; Luanda and Lobito, Angola; and Swakopmund, South-West Africa) are known, and on the

basis of these it is assumed that the species is

found along the entire 12,000-km Atlantic coastline. That this is a very misleading extrapolation

will be seen shortly.

Systematics within the Mystacocarida has always

been simple. Even with the new material from

Maine, there are only four known species (Pennak

and Zinn, 1943; Delamare Deboutteville and Chappuis, 1951; Dahl, 1952; Hessler, 1969b). The differences between these species are slight, in spite of

their complex morphology (Delamare Deboutteville, 1960; Hessler and Sanders, 1966). Clearly the

Mystacocarida is an extremely conservative group.

To some extent this has been ignored by past investigators. Mystacocarids from Angola and SouthWest Africa have been placed with certainty in

Derocheilocaris remanei (Delamare Deboutteville,

1957; Delamare Deboutteville and Chappuis, 1957;

Noodt, 1954), yet, a recent inspection of new material from these areas revealed differences that easily

distinguish these populations from each other and

from the Mediterranean D. remanei. These differences are more extensive than those which separate

D. remanei from D. typicus, two species whose independence has never been questioned. From this

criterion and the fact that great distances separate

the known populations, I conclude that these species are distinct and that D. remanei katesae

(Noodt, 1954) may be yet another species (Hessler, in preparation).

More has been written about the ecology of mystacocarids than any other aspect of their biology

(Delamare Deboutteville, 1960; Noodt, 1961; Fize,

1963; Renaud-Debyser, 1963; Wells and Clark,

1965; Jansson, 1966; Hessler and Sanders, 1966;

Hessler, 1969b). Mystacocarids tend to be described as purely interstitial organisms of intertidal

or nontidal beaches. The sands are siliceous and

generally are well sorted and medium-fine to medium-coarse in size. In tidal beaches, the main concentrations are at midtide to high-tide level, and in

nontidal beaches are most abundant at levels

where the waves soak down into the sand. Mystacocarids survive temperatures ranging from freezing

to 25°C and salinities from 5 to 40 ppt.

While all this is generally valid, there already is

information which indicates there are major gaps

and inconsistencies in our understanding of the

ecology of these animals. Grimaldi (1963) found

mystacocarids in sands primarily composed of calcium carbonate and with a very low sorting coefficient. This appears to contradict some of the more

important generalizations. Both Derocheilocaris remanei (Delamare Deboutteville, 1953b) and D.

galvarina (Dahl, 1952) have been found subtidally.

Other than these two occurrences, nothing is

known about the extent, ecology, or importance of

subtidal distribution. Mystacocarids are notoriously

patchy in their distribution (Wells and Clark,

1965). The inability to explain this phenomenon

and the absence or rarity of mystacocarids on

beaches which are apparently suitable clearly indicate our ignorance of important environmental

controls.

The knowledge of functional morphology is

sketchy. Delamare Deboutteville (1953a) has given

a brief description of movement, emphasizing the

ambulatory method of progression, but the details

of this activity are largely unknown. The animal

bears numerous glands, setal combs, special sensory setae, toothed furrows, and other unusual

structures whose function has not yet been demonstrated (Delamare Deboutteville and Chappuis,

1954; Fize, 1963; Hessler and Sanders, 1966; Cals,

Delamare Deboutteville, and Renaud-Mornant,

1968; Hessler, 1969b). How mystacocarids feed is

not known and there is no proof of the nature of

the food, although the animal probably browses on

detritus or bacterial films (Buchholz, 1953; Jansson, 1966). Internal anatomy is known in only a

general way (Dahl, 1952; Tuzet and Fize, 1958;

Fize, 1963; Hessler, 1964).

The life cycles of Derocheilocaris remanei (Delamare Deboutteville, 1954a) and D. typicus (Hessler and Sanders, 1966) have been documented in

detail. In both cases development is gradual, beginning with a nauplius or metanauplius which is

much like the adult. The eggs are proportionally

large, as indicated by their great size within the

body of the female (Fize, 1963), but because they

are shed freely into the environment, none has

been identified in this free state. Brown and Metz
NUMBER 76 89

(1967) have described the morphology of the

sperm in detail. Tuzet and Fize (1958) and Zaffagnini (1969) have described gametogenesis. Recruitment rate of new individuals is not known, but it

must be low. Reproduction may be continuous

(Delamare Deboutteville, 1960) or seasonal (Hall

and Hessler, in preparation), depending on the

climate.

This review shows that the general features for

most aspects of mystacocarid biology already are

broadly known; however, almost nothing has been

demonstrated in real depth, and as a result most of

the existing information is vague and subject to

unexplained exceptions. The paucity of careful

seasonal studies is particularly noticeable. Future

investigations of this subclass must employ detailed, painstaking observations if the Mystacocarida are to be used to elucidate biological principles.

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90

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

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Comptes Rendus de I'Academie des Sciences, series

D, 246:3669-3671.

Wells, J. B. J., and M. E. Clark

1965. The Interstitial Crustacea of Two Beaches in

Portugal. Revista de Iiiologia, 5:87-108.

Zaflagnini, F.

1969. Quelques Observations sur l'appareil reproducteur

male et femelle de Derocheilocaris remanei Delamare et Chappuis (Crustacea Mystacocarida).

Cahiers de Biologic Marine, 10:103-107.
Summary and Current

Status of the Taxonomy

and Ecology of Benthic

Ostracoda Including

Interstitial Forms

ABSTRACT

The history of the taxonomy of Ostracoda as it

applies to the evolution of the "neontological" and

"paleontological" classifications is reviewed. Zoogeography, abundance, life history, and influence

of environmental factors are considered. Ecology,

in terms of true interstitial ostracods, and possible

morphological adaptations to interstitial life are

discussed.

The taxonomy of Recent ostracods had its

inception in 1772 with the publication by O. F.

Miiller entitled "Observations of some Bivalve Insects Found in Common Water." The taxonomy of

fossil ostracods began some 50 years later with the

publication of a paper entitled "The Mineral Conchology of Britain" by Sowerby (1825, p. 136). The

period of 1850 to 1925 was one of intense activity

in ostracod taxonomy. Such investigators as G. O.

Sars, G. W. Miiller, G. S. Brady, D. Robertson,

and A. M. Norman, to mention a few, established

basic classifications of fossil and Recent ostracods.

It was during this period that the use of two diverse methods for classifying ostracods evolved:

(1) classification based on carapace features with

little regard given to appendages, and (2) classification based on appendages with little regard

Neil C. Hillings, Office of Oceanography and Limnology,

Smithsonian Institution, Washington, D. C. 20560. This paper

is a revision of the one presented at the Conference.

given to the carapace. Results of the first method

have come to be known as the "paleontological

classification," although some zoologists contributed; and results of the second method are known

as the "neontological classification," with some paleontologists making contributions. This divergence perhaps was unavoidable, for zoologists often

and paleontologists always would have only carapaces to study. Some paleontologists working with

living material have continued to base descriptions

of new taxa only on carapace features, while some

zoologists ignore the carapace and describe new

taxa only on appendages.

The Ostracoda originally were described in 1806

by Latreille, who used both the carapace and the

appendages, with emphasis on the latter. Sars

(1866) divided the order into four suborders—Myodocopa, Cladocopa, Platycopa, and Podocopa—on

the basis of soft parts, especially on the structure

of the second antennae. Sars did not include fossil

taxa in his scheme. Many paleontologists erected

their own scheme, necessarily, perhaps, because in

many cases they were dealing with extinct taxa.

Pokorny (1958) was the first to erect a scheme of

classification to include all fossil and Recent ostracods, but the emphasis was on carapace morphology. Hartmann (1963, 1964a) established a neontological and paleontological classification of

ostracods, including only those families with Recent representatives; and where possible, he supplemented the diagnoses with appendage morphology.

Lower taxonomic levels often included diagnosis of

only the carapace (necessary in the case of fossil spe91
92

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

cies) or appendages but, fortunately now, a

diagnosis of both is included where possible. Thus,

Morkhoven (1962) and Hartmann (1963, 1964a)

define all taxa to the subfamily level on the basis

of carapace and appendages. Morkhoven (1962,

pages 96-97) has pointed out:

It is obvious that one uniform classification for both living

and fossil ostracods must be the ultimate goal, and the idea,

advanced by certain authors, of having separate classifications

for living and fossil forms, based on different criteria, must

be rejected. Only a single uniform classification permits a

comparison of Recent and fossil forms, and allows judgment

of phylogenetic relationships, interpretation of ecological

data, etc., without the burden of nomenclatural and taxonomic confusion.

In 1963 a Committee on Recent Ostracoda was

organized during the Naples Symposium on Ostracods as Ecological and Paleoecological Indicators

(see Puri, 1964). The committee was charged with

the responsibility of restudying the type-species of

all living genera and genera which originally were

described as fossil but have living representatives,

the objective being to provide a "natural" classification. Progress toward this objective was reflected

in some of the papers that were presented during a

symposim on The Taxonomy, Morphology and

Ecology of Recent Ostracoda and that later were

published in Neale (1969).

In addition to the carapace-appendage problem

mentioned above, the zoogeographic distribution

in intertidal and shallow water (less than 200 m)

continues to be a problem in that many species

have been reported as cosmopolitan. Thjs is especially true of studies of North American ostracods,

particularly the older published works (see discussion in Hulings, 1966, 1967a,b). Many of the older

studies were based solely on carapace morphology,

and, more often than not, specimens were not directly compared with actual type material, resulting in misindentifications and lumping of diverse

taxa. Some species may be cosmopolitan, but with

more detailed studies of the total organism, including comparison with type material, it probably

will be found that most species have a more restricted distribution than previously reported. A

reason for this is that benthic ostracods lack planktonic larval stages; thus, there is the absence of a

ready mechanism for a wide geographic distribution, such as from the European coast to the Atlantic and Pacific coasts of North America.

The ontogeny and sexual dimorphism of ostracods also have led to difficulties in classification.

Ostracods pass through as many as eight molt

stages or instars before reaching the adult stage.

Drastic changes often occur in both the carapace

and appendages from one instar to the next and,

in many cases, instars have been described as new

species. More studies concerned with ontogenetic

development such as that of Sandberg (1964) are

needed to resolve this problem. Sexual dimorphism

between the sexes as well as within one sex, where,

in some cases, the appendages are modified for reproduction has led to different sexes of the same

species being relegated to different genera.

New approaches and new techniques are adding

measurably to more detailed knowledge of the taxonomy of ostracods. One such approach, numerical

taxonomy, has been used by Kaesler (1969) "to obtain an initial estimate of the usefulness of numerical taxonomic methods in the classification of

ostracods." Kaesler stated that the results of his

study "indicate at a minimum that more work

needs to be done"; nevertheless his results are encouraging. The scanning electron microscope is

providing a new insight to carapace morphology,

as shown by Sandberg and Hay (1967), Puri and

Dickau (1969), and others. Techniques have also

been developed to study appendages with that

instrument.

That ostracods are members of the meiofauna, if

the latter is defined on the basis of size, is beyond

question. But to consider ostracods as members of

the interstitial environment raises a question

which, based on studies to date, one finds difficult

to answer. Obviously the shape and the size of the

grains, which determine the available pore space,

must be considered. The ostracods found on a

gravel bottom, where the pore space is very great,

could be considered interstitial if they permanently

occupy the pores. The same might be true for species found in shell bottoms, "Amphioxus sand,"

etc. But many of these species—as noted by Remane (1940), Elofson (1941), and others—climb

on the large particles; and those living among shell

fragments are considered burrowers and those living among shells are considered surface dwellers.

Furthermore, observations have revealed that many

species dwelling in siliceous sand are typically surface dwellers (episammic) and sometimes these
NUMBER 76 93

forms burrow into the sand to a depth of 1 to 2

cm, remaining there for only a short period of

time. Such burrowing forms are considered by the

author as temporary members of the interstitial

milieu, and, based on available information to

date, these would include most of the sand-dwelling species. Thus, the author considers true interstitial ostracods as those which permanently occupy

the interstitial voids of siliceous sand sediments. As

defined, the author's interpretation of true interstitial ostracods is more restrictive than that of

Swedmark (1964), who included shell gravel and

"Amphioxus sand" species in his discussion of interstitial ostracods.

To date, only a few species of ostracods have

been reported as truly interstitial or mesopsammic.

Elofson (1941) considered Polycope areolata Sars,

Microcythere sp., and Cytherois sp. as mesopsammon ostracoda. In the Mediterranean, Hartmann

(1953) found 13 species in the interstitial, of

which he considered only six—all new species—to

be typically interstitial: Microcythere subterranea

Hartmann, Loxoconcha tuberosa Hartmann, Xestoleberis costata Hartmann, X. delamarei Hartmann, Microloxconcha compressa Hartmann, and

Cytheromorpha elongata Hartmann. In addition,

Hartmann considered two new species of Polycope

Sars to be typically interstitial.

Williams (1969), in studying four intertidal localities on the coast of Angelsey, reported four species—Leptocythere pellucida (Baird), L. castenea

(Sars), Polycope compressa (Brady and Robertson) , and P. orbicularis Sars as "sediment living

species." He stated that he considered none of the

species recorded as a true interstitial form (Williams, 1969, p. 328). Those found in the interstices

were juveniles of surface dwellers. Living juvenile

stages were found to a depth of 15 cm, while the

adults generally were restricted to the upper 2 cm.

The depth of penetration of ostracods, recorded as

such and not identified to species or as living or

dead, has been reported by Rees (1940) as 2 cm in

sand, 5 mm in mud; by Mare (1942) as 5 mm in

mud; by Moore (1931) as 7 cm in subtidal mud;

by Smidt (1951) as 4 cm (maximum) in tidal

sand; by Tietjen (1969) as 5 mm (maximum) in

estuarine sediments. Williams also found that the

"sediment living species" varied with available

pore space.

Thus, only the work of Hartmann (1953) shows

that true interstitial ostracods, as adults, do exist.

It is interesting that, as noted by Swedmark

(1964) in citing the work of Klie (1929, 1936), all

the species reported by Hartmann (1953) as true

interstitial forms were new species, indicating a

specific interstitial ostracod fauna. But since most

of Klie's species came from shell bottoms they are

not considered by the present author as truly interstitial.

Certainly, Hartmann and Williams have approached the problem correctly in that they studied samples collected in a way that made it

possible to determine, by coring and analyzing the

core at regular intervals, whether true interstitial

ostracods do exist. Beyond this, actual laboratory

(or field) observations on the behavior of the individual species are necessary. Studies where the samples were collected by dredging (for example,

Reys, 1961) are of little use in this context.

The possibility of special adaptations in the

morphology of the carapace and appendages of the

true interstitial ostracods are worth considering, although, as Hartmann (1946b) pointed out, little is

known of the correlation between the morphological features of the carapace and the mode of life.

Remane (1940) and Elofson (1941) have shown

relationships between ornamentation of the carapace and the type of substratum on which ostrocods occur. Triebel (1941), working with fossil ostracods, also demonstrated similar relationships

and noted that certain morphological features of

the carapace could be understood only by considering the behavior of the ostracod in relation to substratum.

Elofson (1941) noted that for the forms he considered true mesopsammic the carapace is small

and smooth; in two of the three genera it is elongated, wedge-shaped, and dorsoventrally flattened.

Hartmann (1953) found essentially the same features in the species he considered truly interstitial,

with the one exception of Loxoconcha tuberosa.

The size of the species Hartmann reported (excluding L. tuberosa) ranged in length from 0.17 to

0.35 mm and in height from 0.06 to 0.18 mm. To

use such criteria for characterizing interstitial ostracods is hazardous at the present state of knowledge because many noninterstitial ostracods exhibit

similar carapace features.
94

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Little can be said concerning whether the appendages of interstitial forms differ from noninterstitial

forms. Elofson (1941)—as a result of his own work

and that of Miiller (1893, 1894), Remane (1933),

and Klie (1936)—stated that species living in sand

(and silt) do not exhibit any trends in appendage

morphology. According to Elofson (1941), some

species have medium-thick legs (Microcythere

Miiller and Microxestoleberk Mtiller) and others

have slender appendages (Psammocythere Klie).

The terminal claws of the appendages range from

short (in Microxestoleberis) to long (in Microcythere). But, as in the case of carapace features, these

criteria must be interpreted with caution because

species living in other biotopes exhibit similar appendage morphology.

Abundance and distribution of ostracods vary

primarily with food availability, substratum, and

season. Tietjen (1969) noted that abundance of ostracods increased with the increased abundance of

plant detritus. Mclntyre (1969) has summarized

the density of ostracods in intertidal and subtidal

habitats. The average number of specimens/10 cm2

in the intertidal from three types of sediment—

sand, mud, and coral sand—is 50, with mud having a higher density (218/10 cm2

) than sand

(28/10 cm2). In the subtidal, the average number

of specimens in five types of substrata—mud, sandgravel, sea-grass mud, sand, and mixed clay-sand—

was 17 specimens/10 cm2; the average number for

sand was 34/10 cm2 and the average for mud was

14/10 cm2.

Muus (1967) found that ostracod populations

showed small annual deviations, but with the largest fluctuations being found in winter and spring.

Kornicker (1964) and Kornicker and Wise

(1960a) found that living ostracods were more

abundant during the summer months, although

the abundance of one species remained approximately constant during the year. During a year's

study of New England estuaries, Tietjen (1969)

found that ostracods were most abundant in late

summer, fall, and winter.

Studies on the life history of benthic ostracods are

very sparse. The comprehensive study of Elofson

(1941) included field and laboratory observations

on the reproduction and development from copulation through molting, periodicity of development, and life span of many marine species from

Skagerrak. Elofson also summarized previous studies on the life history of ostracods. Theisen (1966)

studied the growth and reproduction of seven

brackish-water species from Denmark. Hulings

(1969) determined the life cycle of a myodocopid

based on field collections made weekly over a twoyear period in Hadley Harbor, Massachusetts. Hagerman studied the life cycle of several species associated with algae (Hagerman, 1966, 1968) and the

complete life cycle of Hirshamannia viridis

(Miiller), an algal-living species, in 0resund (Hagerman, 1969a).

The influence of environmental factors on

benthic ostracods has received little attention

through laboratory observations. Elofson (1941)

evaluated the influence of substratum, salinity, and

temperature. Kornicker and Wise (1960b), in studying a marine species, determined the salinity and

temperature tolerence, response to light, and sediment preference. Ganning (1966) determined the

salinity tolerance of a rockpool species found in

the northern Baltic. Hagerman (1969a) evaluated

various environmental factors determining the occurrence of Hirschmannia viridis in 0resund and

later (1969b) studied the respiration, anaerobic

survival, and locomotory periodicity of the same

species.

In ecological studies attempting to relate distribution or abundance it is of primary importance

that living specimens be used rather than dead

ones. Dead specimens may represent a select population and are subject to transport and concentration by currents, especially on beaches and in shallow subtidal areas. It has been shown that living

populations fluctuate considerably in certain areas,

and species diversity of dead populations is generally greater than the diversity of dead populations

(Kornicker and Wise, 1960a; Baker and Hulings,

1966; King and Kornicker, 1970).

Williams (1969) noted that there was considerable mixing of species from other biotopes including algae, plant detritus, and deeper water. Species

belonging to the deeper-water biotope usually were

represented by single valves and carapaces. It is important to be aware of potential mixing of species

from other biotopes and to emphasize the presence

of living specimens rather than dead ones.

It is obvious, therefore, that if valid ecological

studies are to be conducted the sampling must be
NUMBER 76 95

for living ostracods and repeated over a sufficient

period of time to take into account seasonal variation in physical, chemical, and biological variables.

And certainly, the taxonomic problems must be resolved so that ecological studies are meaningful.

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1966. Recent Marine Ostracod Assemblages of Puerto

Rico. Publications of the Institute of Marine

Science, 11:107-125.

Elofson, O.

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Canning, B.

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Hagerman, L.

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serratus L., with some Ecological Remarks.

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di Napoli, supplemento 33:550-587.

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1966. Marine Ostracoda from the Western North Atlantic

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1964. The Ostracod Genus Cyprideis in the Americas.

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1967. Study of Microfossils by Means of the Scanning

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1951. Animal Production in the Danish Waddensea.

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1825. The Mineral Conchology of Britain. Volume 5.

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1964. The Interstitial Fauna of Marine Sand. Biological

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Theisen, B. F.

1966. The Life History of Seven Species of Ostracods from

a Danish Brackish-Water Locality. Meddelelser fra

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Tietjen, J. H.

1969. The Ecology of Shallow Water Meiofauna in Two

New England Estuaries. Oecologia, 2:251-291.

Triebel, E.

1941. Zur Morphologie und Okologie der fossilen Ostracoden. Senckenbergiana, 23:294-400.

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1969. Ecology of the Ostracoda from Selected Marine

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Edinburgh: Oliver and Boyd.
Wolfram Noodt Ecology of the

Copepoda

ABSTRACT

The quantitative and qualitative importance of the

Copepoda in the meiobenthos is discussed. Most of

the families of Copedopa seem to be known but

much taxonomic work remains to be done, especially in the Harpacticoida. Very little is known

of the species biology of the benthic Copepoda. A

number of morphological and biological evolutionary trends are defined. Based on these trends,

a system of evolution of "Lebensformtypen" is

given, including the origin of planktonic and parasitic forms. The ecological distribution in the

marine, brackish-water, and freshwater environments is discussed briefly.

The Copepoda are quantitatively and qualitatively

the most important group of the meiobenthos after

the Nematoda and before the Turbellaria, Gnathostomulida, Annelida, and Ostracoda. They

occur widely in the sea, quite often in brackish

water and fresh water, and in semiterrestrial habitats such as moss, humus, and rotten wood.

The Copepoda do not appear to be a very old

group of Crustacea. They may have originated in

shallow seas in the littoral environment during the

Middle Mesozoic, although sufficient information

as to their origin is lacking. The only fossils

known are from freshwater lake deposits of the

Miocene period.

During their morphological evolution, neoteny

and the tendency to dwarfism have played a part.

Thus, similar to the Cladocera, a new branch of

Crustacea has developed and it is still expanding.

The Copepoda, with 5,000 to 6,000 species, constitute about 12 percent of Recent Crustacea (Kastner, 1967). Of the existing copepod species someWolfram Noodt, Zoologisches Institut der Universitdt,

Hegewischstrasse 3, D-23 Kiel, West Germany.

what more than half are described. In the

Harpacticoida a doubling of the list of species is to

be expected. Much taxonomic work remains to be

done, especially with marine copepods; nevertheless, the majority of existing families appear to be

known. This situation (according to unpublished

information) seems likely to hold also for the copepods of the deep-sea benthos.

Among the Copepoda is a very obvious and

enormous variety of morphological forms which

are adapted to special conditions in the various

habitats ("Lebensformtypen," Remane, 1952;

Koepcke, 1955). The analysis of this variation,

however, is still in the pioneer stages. Nevertheless,

it seems worthwhile to attempt a provisional classification of these forms in order to stimulate research in this area. Thus, it seems necessary to

evaluate different "trends" in specialization of Copepoda. The characters given below are regarded

as derived or apomorphic, as opposed to conservative or plesiomorphic (Hennig, 1950, 1957).

(a) There have been progressive reductions in

body size to a minimum of about 180 p.; pigmentation and eyes, especially in subterranean and deepsea forms; numbers of articles, setae, and hairs of

appendages; overall egg number, from about 40 to

60 (or more) to 1 to 2 per brood; and possibly development through disappearance of certain naupliar or copepodid stages.

(b) Progressive morphological specializations

have occurred in the body away from the basic

primitive, somewhat cyclopoidean, type towards

new, more specialized forms; these have included

specialization of the caudal furca, the first antenna,

and sometimes certain other appendages for special

functions; and more efficient development of structures protecting the brood mostly formed by the

fifth pereiopods.

(c) Progressive ecological specializations have

occurred in numerous lineages through increasing

97
98

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

preference for particular substrates (stenoecious

forms); and probably in association with this specialization of diet, of which very little is known;

increasing stenothermy; increasing euryhalinity in

connection with colonization in brackish water and

fresh water (cases of secondary colonization of seawater from freshwater forms are rare); loss of abil

ity to swim (endobenthos and mesobenthos) ; complete independence from contact with the substrate

in eupelagic forms; development of parthenogenesis,

especially in freshwater forms, in which parthenogenesis may be complete, periodic or geographic;

elimination of brood-sacs ("Brutpflege") with eggs

deposited freely; evolution of cysts, eggs, etc., which

are resistant to desiccation, especially in freshwater

forms, perhaps also in certain forms of the marine

and brackish littoral, and in forms of inland salt

waters; and development of parasitic forms through

the following stages: associated forms-ectoparasitesendoparasites.

It must be emphasized that many of these specializations are not necessarily to be seen as

irreversible. Changes in specializations are, obviously, not uncommon in copepod phylogeny.

Thus, the theoretically reconstructed schemes of

ecological and partly morphological specialization

lose their significance for evaluating particular

cases. Such an evaluation will be changed only by

a thorough analysis of each genus, family, etc. Toward this end, as always in systematics, it will be

necessary to make the direct transformation from

ecological investigations (given below) to determinations of the natural affinities, i.e., the real phylogenetic sequence.

The hypothetical ancestral form of Copepoda is

envisioned to be a rather small (2 to 8 mm),

free-swimming, epibiontic marine form of cyclopoidan appearance that probably feeds by seizing

larger particles rather than by filtering. Ecologically

and biologically, several recent groups still resemble this ancestral form and must be placed in the

center of our ecological system (Figure 1). The

different, derived ecological types are characterized

in the following outline.

(A) Tisbe Lilljeborg-Taefiidius Lilljeborg type, possibly resembling the ancestral type ecologically. Members of

this group are cyclopoidean in appearance, rather small

(about 1 mm) , and epibiontic. They swim well, either

continuously or intermittently, near the surface of the

substrate; graze on algae and plant and animal detritus;

and perhaps are predatory on other smaller organisms.

In this group are included several frequent inhabitants

of calm water and of substrates rich in detritus and

diatoms and some inhabitants of brackish water. Often

there is a large number of eggs. Examples of this group

include Tisbidae (partim), Tachididae, and epibiontic

Cyclopoida gnathostoma.

(B) Phytal living forms, possibly mostly derived from Type

A:

(1) Thalestridae type.—Forms vary from cyclopoidan to

pear-shaped; the cross-section is deeply curved; size

ranges from 0.4 to 1.5 mm; often there is a welldeveloped clinging apparatus. The forms often are

brightly colored and are capable of free swimming;

they feed on microalgae and detritus; and the number of eggs is large. This type lives especially in the

phytal, but also in calm waters on substrates rich

in detritus. Examples include Thalestridae, Harpacticidae, Diosaccidae (partim), and Cyclopoida

gnathostoma (partim). More-specialized phytal-living

forms (Type B2) probably are derived from this

type.

(2) Scutellidium Claus-Porcellidium Claus type.—From

flattened, shield-shaped, of middle size (about 0.7

mm). These animals cling closely to the substrate

but still are good swimmers; have reduced egg

numbers and brood pouches; and are especially

adapted to the smooth, flat surfaces of Phaeophycea.

Food not known. Examples include Zausodiinae,

Tisbidae (partim), Porcellidiidae, and Peltidiidae.

(3) Tegastes Norman type.—Small, laterally compressed

forms (less than 0.6 mm) resembling amphipods.

They swim rapidly but cling closely to the substrate

while feeding; they live in the phytal. Egg number

is low. Group includes only Tegastidae.

(C) Sediment-living forms increasingly specialized, derived

from more or less euryoecious forms.

(1) Ectinosoma Boeck type.—Torpedo-shaped forms

round in cross-section; size 0.5 to 1.2 mm; often

brightly brownish colored; good swimmers living in

the phytal, smaller forms also in the mesopsammon;

crawl actively in detritus and algae; feed on detritus

and algae. Egg number small to medium. Includes

most of the Ectinosomidae.

(2) Nitocra Boeck-Mesochra Boeck type.—Large and

slender, vermiform, round to oval in cross-section;

size 0.4 to 1 mm; without obvious specialization of

appendages; mostly good swimmers; feed on detritus and microalgae; egg number medium. Live

on sand, soft bottom, and in the phytal (epifauna,

endofauna, and mesofauna). Examples include

Ameiridae, Canthocamptidae, Diosaccidae (partim),

Laophontidae (partim). Many transitional forms

to Type C3.

(3) Lepotcaris T. Scott-Stenocaris Sars type.—This type,

probably derived from Type C2, appears in several

families through analogous adaptations. Vermiform,

slender, cross-section round; length up to twelve
NUMBER 76 99

times breadth, 0.25 to 0.8 mm long; poor swimmers; feed mostly on detritus; number of eggs often

very low; typical vermiform, writhing inhabitants

of the mesopsammon; also live in ''organic" interstitial systems such as algae, wood, corals, gill

chambers of Brachyura; occasionally occupy detritus

layers of calm marine water, including littoral

and deep sea. Includes Ectinosomidae (partim),

D'Arcythompsoniidae, Diosaccidae (partim), Tetragonicepsidae (partim), Ameiridae (partim), Canthocamptidae (partim), Cylindropsyllidae, Parastenocarididae, and Laophontidae (partim).

(4) Asellopsis Brady and Robertson type.—Compact or

more slender with arched ventral contour; with

adhesive organs for clinging to and moving over

the surface and sand grains; medium size (0.5 to

0.8 mm) ; poor swimmers; browse on the surface of

sand grains (detritus and microalgae) ; egg number

small; epipsammonic and endopsammonic, penetrate

soft bottoms intermixed with sand. Includes Paramesochridae (partim), Cletodidae (partim), Laophontidae (partim), and Cyclopina (partim). Adaptational types have given rise to characteristic forms

of the mesopsammon by extreme reduction of body

size (Type A5).

(5) Paramesochra T. Scott-Leoptopsyllus T. Scott type.

—Small, cyclopoidan to vermiform, flat in crosssection (vermiform types nearly round) ; 0.2 to 0.6

mm long; mostly cling to the surface of sand

grains; practically unable to swim; feed on detritus;

egg number small; occur in the mesopsammon,

sometimes secondarily in the detritus layer of deepsea bottoms. The extreme vermiform type, e.g.,

Leptopsyllus, must here be regarded as apomorphic.

Body size of these forms is extremely reduced, approaching 200 ^i. Includes Paramesochridae and

Cyclopina (partim). Such highly developed forms

in the mesopsammon have their equivalents in

certain forms adopted to soft bottoms. Very little

is known about the biology of these soft-bottom

dwellers. It probably is necessary to distinguish at

least two types, C6 and C7.

(6) Nannopus Brady-Canuella T. and A. Scott type.—

Compact, vermiform, strong-bodied, burrowing

forms, round to oval in cross-section; medium to

large size (greater than 0.4 mm) ; frequently unable

to swim; feed on detritus or sediment; number of

eggs low; endopelos. Includes Longipediidae,

Canuellidae, Cletodidae (partim), and Laophontidae (partim) .

(7) Cervinia NoTman-Laophontodes T. Scott type.—

Cyclopoidan to elongate forms, flat to oval in

cross-section; often with striking spiny processess;

appendages often directed laterally to prevent sinking on soft bottom; medium to large size (0.4 to

2.5 mm) ; poor swimmers; feed on detritus or

sediment; number of eggs questionable; live on

soft bottoms, particularly in greater depths, and

probably on or near the surface of the substrate.

Includes Cerviniidae, Diosaccidae (partim), Cletodidae (partim), Laophontidae (partim), and Ancorabolidae.

(D) Free swimmers.—Probably derived from Type A.

(1) Pseudocyclops Brady type.—Cyclopoidan in form;

swim near the surface of the substrate or among

algae; medium to large size (1.0 to 1.5 mm, with

most 0.5 to 0.8 mm) ; swim continuously or intermittently, or float; filter-feed on detritus stirred up

by their own movements but probably also seize

larger particles; egg number high; live on bottoms

covered with detritus and in the phytal. Includes

Pseudocyclopinae, some Cyclopoida gnathostoma,

and some additional Calanoida.

(2) Euplanktonic forms.—Originating partly from Type

Dl, but partly (e.g., some Cyclopoida, some Harpacticoida) also in several parallel lines from

already strongly specialized bottom-living forms

(e.g., Microsetella Brady and Robertson). Closer

subdivision cannot be made here. The bulk of the

Calanoida is euplanktonic and forms a large and

richly diversified group of copepods.

(E) Parasitic forms.—Probably some thousands of species of

copepods live parasitically or in some close association

with host organisms. Among free-living copepods of

several different families are found so-called "association forms," some of which achieve a stronger attachment to their usually invertebrate hosts. Several lines

of ectoparasites have developed from such intermediate

forms, and some of these lines have given rise to highly

specialized endoparasites, most of which originate from

the "Cyclopoida siphonostoma." Their systematics remains to be clarified. Some interesting examples are

also found in the Harpacticoida. Several main sections

of the Copepoda are parasitic on fish. Little is known

of the biology and ontogeny of parasitic forms (Bocquet

and Stock, 1963).

Ecological distribution of the above-defined

types. As in many other marine groups of animals,

a great diversity of forms and species of the Copepoda lives in the marine littoral, especially in the

phytal and on detritus-rich sand and soft bottoms.

On such substrates in warm seas sometimes more

than 60 species per association are found; such species include representatives of nearly all ecological

types. Coarse marine sands, from subtidal to eulittoral, especially the detritus-rich "Amphioxus sand"

and shell, are inhabited by many species belonging to only a few highly specialized types (C2,

C3, C5). Eulittoral soft bottoms, on the other

hand, may be rich in individuals but poor in numbers of species, among which are found, however,

several specialized forms, such as C6 (Noodt, 1957;

Lorenzen, 1968, 1969). As yet no data on the
100 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

fauna of the deeper abyssal and hadal zones are

available. "Littoral" soft-bottom fauna (primarily

Cletodidae, Laophontidae, Ameiridae, and Diosaccidae) dominates to a depth of at least 2,000 m.

Below 3,000 m the proportion of Type C7—in

which are provisionally included bizarre deep-sea

forms such as Cervinia, Pontostratiotes Brady, Cerviniella Smirnow, Cerviniopsis Sars, Mesocletodes

Sars, and some Ancorabolidae—increases distinctly.

The proportion of "littoral" types, however, still

FIGURE 1.—Programmatic scheme of interrelationships between the most important types of

morphological adaptation ("Lebensformtypen") of the Copepoda. The primitive ancestral type

is represented in the center. The morphological types are arranged according to substrate.

Note the importance of detritus in nearly all environments.
NUMBER 76 101

appears to outnumber the endemic specialists even

in the hadal. Copepoda seem to be well represented in the greatest depths of the ocean. There is

as yet no evidence for the continued occurrence of

"living fossils" among copepods in the ecological

refuge of the deep sea (Bodin, 1968; Por, 1964,

1965; K. H. Becker, personal communication;

Noodt, unpublished observations).

On the whole, the fauna of soft bottoms, endopelos, appears to be very rich in highly specialized

forms, more so than the fauna of mesopsammon.

But forms typical of the mesopsammon (C3, more

of C5), obviously find adequate living conditions

in the detritus layer at great depths in the deep

sea, and this is of great importance in the geographical distribution of this fauna (e.g., Leptocaris, Cylindrotsyllidae, Paramesochridae).

How the copepod fauna changes in transition

from seawater to brackish water and fresh water. It

can be said that in Copepoda the reduction in

ecological types parallels or even exceeds the wellknown phenomenon of decrease of species number

in brackish waters (Remane 1952, 1959; Remane

and Schlieper, 1958). This applies in different degrees to different substrata. Most strongly affected

seems to be the fauna of the phytal (Cl-3). A

more or less unspecialized euryoecious copepod

fauna living on the surface of detritus usually

dominates in the mesohaline brackish water. Exceptions occur, especially in the subterranean zones

of eulittoral sandy beaches, in which a relatively

large proportion of sand-living forms of marine origin (C3 and less C5) reach oligohaline and even

fresh water (Noodt, 1957, 1969).

The rather monotonous picture of the copepod

fauna of brackish water remains much the same in

fresh water. The dominant groups here are from

the Cyclopoida, some Calanoida, and Harpacticoida Canthocamptidae, whereas other groups (except for a few parasites) seldom venture into fresh

water. Freshwater benthos copepods mostly belong

to the less-specialized types, Bl and C2. On the

other hand, tendencies to greater specialization

exist, especially in the "organic" interstitial system

of wood, humus, and moss (e.g., Epactophanes

Mrazek, Moraria T. and A. Scott).

Again, the psammon occupies a special position.

In fresh water, mesopsammon copepods of marine

origin may predominate (types C2 and C3, e.g.,

Nitocrella Chappuis, Schizopera Sars, Parastenocaris Kessler, and type C5, e.g., small cyclopoids

like Graeteriella Brehm).

In this context, the question of the duration of

the phylogenetic history is of importance for biogeographic reasons. Some representatives (Parastenocaris and possibly Nitocrella) obviously are

relatively old immigrants. Others (e.g., Schizopera),

on the other hand, still have near relatives in the

marine environment (Noodt, 1957, 1969).

On the whole, freshwater copepods, including

the few eupelagic lines, although they do consist of

a fair number of species, present a rather monotonous picture in comparison with those of the sea.

Furthermore, the existing small diversity of forms

in fresh water is almost entirely of marine origin.

Fresh water has played no significant part as a center of evolution for benthic or planktonic copepoda.

Literature Cited

Bocquet, C, and J. H. Stock

1963. Some Recent Trends in Work on Parasitic Copepods. Oceanography and Marine Biological Annual

Review, 1:289-300.

Bodin, P.

1968. Copepodes Harpacticoides des etages bathyal et

abyssal du Golfe de Gascogne. Mimoires du Museum National d'Histoire Naturelle, series A 55(1):1-

107.

Hennig, W.

1950. Grundzuge einer Theorie der phylogenetischen

Systematik. Berlin.

1957. Systematik und Phylogenese. Bericht uber die

Hundertjahrfeier der Deutschen Entomologischen

Gesellschaft, pages 50-71.

Kastner, A.

1967. Lehrbuch der Speziellen Zoologie. I (2). Crustacea.

Jena: Verlag Fischer.

Koepcke, H. W.

1955. Las formas de vida y su significado ecologico.

Revista Pesqua y Caza, 6:64-68. Ministerio de Agricultura, Lima.

Lorenzen, S.

1968. Die Meiofauna an der Grenze Watt/Salzwiese im

Bereich der deutschen Nordseekiiste. Dissertation,

Universitat Kiel. 191 pages.

1969. Harpacticoiden aus lem lenitischen Watt und den

Salzwiesen der Nordseekiiste. Kieler Meeresforschung, 25:215-223.

Noodt, W.

1957. Zur Okologie der Harpacticoidea (Crust. Cop.) des

Eulitorals der deutschen Meereskiiste und der
102 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

angrenzenden Brackgewasser. Zeitschrift fur Morphologic und Qkologie der Tiere, 46:149-242.

1969. Substratspezifitat bei Brackwasser-Copepoden. Limnologica, 7(1):139-145.

Por, F. D.

1964. Les Harpacticoides (Crustacea, Copepoda) des fonds

muebles du Skagerak. Cahiers de Biologie Marine,

5:233-270.

1965. Harpacticoida (Crustacea, Copepoda) from Muddy

Bottoms Near Bergen. Sarsia, 21:1-16.

Remane, A.

1952. Die Besiedelung des Sandbodens im Meere und die

Bedeutung der Lebensformtypen fur die Okologie.

Zoologischer Anzeiger, Supplementband 16:327-359.

1956. Die Grundlagen des Naturlichen Systems, der Vergleichenden Anatomie und der Phylogenetik. 2.

Auflage. Leipzig: Geest und Portig.

Remane, A., and C. Schlieper

1958. Die Biologie des Brackwassers. 438 pages. Stuttgart:

E. Schweizerbart.
Irwin M. Newell Problems in the

Study of Subtidal

Halacaridae (Acari)

ABSTRACT

Techniques of collecting, zoogeography, systematics,

and preparation for study of subtidal Halacaridae

are discussed. A sliding box dredge for the collection of meiobenthos is described, illustrated, and

evaluated.

The Halacaridae, or marine mites, are one of the

best-represented metazoan taxa in the intertidal

zone, usually being outnumbered only by the Nematoda, Copepoda, and occasionally other groups

of small organisms. Despite this they are poorly

known by most workers on the intertidal fauna. In

subtidal habitats they are even more poorly

known. They generally are regarded as a "difficult

group," although in reality they need not be. On

the one hand, they are simpler in structure than

the Copepoda, Ostracoda, and other Crustacea. On

the other hand, they possess a great number of

clearly definable and relatively constant structural

features which make them easier to work with

than such groups as the Turbellaria, Tunicata,

Nemertinea, and other soft forms. In these, histological sectioning and other time-consuming techniques are frequently required to analyze the

rather variable morphos and establish criteria for

differentiating between taxa. As in other groups,

the significance of variation between individuals

and species of Halacaridae is not always easy to

evaluate, but the variations themselves are seldom

difficult to quantify. Rather clearly, then, whatever

Irwin M. Newell, Department of Life Sciences, University of

California, Riverside, California 92502. Work supported by

a grant (GB 5027) from the National Science Foundation to

the University of California, Riverside.

makes the Halacaridae a "difficult group" it is not

their structure or their rarity, but other things

which are examined here.

While the subtidal Halacaridae have been emphasized, much of what is reported here is applicable to the family as a whole. The special significance of the subtidal Halacaridae lies in the

numerical relationship between the subtidal and

the intertidal fauna. During Cruise 17 of the

Anton Bruun (Southeastern Biological Oceanographic Program), 33 species of subtidal Halacaridae were collected. Yet, it is estimated that this

number represented no more than 50 percent of

the subtidal species in that part of the southeastern Pacific covered by the cruise (Newell, in press),

and that the total subtidal forms from there eventually will reach 60 species or more. The intertidal

fauna of the Peru-Chile coast and the offshore island groups of Juan Fernandez and San Felix is

still largely undescribed, but a large part of it has

been examined and it appears unlikely that this

intertidal fauna will exceed 60 species, if indeed it

reaches that number. There is some overlap between intertidal and subtidal forms, but the majority probably will be distinct. If the same generalizations can be applied to other parts of the world,

then it would appear that one-half or more of the

living species of Halacaridae are found only below

tidal depths. Clearly, no study of the world fauna

of marine mites can be complete without vastly

greater attention being given to the subtidal fauna

than it has received heretofore.

Collecting Techniques

The specific gear for subtidal collecting will not be

discussed here, but only those principles which

should be incorporated into devices to improve the

103
104

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

efficiency of collecting meiobenthos, including Halacaridae. Subtidal Halacaridae are collected in a

variety of sampling devices. For nonquantitive

studies, the best results are obtained with devices

which cover a large area without digging deeply

into the sediment. In very deep waters (to 5,000 m

or more), some Halacaridae may live on the soft

sediments themselves, but it is more likely that

most of them will be found to be more abundant

on substrates like bryozoan-encrusted rocks, clumps

of hydroids, shells, etc., which are widely and unevenly scattered over the bottom. Small-diameter

coring devices are not suitable for collecting organisms with this type of distribution. Since the Halacaridae are probably limited to the upper few

millimeters of the bottom, grabs or other devices

which go deep into the sediments produce samples

which are difficult to process because the great bulk

of the sample consists of substrate unoccupied by

surface-dwelling forms. Trawls or sliding dredges

which collect only the thin surface layer should give

the best results in nonquantitative studies. But here

it must be remembered that the small size of subtidal Halacaridae (500 n down to 90 n) requires that

mesh size be much smaller than that usually used.

The best single haul of Cruise 17 of the Anton

Brnun was made with a canvas bag cut to fit the

frame of a Menzies trawl. This device brought up

307 Halacaridae, belonging to 10 species, and

many other animals from a depth of 485 m (Newell,

in press). Moreover, the mud, which is washed out

in coarse-mesh dredges, provided a protective matrix

that resulted in far better preservation of mites and

other delicate organisms.

Rigid metal box dredges of one design or another would have certain advantages over bag-type

dredges. They would minimize abrasion of the

specimens, reduce exposure to "winnowing" during

recovery, and protect the animals from extreme

temperature changes during the ascent. The latter

feature could be improved even further by insulated linings, but these have the disadvantage of

producing "bow-wave" effects, and many, but certainly not all, of the lighter organisms would be

pushed aside as the dredge moved over the bottom.

This disadvantage probably can be found in filtertype dredges to a greater degree than realized.

Very likely such dredges become so clogged with

fine sediments after a short time on the bottom

that little filtration occurs anyway, until the bag is

on its way to the surface.

A type of sliding box dredge recently developed

by the author for the collection of meiobenthos is

shown in Figure 1. This is a small prototype

model made for use from a small boat in shallow

waters, but the same principles could be incorporated in larger dredges operated from deep-sea research vessels. Thus far it has been used only on

sandy and rocky bottoms, and has brought up

large numbers of meiobenthos in an excellent state

of preservation. The box is of quarter-inch welded

aluminum, 21 by 10.5 by 3.5 inches outside dimensions, with the leading edges beveled. The baffled

plastic insert is designed to minimize winnowing

during recovery and also to prevent loss of the

sample while the dredge is passing over irregular

bottoms. The insert is held in place by a transverse

rod. The leading edge of the insert is fitted with

short metal "teeth" which keep rocks or sponges

from fouling the throat of the dredge. Thus, the

front section is essentially a rock dredge (Figure

\b). Sediments move into the dredge, sliding over

the bottom. Displaced water moves through the

holes in the plastic insert and exits at the front.

When the bottom chamber is filled, the top chamber then becomes filled, although retention of

lighter sediments probably is less efficient here.

The interior of the dredge is spray-coated with "Teflon" to minimize adhesion of mud. The dredge is

shackled to the cable centrally (Figure lb) so that

most of the working edge passes over undisturbed

bottom. This dredge is not a quantitative sampler,

but it is more effective in getting a good sample of

the meiofauna than are quantitative samplers.

Processing of samples on board is another critical phase in meiofaunal studies. Reports of most

deep-sea expeditions are notably lacking in records

of Halacaridae. Yet it is known that Halacaridae

occur to depths of over 5,000 m, which means that

at least 80 percent of the area of the world oceans

provides potential habitats for Halacaridae (Newell,

1967 and in press; Sokolov and Iankovskaya, 1968).

In many expeditions it has been standard practice to

place the haul on a shaker table or fixed screen of

1-mm mesh and "wash out the silt." This removes

the great majority of the meiofauna, of course,

leaving only the macrofauna. Clearly, such routine

practices must be discontinued if anything is to be
NUMBER 76 105

FIGURE 1.—a, Sliding box dredge with baffle plate removed. The baffle plate is held in place by

the long threaded rod. b, Attaching the shackle assemblage to the dredge. The eye of the

shackle assemblage turns freely on a central rod which is tapped to receive the heavy retaining

bolts. The weight (not shown) is "in line" with the cable.

learned about total fauna. Considering the great

cost of deep-sea work, it is doubtful if any biological expedition can be justified on the basis of

study of macrobenthos alone. At least a portion of

the effort must be allotted to the meiobenthos.

Zoogeographic Problems in Subtidal Halacaridae

From the foregoing remarks it should be apparent

that not enough has been learned of subtidal Halacaridae to provide more than the slighest glimpse

of the total picture of the world fauna. The following discussion is based in part on unpublished

information, undescribed species, and a certain

amount of conjecture. Nevertheless, it serves to

pinpoint some of the directions in which future efforts should be aimed.

To what extent is endemism developed in the

subtidal fauna? The author has seen collections

from subtidal faunas from several parts of the

world, including the Antarctic, southeastern Pacific, Indian Ocean, Bering Sea, and Artie Ocean.

These collections are by no means complete, but

they indicate that the differences between faunas in

these widely separated parts of the world are so

considerable that endemism must be quite high. It

is doubtful that there is any appreciable number

of cosmopolitan species, if any, even in the deep

sea. Most genera appear to be cosmopolitan in subtidal habitats, but even here there are notable exceptions—for example, in the genus Werthella

Lohmann, confined to the southern hemisphere on

the basis of present information.

There are other interesting patterns in the distribution of certain taxa. Arhodeoporus Newell has

been seen subtidally from the Arctic, Indian

Ocean, southeastern Pacific, North Atlantic, and

Mediterranean (Newell, 1947). In the North At-
106

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

lantic and Mediterranean it is represented by intertidal forms as well. This raises the question

whether the intertidal occurrence in the North Atlantic is a primitive or a recent development. In

line with the hypothesis that the North Atlantic is

a relatively young ocean, it would appear that the

latter might be the case. This also parallels the distribution of the genera Rhombognathides Viets

and Metarhombognathus Newell, both restricted to

intertidal and shallow subtidal waters of the North

Atlantic, which would mark them as relatively recent groups (Viets, 1927; Newell, 1947). These

are somewhat speculative points, but the alternatives appear to be few and somewhat less probable.

Recent developments in marine and terrestrial geology, paleomagnetism, etc., strongly support Wegener's theory of the origin of the Atlantic through

continental drift. The Halacaridae promise to be

an excellent group in which to study the faunistic

effects of continental drift.

Systematic Problems

One of the indispensable ingredients of good zoogeography is good systematics. The principal systematic problems in the Halacaridae stem from the

lack of accurate descriptions and illustrations.

Many of the best structural characters that could

be used in this group have never appeared in published keys or descriptions. For example, earlier

writers paid almost no attention to the setae of

Halacaridae, except some of the more obvious ones

on the palpi and on the legs. The setae of the idiosoma (body), the rostrum, and the specialized

setae of the tarsi essentially went unnoticed. The

setae of the idiosoma show important interspecific

differences in position relative to the plates and in

length and form, and these must be carefully described. The same also is true of the setae of the

gnathosoma, some of which have significance at the

generic level, yet they are not even mentioned in

keys and diagnoses, nor shown in figures, except in

occasional and sporadic instances. As a consequence, there are a number of species whose true

generic position cannot be resolved without reference to types or topotypic material, both of which

are expensive and time-consuming. The alternative

is to postpone final resolution of these problems,

which lead to perpetuation of errors in the literature. Examples of such errors are found in relation

to Agaue aculeata (Trouessart), Werthella bouvieri

Trouessart, and Agaue affinis Sokolov. It is suspected that all of these belong in genera other

than the ones to which they are presently assigned,

but there is no way this can be resolved from

existing descriptions, simply because the critical

characters have been overlooked.

Mounting Problems

Unquestionably, the source of many of the systematic problems in the Halacaridae is in the techniques used in preparation of material for study.

Standard practice of many workers in the Halacaridae is to mount specimens in Hoyer's (or Marc

Andre's) medium, or similar media. The refractive

index of these media is such that many important

setal characters have gone unobserved. The advent

of phase microscopy has made such preparations

easier to study, but the important problem of permanence still remains. Hoyer's mounts simply are

not permanent, and while, presumably, there are

techniques to make them permanent, none has

ever stood the test of time. Ringing is the procedure usually recommended, but the results are inconsistent. Trouessart's vitally important type

slides of Halacaridae were faithfully ringed (with

black asphaltum or shellac?), and the closest examination of most of these slides reveals no visible

cracks or separation between glass and sealant. Yet,

without exception, these mounts have dried so

completely that the coverslip in all cases is deformed even to the point of cracking over the specimen, and more than 90 percent of the specimens

are completely surrounded by air. Even when successful, ringing is a time-consuming process, which

often must be repeated two or three times.

Remounting is always possible, but it is timeconsuming and risky. Again, in the Trouessart

collection of Halacaridae several specimens have

been remounted with disastrous results. Appendages

are lost, setae broken, rostrums are badly deformed, etc., making specimens truly worthless for

descriptive purposes. Over-compression of the specimens by shrinkage of the medium has obliterated setae, destroyed surface detail, and produced

artifacts of many kinds. These changes are irrever-
NUMBER 76 107

sible, and even careful remounting by an experienced worker cannot restore the details.

Polyvinyl alcohol, lactophenol media, all have

their adherents, but none of these media has yet

withstood the test of time. A large portion of the

mite collection of the South Australia Museum, in

eluding many types, is totally unusable because it

was mounted in polyvinyl alcohol. In the writer's

experience, only two media of acceptable refractive

index have withstood the test of time, namely

Hyrax and glycerin. Of these, Hyrax is preferable

because it gives more rigid support, is easily adaptable to reversible-mount techniques, and is permanent. A question frequently asked is whether it is

easy to remount from Hyrax. The answer is yes,

but remounting usually is unnecessary. Ringing is

not required, either. The specimens are held rigidly so that oil immersion examination is possible

immediately after labeling. Changes in position of

the mites, or the legs, can be achieved, while examining under the microscope, simply by heating the

slide and pushing and/or compressing the coverslip

until the desired position is achieved. Upon cooling, the mount is rigid again. Compression of specimens to enhance resolution is accomplished in the

same way. Remounting is necessary only if a dissection of a previously mounted specimen is desired.

The oldest Hyrax preparations were made by the

author 30 years ago, and they are as good as the

day they were made, in all respects.

The only disadvantage of the Hyrax technique

is that it requires considerable "tooling up." But

once this has been done, mites can be put into

Hyrax as quickly as into Hoyer's medium on a

per-specimen basis, and this has been tested by detailed time analyses. In 30 years more than 200,000

mites have been mounted in Hyrax by the author

and his assistants. Evidently the Hyrax technique

is not as time-consuming as generally thought.

When one considers the time saved in remounting,

the elimination of ringing, the superior optical

qualities of Hyrax, the simplicity of making reversible mounts, and the total lack of crystallization

and other forms of deterioration which plague the

"simpler" techniques, there appears to be no good

reason for using any mounting medium which is

less durable, has less desirable optical properties,

and which requires just as much time as Hyrax.

The details of the Hyrax technique are given in

Hulings and Gray (1971).

Literature Cited

Hulings, N. C, and J. S. Gray

1971. A Manual for the Study of Meiofauna. Smithsonian Contributions to Zoology, 78:1-83.

Lohmann, H.

1907. Die Meeresmilben der deutschen Siidpolar-Expedition 1901-1903. Deutschen Siidpolar-Expedition,

1(5): 361-413.

Newell, I. M.

1947. A Systematic and Ecological Study of the Halacaridae of Eastern North America. Bulletin of the

Bingham Oceanographic Collection, 10(3): 1-266.

1967. Abyssal Halacaridae (Acari) from the Southeast

Pacific. Pacific Insects, 9(4):693-708.

In press. Halacaridae (Acari) Collected During Cruise 17

of the Anton Bruun, in the Southeastern Pacific

Ocean. Anton Bruun Reports.

Sokolov, I.

1962. New Species of Halacarids from the Antarctic.

Academy of Science of the U.S.SJl., Explorations

of the Fauna of the Seas, Biological Results of the

Soi'iet Antarctic Expedition (1955-1958), l(9):190-

195.

Sokolov, I., and A. I. Iankovskaya

1968. Pervii abyssalnyi predstravitel Halacaridae (Acari)

is raiiona Kurilo-Kamchatskoii vladiny. Doklady

Akademii Nauk SSSR, 179(2):486-488.

Trouessart, E.

1896. Note preliminaire sur les Acariens marins drague a

de grandes profondeurs par M. Koehler dans le

Golfe de Gascogne (Aout-Septembre 1895). Bulletin

de la Socie'te Zoologique de France, 21:102-105.

1914. Acariens. Deuxieme Expedition Antartique Franca ise (1908-1910), pages 1-16.

Viets, K.

1927. Die Halacaridie der Nordsee. Zeitschrift fiir wissenschaftliche Zoologie, 13O(l-2):83-173.

Jeanne Renaud-Mornant and

Leland W. Pollock

A Review of the

Systematics and Ecology

of Marine Tardigrada

ABSTRACT

The affinities, morphology, embryonic develop

ment, systematics, and ecology of the phylum Tardigrada are discussed. A key to the genera is given.

The Tardigrada comprise a well-defined group of

uncertain position, perhaps near the base of the arthropod branch but with affinities suggesting aschelminth relationships. The size rarely exceeds

one millimeter, and the body is stout, bilaterally

symmetrical, superficially annulated, enveloped in

a cuticle, and possesses four pairs of legs with toes

or claws. There are no nephridia (although lateral

and/or dorsal "excretory" structures are found in

most freshwater taxa), no circulatory apparatus,

and no respiratory structures.

The phylum consists of few genera and many

species—especially in freshwater and semiterrestral

habitats—whose affinities are uncertain and whose

characters show similarity to aschelminths, annelids, and arthropods. The aschelminth characters

include several embryological features, nonchitinous cuticle, absence of circular muscles, similarity

in feeding parts and digestive system, and a pseudocoelous body cavity in adults. The annelid characters include a ladder-shaped nervous system and

cephalic appendages. Arthropod characters include

metamerism of the cuticle, growth through molting, and absence of cilia.

In the general scheme of organization, the

Jeanne Renaud-Mornant, MusSum National d'Histoire

Naturelle, 43 Rue Cuvier, Paris V* France. Leland W. Pollock, Systematics-Ecology Program, Marine Biological Laboratory, Woods Hole, Massachusetts 02543.

cuticle is thin, transparent, and (in most marine

species) punctate. It can form into thick ornamented plates in semiterrestral species (plated

Echiniscoidea). Cuticular expansions may be very

important in marine Heterotardigrada such as

Florarctus Delamare Deboutteville and RenaudMornant, Actinarctus Schulz, and Parastygarctus

Renaud-Debyser. In most genera, long cirri (cirrus

E) are located laterally in the posterior portion of

the body. In addition, cephalic appendages in the

form of cirri are present only in the Heterotardigrada and separate them from the Eutardigrada

(Figures 1 and 2). The cephalic appendages include unpaired median cirrus, paired internal median cirri, paired external median cirri, and paired

lateral cirri, each associated with a clava.

There are four pairs of legs, of which the first

three pairs are anteriorly directed and the terminal

pair is posteriorly directed. Each leg terminates

with claws or papillae-bearing toes, or both. Legs

usually are retractable and telescope to the point

that the claws disappear within the leg sheath.

The muscles are composed of striated fibers

forming ventral and dorsal longitudinal bands as

well as dorsolateral and ventrolateral bands. Circular muscles do not occur. There are pedal retractor

muscles and pharyngeal muscles which control the

buccal apparatus.

The nervous system consists of a brain that is

relatively large and is formed in four or five dorsal

lobes. A circumesophageal ring connects the brain

to a ventral nerve chain, which includes two main

trunks connecting ganglia corresponding to each

leg pair. The brain innervates the cephalic appendages (cirri) and possibly the clava. Some tardigrades possess eyes inserted directly on the brain.

The digestive tract consists of a foregut, midgut,

and hindgut. The foregut and midgut are lined

109
110

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

FIGURE 1.—Batillipes mirus, a primitive marine tardigrade with cephalic cirri and toes.

with cuticle and a buccal canal with a pharyngeal

bulb and stylets followed by a short esophagus

leading to a large diverticulated intestine. The

buccal apparatus is complex and important in systematics. In Heterotardigrada stylet supports may

or may not be present. In Eutardigrada (Figure 3)

the cuticular pieces within the bulb ("placoids")

differ in shape and number among the species. On

each side of the buccal canal are two large "salivary glands." These glands play a role in the reformation of a new buccal apparatus during molting.

The intestine is usually filled with a reserve of nutritive material, of vegetal origin, colored brown,

green, or red. In the Heterotardigrada defecation

occurs during molting and products are deposited

in the shed cuticle. The digestive system terminates

in an anus in Heterotardigrada and a cloaca in

Eutardigrada.

The body cavity of adult tardigrades may be a

pseudocoel, although one study suggests that enterocoelic pouches form and then disappear in early

embryology. A coelomic fluid containing numerous

free cells in suspension fills the cavity of eutardigrades. Constant agitation of these cells by the

movements of the body and internal organs functions as a circulatory system. Glands of unknown

function are connected to the posterior part of the

intestine in Eutardigrada only.

Reproductive organs are located dorsally above

the intestine. In tardigrades sexes are always separate. From the sack-shaped gonad leads two vasa

deferentia in males or a single oviduct in females.

FIGURE 2.—Macrobiotus sp., a terrestrial tardigrade without cephalic cirri and toes.
NUMBER 76 111

FIGURE 3.—Buccal apparatus, a, Eutardigrada;

b, Heterotardigrada.

These ducts pass around the intestine and rectum

and exit ventrally. In some Heterotardigrada there

is dimorphism in the shape and location of gonopores, which are located anterior to the anus. In

Eutardigrada gonoducts open directly into the intestine, forming a cloaca.

Methods of fertilization and egg deposition are

unknown in marine heterotardigrades. In eutardigrades, which are mostly semiterrestrial, eggs are

deposited into a recently shed cuticle or in some

other similarly protective location. Other eutardigrades produce highly ornamented eggs which become entrapped in the substratum and are protected from damage. The pattern of these egg-shell

elaborations is used in taxonomy of these species.

Postembryonic development is direct in

Eutardigrada, and the young closely resemble the

adults. In Heterotardigrada, acquisition of the

trunk and caudal appendages is accomplished in

several successive molts. The number of toes or

claws is always reduced in the young. During molting, egress occurs through an opening in the head

region. The old buccal apparatus is lost and a new

one forms during molting. The pedal glands play

an important role in the production of new feet,

toes, and claws.

Table 1 shows the major lines of classification of

Tardigrada suggested by Ramazzotti (1962). A key

to the genera is given below. Two large orders inTABLE 1.—Major lines of classification of phylum Tardigrada.

(Modified from Ramazzotti, 1962.)

1. Order Heterotardigrada

1. Suborder Arthrotardigrada

1. Family Halechiniscidae

1. Florarctus

2. Halechiniscus

3. Pleocola

4. Actinarctus

5. Tetrakentron

6. Styraconyx

7. Tanarctus

2. Family Batillipedidae

1. Batillipes

2. Orzeliscus

3. Family Stygarctidae

1. Stygarctus

2. Parastygarctus

2. Suborder Echiniscoidea

1. Family Oreellidae

1. Oreella

2. Echiniscoides

3. Archechiniscus

2. Family Echiniscidae

1. Echiniscus

2. Parechiniscus

3. Pseudechiniscus

4. Mopsechiniscus

2. Order Mesotardigrada

1. Family Thermozodiidae

1. Thermozodium

3. Order Eutardigrada

1. Family Macrobiotidae

1. Macrobiotus

2. Haplomacrobiotus

3. Hypsibius

4. Itaquascon

2. Family Milnesiidae

1. Milnesium

elude most of the genera, while an intermediate

order possesses only one species from a single locality. Nearly all marine Tardigrada belong to the

Heterotardigrada and are found in the most primitive families of the suborder Arthrotardigrada. In

the suborder Echiniscoides only Archechiniscus

Schulz and Echiniscoides Plate are marine (Figure

4).

Principal characters used in systematics include

the following: presence or absence of the median

cirrus separates the suborders of the Heterotardigrada, as does the presence or absence of toes (Figures 5 and 6) ; distinctive characters of the Eutardigrada are limited to the pharynx placoids and

the claw shape (Figures 7 and 8). There are no sub-
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Key to the Genera of Tardigrada

1. With lateral cephalic cirri (cirrus A) 2

Without lateral cephalic cirri (cirrus A). (Order Eutardigrada) 20

2. Bulbus including dearly separated placoids. (Order Mesotardigrada)....Thermozodium Rahn

Clearly separated placoids lacking. (Order Heterotardigrada) 3

3. With median cephalic cirrus. (Marine) 4

Without median cephalic cirrus 13

4. Body surface with a gelatinous coating including spines Actinarctus Schulz

Body surface without such coating and processes 5

5. Distal end of leg without toes, claws inserted on foot; dorsal plates present on body 6

Distal end of legs with toes 7

6. Head transversally separated in two parts; posterior cephalic plate bearing expanded lateral

processes Parastygarctus Renaud-Debyser

Head not separated into plates; cephalic plate simple without expanded lateral process

Stygarctus Schulz

7. Distal end of toes bearing adhesory discs, or rodlike appendages 8

Distal end of toes bearing claws 9

8. Six toes of different size with spoon-shaped appendages Batillipes Richters

Four toes of similar size with rodlike appendages Oneliscus Bois-Reymond-Marcus

9. Four toes arranged in two different pairs with heterogenous claws; body cuticle with large

lateral aliform processes Florarctus Delamare Deboutteville and Renaud-Mornant

Four similar toes (homodactylous) 10

10. Claws with accessory spurs 11

Claws without accessory spurs 12

11. Body dorsoventrally flattened: lives on Synapta tentacles Tetrakentron Cuenot

Body not dorsoventrally flattened Styraconyx Thulin

12. Clava shorter than lateral cirrus (A), 16 p maximum Pleocola Cantacuzene

Clava longer than lateral cirrus (A), more than 15 /* Halechiniscus Richters

13. Distal end of leg with unequally long toes; or even toes reduced to a small membrane.

(Marine) 14

Distal end of leg without toes, bearing only unstalked claws 15

14. Distal end of leg with two median toes bearing claws, and two lateral claws inserted on

the leg on a short membrane or papillae Archechiniscus Schulz

All daws inserted on toes; hind end bilobed with long cirri Tanarctus Renaud-Debyser

15. Dorsal plates of body cuticle poorly delimited 16

Dorsal cuticle partially or fully covered with thickened plates 17

16. With four claws on each leg Oreela Murray

With five to eleven daws on each leg. (Marine) •. Echiniscoides Plate

17. Dorsal plates not fully developed, only the posterior one is wholly thickened

Parechiniscus Cuenot

Dorsal plates fully developed, including a cephalic plate 18

18. Posterior plate adjacent to second paired plate or third unpaired plate....Echiniscus Schultze

Posterior plate separated from second paired plate or third unpaired plate by a transverse

paired or unpaired plate 19

19. Without buccal internal and external paired cirri Mopsechiniscus Bois-Reymond-Marcus

With buccal internal and external rirri Pseudechiniscus Thulin

20. Mouth surrounded by six rostral and two lateral or ventrolateral papillae; bulbus without

placoids Milnesium Doyere

Mouth not surrounded by papillae 21

21. Legs with two simple, distally bifid claws Haplomacrobiotus May

Legs with two double claws 22

22. The two double-claws are of the same size and symmetrically distributed from the median

axis of the leg Macrobiotic Schultze

The two double-claws are a little or very much different in size and shape and always

asymmetrical from the median axis of the leg 23

23. Bulbus always without placoids Itaquascon Barros

Bulbus with placoids (except in larval stages or during pre-ecdysis time)

Hypsibius Ehrenberg
NUMBER 76 113

FIGURE 4.—Plates of echiniscids. Pseudechiniscus (right,

shaded area) has an additional plate.

borders of Eutardigrada because it is a very homogenous group.

Until recently, marine tardigrades have been reported rarely, and studies of their ecology are few.

Extensive studies of Tardigrada populations appear in the works of Renaud-Debyser (1956,

1959a,b, 1963) and de Zio and Grimaldi (1966).

At present marine tardigrades may be grouped

generally according to habitat: (1) some genera

are limited strictly to interstitial spaces, leading a

subterranean life within the sediment; (2) others

live on algae or vegetal debris, usually in surface

sediments; and (3) others appear to be commensal

on marine invertebrates.

Interstitial or subterranean species which form a

part of the mesopsammon are not always strictly

limited to a specific type of sediment but are able

to colonize sands of different composition. In silicious sand Halechiniscus Richters, Batillipes Richters, and Stygarctus Schulz are frequently found,

but all three also are found in entirely calcareous

coralline sands. Other genera seem more restricted.

Orzeliscus Bois-Reymond-Marcus and Actinarctus

are most frequent in "Amphioxus sand," which is

silicious but contains a large proportion of shell

debris and other calcareous materials. To date,

Tanarctus Renaud-Debyser and Florarctus have

been found only at the surface or in deeper layers

of coralline sands. Parastygarctus can be found in

coralline sand containing a relatively large fraction

of silicious elements.

Certain genera and species are epizoic and are

not limited to intragranular spaces. One often

finds them associated with algal debris settling at

the sediment surface. Included here are Styraconyx

Thulin, Echiniscoides, and Archechiniscus.

Finally, among marine tardigrades are commensal species such as Tetrakentron synaptae Cue'not,

which lives on the tentacles of Synapta galliennii

Herapath. Three other species have been reported

in apparently commensal relationships and are

free-living as well. Echiniscoides sigismundi (Schulz)

has been found within the mantle cavity of mussels,

and Actinarctus doryphorus Schulz has been recorded as an ectoparasite of the echinoid Echinocyamus pusillus (O.F. Miiller). Recently, the junior

author found free-living Plecola limnoriae Cantacuzene in coralline sand from the Bahamas. This

species originally was described from the pleopods

of the isopod Limnoria lignorum (Rathke).

Mesopsammic tardigrades are found from the

high-tide region to the low-tide region along intertidal beaches, and as deep as 1.5 m in the sand.

They show a continuous pattern of distribution

where the settling of sand and the circulation of

water (permeability and slope) permit good oxygenation of the "milieu." For example, Halechiniscus can be found in higher levels of the shore and

Stygarctus occurs in great density at 40 to 60 cm

depth in the sand at the midtide level. Batillipes is

most common in the lower half of the beach, as

are Parastygarctus and Archechiniscus. In atidal

beaches, Batillipes is found near the water's edge

and follows seasonal fluctuations of the water level.

Other genera are characterized by subtidal distributions. Actinarctus, Orzeliscus, and Halechiniscus

are found at several meters depth in "Amphioxus

sand" of the North Atlantic (North Sea, Gullmar

Fjord, and English Channel) ; and Florarctus, Archechiniscus, and Styraconyx are found in subtidal

corraline sand at depths between 2 and 4 m.

It appears that tardigrades may be rare in the

neritic zone. To date the only representative has

been Styraconyx, collected at 380 m. It is likely

that sampling gear and sorting methods are not

well adapted to collecting meiobenthos, and especially tardigrades. The use of such methods may

well be the reason for our lack of knowledge of

deep-sea tardigrades, which have been reported

from depths of 4,690 m.
114

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

FIGURE 5.—Claws of Heterotardigrada, mounted on toes, a, Orzeliscus sp.; b, Halechiniscus sp.;

c, Styraconyx sp.; d, Florarctus sp.; e, Archechiniscus sp.

Concerning geographical distribution, Batillipes,

Actinarctus, Tanarctus, Tetrakentron, Pleocola,

Stygarctus, and Florarctus are Atlantic or Mediterranean; Florarctus, Parastygarctus, Archechiniscus, and Batillipes have been found in the IndoPacific region; and Halechiniscus, Styraconyx,

Orzeliscus, and Batillipes are cosmopolitan.

Among ecological factors, granulometric characteristics are important. Authors have recorded tardigrade populations in silicious sand beaches of

grain sizes varying from 250 to 350 /A in mean

diameter at Arcachon (Renaud-Debyser, 1963) to

800 jx or larger on the east coast of the United

States (Pollock, manuscript in preparation). In

Malaysia, Parastygarctus was found in sand of relatively large grain, of 770 p. diameter. Within broad

limits, it does not seem that grain size by itself

plays a fundamental role in determining tardigrade distribution; however, the shape and arrangement of sediment components primarily determine intragranular living spaces.

The arrangement of sand grains is determined

by the shape of the particles and their settling.

Sorting and homogeneity also are important. Very

tight packing (rhombohedral) and clogging of interstices by fine elements are factors unfavorable to

colonization by tardigrades. It is important, therefore, to know the quantity of very small size particles present in the sediment. Renaud-Debyser and

Salvat (1963) expressed the results of their granulometric analyses as the number of grains in each

fraction clearly showing the amount of finer elements.

In tidal beaches, interstitial water is replaced by

each tide change, providing a fresh supply of oxygen-rich water throughout the beach. Important

displacements of fauna may be caused by this circulation, as shown by Renaud-Debyser (1963) particularly for Stygarctus at Arcachon. Other species

are influenced by the circulation of subterranean

water, especially in atidal beaches.

Seasonal changes affect both population densities
NUMBER 76

115

r.m.

FKURE 6.—Claws of stygarctids, with basal membranes but without toes, A, extended; B retractedc detached from legs, showing membranes. Symbols: a, appendage on median claws; c, claws';

h leg; m, membrane; r.m., retractor muscle.
116

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

FIGURE 7.—Claws: a, of echiniscids; b, of Haplomacrobiotus;

c, of Macrobiotus.

and distributions. Numerical variations may be extremely large. At Arcachon an extreme cold spell

severely reduced interstitial populations. Progressive repopulation occurred through the spring

months and resulted in maxima in May and autumn.

Thorough studies of tardigrade populations have

been developed only recently. Reasons for this are

the difficulties of sampling, extraction, and sorting;

the small size of the animals (especially larval

stages); and difficulty in distinguishing sexes of immature animals.

Marine Tardigrada are phytophagous "pumpsuckers," as shown by their buccal apparatus. The

stylets extrude through the mouth opening and

pierce the phytal material, the liquid contents of

which are pumped out by means of the muscular

pharynx. This food is stored in the intestinal diverticulae, where it is given a green, red, or brown

color. It is likely that the distribution of intertidal

Stygarctus bradypus Schulz is determined by the

presence or absence of abundant appropriate food

within the sediment. Large populations have been

found only within sheltered beaches located close

to abundant beds of Zostera Linne* at Arcachon

and of Sargassum C. Agardh or Thalassia Koenig

and Sims in the Bahamas. These plants are frequently detached from their substrate and washed

onto beaches where they provide abundant vegetal

debris for phytophagous tardigrades.

Regarding salinity, Renaud-Debyser and Salvat

(1963) have observed that tardigrades cannot withstand direct exposure on a beach where an outflow

of fresh water occurs. In the outflow area, the salinity is lowered during the ebb tide from 31 to 8

ppt, and the tardigrades disappear; however, in a

station immediately below, where mixing with the

water of imbibition elevates the salinity to 16 ppt,

the tardigrades recolonize the sediment. The remainder of the selective distribution of different

species along the tidal beach possibly is related to

tolerances of different species to changes in salinity

and other factors produced by the rhythm of tidal

variations.

A comprehensive bibliography on marine tardigrades including general and review articles, original species descriptions, ecological studies, etc., is

available from the authors upon request.

FIGURE 8.—Asymmetrical daws in two genera of Eutardigrada:

a, Hypsibius; b, Milnesium.

literature Cited

Ramazzotti, G.

1962. II Phylum Tardigrada. Memoire dell'Istituto Italiano di Idrobiologia, 14:1-595.

Renaud-Debyser, J.

1956. Repartition de deux Tardigrades, Batillipes mirus

Richters et Stygarctus bradypus Schulz dans un

segment de plage du Bassin d'Arcachon. Comptes

Rendus de I'Acadimie des Sciences, 243:1365-1369.

1959a. Sur quelque Tardigrades du Bassin d'Arcachon.

Vie et Milieu, 10:135-146.

1959b. £tudes sur la faune interstitielle des lies Bahamas.

III. Tardigrades. Vie et Milieu, 10:296-302.
NUMBER 76 117

1963. Recherches ecologique sur la faune interstitielle des tions en microfaune et macrofaune. Vie et Milieu,

sables. (Bassin d'Arcachon, He de Bimini, Bahamas). 14:465-550.

„. . ,,... , ,_ , ,-„ de Zio, S., and P. Grimaldi

Vie et Milieu, supplement 15:1-157. ,n ' , . , . , . ... .

1966. Ecological Aspects of Tardigrada Distribution in

Renaud-Debyser, J., and B. Salvat Sout h Adriati c Beaches. Veroffentlichungen des

1963. Elements de prosperite des biotopes des sediments Instituts fur Meeresforschung in Bremerhaven,

meubles intertidaux et ecologie de leurs popula- Supplementband 2:87-94.

F. Monniot Les Ascidies littorales

et profondes des

sediments meubles

ABSTRACT

The anatomy, methods of collecting and fixing,

techniques for studying, systematics, and ecology of

interstitial ascidians are reviewed. Consideration is

given to shallow-water and deep-sea species.

Les Ascidies du meiobenthos sont de de'couverte

r^cente. Les premieres Ascidies interstitielles ont

6t6 d^crites en 1961 par Weinstein. Elles provenaient de la zone littorale Me^diterran^enne du

Golfe du Lion. Les petites Ascidies des grandes

profondeurs, vivant dans les vases a Globige*rines

ont e"t£ de*crites d'une part a la suite de 1'expedition

de la Galathea, d'autre part tout r^cemment apres

les r^coltes des navires americains Atlantis, Atlantis

II et Chain.

Ces Ascidies vivent dans tous les cas sur des fonds

meubles. Elles sont de tr^s petite taille et habitent

les interstices entre les grains de sable pour les

Ascidies "interstitielles" ou entre les tests de Foraminiferes pour les Ascidies des grandes profondeurs. Les convergences de formes sont frappantes a

premiere vue. Les convergences anatomiques sont

plus e"tonnantes encore. La decouverte d'une me'iofaune de petits Procord&, bien que tres r^cente, a

deja permis une bien meilleure comprehension du

groupe des Ascidies grace a des Echelons eVolutifs

qui manquaient et a des formes d'organisation

insoupc,onnees jusqu'a present. Pour mieux comprendre l'apport des Ascidies de la meiofaune a

l'ensemble de ce groupe, il est n^cessaire de rap

peler leur schema d'organisation g^n^rale avec les

F. Monniot, Museum National d'Histoire Naturelle, Laboratoire de Biologic des Invertebres Marins, Paris, France.

caracteres les plus fre"quemment utilises en syst&natique.

Schema anatomique

Les Ascidies ont une structure generate assez simple, bien que chaque organe soit susceptible de

se compliquer ^norm^ment, je ne parlerai ici que

des Ascidies simples, les Ascidies composers £tant

exceptionnelles dans la me'iofaune.

L'animal (Figure 1) se compose d'un sac constitue1

par le manteau pero£ de deux orifices: les siphons.

L'un sert a l'entre^e, l'autre a la sortie de l'eau. Les

Ascidies fonctionnent comme un filtre. Le manteau

contient des fibres musculaires entrecroise'es et

secrete sur sa face externe une tunique plus ou

moins rigide et plus ou moins epaisse. Sur sa face

interne, le manteau supporte tous les organes, a

l'entre"e de l'orifice buccal il porte une couronne de

tentacules qui arretent les particules de trop grande

taille. Sous ces tentacules est suspendue une sorte

de poche a parois performs: la branchie, au fond de

la poche s'ouvre I'oesophage. L'eau est aspiree par

des battements ciliaires dans la poche branchiale.

Elle est filtre"e au niveau de multiples orifices a

bordure cilie^: les stigmates; elle sort dans la cavite"

g£ne"rale du corps ou cavite" peribranchiale, puis a

l'ext^rieur par l'orifice ou le siphon cloacal. La

ciliature retient au passage les particules nutritives

englue"es sur un film de mucus qui est, lui, dirige"

entre les stigmates vers I'oesophage. Le tube digestif

est relativement simple. L'estomac globuleux, couvert ou non de glandes h^patiques, d^bouche dans

un intestin tubulaire. Ce tube digestif de'crit une

boucle. II est attache de fac,on plus ou moins lache

au manteau. La branchie est retenue par quelques

trab^cules minces a la paroi du manteau. A l'etat

adulte des gonades hermaphrodites plus ou moins

119
120 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

nombreuses se deVeloppent sur la face interne du

manteau faisant saillie dans la cavite generate.

Oeufs et spermatozoides sont e'vacues par le siphon

cloacal avec l'eau sortant de la branchie et les

pelotes fecales.

Les systemes nerveux et vasculaire sont complexes; nous ne pouvons en parler ici en detail, ils

ne sont pas utilises en syst^matique. II existe un

ganglion nerveux ou cerveau qui determine la face

dorsale de 1'animal. L'excretion est assured par des

cellules a accumulation. II existe un rein chez les

Molgulidae seulement, il s'agit d'un organe clos.

siphon buccal

tunique

ganglion nerveux

tentacule

siphon cloacal

anus

branchie

gonade

manteau

cavite'

pe'ribranchiale

intestin

estoma

rhizoide

FIGURE I.—Schema anatomique d'une Ascidic.
NUMBER 76 121

Ce bref schema montre qu'il s'agit d'un animal

mou, deformable en tous sens, creux—les organes

ont toujours des epaisseurs tissulaires tres faibles.

Par contre, chacun d'eux, y compris la branchie,

contient des fibrilles musculaires entrecroisees qui

peuvent se contracter independamment les unes des

autres. L'animal richement innerve peut devenir

m^connaissable en etat de contraction. Cette contractibilite, bien connue chez les Ascidies, a de tres

nombreux inconv&iients: La taille des animaux

peut varier enormement (de 1 a 10); la forme du

corps ne peut que rarement etre precise; une

anestWsie est indispensable pour une etude correcte; et l'etude systematique ne peut avoir lieu

qu'apres fixation (48 heures minimum) pour durcir

les tissus, et surtout apres dissection. Une coloration

est ne"cessaire a cause de la minceur et souvent de

la transparence des tissus.

Mlthodes pratiques de recolte et de fixation

Comme nous l'avons vu pre'ce'demment, les tissus

tres minces des Ascidies sont enferme"s dans une

tunique epaisse, impermeable, herm^tiquement

close par la musculature puissante des siphons. Ces

tissus s'histolysent quand l'animal meurt et en

premier lieu la branchie. II y a une action importante des bacteries qui sont tres abondantes dans

toutes les cavite"s des Ascidies. Les animaux peuvent etre totalement liquefies sans que leur apparence externe aie change. Ce stade est atteint

d'autant plus vite que la temperature est plus

eleven.

Mais avant que l'histolyse ait commence, l'&at

des animaux peut etre tres mauvais: la contraction

musculaire est souvent irreversible et les tissus tres

minces restent definitivement plisses apres la fixation, interdisant toute etude anatomique precise.

Les Ascidies du meiobenthos contiennent tres

souvent dans leur branchie, leur cavite cloacale ou

leur tube digestif des particules sedimentaires. Au

cours des dragages, du tri, ou apres une forte contraction, ces particules minerales lesent les tissus

qui les contiennent.

La recolte des Ascidies s'effectue a la drague.

Pour que les animaux soient moins abimes il faut

que le coup de drague soit court, que le sediment

ne subisse pas un trop grand echauffement avant

le tri. II ne doit done pas etre garde au soleil et

etre conserve dans l'eau si possible. Le tri doit

s'effectuer dans les 24 heures qui suivent le dragage

pour le materiel vivant. Le tamisage abime beaucoup les Ascidies. La methode de tri par lavage et

flottation a donne les meilleurs resultats. Le fixateur est le formol neutre sale 5 pourcent. Les

animaux peuvent etre conserves indefiniment dans

le fixateur, mais il est preferable de les transferer

apres 15 jours de fixation dans l'alcool 75 pourcent

quarante-huit heures de fixation sont suffisantes

pour des animaux de tres petite taille. Tous les

fixateurs pour histologie conviennent, mails ils

donnent de moins bons resultats pour une etude

anatomique, les tissus sont generalement trop

durcis. Les fixateurs acides sont a eviter pour preserver les spicules eventuels.

Techniques de preparation

Les Ascidies fixees au formol neutre pendant

plusieurs jours sont conservees dans l'alcool 75

pourcent. Pour la dissection et la coloration elles

doivent etre progressivement rehydratees.

1. La tunique est debarrassee des particules sableuses qui

la couvrent. Cette operation doit etre fait a la pince

delicatement afin de ne pas dechirer la tunique qui y

adhere parfois fortement.

2. La tunique est enlevee avec precaution sans dechirer le

manteau qu'elle recouvre. Elle possede parfois plusieurs

couches. La region des siphons (tunique interne et

externe) est montee directement entre lame et lamelle

dans une goutte de gomme au chloral; les tissus sont

eclaircis et les spicules s'ils existent peuvent etre observes au microscope.

3. Le manteau est ouvert d'un siphon a l'autre selon la ligne

medio-ventrale, au-dessus de l'endostyle.

4. La branchie est detachee du manteau et des differents

organes en coupant les ponts dermatobranchiaux qui

la retiennent.

5. Coloration.

(a) Branchie: 3 a 5 minutes dans l'hemalun d/Masson.

Rincage 10 minutes dans l'eau; deshydratation

progressive a l'alcool jusqu'a l'alcool 95 pourcent

seulement. Passage a l'alcool butylique 5 a 10

minutes. Montgage au baume de Canada entre

lame et lamelle.

(b) Manteau: Les gonades et le tube digestif doivent

y rester accroches de facpn a conserver leur place

respective. Le deux siphons doivent etre bien

ecartes pour observer les tentacules. Coloration de

1 a 3 minutes seulement, selon l'age du colorant.

Les differents organes se colorent plus ou moins

intensement selon la proportion des tissus en
122

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

mature nudeaire. Le manteau reste assez pile

tandis que les gonades sont tres foncees. Par

contre les conduits genitaux restent clairs et

deviennent visibles sur les gonades. Apres rin^age

a l'eau, deshydratation jusqu'a l'alcool 95 pourcent puis alcool butylique. Montage au baume

de Canada.

Caracteres des Ascidies de la meiof aune:

leur reconnaissance dans le sediment

La taille des animaux est extr£mement r^duite. Les

Ascidies interstitielles mesurent 1 a 3 mm dans leur

grande longueur en extension. Les Ascidies des

vases a Globig^rines de 1 a 4 mm.

La forme est g£neralement arrondie ou en fuseau.

Certains animaux pr&entent des excroissances tunicales (Rhizoides) qui servent a leur ancrage dans

le sediment. Certaines especes peuvent fixer sur

leur tunique des grains de sable ou des Foraminiferes et s'en couvrir completement;

La coloration des Ascidies de la melofaune est

tres terne, grise ou jaunatre. II est rare que la

tunique soit transparente.

Certaines especes sont capables de mouvements

de reptation par allongement et retraction des

siphons et contractions alternees des diverses parties

du corps.

On confond souvent les Ascidies interstitielles

avec les jeunes Molgulidae dont les premiers stades

sont tout a fait comparables. Souvent, seule la

dissection permet de les distinguer. Leur aspect et

leur mode de contraction des qu'on les excite les

fait ressembler egalement a de jeunes Siponcles ou

a des petites Actinies r&ractees.

La systematique

La systematique des Ascidies simples (les Ascidies

composees sont des exceptions dans la m^iofaune)

est basee essentiellement sur la structure fine de la

branchie, la presence ou l'absence d'un rein, la

structure du tube digestif et des gonades. La

branchie joue un role preponderant. Elle peut se

presenter sous diverses formes (Figure 2 de gauche

a droite):

(a) Une lame tissulaire tres mince perforee d'orifices cilies

(Figure 2). II s'agit de la famille des Aplousobranches

a laquelle appartiennent la plupart des Ascidies composees. Aucune Ascidie de la meiofaune n'appartient

a cette famille jusqu'a present.

(b) Sur la lame branchiate dite fondamentale poussent des

papilles entre les stigmates du c6te interne. Ces papilles

s'elevent au-dessus de la lame fondamentale, se bifurquent, se rejoignent formant des sortes de ponts audessus des rangees de stigmate. Les stigmates peuvent

etre des simples trous ronds ou allonges mais Us

peuvent aussi s'enrouler en spirale. Dans ces ponts

passent des sinus sanguins. On appelle l'ensemble de

ces formations sinus longitudinaux.

L'ordre des Phlebobranches possede une branchie

avec des papilles ou des sinus longitudinaux.

Chez les Stolidobranches les sinus longitudinaux

peuvent se grouper, la branchie se plisse, les tissus

faisant saillie a l'inte>ieur du sac branchial. La surface de la lame branchiale est considerablement

augmentee.

Parmi les Stolidobranches on distingue trois

families.

Les Styelidae dont les stigmates sont droits c'esta-dire paralleles aux sinus longitudinaux comme

ce qui a ^te figure jusqu'a present. Les animaux ont

un estomac a cotes longitudinales, pas de foie, des

gonades hermaphrodites disperses sur le manteau,

pas de rein.

Les Pyuridae ont elles, des stigmates spirales a

l'origine, qui souvent sont tellement recouped qu'ils

donnent 1'impression d'etre droits. L'estomac est

partiellement couvert d'une glande h^patique. II

n'y a pas de rein. Dans cette famille la tunique

possede des spicules cornes. II y a parfois des

spicules calcaires.

Les Molgulidae ont toujours des stigmates

spirales, une glande h^patique et un rein.

Place des Ascidies du Meiobenthos dans la

systematique du groupe

Les Ascidies interstitielles et celles des grands fonds

appariennent aux 2 ordres des Phlebobranches et

des Stolidobranches, c'est-a-dire aux Ascidies qui

posseden des sinus longitudinaux. Tous les grands

types d'organisation sont representes. Quelques

exemples:

Phlebobranches

Interstitielles

Psammascidia teissieri Monniot

Dextrogaster suecica Monniot

Corella halli Kott

Grands fonds

Namiella bistigmata Monniot et Monniot
NUMBER 76 123

Stolidobranches

Styelidae

Interstitielles

Psammostyela delamarei Weinstein

Polycarpa pentarhiza Monniot

Polycarpa arnbackae Monniot

Grands fonds

Polycarpa pseudoalbatrossi Monniot et Monniot

Polycarpa delta Monniot et Monniot

Cnemidocarpa digonas Monniot et Monniot

Styela loculosa Monniot et Monniot

Bathystyeloides enderbyanus (Michaelsen)

Pyuridae

Interstitielles

Heterostigma fagei Monniot et Monniot

Heterostigma separ Arnback-Christie-Linde

Heterostigma reptans Monniot et Monniot

Heterostigma gonochorica Monniot

Molgulidae

Interstitielles

Molgula hirta Monniot

A ces Ascidies s'ajoutent une cate"gorie d'animaux

des grandes fonds sans branchie qui sont classes a

part dans la famille des Hexacrobylidae: Hexacrobylus indicus Oka et Gasterascidia sandersi

Monniot et Monniot.

Les Ascidies du m&obenthos ne rentrent pas

toujours facilement dans les cadres systematiques.

On peut les attribuer a une famille assez facilement

(apres coloration, dissection et montage des diffe^-

rents organes sur lame histologique). II est souvent

difficile de les placer dans un genre. Leur branchie

est souvent r&Iuite, avec quelques sinus longitudinaux, sans plis. Mais il s'agit d'une reduction

secondaire ou d'un caractere reste" juvenile. II arrive

tres souvent aussi que la branchie ne possede pas

encore de vrais stigmates. La syst&natique ne peut

plus s'effectuer avec la branchie pour base. Le tube

digestif est tres simplify et le foie n'est parfois

visible que sur coupes histologiques. La taille des

animaux est si recluite qu'il est parfois difficile de

decider, meme apres coloration, si une formation

globuleuse transparente est un coeur ou un rein.

La encore il faut recourir aux coupes.

L'etude systeinatique de tres petites ascidies des

fonds meubles pre"sente, par contre, un grand

int^ret dans l'explication de certaines structures, le

manque de place ne permettant de conserver que

les differentiations essentielles pour chaque groupe.

Beaucoup de formes nouvelles sont certainement a

d£couvrir. Les Ascidies interstitielles ont en tous

cas permis de demontrer la structure essentielle et

les directions eVolutives de Pyuridae.

Inte're't des Ascidies des fonds meubles du point

de vue ecologique

Elles existent a toutes les profondeurs: ascidies

interstitielles littorales et ascidies interstitielles

retrouve"es sur talus continental (exemple: Heterostigma reptans a 300 m). Mais ce milieu n'est pratiquement pas encore prospecte". Actuellement, seule

la zone tout a fait littorale et quelques prelevements dans les fosses oce'aniques sont Studies. La

prospection des fonds meubles est extremement

restreinte, sur tout pour les sediments sableux. La

zone entre 50 et 1,000 m n'est absolument pas

prospected. Or, la faune ascidiologique a ces profondeurs s'est reveled tres riche et tres varied sur

les roches dures; il n'y a aucune raison pour qu'il

n'y ait pas d'ascidies sur les fonds meubles, en particulier a la base du talus continental.

Elles existent dans toutes les mers: On a retrouv^

les ascidies interstitielles sur toutes les cotes

d'Europe, partout ou elles ont &e" recherchees. Les

navires ame'ricains Atlantis, Atlantis II et Chain

ont r&olte* des Ascidies des grands fonds dans

l'Atlantique Nord, pres des Bermudes, au large des

cotes du Br&il et au large du Senegal. Seul le petit

nombre de prelevements effectues a limite* l'abondance et la varied des Ascidies re"pertoriees.

Les Ascidies du m&obenthos sont li^es a des

conditions ^cologiques precises. Pour les Ascidies

intertitielles, la granulome'trie a une importance

pr^pond^rante. Elles vivent dans des zones de courants importants et la presence dans l'eau d'une suspension de particules trop fines limite leur deVeloppement. Aux grandes profondeurs on ne sait rien

des conditions ^cologiques: ou bien les courants

sont presque nuls et la branchie n'est pas encrassee

par des suspensions vaseuses, ou bien la couche de

Foraminiferes sur la vase du fond est suffisamment

epaisse pour que ces organismes jouent le role des

particules se"dimentaires plus grosses qui existent au

littoral. Les Ascidies ^tant des animaux filtreurs

tres actifs, il est logique de supposer qu'il existe

toute de meme un courant de fond suffisant pour

assurer l'apport de nourriture. Les Ascidies de la
124

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Aplousobranches Phlebobranches

Pyuridae + Molgulidae

StoLidobranches

FIGURE 2.—Schema de Involution branchiale dans les divers ordres d'Ascidies.

m&ofaune sont toujours liees a une microfaune

varied: Ostracodes, Polychetes, Cop^podes, Isopodes,

Amphipodes, Nematodes.

Un autre caractere plus discutable m^rite cependant d'etre signal^: l'abondance des Ascidies intertitielles parait liee a une teneur elevee du sediment

en ions metalliques. Les microascidies sont tres

abondantes dans les grands fonds atlantiques, au

voisinage des volcans (Sicile) et dans les zones

schisteuses (Mecliterranee occidentale); par contre,

elles sont rares dans les sables quartziques, les sables

coquilliers. On ignore si la composition chimique

du sediment agit directement sur les Ascidies ou sur

les micro-organismes qui composent leur nourriture.
NUMBER 76 125

FIGURE 3.—Heterostigma fagei.

Conclusion

Les Ascidies forment un groupe dans 1'ensemble

difficile a etudier. Leur systematique est mal fix^e.

Ces difficult^ s'accentuent quand il s'agit d'animaux microscopiques.

Le travail technique de r^colte et de preparation

etant effectue, la determination reste encore delicate. II n'existe pas de cle"s utilisables, meme au

niveau de la famille comme nous l'avons vu pr^o$-

demment. II faut signaler encore, apres toutes les

difficult^ precedentes, la presence de cas teratologique frequents: dedoublement d'organes, malformations, etc.

Beaucoup de difficult^ de determination disparaitront quand une collection de preparations

microscopiques sur lames sera constituee et pourra

etre communiquee. Le travail est en cours, mais

les ascidiologiques ont l'habitude de ne pas faire de

preparations permanentes!

II n'existe aucune clef generale pour la determination des Ascidies. L'ouvrage systematique le plus

complet est Van Name (1945). II peut etre utilise

pour les caracteres familiaux et les grands genres.

Harant et Vernieres (1933) et Berrill (1950) sont

inutilisables pour faire une determination. Faute

d'ouvrages generaux quelques publications d'importance variable peuvent etre facilement utilisees

(Hartmeyer, 1911, 1912; Herdman, 1882; Michaelsen, 1904; Millar, 1955, 1959, 1960, 1962, 1964;

Monniot, 1965, and in press; Monniot et Monniot,

1968, 1970; Tokioka, 1953, 1967).

Auteurs Cites

Berrill, N. J.

1950. The Tunicata with an Account of the British

Species. London: Ray Society.

Harant, H., et P. Vernieres

19SS. Faune de France. Paris: Tuniciers.

Hartmeyer, R.

1911. Die Ascidien der Deutschen Siidpolar-Expedition

1901-1903. Deutsche Siidpolar Expedition, 12(Zoologie 4):407-606.

1912. Die Ascidien der Deutschen Tiefsee-Expedition.

Wissenschaftliche ergebnisse der Deutschen TiefseeExpedition auf dem Dampfer, "Valdivia" 1898-1899,

16:223-392.

Herdman, W. A.

1882. Report on the Tunicata Collected during the

Voyage of H.M.S. Challenger During the Years

1873-1876. Part I. Ascidiae Simplices. Report on

the Scientific Research Voyage of HMS. Challenger,

6:1-285.

Michaelsen, W.

1904. Dis stolidobranchiaten Ascidien der deutschen

Tiefsee-Expedition. Wissenschaftliche ergebnisse der

Deutschen Tiefsee-Expedition auf dem Dampfer

"Valdivia" 1898-1899, 7:181-260.

Millar, R. H.

1955. On a Collection of Ascidians from South Africa.

Proceedings of the Zoological Society of London,

125:169-221.

1959. Ascidiacea. Galathea Report, 1:189-209.

1960. Ascidiacea. Discovery Reports, 30:1-159.

1962. Further Descriptions of South African Ascidians.

Annals of the South African Museum, 46(7): 113-221.

1964. Ascidiacea: Additional Material. Galathea Report,

7:59-62.

Monniot, C, et F. Monniot

1968. Les Ascidies de grande profondeurs recoltees par le

le navire oceanographique americain "Atlantis II."

Bulletin de I'Institut Oceanographique, Monaco,

67(1379): 1-48.

1970. Les Ascidies des grandes profondeurs recoltees par

les navires Atlantis, Atlantis II et Chain (2eme

note). Deep-Sea Research, 17:317-336.
126 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Monniot, F.

1965. Ascidies interstitielles des cotes d'Europe. Mimoires

du Museum National d'Histoire Naturelle, serie A,

35:1-154.

In press. Les Ascidies des grandes profondeurs recoltdes

par les navires Atlantis II et Chain (Seme note).

Deep-Sea Research.

Tokioka, T.

1953. Ascidians of Sagami Bay Collected by His Majesty

the Emperor of Japan. Tokyo.

1967. Pacific Tunicata of the United States National

Museum. Bulletin of the United States National

Museum, 251:1-247.

Van Name, W. G.

1945. The North and South American Ascidians. Bulletin of the American Museum of Natural History,

84:1-476.

Weinsten, F.

1961. Psammostyela delamarei n. g., n. sp., Asddie interstitielle des sables a Amphioxus. Comptes Rendus

de I'Academie des Sciences, serie D, 252:1843-1844.
ECOLOGY OF MEIOFAUNA

Bengt-Owe Jansson Th e "Umwelt" of

the Interstitial Fauna

ABSTRACT

The biotic and abiotic parameters that are considered to be of greatest functional significance to

the sense organs of interstitial animals are discussed. Such parameters include the surface of sand

grains, pore and grain size, pore water, temperature, salinity, oxygen, detritus, light, and currents.

The interaction of the parameters is discussed

briefly.

Though living in the same environment ("Umgebung"), the pigeon and the tick in the same tree

experience their habitat in quite different ways—

the "Umwelt" of the bird is quite different from

that of the arthropod. To exemplify this concept,

stated by the German biologist Jackob von

Uexkiill, I shall tell the story of the cheated tick,

based on the facts given by von Uxkiill in his book

of 1956.

Once upon a time there was a little female tick

sitting in a tree high over the green pasture with

grazing cattle. She waited and waited. All of a sudden she felt that wonderful smell of sweat, she

loosened her grip and, landing on something hairy

she crawled to the barest and warmest spot, pushed

out her proboscis, and started to suck. When she

was several times her original size she fell to the

ground and her life cycle came to an end.

But she was not going to have any young because it was not a cow she had landed upon. It

was the apparatus of a nasty ecologist who had

walked under the tree with a plastic sheet, prepared with butyric acid and cattle hairs which covered a plastic tube filled with body-temperature

water.

Bengt-Owe Jansson, Askolaboratoriet, Trosa, Sweden.

The "Umwelt" of that tick, the components of

the environment that are really perceived, is not

the richly colored and odorous pasture with flowers

and cattle but the smell of butyric acid, releasing

the fall reflex; the perception of hair, repelling the

tick to the most naked area; the highest temperature of a warm-blooded animal, leading the tick to

a blood vessel where the sucking reflex is released.

The tick does not even react to the taste of the

fluid, as it sucks blood and water with the same intensity. The "Umwelt" corresponds to "functional

environment," the "Umbebung" to "generalized environment" of Platt and Griffiths (1965).

As ecologists we must measure those parameters

that are the real components of the "Umwelt" of

the organisms, thereby stimulating taxonomists and

physiologists to obtain sufficient data on the sense

organs and their function in the separate organisms. The present survey attempts to present the

various components of the interstitial habitat

along such lines.

Environmental Components

The Surface of the Sand Grains

Interstitial animals, moving over the proportionally vast surface areas of sand grains will naturally

perceive many different properties of the internal

surface, which is very great. Fenchel (1969) calculated the internal surface as K(l/Md), where K is

a constant dependent on geometrical packing and

Md the median grain size of a sediment of equally

large spheres. Thus, the internal surface of a sediment with a medium grain size of 300 p., a surface

of 1.0 cm2, and a depth of 20 cm is about 0.1 m2.

Zobell and Anderson (1936) pointed out the enormous capacity of the sand for carrying bacteria,

and the investigations of Meadows and Anderson

(1966, 1968) showed the grain surfaces to be anal129
130 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

ogous to "landscapes" with green hills of diatoms

or blue-green algae and vast meadows of bacteria.

Round (1965) studied the freshwater algal associations of sand grains; and Westheide (1968) made

careful investigations on the quantitative distribution of bacteria and yeasts on a tidal beach in the

North Sea. Both authors showed maxima of bacteria at the sand surface in the sandy mud flats and

in the supralittoral zone but no correlation was

found to either oxygen availability or organic content. In his work with marine microbenthos, Fenchel (1968) pointed out the great importance of

the sessile diatoms as food for the ciliates. That

the meiofauna can thrive on microbial populations

utilizing soluble material was shown experimentally by Mclntyre, Munro, and Steele (1970).

Jansson (1966b), in his study of the ecology of

Derocheilocaris remanei Delamare and Chappuis,

suggested the great importance of the bacteria as

food for the interstitial fauna. This, confirmed by

Gray in a series of important studies from 1966 to

1968, may also explain the possible contradiction

of a rich fauna in samples with no visible organic

content (Jansson, 1968; Pennak, 1942; Renaud-Debyser, 1963). The importance of the bacterial film

was shown as a decisive factor for the metamorphosis of certain polychaetes (Wilson, 1955), archiannelids (Jagersten, 1940), and gastropods (Scheltema,

1961) but Gray showed that certain archiannelids

were so specific in their preferences that they preferred sand inoculated with a certain species of

bacteria. This certainly broadens the "Umwelt" of

the interstitial fauna.

How the adsorbed ions on the sand grains are

perceived by organisms is difficult to judge, as has

been pointed out by Stowel (1927). The perception of ions by the organism may be a serious

problem, especially in polluted areas. Dissolved organic matter may precipitate around the sand

grains, especially at the supralittoral fringe, in a

manner similar to the precipitation of organic matter around small air bubbles, as shown by Sutcliff,

Baylor, and Menzel (1963) .

The surface texture of the sand grains, whether

smooth or rough, may also be of importance to interstitial fauna though it has not yet been investigated. The roundness of the grains will affect the

size of the interstices.

The Interstices

PORE SIZE.—Pore space limits the size distribution of the inhabiting fauna. Fraser (1935) proposed the important concepts of "critical ratio of

entrance" and "critical ratio of occupation," both

of which were then used by Renaud-Debyser

(1963) and Jansson (1967a). Measurements in the

field of the diameter and area of pores in soil were

made by Haarl0v and Weis-Fogh (1953). By

means of these measurements Haarl0v (1959)

showed how microarthropods were distributed in

soils. Williams (in a paper in these proceedings)

has shown, by imbedding techniques, that larger

interstitial forms were restricted by the sizes of the

pores, whereas smaller forms were more influenced

by biological factors.

The movement of the nematode Heterodera

schachtii Schmidt in soil of different pore sizes and

water films was studied by Wallace (1958, 1959).

This type of experiment should be repeated with

interstitial animals.

GRAIN SIZE.—Granulometry has long been the

method most frequently used by the ecologist to

measure the pore size of sands, and it has led to an

overestimation of grain size as a biological factor.

Fraser (1935) and Graton and Fraser (1935) discussed the relation between grain size, porosity,

and permeability. Prenant (1960) gave a detailed

bibliography on granulometric literature. In a later

work Prenant (1962) gave a method of translating

frequency diagrams of the sizes into number of

grains. This method then was used by Renaud-Debyser and Salvat (1963) in their study of the microfauna and macrofauna of intertidal beaches. A

principal study of the determination of grain size

was made by Morgans (1956). Much information

on grain size distribution in the field is scattered

in the vast taxonomical literature on interstitial

fauna. Much of the literature is summarized in

the reviews of Delamare Deboutteville (1960),

Swedmark (1964), and Jansson (1967a). Following

are examples of studies stressing a correlation between a certain animal group and grain size: foraminiferans, Blanc-Vernet (1958) ; cnidarians, Salvini Plawen (1966); turbellarians, Sterrer (1965);

gastrotrichs, Schrom (1966); polychaetes, Soika

(1955), Sourie (1957), Amoureux (1966); tardigrades, de Zio (1964) de Zio and Grimaldi (1964,
NUMBER 76 131

1966); crustaceans, Wells and Clark (1965); and

several groups of limnopsammon, Tilzer (1968).

It is very difficult, however, to determine a relationship between grain size and animal distribution without controlling other important parameters. No correlation between grain size and the

distribution of the fauna was found by Schmidt

and Westheide (in press), who stressed the significance of other factors as being responsible for the

faunal distributions.

In general, studies show maximum grain sizes in

the vicinity of the water line and a successively decreasing coarseness of the sand landward. Beaches,

however, can be rather homogeneous, as the tidal

beach of Arcachon (Renaud-Debyser, 1963), the

atidal Canet Plage in the Mediterranean (Delamare Deboutteville, 1960), and the atidal Simrishamn beach in the Baltic (Jansson, 1967a). The

vertical distribution of the grain size may be quite

different. Laterally (i.e., parallel to the water

line), the sand appears to be more homogeneous.

The picture of the grain size frequency distribution of sediments is dependent on the number of

different-size sieves used in the analysis, but more

importantly it is dependent on the size of sample

(Jansson, 1966a, 1967a). The sample size must always be related to the size of the animals. Sorting

must also be determined, because the animals

might react not to the sizes of the grains but to the

size of the pores.

The correlation between the true sand fauna

and their substrate was first stressed by Remane

(1933). Locomotory behavior, termed "Stemmschlageln," was shown for numerous - animals by

Remane (1933). A recent analysis of the adaptive

features of sand fauna was given by Ax (1966).

Renaud-Debyser (1963) and Boaden (1962) used

the experimental approach to show the correlation

between grain size and animal distribution by inserting cylinders of graded sand into beach sand

and analyzing the invasion of the fauna into the

cylinders. Because other parameters were not controlled, the results of Renaud-Debyser and Boaden

may not give the definite response to the space-restricting property of the sand. The same criticism

can be made of the Puget Sound studies by Wieser

(1959), who stressed the correlation between grain

size distribution and occurrence of the animals.

Husmann (1968) applied a "substrate organ" in

his work with biological filters as biotope models.

Husmann's device provides important data on the

affinities of the interstitial freshwater fauna in conjunction with the simultaneous control of the

chemistry of the interstitial water.

Laboratory experiments under controlled conditions have shown a definite correlation between

grain size as a space-restricting measure and the occurrence of several animals. The enchytraeid Marionina subterranea (Knollner) preferred sand of

125 to 500 ju, (Jansson, 1966a). Three species of

Protodrilus—P. symbioticus (Giard), P. rubropharyngeus Jagersten, and P. hypoleucus Armenante—chose 200 to 300, 500 to 1,000, and 250 to

500 fi respectively (Gray, 1966a,b, 1967a,b). Similarly, the harpacticoids Parastenocaris vicesima

Kunz (Jansson, 1967b) and Lepatastacus constrictus Lang (Gray, 1968) preferred 150 to 250 and

246 to 500 /i, grains respectively. These experiments

surely reflect the types of locomotion of the experimental animals, because animals which move

by peristalsis (e.g., Aktedrilus monospermatecus

Knollner) or by gliding (e.g., Coelogynopora

schulzii Meixner) exhibit no preference for sand

of a definite porosity (Jansson, 1967a).

Pore Water

AMOUNT OF PORE WATER.—When pores are not

totally filled with water, the water meniscus takes

over the role as the space-restricting component.

The amount of pore water is a primary requirement for interstitial life (Jansson, 1967a). Most

studies deal with the capillarity and saturation of

sand with different grain sizes rather than with the

actual amount of pore water (Bruce, 1928; Wiszniewski, 1934, 1947; Pennak, 1940, 1942, 1951; Neel,

1948; Davant and Salvat, 1961; Ganapati and Rao,

1962; Ruttner-Kolisko, 1962; Callame, 1963).

The quantity of different grades of sand is the

determining factor for the amount of pore water

rather than the medium grain size (Fraser, 1935;

Ruttner-Kolisko, 1962). Porosity is determined by

both the coarseness and the sorting of sand. A superficial layer of sand may, therefore, contain more

water than a deeper layer that is near the groundwater table (Jansson, 1967a; Rullier, 1957). The

space available for the animals may be adequately
132

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

determined from mean grain size, sorting, and

water content of the different layers of sediment.

A correlation between the distribution of tardigrades and the amount of interstitial water was

found by de Zio and Grimaldi (1964, 1966). Salvat

(1964) divided a tidal beach into four zones in his

work with sand isopods. In soil habitats Wallace

(1959) studied the movement of eel worms in

water films and found a strong correlation between

the length of the worms, the amplitude of their

"Stemm-schlageln," and the thickness of the water

films. In Swedish sandy beaches Jansson (1968)

showed a stratification of the fauna. The harpacticoids, being the group most sensitive to pore water,

were limited by a water content of about 7 percent

net weight. The harpacticoids, which dominated

the deepest layers, were followed in abundance by

turbellarians. The oligochaetes, which are able to

live in sand with a very small content of water, occupied the top layers of sand. A similar limit of

pore water for the harpacticoids can be calculated

from the tables of Pennak (1942). This limit for

harpacticoids was confirmed by Enckell (1968) in his

studies of meiofauna from Swedish freshwater

beaches. A landward submergence of beaches because of decreasing amounts of pore water in the

upper layers of sand was reported by Pennak

(1940), Ganapati and Rao (1962), and Schmidt

(1969). The abundance of animals decreased towards the groundwater table more rapidly in the

atidal beaches (Fenchel, Jansson, and von Thun,

1967; Jansson, 1968; Enckell, 1968; Pennak, 1940)

than in tidal beaches (Renaud-Debyser, 1963; Ganapati and Rao, 1962; Schmidt, 1968). This may be

due to greater oxygen availability in the tidal

groundwater resulting from tidal movements

(Emery and Foster, 1948; Davant and Salvat, 1961;

Renaud-Debyser, 1963).

TEMPERATURE OF PORE WATER.—Temperature affects both sand and water (Kinne, 1963). Detailed

temperature measurements from sandy beaches are

rather scarce. Pennak (1940), Wiszniewski (1934),

Angelier (1953), and Ruttner-Kolisko (1953,

1954) have given measurements from freshwater

beaches. Linke (1937) gave values for the heat

conductivity of sand containing different amounts

of mud. Mclntyre (1963) reported very high temperatures from New Zealand beaches, and Swedmark (1955) studied the temperature variations in

a tidal beach at Roscoff during different intensities

of insolation. Annual variations of temperature in

beaches were measured at Arcachon by Renaud-Debyser (1963), in California by Johnson (1965),

and on the island of Sylt, North Sea, by Schmidt

(1968). The influence of air and sea water temperatures upon sand temperatures was shown by Salvat

(1967). A detailed analysis of the diurnal and seasonal temperature variations at different depths in

a Baltic sandy beach was made by Jansson

(1967b). These studies and the investigations of

others support the following generalizations for

temperatures of sandy beaches of the boreal region.

The seasonal minima occur during the winter,

when frost often occurs to 1 m depth in northern

countries. In the spring diurnal, temperature often

fluctuates as much as 40 degrees. The highest temperatures are found during the summer, when the

temperature of the sand, even in temperate areas,

may reach values of 50° C. Vertical stratification is

very pronounced, and a decrease in temperature of

more than 10° C within the upper 2 cm of sand is

by no means uncommon. In the autumn, in northern countries, temperatures decrease and night

frosts appear, resulting in high diurnal ranges. Annual ranges of temperature taken in the sand of a

Swedish sandy beach were 49.7° C for the surface,

27° C for 10 cm depth, and 18.1° C for 70 cm

depth (Jansson, 1967d). The more seaward parts

of the beach showed smaller amplitudes of temperature. Higher values may be found at higher altitudes during the summer; for example, 55° C at

the sand surface on New Zealand beaches (Mclntyre, 1963).

Interstitial fauna is subjected to great temperature variations both in space and time. In northern countries interstitial fauna may be captured in

frozen sand for long periods but evidently may thaw

out and show a high percent survival (Barnett,

1968; Jansson, 1968). Specimens of Protodrilus

symbioticTM survived negative temperatures without ice formation (Gray, 1965). Schmidt (1968)

considered temperatures of 5° to 10° C as the

lower limit for the spawning of interstitial fauna.

This temperature limit for spawning resulted in a

minimum of animals in the spring and a maximum in the autumn. Seasonal fluctuations of interstitial fauna also were found by Brenowitz (in press)

in Long Island beaches. As was shown by Renaud-
NUMBER 76 133

Debyser (1963) for the Arcachon beaches and by

Schmidt (1969) for the beaches of Sylt, the fauna

was abundant throughout the year but migrated

downward during the coldest period.

The temperature tolerance of several turbellarians, oligochaetes, and harpacticoids was investigated by Jansson (1966a, 1967b, 1968). Most of

the species survived for three or four days when

kept in their optimal salinities. Exceptions were

the turbellarian Haplovejdovskya subterranea Delamare Deboutteville and the enchytraeid Marionina subterranea, both of which survived only two

to three hours, and the harpacticoid Parastenocaris

phyllura Kunz, which survived nearly one week.

A well-established horizontal and vertical gradient of temperature in the beach and a sensitivity

to high temperatures of the organisms were shown

in experiments with Marionina subterranea by

Jansson (1966a) and with Protodrilus symbioticus

by Gray (1965). More of these kinds of experiments should be attempted.

SALINITY OF PORE WATER.—The significance of

salinity for aquatic organisms was summarized for

numerous animals in various habitats (Kinne,

1964a-c, 1966). Salinity records from sandy

beaches are presented in many taxonomic papers

but more detailed studies of salinity are few. In

atidal beaches the salinity decreases landward

(Brinck, Dahl, and Wiser, 1955; Ax, 1954; Munch

and Petzold, 1956; Jansson, 1966a,b, 1967b,d, 1968;

Fenchel, Jansson, and von Thun, 1967). In tidal

beaches a landward decree of salinity is affected

by the tidal movements (Bruce, 1928; Linke,

1937; Sourie, 1957; Ganapati and Rao, 1962; Davant and Salvat, 1961; Renaud-Debyser, 1963; Govindankutty and Nair, 1966; Johnson, 1967; Salvat,

1967; Schmidt, 1968). The surface layers of the

submerged part of the beach may show hypersalinites because of evaporation (Gerlach, 1954; McIntyre, 1963; Jansson, 1967d; Barnett, 1968). The

effect of rain is minimal in temperate, sandy

beaches (Linke, 1937) but more important in mud

flats (Barnett, 1968), freshwater beaches (Pennak,

1951), and tropical beaches (Ganapati and Rao,

1962. When the overflowing water was hyposaline

the interaction between the interstitial water and

an overflowing water of different salinity was minimal (Reid, 1930; Callame, 1963). Jansson (1967d)

found that the influence of intermediate waves on

the salinity of water-filled interstices of beach sands

was small. Complex interactions between seawater,

groundwater, and rain anomalies may occur in the

beach with "tongues" of saltier water in intermediate layers (Fenchel, Jansson, and von Thun,

1967).

Wide fluctuations in salinity exert a great stress

upon interstitital organisms, as shown by simple

tolerance experiments on ciliates (Ax and Ax,

1954), turbellarians (Jansson, 1968), archiannelids

(Boaden, 1962, 1963; Gray, 1966c), and crustaceans (Jansson, 1966a,b, 1967b, 1968). Many interstitial animals, including the mystacocarid Derocheilocaris remanei and the enchytraeid Marionina

southerni (Cernosvitov), have a physiological tolerance of salinity ranges of more than 15 ppt

(Jansson, 1966b, 1968). Others, including the harpacticoids Paraleptastacus spinicauda (T. and A

Scott), Parastenocaris vicesima Klie and P. phyllura Kiefer, have a rather restricted range of less

than 7.5 ppt (Jansson 1967d, 1968). Some animals

(e.g., Marionina southerni and Schizopera baltica

Lang) may display a strong preference for narrow

salinity ranges in spite of their euryhalinity (Jans

son, 1968). Specimens of Protodrilus symbioticus,

however, showed no preference reaction to salinity

(Gray, 1966c).

The ecological tolerances may not always coincide with the physiological tolerances. Paraleptastacus spinicauda, Marionina subterranea, and M.

preclitellochaeta Nielsen and Christensen show a

wide geographical distribution (Noodt, 1957; Remane, 1958; Lasserre, 1966, 1967) but a small

physiological tolerance (Jansson, 1962, 1968). This

raises the question of nongenetic and genetic adaptation (Kinne, 1964b). Reuter (1961) has shown

genetic adaptation to different salinities for three

populations of the turbellarian Gyratirix hermaphroditus (Ehrenberg).

OXYGEN IN PORE WATER.—The dissolved oxygen

(DO) content of interstitial sediments has been

little studied. Most oxygen values refer to tidal

beaches (Ganapati and Rao, 1962; Renaud-Debyser, 1963; Amoureux, 1963; Brafield, 1964, 1965),

and few oxygen determinations have been taken

from atidal beaches (Pennak, 1940; Angelier, 1953;

Munch and Petzold, 1956; Ruttner-Kolisko, 1954,

1962). The oxygen valves for tidal sand flats at 5 to

15 cm depth often are below 0.5 ml/liter but vary
134

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

with grain size, drainage, amount of organic matter, and slope. Atidal beaches have oxygen values

comparable to those of tidal beaches with good

drainage. Severe fluctuations of oxygen, pH, temperature, and salinity have been reported in tidal

pools of a sandy mud flat in the Elbe estuary

(Ktihl, 1964). The changes were correlated with

the occurrence of benthic diatoms.

Stressing the fact that interstitial organisms perceive oxygen not as concentration but as availability, Jansson (1966a,b) introduced a method from

soil science to marine biology, namely, the oxygen

diffusion rate (ODR). This measure, expressed as

gO2/cm-j electrode surface/minute, incorporates not

only oxygen concentration but also temperature,

porosity, and interstitial water flow. Therefore, the

ODR constitutes a more important ecological

measure of the oxygen conditions than DO. The

distributions of ODR both in atidal (Jansson

1966a,b; 1967b,c; 1968; Fenchel and Jansson, 1966;

Fenchel, Jansson, and von Thun, 1967; Enckell,

1968) and tidal (Westheide, 1968) beaches show

low values in and below the groundwater table,

high values in intermediate layers, and low values

at the sand surface. The latter are sometimes artifacts, caused by the small amounts of interstitial

water present which are not sufficient to totally

moisten the electrode. The somewhat higher values

of oxygen in the groundwater of tidal beaches are

explained by the better ventilation due to tidal

movements (Schmidt, 1968) . The direct effect of

waves upon the ODR has been shown by both

field measurements and laboratory experiments

(Jansson, 1967c).

A correlation between the oxygen content of interstitial water and the distribution of interstitial

fauna was found by Pennak (1940), Jansson

(1966b, 1967b,c), Fenchel and Jansson (1966),

and Fenchel, Jansson, and von Thun (1967). Very

little is known of the response of the interstitial

animals to oxygen. Gray (1966c, 1967a) found that

Protodrilus symbioticus and P. rubropharyngeus

moved towards the highest oxygen concentration

when placed in an oxygen gradient. The lower

ODR limit for the harpacticoid Parastenocaris vicesima was found by Jansson (1967b) to be

around lg~7 cnr^min-1. This harpacticoid was absent at the low values in the field, as were harpacticoids investigated by Enckell (1968) in a Swedish

freshwater beach. The enchytraeids Marionina

achaeta Lasserre and M. spicula (Leuckart) colonize different parts of the beach because they have

different respiration rates at high temperatures

(Lasserre, in press).

DETRITUS IN PORE WATER.—Animals perceive detritus partly as food and partly as a space-restricting medium. Besides the important work of Perkins (1958), few investigations have been carried

out concerning the food of interstitial fauna. Bacteria have been mentioned previously as an important food resource. In his comprehensive study of

the harpacticoids of the German coasts Noodt

(1957) mentioned detritus as a frequent food. The

importance of detritus for the total fauna was

stressed by Remane and Schultz (1934), Remane

(1952), and Renaud-Debyser and Salvat (1963);

however, no correlation between the amount of detritus and the interstitial fauna was found by Ganapati and Rao (1962) or by Renaud-Debyser

(1963). The suggestion by Jansson (1966a) that

the amount of bacteria in the beach is not necessarily correlated to the detritus factor was supported by Westheide (1968).

Detritus often is irregularly distributed within

the beach (Jansson, 1967a,b, 1968; Schmidt, 1968),

but it may show a maximum in the sand flats

(Westheide, 1968) or in the back-shore (Pennak,

1940; Salvat, 1967). Sometimes dark, concentrated

bands of decaying organic material is found in the

sand, thus excluding most interstitial life (Jansson,

1966a, 1967a,b). The finer particles may show an

increase towards the groundwater level (Westheide,

1968).

Increased organic material favors increased bacterial activity and, as a consequence, the ODR values and the redox potential (Eh) fall. Under

anaerobic conditions H2S formation will occur,

eliminating much of the meiofauna, which usually

concentrates in the upper layers (Fenchel and

Jansson, 1966). Elimination of meiofauna by H2S

also has been recorded in freshwater beaches by

Enckell (1968). The dynamics of detritus-rich sediments are exhaustively treated in the important

study of Fenchel (1969).

OTHER PARAMETERS IN PORE WATER—Because the

maximum penetration of light into the sand is 5 to

15 mm (Neel, 1948; Pennak, 1951; Gray, 1966b),

few animals are subjected to strong insolation. The
NUMBER 76 135

archiannelids Trilobodrilus heideri Remane, Protodrilus symbioticus, and P. rubropharyngeus, however, show a negative klinokinesis (Boaden, 1963;

Gray 1966b, 1967a). A photonegative response also

is exhibited by the harpacticoids Schizopera baltica

and Nitochra fallaciosa Klie f. baltica Lang and

Leptastacus constrictus (Jansson, 1968; Gray,

1968).

Currents are a common phenomenon of tidal

beaches. A rheoactive behavior has been found in

Trilobodrilus heideri (Boaden, 1963). Boaden

(1968) showed the negative influence of turbulence upon interstitial animals. Similarly, the seaward limit for the distribution of Derocheilocaris

remanei in Canet Plage was found to be controlled

by turbulence (Jansson, 1966b). Tilzer (1968)

found that the interstitial fauna of mountain

streams migrated better along the water flow than

against it, although examples of upstream migration also were noted.

Boaden (1963) demonstrated gregarious behavior by Trilobodrilus heideri. Gray (1967a) showed

that Ptotodrilus rubropharyngeus is attracted to

members of the same species and to sand recently

inhabited by members of the same species. Similarly, Boaden and Erwin (in press) found that Protodrilus symbioticus produced a substance that made

sand unattractive to the gastrotrich Turbanella

hyalina Schultze.

Negative geotaxis was shown for Protodrilus

symbioticus, P. rubropharyngeus, and Leptastacus

constrictus by Gray (1966a, 1967a, 1968).

Interaction Between Parameters

This presentation is not totally adequate, as

the different parameters of the interstitial animals'

"Umwelt" do not interact with each other or upon

the animals singly but in aggregate. Often, several

parameters may dominate in a given situation or

act synergistically. The sizes and shapes of the sand

grains indirectly affect the oxygen availability,

which, in turn, determines the aeration of the interstitial water (Jansson, 1967a) . If 30 percent of

the sand consists of grains of 250 p. the oxygen

drops to near zero (Ruttner-Kolisko, 1961). A

close correlation between oxygen content and grain

size also was found by Brafield (1965). Jansson

(1966b) showed high ODR values in sand of 200

to 300 fi. Wieser (1959) showed from field studies

that "the critical grain size" of 200 /i was the lower

limit of grain sizes for the occurrence of interstitial

animals. When tested in the laboratory for their

space-restricting property, however, 200-/1 sands

could not be shown to affect the animals (Jansson,

1967a).

It has been proved clearly that animals react to

gradients of temperature, salinity, oxygen, and light

and that they perceive pore space, gravity, currents, and chemical substances from their own species. The aggregate and intensities of the various

parameters will determine the field distribution of

interstitial fauna. The patchy distribution of the

harpacticoid Parastenocaris vicesima was attributed

to its preference for salinities below 5 ppt, sensitivity to ODR values below lg~T

 cnr^min-1, and preference for grain sizes between 250 and 125 /i (Jansson, 1967b).

But preferences may change. As for certain

terrestrial invertebrates, the intensity of a certain

factor may displace the preference zone of another.

Salinity preference may change if the animal is

able to adapt to other salinities. Efforts to displace

the preference zone of the tubificid Aktedrilus

monospermatecus, however, were in vain (Jansson,

1962). The euryhaline enchytraeid Marionina

southerni was shown to have a narrow preference

zone, but this could be affected by keeping the animals in higher salinities for more than eleven days,

as shown in Figure la (Elmgren and Jansson, unpublished) .

Salinity may be perceived by animals not as a

salt concentration but as osmotic pressure. Oxygen

availability also is involved, because osmotic work

of an organism requires oxygen. The preference

zone for three groups of specimens of Marionina

southerni from the same population was found to

be clearly dependent upon temperature (Figure

Ib). While the animals held at 15° C showed distinct preference for neither 1 nor 5 ppt, those held

at 5° C clearly preferred 1 ppt and those held at

30° C preferred 5 ppt (Elmgren and Jansson).

One must not only know the ranges of the different environmental parameters and how the animals react to them but also the intensities to

which the animals have become acclimated in the

field.
136

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

100

75

50

2 25 10%o~ ADAPTED

5%o - ADAPTED

10 15 20 78

ADAPTIO N TIME . DAYS

100

O 80

O

Z

§ 50

O

x

u

2 0 •

_ <

b

1 2 3 4

A DAPTION TIME , DAYS

FIGURE 1.—Successive displacement of salinity preference of the enchytraeid Marionina southemi:

a, from 7 ppt after adaption to different salinities at 15° C; b, after adaption to different

temperatures in 6.5 ppt. Vertical bars indicate 95 percent confidence intervals.

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1963. £tude des teneurs en oxygene dans les eaux interstitielles de l'Aber de Roscoff. Cahiers de Biologie

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Angelier, E.

1953. Recherches ecologiques et biogeographiques sur

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1954.

1966.

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Die Bedeutung der interstitiellen Sandfauna fur

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Meersforschung in Bremerhaven, Sonderband 2:

15-65.
NUMBER 76 137

Ax, P., and R. Ax

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Siisswasser. Biologisches Zentralblatt, 79:7-31.

Bamett, P. R. O.

1968. Distribution and Ecology of Harpacticoid Copepods

of an Intertidal Mudflat. Internationale Revue der

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Blanc-Vernet, L.

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Bulletin de I'Institut Oceanographique, Monaco,

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Boaden, P. J. S.

1962. Colonization of Graded Sand by an Interstitial

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Leland W. Pollock Ecology of

Intertidal Meiobenthos

ABSTRACT

Environmental factors including sediment, water

saturation, temperature, salinity, oxygen, organic

detritus, and microflora are reviewed in terms of

their influence on intertidal meiofaunal populations.

As a comparatively young area of study most research on meiobenthos has remained taxonomic

and descriptive. While the list of known intertidal

meiofauna includes representatives of nearly every

phylum of invertebrates, few investigators have attempted thorough ecological studies in this area.

Within the last decade portions of four review articles have summarized available ecological information (Delamare Deboutteville, 1960; Swedmark,

1964; Jansson, 1968b; Mclntyre, 1969) .

Using these basic references and additional citations, the general aspects of intertidal meiofaunal

populations are reviewed here, with consideration

given to important intertidal parameters along

with an estimate of their influence on the distribution of meiofauna. Any review of beach ecology

must include also the valuable material compiled

by Jansson (1962, 1966, 1967a-d, 1968a,b) Fenchel (1967, 1968) and Fenchel and Jansson (1966)

on littoral beaches in the atidal Baltic Sea.

Meiofaunal Populations

Accurate quantitative information on meiofauna is

difficult to obtain; therefore, literature in this area

is limited. In coarse sandy tidal beaches, interstitial

fauna occupy an area from low to high tide and

Leland W. Pollock, Systematics-Ecology Program, Marine

Biological Laboratory, Woods Hole, Massachusetts 02543.

Systematics-Ecology Program Contribution Number 212.

from the sand surface to depths of several meters

(Delamare Deboutteville, 1960; Renaud-Debyser,

1963). In fine sandy beaches, meiofauna generally

is restricted to the upper 5 cm of sand (Perkins,

1958), while in mud flats it is concentrated in the

top centimeter of sediment (Rees, 1940; Barnett,

1968). In standardizing records of intertidal meiofaunal abundance, Mclntyre's (1969) data suggest

a decrease in meiofaunal abundance from coarse

intertidal sediments, where diversity of taxa is

maximal, toward finer sand sediments. Nevertheless, maximal meiofaunal density is reached in very

fine sediments of mud flats, although here diversity

of taxonomic groups probably is lowest. Ganapati

and Rao (1962) described a relationship between

density and size wherein small forms exist in large

numbers but large forms tend to be more scarce.

Sediment

Intertidal environments supporting interstitial

meiobenthos include particulate sediments ranging

from large-diameter shell-gravel to fine particles of

clay and silt on mud flats. Characteristics of sedimentary particles determine the dimensions and

extent of the interstitial labyrinth of capillary

spaces and its penetrability by water burrowing

meiofauna, and especially those forms of meiofauna that are too small to move particles of sediment and so are restricted to the interstitial spaces

(Callame, 1963; Graton and Fraser, 1935; Rees,

1940; Ruttner-Kolisko, 1961). While surveys of

particle-size composition by weight contribute

meaningfully, particularly in studying homogeneous, fine sediments (Prenant, 1960), several investigators have observed that more emphasis must

be placed on measuring spaces between particles in

coarser intertidal areas (Enckell, 1968; Jansson,

1967b). Perhaps recently developed techniques for

measuring spaces directly will prove valuable in as141
142

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

sessing this parameter (Haarl0v and Weis-Fogh,

1953; and the paper by R. Williams in these proceedings) .

The sorting (or degree of heterogeneity of particle sizes), the tightness of sediment packing, and

the shape of individual grains determine interstitial porosity, which comprises 36 to 44 percent of

most beach sand samples (Ruttner-Kolisko, 1961,

1962). Grain size, sorting, tightness of packing,

and shape of particles are factors in controlling porosity and permeability of sediment to water (Graton and Fraser, 1935; Ruttner-Kolisko, 1961; Salvat, 1967). These sedimentary characteristics reflect

the availability of interstitial space both for

meiofauna and environmental parameters. Salvat

(1967) distinguished four zones along the surface

of beaches with medium-fine sand which differ in

interstitial hydrodynamic characteristics. The zone

of dry sand is reached only by extremely high

tides. The zone of retention is reached by all high

tides but loses much of its pore water at tidal

emersion. A zone of resurgence is the site of intense circulation of interstitial water at both rising

and falling tide and a zone of saturation lies below

the area drained by low tide. Salvat correlated distributions of several macrofaunal forms with this

environmental zonation.

Physical dimensions of the capillary network

influence interstitial animals and environmental

parameters. As Jansson (1967b) pointed out,

aquatic intertidal meiofauna occupy only that portion of an interstitial space which contains pore

water. At low tidal drainage, this may take the

form of water films surrounding individual sediment particles (Pennak, 1951). Living in this unusual environment, interstitial meiofauna has

evolved, in remarkably convergent directions, a series of morphological adaptations (Delamare Deboutteville, 1960; Remane, 1952; Swedmark, 1964).

These include small body size, elongation, flattening, fragility, adhesive organs, reduced number of

eggs, and direct larval development.

For interstitial meiofauna, which pass through

sediment spaces without moving the particles

themselves, dimensions of interstitial pores may be

limiting, especially when the proportion of fine

grain-size materials is great (Renaud-Debyser and

Salvat, 1963). Morphological adaptations and locomotor activity in several groups of meiofauna have

been linked to specific ranges of sediment size

(Gray, 1968; Swedmark, 1964). Wieser (1959) suggested that sand less than 200 /x in diameter may

be a "critical grain size," preventing establishment

of abundant interstitial meiofauna. Jansson

(1967b), for one, suggested that smaller grain sizes

often are indirectly important by diminishing

water flow and consequently changing oxygen and

food availability.

Tidal movements of seawater and local topography are important determinants of sedimentary

characteristics and distribution. Through tidal

wave activity, sediment particles of greatest diameter accumulate near the low-tide region (Barnett,

1968; Ganapati and Rao, 1962; Pennak, 1951;

Rees, 1940). Generally, exposure to heavy surf produces either steep beaches of large particle size or

more gently sloping beaches of fine sand, depending upon surrounding geoogical conditions.

Usually moderate wave activity is associated with

medium-to-coarse sandy beaches. Gentle water

movements frequently produce broad flats of fine

sediment.

Water Saturation

The chemical composition of intertidal interstitial

water is determined by tidal seawater and limited

quantities of fresh water from precipitation, runoff, and groundwater seepage. Superficial areas also

lose water through evaporation during low tidal

exposure (Bruce, 1928a,b; Gerlach, 1954; Johnson,

1965). The slope, porosity, and grain size of the

sediment; tidal movements of seawater; distance

from the water line; duration of low tidal exposure; and the strength of preipitation and/or evaporation all determine the specific amount of water

present in intertidal sediments (Bruce, 1928a,b;

Callame, 1963; Gerlach, 1954; Graton and Fraser,

1935; Jansson, 1967a; Johnson, 1965; Rees, 1940;

Rullier, 1957). Capillary forces, which vary with

grain size and sorting, are important in retaining

water in pore spaces not exposed to broad tidal-water movements (Ruttner-Kolisko, 1962) .

Restriction of water flow through the interstitial

network is determined by the permeability of the

sediment (Brafield, 1964; Emery and Foster, 1948).

Ruttner-Kolisko (1962) and Brafield (1964) related diminished water circulation directly to an
NUMBER 76 143

increasing proportion of particles less than 250 ju,

in diameter. Fine sediments lose little more than

superficial water during low tide and interstitial

water tends to stagnate in capillary spaces (Callame, 1963). While coarser sediments undergo extensive drainage at low tide (to a depth of 1 m or

more in some cases, Renaud-Debyser, 1963), movements of water within the beach still are restricted

to some degree and lag behind movements of the

adjacent sea water for periods of several hours

(Emery and Foster, 1948; Renaud-Debyser, 1963;

Salvat, 1967).

Intertidal meiofauna is least abundant in sediments always saturated with water or in nearly dry

layers (Ganapati and Rao, 1962). Usually meiofauna is limited to sediments containing more

than 10 percent of their saturation water (de Zio,

1965; Enckell, 1968; Pennak, 1951). Water content

apparently constitutes an important environmental

determinant of littoral meiofaunal distributions

(Jansson, 1967b, 1968a).

Temperature

The temperature of intertidal sediments is regulated by more-general factors such as seasonal and

climatic weather conditions and time of day. These

in turn are frequently modified by more-specific

and local factors such as slope of the beach, moisture held in sedimentary spaces, the temperature of

both air and seawater, and the insulation of the

sediment (Bruce, 1928a,b; Pennak, 1942; Jansson,

1967c; Johnson, 1965; Salvat, 1967) .

Temperatures naturally are highest during summer in superficial layers of sediment, which may

undergo abrupt changes accompanying inundation

by flooding tide (Bruce, 1928a,b; Jansson, 1967c;

Johnson, 1965; Linke, 1939; Salvat, 1967). Generally a gradient of declining temperature forms

with increasing depth in intertidal sediment

(Bruce, 1928a,b; Jansson, 1967c), although this

gradient may become reversed at night (Ganapati

and Rao, 1962), during winter (Jansson, 1967c),

and at flood tide (Salvat, 1967). While the severity

of these gradients varies seasonally and by geographic location, little change in temperature occurs below about 20 cm depth (Bruce, 1928a; Jansson, 1967c). While Ganapati and Rao (1962) feel

that most interstitial animals cannot tolerate broad

changes in temperature, several intertidal meiofaunal animals survive exposure to extremely low

temperatures (Gray, 1965; Jansson, 1968a; Moore,

1931). Renaud-Debyser (1963) demonstrated seasonal changes in overall distribution of meiofauna

which live deeper in sand in winter, avoiding extremes in both temperature and salinity. Johnson

(1965) suggests that animals living in the upper

centimeter of fine sandy beaches are exposed to

daily temperature ranges up to three times that experienced by subtidal individuals, while those living at 10 cm or deeper experience temperatures

comparable to those in subtidal environments.

Some meiofauna from mud flats are restricted in

movements to the uppermost layers of sediment

and, therefore, must endure the full range of environmental variation (Barnett, 1968; Rees, 1940).

In this case, physiological resistance must be an

important determinant of field distribution.

Salinity

In tidal beaches, seawater conditions dominate the

chemistry of interstitial water. Except in areas of

unusually concentrated precipitation, interstitial

salinity remains approximately comparable to that

of the seawater (Ganapati and Rao, 1962; Johnson, 1967), in a few cases slightly higher (Fenchel

and Jansson, 1966; Ganapati and Rao, 1962), and

in most other cases somewhat lower (Jansson,

1967c; Kiihl and Mann, 1966; Renaud-Debyser,

1963; Salvat, 1967). Generally, gradients of decreasing salinity exist horizontally between the seawater and shoreward areas where terrestrial sources

of fresh water may be important (Jansson, 1967c),

and between the sedimentary surface where evaporation increases salinity (Gerlach, 1954; Johnson,

1967) and dilution by groundwater at greater

depths (Jansson, 1967c). Gradients in salinity may

be steep and variable in tidal areas (Jansson,

1967c) but are less so on tidal beaches where flooding and draining seawater prevents accumulation

of fresh water (Linke, 1939; Reid, 1930). Variations in salinity are greatest high on sandy beaches

and lowest towards the sublittoral (Johnson,

1967). However, less porous intertidal habitats,

such as mud flats, are subject to more drastic variations of superficial salinity—the salinity increasing
144

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

with evaporation and decreasing during precipitation (Barnett, 1968; Capstick, 1957).

At least under local extremes, salinity has an important influence on microfauna and meiofauna.

Anderson and Meadows (1969) found that fresh

water or rainwater removed some of the microbial

flora from sand grains, thereby removing important food materials for meiofauna. Govindankutty

and Nair (1966) and Ganapati and Rao (1962)

recorded severe reductions in meiofaunal abundance during reduced salinity accompanying monsoon periods of heavy rain. In addition, meiofauna

apparently seek deeper levels in the sediment in

the presence of lowered salinity (Govindankutty

and Nair, 1966; Jansson, 1968a). In fine sediments

where mobility is restricted to superficial regions,

Barnett (1968) observed that all but a few harpacticoids remained within 0.5 cm of surface of the

mud flat despite exposure to heavy rains which

drasticially reduced the salinity of interstitial

water. Boaden (1963) studied the effect of lowered

salinity on normal orientations of an archiannelid

to water current. He demonstrated that a balance

between variable responses to salinity changes and

to current flow can maintain a population of motile animals within a restricted intertidal zone.

Oxygen

In an oversimplified sense, oxygen is present

within interstitial spaces in decreasing abundance

from the water's edge toward the shore and from

the sand surface toward greater depth (Jansson,

1967d; Pennak, 1951). However, patterns are frequently irregular and difficult to distinguish (Jansson, 1967d). In some cases, increased oxygen levels

are associated with groundwater flow (Jansson,

1966, 1967d).

The abundance of oxygen within a beach is related to the permeability of sediments to water

(Brafield, 1964). In beaches containing large

quantities of clay, silt, or organic debris (Jansson,

1967d; Rullier, 1957), in beaches of very fine-grain

sand (Brafield, 1964; Ruttner-Kolisko, 1961), or

where ice-cover prevents exposure to air and waves

(Jansson, 1967d), a black layer of ferrous and hydrogen sulfides forms close to the sedimentary surface and often indicates the depth at which anaerobic conditions prevail (Bruce, 1928b; Gordon,

1960).

Replenishment of oxygen depends largely upon

circulating water during the rising tide (Brafield,

1964; Gordon, 1960), on out-flow of groundwater

(Jansson, 1966, 1967d), and on wave activity

(Gordon, 1960; Jansson, 1967d). In field studies,

Ruttner-Kolisko (1962) and Brafield (1964) related increased abundance of oxygen to increased

water movements, and recently Enckell (1968)

quantified this effect in laboratory studies of freshwater movement.

In several cases, meiofaunal distributions were

shown to be limited by lack of oxygen (Jansson,

1968a, for a review). Animals living at depths

greater than 10 cm in fine intertidal sediments

must be capable of surviving extended periods of

anaerobiasis (Fenchel, 1967; Fenchel and Jansson,

1966; Gordon, 1960; Pamatmat, 1968; Riedl, 1969;

Wieser and Kanwisher, 1961). Fenchel (1967) observed that ciliate Protoza dominate in anaerobic

conditions where most Metazoa did not survive.

Nevertheless, some meiofaunal Metazoa, apparently

living anaerobically, are found at depths well below

the "black layer" (Wieser and Kanwisher, 1961).

In intertidal areas of larger sediment size, the

oxygen content is often low but is seldom zero

(Ganapati and Rao, 1962; Jansson, 1967d; Renaud-Debyser, 1963). Renewal of interstitial water

during tidal ebb and flow is important to the

maintaining of oxygen abundance in intertidal

beaches (Gordon, 1960; Pennak, 1951). Some meiofauna living in beaches of coarser grain showed a

clear preference for areas of increased oxygen

abundance (Gray, 1966b, 1967a; Jansson, 1967a,d).

Acidity-Alkalinity

Several investigators have studied the pH of interstitial water and reported readings similar to those

from adjacent seawater (Bruce, 1928b; Ganapati

and Rao, 1962; Renaud-Debyser, 1963; Salvat,

1967). Apparently variations in pH are not great,

and the interstitial water in most marine beaches

is only slightly more acid than the sea. Bruce

(1928b) observed that pH changes are moderated

by an alkali-reserve buffering effect of calcareous

material in the sand.
NUMBER 76 145

Organic Detritus

Generally, organic detritus is available in small

quantities in sandy beaches (Ganapati and Rao,

1962; Renaud-Debyser, 1963; Salvat, 1967) but is

more abundant in fine intertidal sediments (Meadows and Anderson, 1966). Accumulation of debris

in an intertidal area depends upon wave exposure,

water currents, slope of the beach, coarseness of

the sand, and the amount of vegetation in nearby

areas (Dahl, 1953). The importance of this material to intertidal organisms is physical, chemical,

and biological. In contrast to relatively even gradients in most intertidal parameters, distribution

of decaying organic matter tends to be patchy

(Jansson, 1968a). As small paniculate material,

debris accumulates and clogs pore spaces, sometimes limiting interstitial spaces severely, changing

their penetrability and capacity for water retention

(Jansson, 1967b; Pennak, 1942). In addition, this

material contributes to the formation of a ferrous

sulfide layer in the sand and, through by-product

of its degradation, to the general chemistry of interstitial water (Bruce, 1928a,b). Finally, organic

detritus has been considered an important source

of food in intertidal communities (Dahl, 1953;

Perkins, 1958; Remane, 1952; Renaud-Debyser and

Salvat, 1963). Abundant intertidal meiofauna

usually is associated with an intermediate abundance of organic material—not in beaches thoroughly cleaned by waves, nor in sediments clogged

by debris (Pennak, 1942; Renaud-Debyser and Salvat, 1963).

Intertidal food materials include organic detritus, algae living on grains of sand or washed in

from near-shore water, bacteria, and the meiofauna

themselves. As Jansson (1968a) suggested, the

range of materials generally termed "detritus" is

broad in composition. Studies of microfauna and

microflora of marine intertidal sediments have

demonstrated a great diversity and abundance of

organisms in this material (Anderson and Meadows, 1969; Meadows and Anderson, 1966, 1968;

Steele and Baird, 1968). In addition, careful determinations of food chosen by meiofauna indicate

that "detritus feeders" may be highly selective in

the portions of detritus they choose (Fenchel,

1968; Thane-Fenchel, 1968).

Microflora

While heavy surf limits their distribution to low

tidal regions on exposed beaches (Steele and

Baird, 1968), microalgae are extremely abundant

in flats of fine particle size. Steele and Baird

(1968) predicted that in situ productivity of intertidal areas should increase with decreased wave exposure. Pamatmat (1968) conducted a study of

community metabolism in an intertidal sand flat.

He found that microflora provided most of the primary productivity (about 200 to 300 liters of

oxygen/m2/year) of the area. He estimated that

community respiration was 140 to 226 liters of

oxygen/m2/year. Although seasonal and tidal fluctuations in both of these measurements make studies of this sort still more complex, he found that

the portion of community respiration produced by

the complex of bacteria-microfauna-meiofauna was

greater than that contributed by the macrofauna.

Studies of bacterial distribution in intertidal

areas should be valuable in interpreting distributions and ecology of meiofauna browsing on films

of bacteria (Anderson and Meadows, 1969; Meadows and Anderson, 1966, 1968; Westheide, 1968).

Several taxa have shown attraction to sediments

possessing films of organic materials (Gray,

1966a,b, 1967a,1968; Jagersten, 1940; Wilson,

1955). In some cases, the attractiveness is specific

for particular groups of bacteria or to by-products

of their presence in the recent past (Gray, I967a,b,

1968). Bacterial abundance apparently is greatest

in areas of low wave exposure (Anderson and

Meadows, 1969). In medium-coarse sands maximal

densities occurred near the sand surface in low and

high tidal regions (Westheide, 1968). Presumably

microbial flora is extremely rich in flats of sand

and mud (Zobell, 1946).

Information presently available on the ecology

of intertidal sand areas includes general characterizations of the substratum and chemical analyses of

seawater and groundwater, mostly from low-tide

measurements. While much more of this kind of

data are needed, future studies must also include

analyses of conditions through tidal, daily, and seasonal changes in order for us to visualize the dynamics of the environment. In addition we must

design equipment and techniques for studying environmental parameters in "microhabitat" dimensions of water films surrounding grains of sand.
146 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

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NUMBER 76 147

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148 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

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1959. The Effect of Grain Size on the Distribution of

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A.D.Mcintyre Observations on the

Status of Subtidal

Meiofauna Research

ABSTRACT

The regional distribution, vertical distribution,

seasonal fluctuations, and composition of populations of subtidal meiofauna and the effects of

sampling techniques on estimates of subtidal meiofauna are reviewed. It is concluded that geographic

and depth sampling must be extended, seasonal

changes in meiofauna must be studied in more

detail, and sampling techniques must be refined.

In recent years the increase of interest in meiofauna has produced an expanding volume of

literature on many aspects of this field. However,

because of the obvious advantages of sampling

close to laboratory facilities, and of easier accessibility, much of the work has been concerned with

beaches, tidal or atidal. Further, there has been a

marked concentration on sandy areas, so that the

interstitial fauna has received greater attention

than those forms which crawl on the surface (epipelic) or burrow into the sediment (endopelic). A

comprehensive review has recently appeared (McIntyre, 1969) but the availability of new data and

the desire to highlight the subtidal situation make

it useful to reconsider this aspect. The present

paper brings together published data on quantitative aspects of marine meiofauna populations and

their ecology from sediments below the low-water

mark of spring tides. There are only 20 relevant

papers, all published within the last 38 years, and

these are summarized in Table 1.

A. D. Mclntyre, Marine Laboratory, Aberdeen, Scotland.

Regional Distribution

For the continental shelf it is convenient to divide

the data according to three habitats—sea-grass,

sand, and mud—and we may consider first the regional coverage of the information. The sea-grass

communities are found in shallow coastal waters,

and most of the sampling has been done at less

than 1 m depth. Work in Japan (Kikuchi, 1966)

is based on only a few samples from beds of Zostera marina Linnet but in Danish waters studies

have been much more extensive (Muus, 1967),

and other macrophytes (Ruppia maritima Linn£

and Chaetomorpha linum (Miiller)) were present

as well as Zostera Linn£ in the sampling area. In

America, work at Miami dealt with the nematodes

only of a Thalassia testudinum Koenig and Sims

community, and Tietjen (1969) made a detailed

investigation of meiofauna populations in Zostera

areas of two New England estuaries. Data are

available also on Spartina alterniflora Loiseleur

from flats on the American east coast at Massachusetts and Georgia (Wieser and Kanwisher, 1961;

Teal and Wieser, 1966), and although these refer

to intertidal areas they have been included in

Table 1 for comparison.

On sandy grounds of the subtidal shelf, there is

information from ten investigations. From tideless

areas, Purasjoki (1947) in the Gulf of Finland,

and Fenchel and Jansson (1966) in the Baltic

worked at low salinities of 3 to 7 ppt, while Bregnballe (1961) and Muus (1967) sampled the Kattegat in salinities ranging from 5 to 18 ppt. In the

North Sea, sand in fully saline conditions was examined off the Danish coast by Smidt (1951). In

warmer waters, observations are available from off

Banyuls in France (Guille and Soyer, 1968) and

from calcareous sand on the shelf inshore at Ber149
150

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

muda (Coull, 1968). Farther north, on the American coast, Wieser (1960) provided data from Buzzards Bay in Massachusetts while nearby, on the

shelf, Wigley and Mclntyre (1964) sampled stations at several depths. Finally, Tietjen (1969)

studied two sandy stations (median grain sizes 210

fi and 440 p) in two New England estuaries.

For subtidal mud on the shelf, eleven areas have

been examined. The studies of Purasjoki (1947)

in Finland and Muus (1967) in the Kattegat, already referred to for sand, were extended into

muddy grounds, while additional information for

the Baltic region is available from Krogh and

Sparck (1936) from the 0resund. Round the British Isles, Mare (1942) worked in the English

Channel, Moore (1931) in the Clyde, and Mclntyre (1964) in the sea lochs of the Scottish west

coast as well as in the North Sea off the east coast.

Bougis (1946, 1950) and Guille and Soyer (1968)

sampled mud off the Mediterranean coast of

France, and some of the investigations already referred to for sand off New England (Wieser, 1960;

Wigley and Mclntyre, 1964) and off Bermuda

(Coull, 1968) also dealt with muddy grounds.

Beyond the continental shelf, little quantitative

information is available. Wigley and Mclntyre

(1964) described two samples from silt-clay and

fine sand on the slope off New England, and from

the abyssal regions Thiel (1966) gave a preliminary account of work done in the Indian Ocean.

TABLE 1.—Summary of Subtidal Meiofauna Data.

Habitat

SeaGrass

Sand

Mud

Reference

Kikuchi

Muus

Hopper & Meyers

Tietjen

Wieser & Kanwisher

Teal & Wieser

Purasjoki

Fenchel & Jansson

Bregnballe

Muus

Smidt

Guille & Soyer

Coull

Wieser

Wigley & Mclntyre

Tietjen

Muus

Krogh & Sparck

Purasjoki

Wieser

(1966)

(1967)

(1967)

(1969)

(1961)

(1966)

(1947)

(1966)

(1961)

(1967)

(1951)

(1968)

(1968)

(1960)

(1964)

(1969)

(1967)

(1935)

(1947)

(1960)

Bougis (1946/50)

Guille & Soyer

Mare

Moore

Mclntyre

Mclntyre

Wigley & Mclntyre

Wigley & Mclntyre

Thiel

Coull

(1968)

(1942)

(1931)

(1964)

(1964)

(1964)

(1964)

(1966)

(1968)

Water

depth

< 5

< 1

< 1

1

Intertidal

Intertidal

15-40

< 0.5

< 1.5

< 1.0

2-3

15-91

3-13

12-30

40-58

1

< 1

5-54

9-55

18

30

30-85

45

24-166

146

101

69-179

366-567

1000-5000

27

m

m

m

m

m

m

m

m

m

m

m

m

m

m

m

m

m

m

m

m

m

m

m

m

m

m

m

Region

Japan

Baltic

USA (Miami)

USA (New England)

USA (New England)

USA (Georgia)

Gulf of Finland

Baltic

Baltic

Baltic

North Sea

^Tf*H i tprn i n f*zt n

iTicunci i oiltall

Bermuda

USA (New England)

USA (New England)

USA (New England)

Baltic

Baltic

Gulf of Finland

USA (New England)

Mediterranean

Medi terra nean

English Channel

Scotland (Clyde)

North Sea (northern)

Scotland (west coast)

USA (New England)

USA (New England)

Tnriiafi Orran

Dominant group and

Season

August

May—July

All Year

All Year

Nov. & June

March

January

July-Aug.

June

Apr.-July

All Year

All Year

July-Aug.

June

All Year

Mar.-June

Aug.-Jan.

January

July-Sept.

Mar.-May

Mar.-May

Single season

All Year

All Year

June

June

Bermuda (Devils Hole) All Year

its mean density

(individuals

per 10cm2)

Nematoda

Nematoda

Nematoda

Nematoda

Nematoda

Nematoda

Nematoda

Rotifera

Nematoda

Nematoda

Nematoda

"WpfVlS t f\l\ Q

11 Cilia lUUa

Nematoda

Nematoda

Nematoda

Nematoda

Nematoda

Nematoda

Nematoda

Nematoda

Nematoda

Nematoda

Nematoda

Nematoda

Nematoda

Nematoda

Nematoda

Nematoda

XT * A

ii ema locia

Nematoda

534

430

796

2,030

1,870

12,400

2

97

789

658

132

191

423

364

553

2,132

220

53

23

798

614

79

83

193

1,845

853

355

114

38

Total

meiofauna

mean per

10 cm>

670

643

2,369

5

376

968

9fi9

580

375

663

2,626

365

88

41

838

818

150

145

237

1,959

1,008

395

122

TO

40
NUMBER 76 151

This summary draws attention to the restricted

global coverage of the data from subtidal zones. A

high proportion of the samples were taken in the

waters of northwestern Europe, and there is

clearly great scope for extension of comparable

work into other regions. Sufficient information has

not yet accumulated to permit detailed comparisons to be made of populations on a regional basis.

Depth

As indicated above, the depth coverage also is severely restricted. Most of the samples were taken

in water of only a few meters depth, and samples

from over 50 m are available from a very small

number of cores.

Vertical Distribution

Similar restrictions apply to our knowledge of the

vertical distribution of organisms in the sediment

because of the difficulty of obtaining long-undisturbed cores from subtidal grounds. In most of the

surveys referred to in Table 1, sampling was confined to the top 4 to 6 cm of deposit. On muddy

grounds, a high proportion of the fauna is confined to these surface layers, but this is not so for

all animal groups in sand. Tietjen (1969) used

cores of 5 cm and showed that harpacticoids, ostracods, and polychaetes were greatly reduced or

absent at the 4 to 5 cm level but substantial numbers of nematodes were still present. Mclntyre (unpublished) examined cores 23 cm long collected in

Scotland by divers from a sandy ground (median

grain size 200 ju,) at 1 to 8 m depth, where he

found mainly nematodes, but he also found several

other groups down to the deepest section of the

cores. Numbers were much reduced below 16 cm,

but strongly bimodal vertical distributions have

been recorded from intertidal areas, and a similar

picture may be found in some subtidal areas when

suitable sampling devices are developed.

Seasonal Fluctuations

Details of seasonal fluctuations also are sparse

Only five of the investigations listed in Table 1

give data collected throughout a full year, and

most refer to a single season or even to a once-only

sampling; consequently, knowledge of overall

changes in subtidal populations is limited.

Workers from shallow Danish waters agree that

nematodes are at a minimum in winter months

and that there are marked seasonal fluctuations in

harpacticoids—apparently associated with reproduction—while ostracod populations, by comparison, are much more stable throughout the year. At

Bermuda, Coull (1968) noted distinct seasonal

patterns, with the lowest values for total populations occurring in winter and the highest in late

spring, although nematodes often reached highest

numbers in winter at the time of lowest temperatures. Coull was able to show that seasonal fluctuations in density were related not only to the reproductive activity of the animals, stimulated

apparently by temperature increase, but also to

regular physical events which caused changes in

the sediments. For example, at one site harpacticoids declined when the well-sorted, coarse-grained

sediments characteristic of summer months received a considerable input of silt-clay material as

a result of winter hydrographic conditions. Such

regular annual fluctuations may have habitat

changes on a larger scale superimposed on them.

Hopper and Meyers (1967), for example, showed

how gradual deterioration of the plants in a seagrass bed could complicate the interpretation of

seasonal changes. A further difficulty in this respect

is that in many investigations meiofauna species

are not identified but are lumped together in the

presentation to give total counts for major taxonomic groups. Because of the ecological diversification which exists within such groups, greater taxonomic discrimination would undoubtedly help in

the interpretation of seasonal patterns. Thus Tietjen (1969), by dividing the nematodes he studied into feeding types, found significant peaks in

epigrowth feeders in spring and summer, after

which there was a rapid decline, apparently associated with changes in the microflora. Peaks were

less obvious in other feeding types, but deposit

feeders tended to peak in the fall, winter, and

early spring when epigrowth feeders were least

abundant.

Marked seasonal fluctuations might not be expected in deep water where conditions are much

more uniform. Mclntyre (1964) could not detect

significant differences due to season in meiofauna
152

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

populations at about 100 m off the Scottish coast.

Matthews (1964), working on benthic copepods of

deep Norwegian fjords, also found no great seasonal changes, but he did observe that the copepods were most abundant when the plankton of

the upper waters was in decline, suggesting a scavenging role for these benthic forms.

Composition of the Populations

It is clear from the surveys shown in the table that

nematodes are overwhelmingly the dominat group

numerically, often making up over 90 percent of

the metazoan fauna. Occasionally in single samples, or on a particular ground, copepods are more

abundant than nematodes, but in general they are

a poor second in the subtidal zone. Other groups,

such as ostracods in shallow brackish water, have

only occasionally been recorded as quantitatively

important.

Some of the earlier surveys produced very low

counts of population density, but the more refined

techniques of recent years have resulted in total

meiofauna counts from single subtidal samples

ranging from 95 to 1,269 individuals per 10 cm2

for sand, and 177 to 3,163 per 10 cm2 for mud.

While it is probably true that nematodes are the

most important group numerically, it may well be

that their importance has been exaggerated because of the comparative ease with which they can

be preserved and counted. Unfortunately, it often

is necessary to work on preserved samples for subtidal studies, so recognition of soft-bodied taxa is difficult. Knowledge of such groups as Turbellaria

and Gastrotricha, which has advanced so much recently in intertidal areas, depends on examination

of live material, and it is probable that such

groups will be found in greater numbers when

suitable techniques can be applied to subtidal deposits.

Effects of Sampling Techniques

As suggested above, the sorting and processing

techniques used may affect the relative quantitative

picture of the meiofauna. The methods used in

collecting the original sample may be of even

greater importance. Three main techniques were

used in the surveys listed in this review. In very

shallow water, samples were collected by hand in

core tubes or small containers; second, some form

of gravity corer was used; and third, subsamples

were taken from a grab. Of the three methods,

there is no doubt that the diver-collected core is

the most satisfactory. On sandy ground, where there

may be marked substrate differences within short

distances, the diver can note the exact situation

from which the sample is taken, whether from a

crest or a trough in ripple areas, for example, and

whether the spot is representative of a wider area.

Further, the diver usually is able to collect a core

of the desired length and bring it to the surface

more or less intact—a useful achievement on a

sandy ground.

Muddy grounds may seem to present less of a

problem since they often are more uniform and

frequently yield an apparently intact sample in a

gravity corer. It is known, however, that the flocculent surface layer is easily washed aside by the

downwash of a sampler. Work presently in progress by the Aberdeen Marine Laboratory in a Scottish sea loch at 25 m has shown that when using

an open core tube of just over 2 cm internal diameter it is extremely difficult for a diver to collect a

vertical core which includes the intact surface

layer. Even a tube of over 4 cm diameter caused

some washing aside of the flocculent material in

spite of the most gentle insertion into the deposit.

It was only when tubes of a much larger size—almost 10 cm diameter—were used that the divers

felt confident of obtaining a completely intact surface layer. It seems unlikely that any existing instrument could compete with this method of

collection. Our present procedure is to collect an

intact sample in a wide tube and slowly siphon off

all but the last 1 cm of supernatant water. It then

is possible to subsample with narrow tubes without

disturbing the surface. Comparative counts are

now being made on samples taken by this method

and from a free fall corer, and initial results indicate that the diver-collected core gives a significantly higher estimate of fauna for the upper

layer. This procedure eliminates error from another source—core shortening. On the ground referred to above, divers observed that pushing a 2-

cm tube into the mud beyond 6 to 8 cm caused

shortening of the core, so, in long samples, the validity of the vertical layering was in doubt. By sub-
NUMBER 76 153

sampling from a large core in the laboratory, this

could be allowed for, but with a remote gravity

corer, shortening of the sample could take place

without this being obvious to the operator.

It would seem, then, that the best subtidal meiofauna samples are those collected by hand by diving—an activity restricted to about 30 m. At

greater depths, remote core devices must be used,

or subsamples taken from a grab. For remote coring it must be accepted that there will be some

loss of surface material, and shortening of the core

during penetration may produce distortion of the

layers. For grab sampling, care must be taken to

use only those hauls which produce comparatively

undisturbed sediment surfaces.

Conclusions

It is clear that information on the subtidal meiobenthos is very sparse indeed. We require a great

extension of sampling, both geographically and

depth-wise, and we also need detailed work

throughout the year to define seasonal changes.

Even sampling methods are by no means satisfactory except in shallow water where SCUBA can be

used. Because of all these deficiencies, ecological

knowledge for the subtidal region, either from the

autecological or the synecological aspect, is almost

nonexistent.

Literature Cited

Bougis, P.

1946. Analyse quantitative de la micro-faune d'une vase

marine a Banyuls. Comptes Rendus de I'Academie

des Sciences, 222:1122-1124.

1950. Methode pour l'etude quantitative de la microfaune

des fonds marins (Meiobenthos). Vie et Milieu,

1:25-37.

Bregnballe, F.

1961. Plaice and Flounders as Consumers of the Microscopic Bottom Fauna. Meddelelser fra Danmarks

Fiskeri-og Havundersfgelser, 3(6) :133-182.

Coull, B. C.

1968. Shallow Water Meiobenthos of the Bermuda Platform. Unpublished PhJD. dissertation, Lehigh University.

Fenchel, T., and B.-O. Jansson

1966. On the Vertical Distribution of the Microfauna in

the Sediments of a Brackish-Water Beach. Ophelia,

3:161-177.

Guille, A., and J. Soyer

1968. La Faune benthique des substrats meubles de Banyuls-sur-Mer. Premieres Donnees qualitatives et

quantitatives. Vie et Milieu, 19:323-360.

Hopper, B. E., and S. P. Meyers

1967. Population Studies on Benthic Nematodes within

a Subtropical Seagrass Community. Marine Biology,

1 (2) :85-96.

Kikuchi, T.

1966. An Ecological Study on Animal Communities of the

Zostera marina Belt in Tomioka Bay, Amakusa,

Kyushu. Publications from the Amakusa Marine

Biological Laboratory, Kyushu University, 1 (1) :1-

106.

Krogh, A., and R. Sparck

1936. On a New Bottom-Sampler for Investigation of the

Micro Fauna of the Sea Bottom with Remarks

on the Quantity and Significance of the Bottom

Micro Fauna. Kongelige Danske Videnskabernes

Selskabs Skrifter, Biologiska Skrifter, 13(4):1-12.

Mclntyre, A. D.

1964. Meiobenthos of Sub-Littoral Muds. Journal of the

Marine Biological Association of the United Kingdom, 44 (3) :665-674.

1969. Ecology of Marine Meiobenthos. Biological Reviews,

44:245-290.

Mare, M. F.

1942. A Study of a Marine Benthic Community with

Special Reference to the Micro-Organisms. Journal

of the Marine Biological Association of the United

Kingdom, 25(3):517-554.

Matthews, J. B. L.

1964. On the Biology of Some Bottom-Living Copepods

(Aetideidae and Phaennidae) from Western Norway.

Sarsia, 16:1-46.

Moore, H. B.

1931. The Muds of the Clyde Sea Area. III. Chemical

and Physical Conditions; Rate and Nature of

Sedimentation; and Fauna. Journal of the Marine

Biological Association of the United Kingdom,

17(2): 325-358.

Muus, B. J.

1967. The Fauna of Danish Estuaries and Lagoons. Distribution and Ecology of Dominating Species in the

Shallow Reaches of the Mesohaline Zone. Meddelelser fra Danmarks Fiskeri-og Havundersfigelser,

5(1): 1-316.

Purasjoki, K. J.

1947. Quantitative Untersuchung fiber die Mikrofauna

des Meeresbodens in der Umgebung der Zoologischen Station Tvarminne an der Siidkiiste Finnlands. Societas Sdentiarum Fennica, Commentationes Biologicae, 9(14): 1-24.

Smidt, E. L. B.

1951. Animal Production in the Danish Waddensea.

Meddelelser fra Kommissionen for Danmarks

Fiskeri-og Havunders0gelser, Series Fiskeri, ll(6):l151.
154 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Teal, J. M., and W. Wieser

1966. The Distribution and Ecology of Nematodes in a

Georgia Salt Marsh. Limnology and Oceanography,

ll(2):217-222.

Thiel, H.

1966. Quantitative Untersuchungen viber die Meiofauna

von Tiefseeboden. Veroffentlichungen des Institute

fur Meeresforschung in Bremerhaven, Sonderband

2:131-147.

Tietjen, J. H.

1969. The Ecology of Shallow Water Meiofauna in Two

New England Estuaries. Oecologia, 2(3):251-291.

Wieser, W.

1960. Benthic Studies in Buzzards Bay. II. The Meiofauna. Limnology and Oceanography, 5(2): 121-137.

Wieser, W., and J. Kanwisher

1961. Ecological and Physiological Studies on Marine

Nematodes from a Small Salt Marsh near Woods

Hole, Massachusetts. Limnology and Oceanography, 6(3)262-270.

Wigley, R. L., and A. D. Mclntyre

1964. Some Quantitative Comparisons of Offshore Meiobenthos and Macrobenthos South of Martha's Vineyard. Limnology and Oceanography, 9(4):485-493.
M. T. Gomoiu Ecology of

Subtidal Meiobenthos

ABSTRACT

The difficulties of conducting synecological studies

of meiobenthos are discussed. Studies on the

benthic population dynamics and biomass, with

emphasis on meiobenthos that have been conducted

in the Black Sea by Romanian investigators, are

reviewed. The importance of meiobenthos in the

economy of the sea is emphasized.

The fact is well known that in the last few years

the tiny world of bottom marine organisms has

drawn the attention of more and more research

workers. Studies undertaken so far have revealed

not merely the qualitative and quantitative richness of microbenthos but also the great importance

of the latter in sea-economy. Many of the difficulties that occur during microbenthic ecological investigations have been recorded. The most difficult

problem in microbenthic synecological studies is

the necessity for a great number of specialists to

work as a team for the various groups of organisms

(Ciliata, Nematoda, Tardigrada, Harpacticoida,

Ostracoda, Foraminifera, Diatomea, etc.).

Microbenthos is defined in this paper according

to the following scheme proposed at the seminar

on the "Quantitative Methods for Benthos Studies

and Dimensional Scale of the Benthos" held at

Marseilles in November, 1963:

Macrobenthos Megistobenthos

Megabenthos

Microbenthos Mixobenthos

Meiobenthos

Nanobenthos

Hypo benthos

2 mm

1 mm

0.1 mm

0.01 mm

M. T. Gomoiu, "Traian SSvulescu" Institute of Biology, Department of Marine Biology, Constantza, Romania.

Thus, the usage of the term microbenthos appears

wider and slightly more imprecise than that of

meiobenthos, which is fairly restricted and generally agrees with the opinions of different authors.

It is, nevertheless, very difficult to find a precise

basis for defining the size categories of benthos

(Mclntyre, 1969).

Other difficult problems in the study of subtidal

benthos reside in the complexity of abiotic and

biotic conditions of the shallow-water subtidal

zone. A specific bathymetrical delimitation of intertidal zone is necessary. The scheme proposed by

Peies and Picard (1959) with regard to the range

of benthal formations includes the subtidal zone

infralittoral (in French terminology) as follows:

L'ltage infralittoral est limits vers le haut par le niveau a

partir duquel les peuplements sont toujours, ou a peu pres

toujours immerges (toute Emersion prologee entrainant la

mort des especes constituant le peuplement). Sa limite inKrieure est celle qui est compatible avec la vie des

Phane'rogames marines ou des Algues photophiles. Le classement des algues en photophiles et sciaphiles est resolu par

l'&ude des passages lateraux par rapport aux Phan&ogames

marines prises comme base de re'fe'rence.

The environmental factors of the shallow-water

zone 20 to 30 m deep are in a state of perpetual

instability. Environmental dynamism is quite amplified in estuarine regions. In shallow-water zones,

topographical, geological, climatological, hydrological, hydrochemical, and even anthropological factors permanently interact and constantly change,

and their actions upon marine organisms are complex and multilateral. Thus, as many environmental factors as possible should be recorded when

studying the ecology of benthos.

As an example, wind, a complex meteorological

factor, acts in many ways. It produces gales resulting in waves, forming currents, changing sea level,

moving and replacing water masses, etc. Waves and

currents, in turn, act directly or indirectly upon

155
156

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

living organisms—such as displacing organisms

from the substratum, moving them, or destroying

them. Bottom topography may be modified, sediments moved and redeposited, sediment structure

modified, and suspensions raised into the water

mass thereby fertilizing it. By moving water masses,

winds thus modify saline and thermic regimes,

water transparency, and color. Thus, within a few

hours, organisms of shallow zones can be exposed

to waters of diverse properties and qualitatively to

new environmental conditions (Gomoiu, 1968).

This example, with its several aspects, illustrates

the necessity of recording as many environmental

factors as possible to obtain as complete an image

as possible of the environment in which the organisms live.

In interpreting data and establishing causal

connections, the complex action of environmental

factors on the organism should be considered. Present-day tendencies of establishing connections between single environmental factors and the evolution of organisms should be avoided. Encountered

are studies of the distribution of organisms or

other aspects of their biology based on a single factor such as substratum, on organic substances, or

other elements. Such relations undoubtedly are important, but they are insufficient. The parallel

study of the action of different factors upon organisms, followed by studies of their combined influence which results in a complex physioecological

study, will yield the clue to causalities and may explain the dynamics of benthal populations (Gomoiu, 1966).

Two difficult problems arise in a complex ecological study of meiobenthos: the collection of

material and its processing and sorting. Various authors point out that small core tubes are convenient for collecting meiofauna. Core tubes are satisfactory under certain conditions, especially when

one station and several samples are to be collected.

How many depends on the distribution of organisms as determined by a preliminary study. The

distribution of organisms is not uniform, most organisms having a patchy distribution. Thus, a very

large number of small samples will be necessary

from one station for statistical treatment of the

material.

The collection of larger samples from greater

areas, though necessitating more labor for processing (although subsamples may be taken for individual analysis), will yield better results as far as

real meiobenthos abundance is concerned and perhaps will provide better correlation with the

abundance of macrobenthos. It is up to each investigator to analyze his collecting and processing

methods. Before starting a complex study on a

large zone it is necessary to undertake a preliminary investigation in order to determine the most

adequate methods.

Another widely discussed but unsolved problem

which deserves particular attention is that of expressing biomass. Biomass has been expressed in

various ways, including wet weight, dry weight,

weight of ash, etc. Thus, it is very difficult to make

comparisons and to realize the richness of meiobenthos from one zone to another. The author considers that the expression of meiobenthos biomass

in wet weight, though apparently somewhat difficult, is the most adequate. The very etymology of

the word "biomass" indicates that it must be considered as the weight of living matter. Meiobenthos enters the food chain in its natural, wet

weight. Fish reserves are assessed and fishing or certain problems connected with their biology are expressed by wet weight. When biomasses are indicated in any form, conversion modalities should be

specified or conversion tables given. Both biomasses

and densities should be related to area dimensions

which can easily be related to a square meter.

Romanian studies of bottom population dynamics in the Black Sea over the last ten years are

characterized by a simultaneous approach to both

macrobenthos and microbenthos. The importance

of microbenthos has been shown many times in

Romanian works (Bacescu, 1961, 1963,1966).

A brief systematic survey of recent studies of Romanian Black Sea waters revealed over 160 microzoobenthonic and 210 microphytobenthonic species. Many of these are new species, not only for

the Black Sea but to science. Thus, of 20 nematodes found, 3 were new to science; of 35 ostracodes, 8 were new species; of 6 oligochaetes, 2 were

new; of 40 harpacticoids, 12 were described for the

first time. All of these species were studied qualitatively, quantitatively, and seasonally (Bacescu,

Dumitrescu, Manea, Por, and Mayer, 1957; Bacescu, Dumitrescu, Marcus, Paladian, and Mayer,

1963; Bacescu, Gomoiu, Bodeanu, Petran, Miiller,
NUMBER 76 157

and Stanescu, 1965; Bacescu, Gomoiu, Bodeanu,

Petran, Miiller, and Manea, 1965; Bacescu, Gomoiu, Bodeanu, Petran, Mtiller, and Chirila, 1967;

Gomoiu and Miiller, 1962).

Over 100 animal species were identified on the

quartzose-micoceous fine-sand bottoms, a holocoenose characterized by the presence of the small bivalve Corbula Bruquiere. Among these species more

than 40 are typically psammothalassobiontic, i.e.,

living in sand and exhibiting special adaptations

to life in sandy environments; the rest are more or

less psammoxenic. Typical species include the harpacticoids Ectinosoma intermedia Nicholls, Canuella perplexa Scott, and Canuella furcigera Sars,

the ostracode Pontocythere bacescoi (Caraion), the

cumaceans Pseudocuma longicornis maeotica Bacescu and Iphinoe maeotica (Sov.) Bacescu, the

amphipods Bathyporeia guilliamsoniana (Bate)

and Perioculodes longimanus Bate, and various

species of Archiannelida and Polychaeta including

Spio filicornis O. F. Mtiller, Nerine cirratulus

(Delia Chaje), Nephtyes Cuvier, and Glycera Savigny. Some meiobenthic species are so numerous

and so typical that they can be defined as well as

the mollusc subcoenotic units. Thus, we can recognize the following subcoenoses: Corbula-ChioneHarpacticus ftexus, Corbula-Canuella, CorbulaStreblus, etc.

The dominant meiobenthic organisms exhibiting

the highest diffusion index in the sandy Corbula

coenose include Streblus Fischer and Ammovertellina Cushman, 100 percent; Canuella perplexa and

Spio filicornis, over 90 percent; Ectinosoma Boeck,

Microarthridion littorale Poppe, and Harpacticus

flexus Brady and Robertson, over 70 percent;

Ameira Boeck, Acartia Dana, and Parathalestris

Brady and Robertson, nearly 65 percent; Leptinogaster histrio (Pelseneer), Pontocythere Dobowsky,

and Asellopis Brady and Robertson, nearly 60 percent.

On the littoral stony bottoms of the Romanian

Black Sea, nearly 100 zoobenthonic species were

identified, of which 73 belong to meiobenthos.

Some meiobenthonic species are new to science

(Tegastes elenae Marcus, Mesochra pontica Marcus,

Centroderes spinosus agigensis Bacescu), many are

new to the Pontic basin (Amphiascella subdebilis

(Willey), Psylocamptus minutus Sars, Tricoma

nematoides (Greeff), Halichoanolaimus DeMan),

and many others are new to the Romanian fauna.

Beyond subtidal boundaries and toward the

deeper water of the Romanian Black Sea coast

there is a gradual disappearance of macrobenthic

forms to a depth of 180 m. Only dwarfed specimens of Terebellides stroemi Sars can be found

below 180 m, together with another few meiobenthonic species including species of Lagena Walker

and Jacobs and a few nematodes of the genus Sabatiera deRouville which occur to a depth of 220

"m. A new coenose was established in the Black Sea

periazoic zone on the basis of the presence of certain meiobenthonic taxa dominated by the foraminiferan Lagena, the hydrozoan Bougainvillea

Forbes, and the nematode Spirina parazitifera.

An analysis by groups of the main meiobenthic

organisms of Romanian Black Sea littoral reveals

the following. In terms of density, Foraminifera

represent one of the main constituents of sediments and of the benthos of sandy zones, usually

numerically exceeding the rest of the organisms.

Of more than 50 species quantitatively reported

from the Black Sea, the most abundant are Ammonia becarri (Linn^) and Ammovertellina prima

(Suley.), particularly in sandy bottoms, and species of Lagena, Pyrgo Defrance, and Quinqueloculina d'Orbigny in silty bottoms. Sometimes the

Foraminifera from sand are so numerous that they

give the sediment the appearance of a "pure culture." Cases in which the density of these Protozoa

exceeds 4.5 million specimens/m* (= 215 g/m2)

are fairly common. Thus, Foraminifera constitute

a fairly abundant and permanent source of food

not merely for the small psammophagous organisms (the gastropod Retusa Brown for instance;

Bacescu and Caraion, 1956) but also for some

fishes which appear to select Foraminifera from the

sand with great facility. There is no doubt that the

nutritional value of Foraminifera is not of the

same importance as that of copepodes, nematodes,

or of many other meiobenthonic organisms as fish

food, but they are at least equal and in proportion

to that of molluscs.

Worm groups, including numerous meiobenthic

forms, are well represented in all biotopes. The nematodes, including over 150 species in the Black

Sea, are numerically dominant among the worms.

The psammobionts, species living on or in sand,

though small (mostly under 1 mm) and weighing
158

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

between 0.003 and 0.0047 mg each, have an important role in the biocenose due to their ubiquitous

nature (100 percent diffusion index) and the fact

that their densities may easily exceed 250,000

specimens/m2. The mesopsammic or interstitial

worm fauna is dominated by Enoplus littoralis Filipjev, Epsilonema Steiner, Sabatieria, and others.

Although the densities of nematodes are very high,

their biomasses are small and their trophic importance is far from negligible. Nematodes represent

the food of microphagous young fishes during this

most critical period.

As nematodes are dominant in terms of density,

the polychaetes are dominant in terms of biomass

and contribute considerably to raising the general

trophic value of biocenoses. Of the nearly 200 polychaete species in the Black Sea, the great majority are microbenthic, while the others have meiobenthic juvenile stages. In sand zones, the density of

Spio filicornis, Micronephtys stammeri (Augener),

and Nephtys cirrosa Ehler. determines the general

abundance of polychaetes, which sometimes exceeds 10,000 specimens/m2

. Among petricolous species, Grubea clavata (Claparede) is found in densities of over 10,000 specimens/m2

, Exagone gemmifera Pagenstecher 50,000 specimens/m2

, and

Fabricia sabella (Ehrenberg) 74,000 specimens/m2.

Oligochaetes also play an important role in

benthic economy. The 35 species known to occur

in the Black Sea include Peloscolex svirenkoi (Jarus)

and Peloscolex euxinicus Hrabe which may reach

densities of 2,500 specimens/m2. Tubifex euxinicus

Hrabe, which is at the limit of microbenthos in

size, reaches densities of 15,000 specimens/m12.

Turbellaria are less abundant and their densities

vary greatly. As many as 140 specimens have been

recorded from 1 cm3 of sand. The Kinorhyncha

are fairly abundant. In the more muddy zones the

most abundant is Echinoderes dujardini Claparede,

followed by Pycnophies ponticus (Reinhard) and

Pycnophies kielensis (Zelinka). From more than

600 quantitative meiobenthos samples of the Romanian littoral, the highest density of kinorhynchs

was 7,980 specimens/m2. Among typical psammobiontic nemertines are the meiobenthic species Arenonemertes microps Friedrich, Prostomatella

arenicola Friedrich, Amphiporus Ehrenberg, and

Pontolineus arenarius G. I. Muller. These are,

however, only of minor importance in terms of

density and biomass in the economy of the cenoses.

Although the other worms (Gastrotricha, 23 species; Rotifera, 11 species) have likewise been studied from the systematic point of view, they are not

presently included in synecological studies.

Next to the worms, the crustaceans represent the

group with the most numerous meiobenthic representatives. Crustaceans also are of high trophic

value and of considerable importance in benthic

economy. Among crustaceans, the major meiobenthic forms with respect to density and biomass

are the copepods. Most species of this group are

represented by harpacticoids, with the following

species in the sand zones: Canuella perplexa,

Canuella furcigera, Ectionosoma elongatum Sars,

Nannopus palustris Brady, Parathalestris harpacticoides (Claus), Harpacticus flexus, Ameira parvula (Claus), Microarthridion littorale, Asellopsis

sarmatica Jakubisiak, Enchydrosoma longifurcatum

Brady, and Stenhelia palustris Brady. These species

often are found in densities of the order of 150,000

to 170,000 specimens/m* depending on depth and

season. Microarthridion littorale is the most abundant.

The ostracodes are represented in the Black Sea

by nearly 50 species, and they have two typical

psammobiontic representatives: Cyprideis littoralis

Brady, occurring in the more freshwater zones, and

Pontocythere bacescoi, a more halophilous and

stenotopous species strictly limited to the Corbula

cenose. The density of ostracodes generally is

small, seldom exceeding a few hundred specimens/

m

a

.

Cumaceans and mysids are meiobenthic forms of

a relatively small abundance, rarely reaching 5,000

specimens/m2. Among the species living on sandy

bottoms are Iphinoe maeotica Bacescu, Pseudocuma ciliata Sars, Cumopsis goodsiri (van Beneden), Bodotria arenosa mediterranea Stener, Paramysis Czerniavsky, and Gastrosacus Meyer.

The 107 species of amphipods are of particular

importance in the Black Sea. Some species, including Talorchestia Dana, Orchestia Leach, and Pontogammarus Sowinsky, are dominant in certain

biocenoses. They have large biomasses and, based

on size, they are situated at the upper limit of

meiobenthos. Restricted to the biocenose of fine

sands with Corbula are Bathyporeia guilliamsoniana and Perioculodes longimanus, which are char-
NUMBER 76 159

acteristically interstitial in the intertidal. Other

species, including Ampelisca diadema (Costa), Nototropis guttatus (Costa), Gammareus carinatus

Rathke, Cardiophilus baeri Sars, and Corophium

Latrielle are either cenophilous, i.e., accidental occurrences, or originate from neighboring biotopes.

Psammobiontic isopodes (Euridice pontica Czerniavsky and Euridice dollfusi marisnigri Bacescu),

inhabiting the upper intertidal and the wavebreaking zone, do not play an important role in

benthic economy but do exhibit interesting adap

tive characters.

In the Black Sea, only the most important

groups with meiobenthic representatives that can

be studied quantitatively from a single sample

have been mentioned. There is no doubt that the

list of Pontic basin meiobenthos is fairly long.

Benthic ciliates alone total nearly 280 species and

their contribution is far from negligible. This review emphasizes the contribution and role of

meiobenthic elements, especially of the psammobiontic ones, in the framework of the bottom

fauna rather than showing the relationship between organisms and environmental conditions

which have been amply expounded in various Romanian ecological works (Bacescu, Dumitrescu,

Manea, Por, and Mayer, 1957; Bacescu, Gomoiu,

Bodeanu, Petran, Miiller, and Stanescu, 1965; Bacescu, Gomoiu, Bodeanu, Petran, Miiller, and

Manea, 1965; Bacescu, Gomoiu, Bodeanu, Petran,

Muller, and Chirila, 1967; Gomoiu, 1966, 1968,

1969; Gomoiu and Muller, 1962).

Another problem in meiobenthic ecology which

will be emphasized is that of microphytobenthos.

Among sources of food for benthos—other than

animal and vegetable, organic debris, dead and

dying animals, suspended plankton and organic detritus—algal microflora represent a highly importance source. Literature on the microflora of silty

and rocky bottoms is rather abundant but studies

of sandy bottoms are only beginning. Bodeanu has

found in the last few years a varied and rich flora

of psammophilous diatoms (Bodeanu, 1964, 1968).

Over 210 microbenthic diatoms species have

been identified in the fine, quartziferous sand zone

of the Romanian littoral. Most of these forms, represented by Pennata, are mobile, noncolonial diatoms and are adapted to the very harsh conditions

of the sand biotope. Many of these are smaller

than 20 p. Not only are the psammobiontic microphytobenthos interesting from a qualitative point

of view but the quantitative values recorded are

quite striking.

The average size of sand grains on sandy bottoms is 90 fi at a depth of 8 to 16 m. Here, environmental conditions are rather constant as compared to those in shallower depth, and diatom

concentrations of 85,600 cells/cm2 (or 856,000,000

cells/m2) have been recorded. These records are

far higher than the number of planktonic microphyta in a cubic meter! In the Romanian littoral,

the variable quantities of psammobiontic microphytobenthos have an average of about 72,000,000

cells/m2 and 253 mg/m2 (Bodeanu, 1968). In

spite of these variations, the benthic microflora is

still the only autotrophic photosynthesizing element that increases the primary trophic level,

being the main supplier of psammobiontic microfauna food. Thus, the microphytobenthos is an important trophic element on the sea bottom, being a

source of nutrition for many benthophagic animals,

viz. filter feeding or actively "grazing" molluscs,

ciliates, copepods, ostracodes, and certain fishes (juveniles of Pleuronectres flesus Linn^, Mugil Linne\

and, presumably, Pomatoschistus microps Kessler,

Callionymus belenus Risso, Blennus Walbaum,

etc.). The significance of the microphytobenthos in

the nutrition of molluscs has been demonstrated

(Bodeanu and Gomoiu, 1964). Analysis of the diet

of ten mollusc species, mostly psammobiontic,

yielded 92 microphytic species of which 75 species

are exclusively benthic.

Thus, we see the great importance of meiobenthos in the economy of the sea. It is vitally necessary to analyze in detail the complex ecology of

meiobenthos, as shown above, as well as all possible abiotic and biotic environmental factors.

Literature Cited

Bacescu, M.

1961. Cercetari fizico-chimice §i biologice romanefti la

Marea Neagra, efectuate in perioada 1954-1959.

Hidrobiologia, 3:17-46.

1963. Contribution a la biocoenologie dc la Mer Noire.

L'£tage periazoique et le fades dreissenifere, leurs

caracteristiques. Rapports et Proces-Verbaux des

Reunions, Commission Internationale pour I'Exploration Scientifique de la Mer Me'diterranee,

17:107-122.
160

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

1966. CercetSri romanesti privind microbentosul Marii

Negre. Studii si Cercetari de Biologie, seria Zoologie, 18(5) :415-423.

Bacescu, M., and F. £. Caraion

1956. Animate mincStoare de Foraminifere. ComunicSrile

Academiei Republicii Populate Romdne, 6(4):551-

553.

Bacescu, M.; H. Dumitrescu; V. Manea; F. Por; and R. Mayer

1957. Les sables a Corbulomya (Aloidis) maeotica Mil.—

base trophique de premier ordre pour les poissons

de la Mer Noire. I. Aspect hivernal de la biocenose.

Travaux du Museum d'Histoire Naturelle "Grigore

Antipa," 1:305-374.

Bacescu, M.; £. Dumistrescu; A. Marcus; G. Paladian; and

R. Mayer

1963. Donnees quantitatives sur la faune petricole de la

Mer Noire a Agigea (secteur Roumain), dan les

conditions speciales de l'annee 1961. Travaux du

Museum d'Histoire Naturelle "Grigore Antipa,"

4:131-155.

Bacescu, M.; M. T. Gomoiu; N. Bodeanu; A. Petran; G.

Miiller; and S. Stancscu

1965. Recherches ecologiques sur les fonds sablonneux de

la Mer Noire (Cote Roumaine) . Travaux du

Museum d'Histoire Naturelle "Grigore Antipa,"

5:33-81.

Bacescu, M.; M. T. Gomoiu; N. Bodeanu; A. Petran; G.

Miiller; and V. Manea

1965. Studii asupra varia^iei viefii marine in zona

litorala nisipoasS la nord de Constanta. Ecologie

Marina, 1:7—138.

Bacescu, M.; M. T. Gomoiu; N. Bodeanu; A. Petran;

G. I. Muller; si V. Chirila.

1967. Dinamica populajiilor animale si vegetate din zona

nisipurilor fine de la nord de Constanta in conditiile anilor 1962-1965. Ecologie Marina, 2:7-167.

Bodenau, N.

1964. Contribution a l'etude quantitative du microphytobenthos du littoral roumain de la Mer Noire.

Revue Roumaine de Biologie, series Zoologie,

9(6):435-445.

1968. Recherches sur le microphytobenthos du littoral

roumain de la Mer Noire. Rapports et ProcesVerbaux des Reunions, Commission Internationale

pour I'Exploration Scientifique de la Mer Mediterranee, 19:205-207.

Bodeanu, N., and M. T. Gomoiu.

1964. Donnees sur l'importance des microphytes dans la

nourriture des Mollusques. Revue Roumaine de

Biologie, series Zoologie, 9:211-220.

Gomoiu, M. T.

1966. Ccodynamique du bivalve Aloidis (Corbulomya)

maeotica Mil. de la Mer Noire. Travaux du Museum d'Histoire Naturelle "Grigore Antipa," 6:39-56.

1968. On the Effects of Water Motion on Marine Organisms in the Mesolittoral and Infralittoral Zones of

the Rumanian Shore of the Black Sea. Sarsia,

34:95-108.

1969. Studiul sedimentelor nisipoase de la litoralul

romanesc al MSrii Ncgre. Ecologie Marina", 3:227-

325.

Gomoiu, M. T., and G. I. Miiller

1962. Studies Concerning the Benthic Association Dominated by Barnea Candida in the Black Sea. Revue

de Biologie, Academie de la Ripublique Populaire

Roumaine, 7:255-271.

Mclntyre, A. D.

1969. Ecology of Marine Meiobenthos. Biological Reviews, 44:245-290.

Peres, J. M., and J. Picard

1959. On the Vertical Distribution of Benthic Communities. Preprints of the First International Oceanographic Congress, New York, pages 349-350.
Siegfried Husmann Ecological Studies On

Freshwater Meiobenthon

in Layers of

Sand and Gravel

ABSTRACT

The sand and gravel sediments of freshwater

streams contain a rich meiofauna. The biotopes

are considered as biozones of the groundwater

ecosystem. The ecological relationships of the interstitial meiofauna to groundwater biotopes are

discussed.

Investigation of interstitial water in benthal1 layers of sand and gravel shows that the microcaverns

in such subtrates can be typical biotopes of a rich

freshwater meiofauna. Benthal biocoenoses of this

sort can consist of freshwater organisms of the following taxa: Hydrozoa, Turbellaria, Nematoda,

Oligochaeta, Cladocera, Harpacticoida, Cyclopoida,

Syncarida, Amphipoda, Halacaridae, Hydrachnellae, and young larvae of insects. The biotopes of

such benthal interstitial fauna are to be considered

as biozones of the ecosytem "groundwater" (stygocoen). This concept is indicated by Thienemann

(1925) in his definition of the term "ground

water": "By ground water we mean all water

under the surface of earth and circulating in the

outermost crust of the earth." In this sense, water

in interstitial benthal regions may be considered as

a part of the groundwater. Moreover, Thienemann

mentioned in this definition that groundwater can

i Terms ending in "al" describe a biotope, those ending in

"on" describe a biocoenose, and those ending with "coen"

describe the complete ecosystem.

Siegfried Husmann, Limnologische Flusstation, Max-PlanckInstituts fur Limnologie, Schlitz, West Germany.

be in contact with surface water in the beds of rivers and l<ikes.

Nearly 20 years after the publication of the cited

definition Chappuis (1942) discovered biocoenoses

of stygobiont, stygophile, and stygoxene freshwater

organisms living together in interstitial waters of

sandy and gravelly riverbeds. His discovery (see

also Chappuis 1944) and the investigations of

other authors (Karaman, 1935; Angelier, 1953;

Ruttner-Kolisko, 1953, 1954, 1956; Viets, 1955,

1959; Husmann, 1956; Motas, 1958, 1962; Orghidan, 1959; MeStrov, 1960; Ponyi, 1960; Schwoerbel,

1961a,b, 1964, 1967; Picard, 1962; Sterba, 1965;

Bou and Rouch, 1967; Gourbault and LeisherMoutou6, 1967; Rouch, 1968; Tilzer, 1968) have

added new points of view in regard to benthal productivity, especially in sandy and gravelly riverbeds.

The stygophile meiofauna elements of such ecosystems have otherwise generally been found as

sporadic individuals in deposits of mud and detritus or in moss (Dittmar, 1955; lilies, 1952). Apart

from these investigations, most researchers have

dealt particularly with the macrobenthon.

The investigations of interstitial benthal meiofauna, however, show that the interstitial waters

of sandy and gravelly beds of streams are by far

the princpal biotopes of these freshwater meio-organisms and also show the highest productivity in

these ecosystems (Schwoerbel, 1967).

As mentioned, the biotopes of these benthalmixed biocoenoses of stygobiont, stygophile, and

stygoxene interstitial freshwater organisms are to

be regarded as a part of the ecosytem "groundwater." This also seems to correspond to the similar

biotopes of lakes (Noodt, 1952, 1954, 1955; Pen161
162

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

nak, 1939, 1940, 1951; Ruttner-Kolisko, 1953, 1954,

1956; Husmann, 1969).

The position of those benthal-mixed biocoenoses

within the various communities of subterranean

freshwater organisms may be determined by manysided ecological investigations of groundwater

fauna.

Investigations of the subterranean freshwater

fauna in sandy and gravelly riverbeds as well as in

wells, springs, and caves of a geomorphologically

heterogeneous region in the Weser-System (Germany) produced the first information about the

ecological relations of interstitial benthal to other

groundwater biotopes (Husmann, 1956).

The clearly proved dependence of stygobiont

groundwater organisms on the structure of the subterranean biotopes show that interstitial waters in

sand and gravel were the main biotopes of nearly

all the stygobionts caught. Continuous intersitial

biotopes in layers of sand and gravel can reach

from terraces and valley floors into sandy and gravelly riverbeds. Therefore, in such underground regions there are no ecological limits conditioned by

substratum for interstitial groundwater organisms.

Because of underground conditions of this sort, it

is understandable that most of the stygobionts living in the interstitial underground water of terraces and valley floors also could be caught in

interstitial waters of sandy and gravelly riverbeds

(Figure 1).

Those stygobionts which are ubiquitous in waters of sand and gravel may, as already mentioned,

form mixed biocoenoses with elements of the

surface or epigean freshwater fauna.

The existence of two very different interstitial

biozones results from the following underground

ecological conditions: (a) subterranean, interstitial

biotopes situated far from rivers and, moreover, extremely isolated from coenological influences of

surface waters; and (b) benthal biotopes in layers

of sand and gravel in riverbeds with coenological

influences of the interstitial groundwater biocoenoses of the neighboring valley floor, and with immigration of organisms living in the connected surface water.

By and large, the first biozone is colonized by

stygobionts, here and there united with extreme

stygophile species that live there only sporadically.

This stygozone, which is extremely isolated against

coenological influences of surface-water biocoenoses, is to be regarded as the kernel zone of the

ecosytem "stygocoen." It can be characterized by

the designation "eustygocoen."

Because benthal biotopes in sand and gravel are

biozones with coenological influences from groundwater and surface water, they can be characterized

by demonstrable terms. Accordingly, the interstitial

benthal ecozone of mountain streams was named

"rhithrostygocoen" in reference to the surface-water ecosytem "rhithrocoen" (lilies, 1961; Husmann,

1970) and the groundwater ecosytem "stygocoen."

In this way the interstitial stygozone of rivers (ecosystem "potamocoen") and of lakes (ecosystem

"eulimnocoen") have been characterized as "potamostygocoen" and "eulimnostygocoen" (Husmann,

1970).

The colonization of intersitial biotopes in sand

and gravel by elements of the freshwater intersitial

fauna is dependent on the size of the interstitial

spaces, which, in turn, depends on the grain size.

The nature of substrate is to be seen, therefore, as

the most important factor for the characterization

of our interstitial biotopes.

The components of sand, gravel, and shingle are

classified by geologists as "Psammite" (diameter, 2

to 0.02 mm) and as "Psephite" (diameter, 2 mm).

Biotopes in psammite are named "mesopsammal"

(Remane, 1940), those in psephite are called "mesopsephal" (Husmann, 1966). The biocoenoses living in these biotopes are "mesopsammon" and

"mesopsephon."

Sandy and gravelly biotopes of intersitial ecozones and the biocoenoses living in them are

marked more clearly with regard to the nature of

substrate; for example, "eustygopsammal" (mesopsammal of eustygocoen) and "potamostygopsammon" (mesopsammon of ecosytem potamostygocoen). See Figures 2, 3.

The ecological system of benthal and eustygal

interstitial freshwater biocoenoses given here may

be completed by characterizing two other biotopes

of benthal interstitial biocoenoses. One of these is

to be found in sandy and gravelly deposits in the

outflows of springs called "krenostygopsammal"

and "krenostygopsephal," respectively. The other is

the interstitial benthal of streams in caves called

"troglostygopsammal" and "troglostygopsephal"

(Figure 4).
NUMBER 76 163

Turbellaria (STMJOEIWOKMII)

Proromonofrasis cenfrophora MISMOER

Dendrocoefum boeffgeri AN on LAN

Archiannelida (URRiNOELWifeMER)

Trogfochaetus beranecfci DCLACHAUX

Ostracoda

Candona triqumtra KIM

Candona n. »p. i

Candona n. sp. 2

Candona n. ip. 3

Copepoda (RUMRFUSSKRIBU)

ChappuMNis sjnaari CHAFPUIS

(Moraria varica oCAtm)

Parasfanocaris fontinali* SCHNITT. * CHA*».

Parasrenocaris phyllura KIEFER

Parasfenocaris nol/i Kltn*

Poro*»«nocori* htumannt CHAPPMS

(Acanf hocyclops venuir us NORMAN a SCOTTJ

(Diacyclops /ongutdoidas - Grwppa)

Gremtarimlla unhetiger MAITI *

Syncarida

Bathynalla spec.

Amphipoda (FIOHKKBSI)

Niphargut fontamn IATI

Niphargut aquihx sotiovn

Nipfiargu* scheflenbergi KARAMAN

Niphargmllu* nolli soHUINMRa

Mkronjpharguc leruthi SCHELLENMRG

Crangonyx •ubferranaus BATI

Bogidimlla albitrtimagni HIRTZOO

Isopedo (ASSEIN)

Asa//u* (Proatallus) cavaticu* SCHIOOR

Acorina (MILKN)

lobonalocarus weberi quadrip. (WALTER)

So/doneMonyx chappuisi WALTER

StygonVemlMUin fcercyniensis vim

Lebarfia fleborfio) husnranni VKTS

Sandakra apaciesa VIETS

Atrattides aeufiros/ris gifafcerimorgin. v.

Faltria M(btarranea VKTS

Mtria pugionipalpi* VIETS

latnaxena pygmoua VIETS

Kongsbaram angucta WAITER

Kongsbargta pecfinigara MOT.* TANNASKongsbargia danfala WALTER

Srygamomoma fafqsas SZALAT

Naoocorus fiibarn/cus MALIERT

Biotopes of the Subterranean Water Fauna

in the Harz - Weser - Region

Interstitial Water

in Sand and Gravel

tank* of H M rl».r.

bivastigatad

w

i _

• • •

5 5

• ••

L

• • •

1

•tea

•••a

• ••

• ••

O

RBBR

••• 1

••••

• • •

• • •

••••

Rtaa

• B H

• • •

• • •

•••

••• R

Valley FlMr ond

RalMd IfrracH

w

• • •

RHR1

5H

• H i

• •

• • •

L

• • 1

mmm

RRRRB

• • •

•RRR1

o

• ••

Water in Caves

and Crevices

ii

1—1—

• •

Spring. | W.ll.

of tho *r.o fcm*tie«t*d

L o

RRRM

' w L O

RBRH

FIGURE 1.—The ecological distribution of stygobiont groundwater organisms in various valleys

of the Weser-system (W, Weser; L, Leine; I, Innerste; O, Oker) and in caves of the Harz

Mountains.

The limnobenthal interstitial-mixed biocoenoses

"rhithrostygon," "potamostygon," and "eulimnostygon" cannot be separated from the coenologically

isolated biocoenoses "eustygopsammon" and "eustygopsephon" (Figure 4) by clear ecological limits.

On the contrary, there are between them biozones

of ecological indistinctness which correspond to the

zones of ecological "Unscharfe" of Schwabe and
164 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

RHtTHROSTYGOPSEPHAl

EUSTYGOPSEPHAL

POTAMOSTYGOPSEPHAL

Stygopsephal

PSEPHITE

0 > 2mm

Stygopsephon

RHITHROSTYGOPSEPHON

— | EUSTYGOPSEPHON

POTAMOSTYGOPSEPHON

Biotopes Sand, gravel, shingle Biocoenoses

RHITHROSTYGOPSAMMAL

EUSTYGOPSAMMAL

POTAMOSTYGOPSAMMAL

Stygopsammal

PSAMMITE

0 2-0,02mm

Stygopsammon

RHITHROSTYGOPSAMMON

EUSTYGOPSAMMON

POTAMOSTYGOPSAMMON

FIGURE 2.—Biotopes and biocoenoses of groundwater organisms in sand, gravel, and shingle

of the following ecosystems: rhithrocoen (mountain streams, I, O, as in Figure 1); potamocoen (rivers in lowlands, W, L, as in Figure 1); and eustygocoen (underground of valley floors

and raised terraces without coenological influences out of surface waters; see Figure 1).

Rhithrocoan

Rhithrobanthal

Rhithrostygcri

RhifhrO"

-

Rhithro—

stygopsaphal

Potomecoti

Potamobanthol

Potamostygal

PotomoEUSTYGOPSAMMAL

..r^P^a.

EUSTYGAL

STYGOCOEN

Eulimnocoan

|

Eullmnobanthal

1

Eulhnnottygal

EulimnoEUSTYGOPSEPHAL

Eulh

stygo

nneisaphal

FIGURE 3.—The ecological system of groundwater biotopes in layers of psephites and psammites of benthal and eustygal underground regions.

Klinge (1960). The ecological indistinctness mentioned in such intermediary biozones is characterized by a diminution of stygophile freshwater organisms in proportion to the distance from benthal

biotopes of the interstitial-mixed biocoenoses. With

the increase in distance from the benthal interstitial biocoenoses there is an increase in the number

of stygobionts until the coenological state of "eustygocoen" is reached (Figures 3, 4).

The variety of coenological conditions, depending on the distance from eustygon or from

benthostygon, demonstrates the impossibility of integrating the biocoenoses of such intermediary biozones in a typological system. It is only possible to

mark (as we have done) on both sides of these indefinite ecological border zones the clearly definable kernel regions "eustygocoen," respectively

"rhithrostygal," "potamostygal," and "eulimnostygal" (Figure 3).

The mesopsammal and mesopsephal biotopes are

found in deposits of varying size in the benthal

and eustygal regions. Compared to the mesopsephal, the mesopsammal is found much more in nature. Apart from homogeneous deposits of sand in

beaches of lakes or in banks of rivers, mesopsammal biotopes often fill the interstices in gravel and

in coarse-grained rubble forming an interpsephite

mesopsammal biotope. In this way the extent of
NUMBER 76 165

RHITHRON POTAMON EULIMNON

Rhithrostygon Potamostygon Eultmnostygon

Rhithrostygopsammon

Rhithrostygopsephon

Potamostygopsammon

Potantostygapsephon

Eulbnnostygopsomman

Eulimno-

«tygop««ph©n

EUSTYGOPSAMMON

Krenostygepsammon

Krenostygopsephon

Krenostygon

EUSTYGOPSEPHON

EUSTYGON

STYGON

Troglostygon

Troglostygopiamnr

Troglostygopsaphon

FIGURE 4.—The ecological system of groundwater biocoenoses in layers of psephites and psammites of eustygal and benthal underground regions including the groundwater fauna in caves

(troglostygon) and springs (krenostygon).

RHITHROSTYGON

Fuldo, Germany

POTAMOSTYGON

Lulejaure, Sweden

EULIMNOSTYGON

Storsjon, Sweden

Hydrozoa

Turbellaria

Namatoda

Oligochaeta

Cladocera

Ostracoda

Harpacticoida •

Parcutenocori* I

Cyclopoida •

Bathynel/o I

Niphargus •

Limnohalacaridae •

Hydracnnellae I

Ephemerida, La. H

Plecoptero, La. I

Coleoptera,La. I

Chironomidae, La. •

30 40 0 3 10 20 30 40 0 5 10 30 SO

Parcont of tota l catch

FIGURE 5.—The percentage quota of biomass from interstitial biocoenoses of sandy and gravelly

benthal biotopes of a mountain stream (rhithrostygon; Fulda), of a lowland river (potamostygon;

Lulejaure) and of a lake (eulimnostygon; Storsjon).

mesopsephal biotopes in mixed deposits of sand

and gravel is greatly reduced. Consequently, most

interstitial organisms in all the mentioned biotopes

are recruited from elements of freshwater meiofauna (see Figure 1).

In benthal-mixed biocoenoses, Nematoda, Oligochaeta, Harpacticoida, and Cyclopoida comprise

the most important meio-elements of interstitial

biocoenoses. This applies to interstitial biotopes in

European as well as in tropical regions (Figures 5,

6). In temperate and tropical regions species of the

family Bathynellidae and of the copepod genus

Parastenocaris Kessler are the most characteristic

elements of mesopsammal freshwater meiofauna.

This is so in the eustygocoen as well as in the

rhithro-, potamo- and eulimnocoen. In contrast

with stygobionts of such a ubiquitous occurrence

in interstitial waters, many Hydrachnellae species

are found only in the benthal interstitial of rhithrostygocoen. The ecological findings of investiga-
166

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

RHITHROSTYGON

Brooklet near Belem

Amazon Region

POTAMOSTYGON

Rio Tapajos

Amazon Region

Namatoaa •

Oligochaeta •

Cladocera

Harpactkoida I

Parastenacaris •

Cyclopoiaa

Leptobathynalla •

Limnohalacaridae I

Chironomidae I

Dryopidaa

O S 10 2 0 ' 3 0 ' 4 0 5 0 6 0 7 0 0 3 10 1030405 0 6 0 7 0

Percent of tota l catch

FIGURE 6.—The percentage quota of biomass from interstitial biocoenoses in tropical sandy

and gravelly benthal biotopes of rhithrostygon (sampled by W. Sattler) and of potamostygon

(sampled by H. Sioli).

Hydrachnellae Zone

Ooo

°

Limnohalacaridae Zone

FIGURE 7.—The gravelly and sandy riverbed of the Oker mountain stream in the Harz Mountains with a schematic cross section of one riverside showing the distribution of Hydrachnellae

and Limnohalacaridae in the interstices of substratum and, with this, the forming of the

"Hydrachnellae Zone" and the "Limnohalacaridae Zone."

tions about the benthal interstitial fauna in rhithrostygocoen of European countries showed that

coenobiont and coenophile Hydrachnellae are connected with Limnohalacaridae in their distribution

in sandy and gravelly riverbeds. They can mark two

biozones that are called the "Hydrachnellae zone"

and the "Limnohalacaridae zone" (Husmann,

1966). See Figure 7. The biocoenoses of eustygo-
NUMBER 76

167

STYGOCOEN

STYGOPSAMMAL STYGOPSEPHAL

(MIXO-)OLIGOHALINE

"•S-—0.3

(MIXO-)OLIGOHAUNE

(MIXO-)MESOHALINE

~ 30 18

(MIXO-)POLYHALINE

EUHALINE

HYPERHALINE

THALASSOPSAMMAL THALASSOPSEPHAL

ENDOGAEOTHALASSOCOEN

FIGURE 8.—Zones of halinity in the mesopsammal and mesopsephal passage between stygocoen

and endogaeo-thalassocoen with marks of salinity (ppt).

Mariiflla

Traglochaetus

Parattenocari*

Nifocrelfo

Stygopscmmen

- I

•

e

m

•<

<Q

0

3

-

Stygopssphon

STYGON

- TROGLON -

|THALASSON|

Thalassopsammon

•4

a

» • ito «T

n

Thalassopsephon

MicropaniMffus

Mkrocharon

Angtlhra

Microeerbarws

Niphargus

Salentinmlla

BogUMIa

Ingolfimlla

FIGURE 9.—Mesopsammal and mesopsephal stygo-organisms of marine origin and their distribution in subterranean freshwater biocoenoses.

coen may also be characterized by stygobionts,

which are found only in these coenologically isolated regions (Figure 1).

As mentioned earlier, the interstial benthal biocoenoses rhithrostygon, potamostygon, and eulimnostygon exist in the ecological periphery of the

interstitial groundwater eco-region, which is characterized by mixed biocoenoses of stygobiont, stygophile, and stygoxene freshwater meio-organisms.

The benthal coenoses rhithrostygon, potamostygon, and eulimnostygon are not the only mixed

biocoenoses on the ecological periphery of the sty-
168

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

gocoen. Coastal groundwater is another such mixed

biocoenosis; it is composed of elements of stygon

and those of the neighboring interstitial marine

water.

The coastal groundwater biocoenosis is of special

importance because the (mixo) oligohaline thalassopsammal and thalassopsephal zones are to be regarded not only as zones of ecological contact between marine and limnic meiofauna (Figure 8)

but also as palaeobiotopes of a number of stygobiont freshwater organisms which have immigrated

into the benthal and eustygonal biotopes of the

limnic groundwater fauna (Figure 9).

So, the ecological problems of the coastal groundwater form a meeting point for meiobenthologists

of marine and freshwater ecology, and the many

common problems (Husmann, 1967) may give rise

to a cooperation of marine ecologists and limnologists.

Literature Cited

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1953. Recherches Icologiques et bioge'ographiques sur la

faune des sables submerges. Archives de Zoologie

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Bou, C, and R. Rouch

1967. Un nouveau champ de recherches sur la faune

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Chappuis, P. A.

1942. Eine neue Methode zur Untersuchung de Grundwasserfauna. Acta Scientifica Mathematica et Naturalia Universitalis Francois-Joseph, 6:1-7.

1944. Die Grundwasserfauna de Koros und des Szamos.

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1-42.

Dittmar, H.

1955. Ein Sauerlandbach. Untersuchungen an einem

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Gourbault, N., and F. Lescher-Moutoue"

1967. Sur la Faune hypoge'e peuplant le sous-e"coulement

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Husmann, S.

1956. Untersuchungen uber die Grundwasserfauna zwischen Harz und Weser. Archiv fur Hydrobiologie,

52:1-184.

1966. Versuch einer okologischen Gliederung des interstitiellen Grundwassers in Lebensbereiche eigener

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1967. Klassifizierung mariner, brackiger und limnischer

Grundwasserbiotope. Helgoldnder wissenschaftliche

Meeresuntersuchungen, 16:271-278.

1970. Weitere Vorschlage fur eine Klassifizierung subterraner Biotope und Biocoenosen de Siisswasserfauna. Internationale Revue de gesamten Hydrobiologie, 55:115-129.

lilies, J.

1952. Die Molle. Faunistisch-okologiesche Untersuchungen in einem Forellenbach im Lipper Bergland.

Archiv fur Hydrobiologie, 46:424-612.

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Karaman, S.

1935. Die Fauna der unterirdischen Gewasser Jugoslaviens.

Verhandlugen der Internationale Vereinigung fur

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Kulhavy, V.

1961. Uber das Vorkommen der west- und osteuropaischen

Elemente in der Crustaceenfauna der bohmischen

unterirdischen Gewasser. Acta Societatis Zoological

Bohemoslovenicate, 25:297-301.

Mestrov, M.

1960. Faunistisch-dkologische und biozonologische Untersuchungen unterirdischer Gewasser des Save tales.

Bioloski Glasnik, 13:73-109.

Motaj, C.

1958. Freatobiologia, a noua ramura a Limnologiei. Natura, 10:95-105.

1962. Proe'de's de sondages phrlatiques. Divisione du domaine souterrain. Classification £cologique des animaux souterrains. Le psammon. Acta Musei Macedonici Scientiarum Naturalium, Skoplje, 8:135-173.

Noodt, W.

1952. Subterrane Copepoden aus Norddeutschland. Zoologischer Anzeiger, 148:331-341.

1954. Copepoda Harpacticoida aus dem limnischen Mesopsammal der Turkei. Veroffentlichungen der Hydrobiologischen Naturwissenschaftlichen Fakultdt

der Universitat Istanbul, 2:27-40.

1955. Limnisch-subterrane Harpacticoiden (Crust. Cop.)

aus Norditalien. Zoologischer Anzeiger, 154:78-85.

Orghidan, T.

1959. Ein neuer Lebensraum des unterirdischen Wassers:

der hyporheische Biotop. Archiv fur Hydrobiologie,

55:392-414.

Pennak, R. W.

1939. A New Copepod from the Sandy Beaches of a

Wisconsin Lake. Transactions of the American

Microscopial Society, 58:224-227.

1940. Ecology of the Microscopic Metazoa Inhabiting the

Sandy Beaches of some Wisconsin Lakes. Ecological

Monographs, 10:537-615.

1951. Comparative Ecology of the Interstitial Fauna of

Fresh Water and Marine Beaches. Annales de

Biologie, 27:449-480.

Picard, J. Y.

1962. Contribution a la connaissance de la faune psammique de Lorraine. Vie et Milieu, 13:471-505.
NUMBER 76

169

Ponyi, J.

1960. tJber im interstitialen Wasser der sandigen und

steinigen Ufer des Balaton lebende Krebse (Crustacea). Annales de Biologie Tihany, 27:85-92.

Riemann, F.

1966. Die interstitielle Fauna im Elbe-Aestuar. Verbreitung und Systematik. Archiv fur Hydro biologie,

supplement, 31:1-279.

Remane, A.

1940. Einfiihrung in die Zoologische Okologie der Nordund Ostsee. Tierwelt der Nord- und Ostsee. 238

pages.

Rouch, R.

1968. Contribution a la connaissance des Harpacticides

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Ruttner-Kolisko, A.

1953. Psammostudien I. Das Psammon des Tornetrask in

Schwedisch-Lappland. Sitzungsberichte der Osterreichischen Akademie der Wissenschaften, mathematisch-naturwissenschaftliche Klasse, 162:129-161.

1954. Psammostudien II. Das Psammon des Erken in

Mittelschweden. Sitzungsberichte der Osterreichischen Akademie der Wissenschaften tnathernatischnaturwissenschaftliche Klasse, 163:301-324.

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Idrobiologia, 9:365-402.

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1960. Gewasser und Boden als Forschungsgegenstand.

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Schwoerbel, J.

1961a. Ober die Lebensbedingungen und die Besiedlung

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Sterba, O.

1965. Plazivsky (Copepoda, Harpacticoida) Moravy a

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Thienemann, A.

1925. Die Binnengewasser Mitteleuropas. Die Binnengewasser I. 255 pages. Stuttgart: Schweizerbart.

Tilzer, M.

1968. Zur Okologie und Besiedlung des hochalpinen hyporheischen Interstitials im Arlberggebiet (Osterreich). Archiv fur Hydrobiologie, 65:253-308.

Viets, K.

1955. In subterranen GewSssern Deutschlands lebende

Wassermilben (Hydrachnellae, Porohalacaridae und

Stygothrombiidae). Archiv fur Hydrobiologie, 50:

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H. Kiihl On Changes of the

Interstitial Water

after Decomposition of

Organic Matter

ABSTRACT

The production of NH4

+

, NO2~, and NO3- from

decaying organic matter under laboratory conditions was investigated in a series of experiments

utilizing various grain sizes of sediment. The relationship between the production of these compounds and various environmental parameters (pH,

alkalinity, and oxygen) is noted and the relationship between the products of decay investigated

and grain size is discussed.

It often has been reported in studies carried out

on meiofauna that certain groups of organisms have

disappeared when the same place was re-investigated at a later date. Investigations have shown

that interstitial water does not necessarily have the

same chemical composition as the surrounding

water above the bottom—for example, the flotsam

lying on the bottom had eutrophied the interstitial

water. Initially, the oxygen content was reduced.

Such changes in the environment can take place

very rapidly. It may be that this condition could

cause the disappearence of a population of a certain species (Kiihl and Mann, 1966a,b).

Previously, the author found that in a large bed

of Mya arenaria about 80 percent of the individuals

had died in a short period of time. The excavated

sediment had a strong odor of H2S and a black

color to a depth of 20 cm. The density of the Mya

population was about 100 to 150 specimens/m2

(Kiihl, 1952). The question arose as to what would

happen to the decomposition products of larger

H. Kiihl, Institut fur Kiisten- und Binnenfischerei, Laboratorium Cuxhaven, Cuxhaven, West Germany.

macro-organisms—such as molluscs, worms, etc.—

that are produced in the sediment at a certain

depth. Do such products come to the surface water;

are they partially washed away; or do they remain

in the sediment, and, if so, to what extent do diey

influence the surrounding interstitial water?

The experiments reported in this paper were a

continuation of previous investigations on nitogen

metabolism in aquaria (Kiihl and Mann, 1956,

1961, 1962). The organic breakdown was not investigated during these experiments but has been

studied by Hecht (1933) and Krause (1959, 1961).

Only the final products of decay—including NH4

+

,

NO2" and NO3~, which can be poisonous to organisms—water temperature, salinity, pH, alkalinity,

and oxygen content were investigated. The methods

used were the same as in the previous experiments

(Kiihl and Mann, 1956, 1961, 1962).

The experiments were conducted in unaerated,

5-liter aquaria. From 5 to 10 g of mussel flesh

(Mytilus and Mya) was put into the sediment at a

depth of 5 cm. Four different grain sizes were used

—mud, sand, and two different coarse sands with

broken shells (Figure 1). The sediment was washed

and dried, but not ashed. A control experiment

without flesh demonstrated the normal decomposition, of importance especially in the mud series.

Further experiments were made in glass tubes with

lengths of 30 and 55 cm and a diameter of 5.5 cm.

The tubes had two and five lateral outlets. In this

way the dispersal of the decomposition products

could be determined.

In the first series of experiments (series 1), 5 g

of Mya flesh were placed in three separate aquaria.

In aquarium 1, the flesh was placed on the surface

of the sediment; in aquarium 2, the flesh was placed

171
172

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

v.

«o

90.

60

70

SO

SO

40

30

X

10

<!25fJ'0Jm/.

Htttrag medium- eoorst-sand

without grant

100

90

to

70

SO

SO

to

30

20

K

Htttrog. coarse- sand

Md tSOfJ

m

90

to

70

60

SO

to

30

X

10

<63/J .59%

Htttrog. silt*fine sand

wo §

90

SO

70

SO

SO

30

X

10

Hotnog. fintSotut

6X BOO

S3 125 250 500 1000 2000 4000

FIGURE 1.—Grain size of the bottom material used in experiment series 2-5.
NUMBER 76

173

into sandy mud sediment. Aquarium 3 served as a to 17 June 1953; the salinity was 22.43 ppt and

control, i.e., no Mya flesh was placed in the aquar- the water temperature 16.5° to 22.8° C. The results

ium. This series was conducted from 13 May 1953 of this series are shown in Figure 2. The ammoni25 •

20 •

75

10

9 •

8

WT °C

PH

t / c

• • — -

"*~"~ o

— «

9

o o

•• •

7

6

5

4

3

2 :\f

16 •

14

12

10

6

6

4

2

SBV (=m - alkalinity )

• ' \

• Aquarium I (Mya in the bottom )

• • Aquarium I! (Mya on the bottom)

o o Aquariumll (Control )

\

250*1

200\

100 , ' • x

*"°--»> -'->

June 7953

FIGURE 2.—Experiment series 1.
174

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

fication started immediately after beginning the

experiment. In aquarium 1, the highest ammonia

content, 15 mg/liter, was found after 19 days. In

aquarium 2 there was decay in the sediment and

NH4

+

 was found in the surrounding water but after

13 days the NH4

+

 content was only half that of

aquarium 1. In aquarium 3, without additional

organic matter, NH4

+

 appeared to be coming from

the muddy sediment and the maximum of 4 mg/

liter was found within 9 days.

Nitrite and NO3- were not detected before the

end of the experiment in aquarium 1. In aquaria

2 and 3 quantities of these compounds were very

low, a maximum of 0.8 mg NO2~ and 0.4 mg NO3~.

In aquarium 3 these compounds were detected at

the beginning of the experiment and disappeared

later.

The pH and alkalinity differed significantly in

the three experiments. In aquarium 1 green algae

began to grow on June 1. The pH increased

rapidly, the alkalinity decreased, and the oxygen

content reached very high values (238 percent oversaturation) as a result of assimilation. The pH and

alkalinity cycles were more normal in aquaria 2

and 3; the alkalinity showed slightly more increase

in aquarium 2 than in aquarium 3.

The loss of oxygen in aquaria 1 and 2 was very

clear, with an increase beginning after one week.

In aquarium 2 the oxygen content was not very

high, about 50 percent of saturation.

The experiments of series 2 involved the use of

two types of sediment of different grain size, one

being coarse sand (500 fi) and the other coarse sand

with some shell particles (850 p). Four aquaria,

with the following combinations, were used: aquarium 1, 5 g of Mytilus flesh placed within 500-/1

sediment; aquarium 2, 5 g of Mytilus flesh placed

on the surface of the 500-/x sediment; aquarium 3,

control, only 500-/X, sediment; and aquarium 4, 5 g

of Mytilus flesh placed within 850-fi sediment. The

experiment was conducted from 8 March 1968 to

22 April 1969; the salinity was 31.13 ppt and the

water temperature was 19.6° to 22.6° C.

In aquarium 3, the control, no nitrification was

observed during the experiment because the sandy

bottom was without additional organic matter. The

pH values were 8.0 to 8.1. Within 40 days the alkalinity increased from 2.5 to 2.9. The oxygen content

varied between 89 and 140 percent of saturation. In

aquarium 2, decomposition occurred on the surface

of the sediment and ammonification started immediately; the maximum of 6.5 mg/liter NH4

+

 was

reached after 14 days. After an additional 14 days

the NH4

+

 disappeared (Figure 3). In aquarium 1

with mussel flesh in the sediment, ammonification

was observed after 12 days, and the maximum

(7 mg/liter) was reached a week later. Ammonification in aquarium 4, with coarse sandy sediment,

started within 4 days from the beginning of the

experiment. The amount of ammonification was

higher than in aquaria 1 and 2. After the decrease

of NH4

+

, the formation of NO2- and NO3~ in

aquarium 1 was less than in aquaria 2 and 4. The

disappearance after a short time apparently was

caused by the growth of a diatom layer on the

bottom.

The changes in the oxygen content were very

interesting. As expected, the oxygen content in

aquarium 2 was reduced to a minimum after a

short time. Fourteen days later, an increase began

approaching 100 percent saturation. Similarly, but

some days later, the oxygen in aquarium 4 diminished; on the other hand, the oxygen deficit was

not so obvious in aquarium 1, with the decrease

reaching only 70 percent of saturation. A second

decrease of oxygen probably was caused by the

oxidation of nitrogen compounds.

The experiments of series 3 were designed to

compare decomposition of mussel flesh in four

different sediments of different grain size. In aquarium 1, 5 g of mussel flesh was placed 5 cm deep in

sand having a median diameter of 500 p.; in

aquarium 4, the same, except for the sediment,

which was coarse sand with a median diameter of

850 fi; in aquarium 5, the same, except with mud

(median diameter, 50 to 60 /*); in aquarium 6, the

sediment was fine sand (median diameter, 200 p).

This series of experiments was conducted from

7 May 1968 to 21 June 1968; the salinity was 34.08

ppt and the water temperature 19.2° to 21.8° C. As

seen in Figure 4, ammonification occurred in all

aquaria. In the aquaria with sand—aquaria 1, 4,

and 6—ammonification started after 14 days. The

maximum value was between 2 and 3 mg/liter

NH4

+

. This was contrary to the results in aquarium

5, with the mud layer. Ammonia appeared in the

water 30 days later and very quickly reached a high
NUMBER 76

175

•—• •

w

8

6

4

2

I.S

Ifi

Ofi

4

3

2

I

NHT ' Aquariuml: MytHut in the bottom (Md 500(j)

Aquarium 2: M/titus on the bottom (Md 500 fi

Aquarium*: My til us in the bottom (850/j MU )

NO 2

diatoms

20 30 40

FIGURE 3.—Experiment series 2.

so days

value of 18 mg/liter. In the control (mud) the amnonificadon began sooner and increased to a high

amount (Figure 4). This apparently was caused by

organic substances in the mud layer. The formation

of NO2~ and NO3~ in aquarium 5 was higher than

in the other aquaria. Nitrate was seen only for a

short time, probably because diatoms grew on the

bottom. The oxygen content decreased before the

ammonification started in aquarium 5. The loss of

oxygen was high; in the other aquaria the oxygen

was reduced to 10 to 40 percent saturation.

In series 4, sand (median diameter, 500 /i) was

placed in a glass tube that was 55 cm long and 5.5

cm in diameter and that had outlets at 10 cm

intervals. Five grams of Mytilus flesh was placed

at a depth of 18 cm between outlets 2 and 3 (Figure 5). This experiment was conducted from 25

April 1968 to 21 June 1968; the salinity was 31.5

ppt and the water temperature was 19.8° to 22.5° C.

After three days the sediment surrounding the

mussel flesh turned black. Within the next eight

days the zone of reduction extended downward to

the bottom of the tube, but not to the upper end

at outlet 2. The ammonification was strongest at
176

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

40 45 days

FIGURE 4.—Experiment series 3.

outlet 3 (Figure 5) and less at outlets 4 and 5.

Above outlet 3, no NH4

+

 was observed. After 30

days NO2- appeared at outlet 2 above the decay

(Figure 5).

Series 5 was a similar experiment, except that the

glass tube was 30 cm long and 5.5 cm in diameter

tube was filled with coarse sand mixed with broken

shell (median diameter, 850 p) and 5 g of Mytilus

flesh was placed at a depth of 15 cm between outlets 1 and 2.

This experiment was conducted from 30 June

1968 to 29 August 1968; the salinity was 34.5 ppt

and had two outlets at a distance of 10 cm. The and the water temperature was 21.3° to 23.0° C.
NUMBER 76 177

NO/: 0

Z 2

NO 2-0 * 30-

$20

J

NO jo X

70 20 30 40 SC 60 70

FIGURE 5.—Experiment series 4, decomposition of Mytilus

flesh in a glass tube with five outlets in a sand (Md, 500 /t).

The results were very similar to those of series 4,

with differences caused by the use of sediment of a

different grain size. The black coloring below appeared sooner, reaching the lower end after 5 days,

but the reduction zone extended above outlet 1.

The oxidation zone was only some centimeters

broad and the limit not sharp.

The formation of NH4

+

 was very intensive in the

region of the mussel flesh. The maximum of 40

mg/liter was reached after ten days, and the decrease was very slow. Ammonification was observed

at the upper outlet 1, the maximum being 12 mg/

liter. Nitrite and NOS- appeared only at outlet 1,

above the decomposition spot.

The decomposition of organic substances in the

water column or in the bottom sediments is a complex interaction of abiotic and biotic factors. Likewise, nitrogen metabolism is of considerable complexity (Brand, Rakestraw, and Renn, 1937, 1939;

Cooper, 1937; Postma, 1966; Ulken, 1963; Wuhrmann and Woker, 1948, 1953). Botan, Miller, and

Kleerekooper (1960) report eleven reaction stages.

In the experiments reported here, only NH4+ and

the nitrification from NO,- to NO3- (series 2 and 3)

were analyzed.

Ammonia compounds can split in the following

manner: NH4

+

 + OH- ^ NH, + H^O, depending

on water temperature and pH. It is NH3 that is

very poisonous to organisms. Several groups of bacteria participate in all the transformations of NH4

+

to NO3~ but with different requirements of oxygen.

Nitrogen metabolism (denitrification) can be reversed, NO3- -» NO2- -> NH4

+

 (Gessner, 1960;

Green, 1968).

In previous experiments on nitrogen metabolism

in aquaria (Kiihl and Mann, 1956, 1961, 1962) it

was found that ammonification proceeds rapidly

through biological activity. In aerated water, with

abundant oxygen, the decay is accelerated, the ammonification is abbreviated, and the formation of

nitrite and nitrate increases. During this process,

oxygen diminishes as a result of oxidations. The

loss of oxygen by biological activity remains the

same.

Nitrification is completed earlier in fresh water

than in brackish water or seawater, but the quantity of nitrites and nitrates increase with increased

salinity. If algae or other plants are present, the

nitrate suddenly disappears.

The experiments on the decay of organic matter

in bottom sediments indicate that the above processes are the same as in the water column but are

modified by grain size, morphology of the grains,

pore volume or actual water content of the pore

space, rate of diffusion, and oxygen content. The

products of decomposition can appear on the surface of the sediment and in the water column. The

nitrates, or, in the case of denitrification, ammonia,

can be an important factor in the formation of a

layer of diatoms on the sediment.

Berner (1963) conducted experiments similar to

those reported in this paper. Bick (1964) studied

the production and toxicity of ammonia and other

compounds. Fenchel (1969) has reviewed the complex interaction of nitrogen compounds and
178

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

including factors controlling the depth of the reduction layer and toxicity. Other published works

concerning the nitrogen cycle, bacterial activity,

ecology of meiofauna, etc., include Beyers (1965),

Brafield (1965), Callame (1963, 1966), Dietrich,

Hohnk, and Manzel (1965), Fenchel and Jansson

(1966), Jansson (1966, 1968a,b, 1969), Mare (1942),

Muus (1967), Rheinheimer (1959), Waksman,

Hotchkiss, and Carly (1933), and Zobell (1946).

The complexity of the problem has been aptly

stated by Jansson (1966): "In my opinion the only

way to elucidate a habitat so well-known for its

instability and changes is perhaps to put a great

number of such snapshots together to get an entire

slow motion 'film' of the processes."

The results of the experiments show that the decomposition products can reach the surface of the

sediment after a certain time. This time depends on

the grain size of the sediment. The grain size also

is important for the extension of the reduction

zone. In coarse sand it penetrates deeper and

shallower. In a fine sediment, the decomposition

products remain for longer periods in the deeper

layers than in coarse sand or in sediment mixed

with broken shells. The oxygen in the area of

decomposition can be diminished to zero for a week

or longer. In a well-aereated region the time is

significantly reduced.

I am much indebted to Dr. Liineburg of the

Hydrographische Abteilung, Institut fur Meeresforschung, Bremerhaven, for the determination of

the grain size.

Literature Cited

Berner, R. A.

1963. Electrode Studies of Hydrogen Sulfide in Marine

Sediments. Geochemica et Cosmochimica Ada,

27:563-575.

Beyers, R. J.

1965. The Pattern of Photosynthesis and Respiration in

Laboratory Microecosystems. Memoire dell' Istituto

Italiano Idrobiologia, supplement 18:61-74.

Bick, H.

1964. Die Sukzession der Organismen bei der Selbstreinigung von organisch verunreinigtem Wasser unter

verschiedenen Milieubedingungen. Min. ELF Land

Nordrhein-Westfalen, Diisseldorf. 139 pages.

Botan, E. A.; J. J. Miller; and H. Kleerekooper

1960. A Study of the Microbiological Decomposition of

Nitrogenous Organic Matter in Freshwater. Archiv

fur Hydrobiologie, 56:334-354.

Brafield, A. E.

1965. Quelques Facteurs affectant le teneur en oxygene

des eaux interstitielles littorales. Vie et Milieu,

16:889-897.

Brand, T.; N. W. Rakestraw; and C. N. Renn

1937. The Experimental Decomposition and Regeneration

of Nitrogenous Matter in Seawater. Biological Bulletin, 72:165-175.

1939. Further Experiments on the Decomposition and

Regeneration of Nitrogenous Matter in Seawater.

Biological Bulletin, 77:285-296.

Callame, B.

1963. Le Milieu interstitiel dans les sediments sableaux

intercotidaux. Bulletin de I'Institut Oceanographique, Monaco, 60(1271) :l-32.

1966. Sur la Diffusion de l'oxygene a l'interieur des sediments marins. Cahiers de la Station Ocianographique, La Rochelle, pages 1-14.

Cooper, L. H. N.

1937. The Nitrogen Cycle in the Sea. Journal of the

Marine Biological Association of the United Kingdom, 22:183-204.

Dietrich, R.; W. Hohnk; and W. D. Manzel

1965. Studien zur Chemie organischer Bodenproben. III.

Beziehengen zwischen physikalischen und chemischen Griissen in den Boden der Nordsee und der

Aussenweser. Veroffentlichungen des Instituts fur

Meeresforschung in Bremerhaven, 9:242-278.

Fenchel, T.

1969. The Ecology of Marine Micro benthos. IV. Structure

and Function of the Benthic Ecosystem, Its Chemical and Physical Factors and the Microfauna Communities with Special Reference to the Ciliated

Protozoa. Ophelia, 6:1-182.

Fenchel, T., and B. O. Jansson

1966. On the Vertical Distribution of the Microfauna in

the Sediments of a Brackish-Water Beach. Ophelia,

3:161-177.

Gessner, F.

1960. Die Leistungen des pflanzlichen Organismus.

Handbuch der Biologic, 4:34-186.

Green, J.

1968. The Biology of Estuarine Animals. 401 pages.

London: Sidgwick and Jackson.

Hecht, F.

1933. Der Verbleib der organischen Substanz der Tiere

bei meerischer Einbettung. Senckenbergiana, 15

(3-4): 165-249.

Jansson, B. O.

1966. Microdistribution of Factors and Fauna in Marine

Sandy Beaches. Veroffentlichungen des Instituts

fur Meeresforschung in Bremerhaven, Sonderband

2:77-86.

1968a. Quantitative and Experimental Studies of the Interstitial Fauna in Four Swedish Sandy Beaches.

Ophelia, 5:1-71.

1968b. Studies on the Ecology of the Interstitial Fauna of

Marine Sandy Beaches. Thesis, University of

Stockholm. 16 pages.
NUMBER 76 179

1969. Factors and Fauna of a Baltic Mud Bottom. Litnnologica, 7:47-52.

Krause, H. R.

1959. Biochemische Untersuchungen iiber den postmortalen Abbau von totem Plankton unter aeroben und

anaeroben Bedingungen. Archiv fur Hydrobiologie,

supplement 25:67-82.

1961. Einige Bemerkungen iiber den postmortalen Abbau

von Siisswasser-Zooplankton unter La bora tori urns—

und Freilandbedingungen. Archiv fur Hydrobiologie, 57:539-543.

Kuhl, H.

1952. Studien iiber die Klaffmuschel My a arenaria. Die

Myasiedlungen am Hakensand (Elbmundung).

Archiv fur Fischereiwissenschaft, 4:126-132.

Kuhl, H., and H. Mann

1956. Unperiodische Aenderungen im Stoffhaushalt von

Seewasser-aquarien. Hydrobiologia, 8:66-78.

1961. Vergleich des Stickstoffabbaus in See- und Siisswasser-aquarein. Vie et Milieu, 11:532-545.

1962. Modellversuche zum Steffhaushalt in Aquarien bei

verschiedenem Salzgchalt. Kieler Meeresforschungen, 18:89-92.

1966a. Chemische Unterschungen am Sandstrand von Cuxhaven und Helgoland. Veroffentlichungen des Instituts fur Meeresforschung in Bremerhaven, Sonderband 2:67-76.

1966b. Aenderungen im Chemismus des Interstitialwassers

am Strand von Cuxhaven wShrend einer Tide. Helgoldnder wissenschaftlichen Meeresuntersuchungen,

13:238-245.

Mare, M. F.

1942. A Study of a Marine Bent hie Community with

Special Reference to the Micro-Organisms. Journal

of the Marine Biological Association of the United

Kingdom, 25:517-554.

Muus, B.

1967. The Fauna of Danish Estuaries and Lagoons. Meddelelser fra Danmarks Fiskeri-og Havunders0gelser,

5:1-316.

Postma, H.

1966. The Cycle of Nitrogen in the Waddensea and Adjacent Areas. Netherlands Journal of Sea Research,

3:186-221.

Rheinheimer, G.

1959. Mikrobiologische Untersuchungen iiber den Stickstoffhaushalt der Elbe. Archiv fur Mikrobiologie,

34:358-373.

Ulken, A.

1963. Die Herkunft des Nitrits in der Elbe. Archiv fur

Hydrobiologie, 59:486-501.

Waksman, S. A.; M. Hotchkiss; and C. Carly

1933. Marine Bacteria and Their Role in the Cycle of

Life in the Sea. Biological Bulletin, 65:137-167.

Wuhrmann, K., and H. Woker

1948. Experimentelle Untersuchungen iiber die Ammoniak- und Blausaurevergiftung. Schweizerische Zeitschrift fur Hydrologie, 11:210-244.

1953. Ueber die Giftwirkung von Ammoniak- und Zyanidlosungen mit verschiedener SauerstofTspannung

und Temperatur auf Fische. Schweizerische Zeitschrift fur Hydrologie, 15:236-260.

Zobell, C. E.

1946. Marine Microbiology. 240 pages. Waltham, Massachusetts: Chronica Botanica.

SAMPLING FOR MEIOFAUNA

/. B. j . weiis A Brief Review of

Methods of Sampling

the Meiobenthos

ABSTRACT

The requirements for a valid sample of meiobenthos are discussed and evaluated in terms of collecting by use of coring devices, grabs, and dredges.

The advantages and disadvantages of specific collecting devices are discussed as to their efficiency in

obtaining samples of meiobenthos.

To be of maximum value a sample of meiobenthos

should provide a sufficient quantity of fauna to

allow a reasonable estimate of population density

to be made, should furnish information on the

vertical zonation of the fauna and on the nature of

the substratum, and should contain all elements of

the fauna, from the smallest species to the largest.

Three basic types of equipment are used to take

samples of meiofauna: coring devices, grabs, and

dredges. The method to be used for any particular

program depends to a large extent on the area of

seabed being investigated—whether the littoral region or shallow-water or deep-water substrata.

Sampling in the littoral region is best done by

hand with a coring device. Many workers use a

simple tube of metal or plastic to take a vertical

core, pushing it into the sand to the required

depth, corking the upper end, and withdrawing it.

It may be preferable to dig to the bottom of the

tube and lift it bodily from the substratum. This

method is simple and quick and satisfies all the requirements given above. However, if the sample is

to be used to provide information on the vertical

zonation of the fauna it should be removed from

J. B. J. Wells, Department of Zoology, University of Aberdeen, Aberdeen, Scotland.

the tube and cut into sections of suitable length as

soon as possible, to avoid errors due to migration

of the animals. The method of removal of the core

also is critical. Pushing out the core with the

plunger disturbs the surface and probably will

cause compression of the sample. If the substratum

is sufficiently moist it is likely to slide out of the

tube under its own weight when the cork is removed; sections can be cut from it as it does so.

Jansson (1967) has developed a method which

avoids compression of the core during removal

from the tube and, at the same time, provides a series of vertical subsamples. The coring tube is composed of a series of rings of uniform height (1, 2,

and 5 cm are the sizes most commonly used)

which fit closely within an outer tube. The sampler is pushed into the deposit and a core obtained. The inner, sectional tube is pushed out by

a plunger which bears on the rings and not on the

sediment, thus avoiding compression. The rings are

removed separately as they emerge.

Transparent plastic tubing is preferable to metal

tubing as the core seems to slide better in this material, and, being transparent, calibration is easier.

Compression of the deposit can occur during insertion of the sampler. With transparent tubing this

can more easily be seen to be happening and precautions can be taken. Various sizes of tubing are

used, but it seems that a cross-sectional area of

about 10 cm2 is the most satisfactory, giving a sample large enough to be meaningful but small

enough to permit rapid sorting of the fauna that it

contains.

In most cases sampling to a depth of 25 to 30

cm is adequate, as the majority of the animals live

in this zone. However, on the upper shore of many

beaches the permanent water table lies deeper than

this, and for a complete profile of the vertical dis183
184

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

tribution of the fauna samples must be taken to

the level of the water table. This involves a multiple-layer technique in which the tube is pushed

down to 25 to 30 an, the sand dug away to the

bottom of the tube, and another tube inserted at

the point reached by the first one. This process is

repeated until the water table is reached. This

method undoubtedly involves inaccuracies at the

point of changeover of tubes. A square-section demountable corer of the Renaud-Debyser type (Renaud-Debyser, 1957) obtains apparently undisturbed cores of up to 1 m in length, which may be

sufficient for this purpose.

In the sublittoral, shorter cores usually suffice

and simple hand-coring of the type described can

be carried out by using SCUBA to a depth of about

50 m. Beyond this, limitations of SCUBA outweigh

its advantages and for deeper water specialized

gear worked from a vessel is required.

It is possible to use for the meiobenthos most of

the quantitative gear devised for macrobenthos

studies (Holme, 1964; Hopkins, 1964). However,

since a small sample usually is adequate for meiobenthos studies the various coring devices offer

practical advantages over the grabs and dredges.

Also, coring is the only type of sampling that fully

satisfies the requirements outlined at the beginning

of this paper. In practical terms, corers have an advantage in their light weight and ease of handling

—which means that they can be worked in more

severe weather conditions than can most grabs or

dredges—and also in the speed with which successive samples can be taken.

Much of the early work in this field (e.g., Mare,

1942) was done with lightweight gravity corers initially designed for sampling mud substrata (Moore

and Neill, 1930; Krogh and Sparck, 1936). These

samplers are generally quite adequate for the

meiobenthos, as deep cores are not necessary, the

major part of the fauna being restricted to the

upper few centimeters of the substratum (Smidt,

1951; Muus, 1964). Such samplers have been used

successfully by several workers, usually with some

minor modifications to their basic design (Bougis,

1950; Mclntyre, 1961, 1964). Even in their modified state, however, they are suitable only for softer

substrata, penetration being poor in sand and the

sample sometimes being lost in hauling. Penetration can be improved by increasing the weight of

the sampler and retention of the sample by fitting

a core retainer, but the conventional internal retainer is useless because it disturbs the surface of

the sediment, the very region with most interest.

Mills (1961) has designed an external core retainer

for use with the heavy "geological" corers, but for

the lightweight instruments the simple rubber-ball

closing mechanism is more suitable. Fenchel

(1967) has thus modified a Moore and Neill sampler, and Willimoes (1964) and Craib (1965)

have designed specialized coring devices using this

method, in which the lower end of the coring tube

is closed by a rubber ball as it is withdrawn from

the substratum. The area sampled by most of these

devices is about 9 to 10 cm

2

. In the Fenchel and

Craib systems the ball-release mechanism is external to the tube and the only disturbance caused to

the core sample is at its bottom edge. In the Willimoes sampler the ball is hauled up to close the

bottom of the tube by means of a cord running

through the tube. This method causes disturbance

of the core, and although a quantitative sample

may be obtainable it cannot be used to study vertical zonation of the fauna. Also, as the ball hangs

free a small distance beneath the tube during lowering, it is likely that it will disturb the surface of

the deposit as the sampler approaches the bottom.

In coarse sand and gravel these samplers are unsatisfactory on two counts. First, the corer may not

penetrate the substratum as the particles may be

too large, and, second, the tube may lose the deposit when it is being withdrawn. Under these conditions the Craib corer, with a tube diameter of

5.7 cm, is more efficient than the smaller machines.

Another approach to the problem of core retention is the use of a cutting knife, which swings

round from the horizontal position, cutting

through the substratum adjacent to the coring

tube, to seat beneath the tube. This method is less

efficient than the rubber-ball method as it does not

achieve such a close seal, but it does allow the use

of a large core tube. Samplers employing this principle have been designed by Reineck (1963) and

Drzycimski (1967). Both of these samplers work

well in a range of substrata from loose mud to

hard sand but their efficiency in coarse sand and

gravel is suspect. There are two versions of the

Reineck sampler, one weighing 150 kg, the other

750 kg. Drzycimski's sampler, which weighs only 7.5
NUMBER 76

185

kg, samples an area of 82 cm2 to a depth varying

from 3 to 5 cm in clay to 15 to 20 cm in loose mud.

It can be used from a small boat and may be a useful device for sampling in fairly shallow waters.

The weight of the sampler is an important consideration. Heavier instruments are required for sand

than for mud, and it may be necessary to adjust

the weight according to the type of sediment under

investigation.

Two major problems are involved in the use of

coring devices—compression of the core in the

tube as the sample is taken, and disturbance of the

surface of the deposit by the instrument as a whole

as it approaches the substrate and by the core tube

as it penetrates. These problems are more acute for

mud deposits than for sand, particularly where the

surface is of loose, flocculent material. Observations by SCUBA divers have shown that these problems are common to all free-fall or gravity corers.

In shallow waters, within the operational limits of

SCUBA, hand sampling obviates this damage. Craib

(1965) claims that his sampler, which is set down

on the bottom before the coring tube is activated,

takes an undisturbed sample. Evaluation of the degree of disturbance of samples taken without observation by a diver is difficult, as a sample may appear to be undisturbed when, in fact, it has lost

the superficial flocculent layer.

An important, if temporary, part of the sublittoral meiobenthos is formed by the newly settled

stages of macrobenthic species. Qualitative samples

of these animals and of the larger, more mobile

meiobenthic species can be taken with the sled

samplers of Mortensen (1925) and Ockelmann

(1964). Muus (1964) has pointed out the difficulties of quantitatively sampling this element of the

fauna—which inhabits the surface layer of the substratum—with the various coring devices discussed

above, and his "mouse trap" sampler and the

much more complicated device of Corey and Craib

(1966) are the only pieces of apparatus that can

perform this task.

Grabs are not entirely satisfactory for meiobenthos work. In the best of them, water drains out

through the jaws and along the seams between the

halves of the bucket during hauling, almost certainly washing away the animals on or near the

surface of the sample. Another disadvantage is the

disturbance that they cause to the surface of the

sediment as they approach it. This problem can be

alleviated by fitting a gauze cover to the top of the

bucket, as in the Smith-Mclntyre grab (Smith and

Mclntyre, 1954). Grab hauls can be subsampled

with short cores (Wigley and Mclntyre, 1964).

Thiel (1966) has devised a special subsampler for

this purpose.

Dredges are semiquantitative at best, and they

should be reserved for those occasions when it is

impracticable to use other types of gear. In very

deep waters, where the time taken to obtain a sample is considerable, a dredge has the very real advantage of providing a large sample. Of all the

varied types only the anchor dredge (Forster,

1953) is suitable, as it retains the entire sample,

but the depth of bite is unnecessarily deep. Sanders, Hessler, and Hampson (1965) designed a modified anchor dredge which takes a shallow slice of

the subtratum and provides a large sample. This

type of dredge probably is adequate for the meiobenthos, but Hessler and Sanders (1967) point out

that the more mobile elements of the epibenthic

macrobenthos probably are not taken. A more

efficient sampler is the epibenthic sled of Hessler

and Sanders (1967), but this instrument has had

insufficient use, as yet, for a proper evaluation to

be made. A similar instrument is the sled sampler

of Riedl (1960) but, again, information on its use

for meiobenthos is lacking.

Literature Cited

Bougis, P.

1950. M&hode pour l'etude quantitative de la microfaune

des fonds marins (Meiobenthos). Vie et Milieu,

1:25-37.

Corey, S., and J. S. Craib

1966. A New Quantitative Bottom Sampler for Meiofauna. Journal du Conseil, 30:346-353.

Craib, J. S.

1965. A Sampler for Taking Short Undisturbed Marine

Cores. Journal du Conseil, 30:34-39.

Drzycimski, I.

1967. Czerpacz Rurowy do Pobierania Prob Cennych.

Ekologia Polska, series B, 13:273-275.

Fenchel, T.

1967. The Ecology of Marine Microbenthos. I. The Quantitative Importance of Ciliates as Compared with

Metazoans in Various Types of Sediments. Ophelia,

4:121-137.

Forster, G. R.

1953. A New Dredge for Collecting Burrowing Animals.
186

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Journal of the Marine Biological Association of the

United Kingdom, 32:193-198.

Hessler, R. R., and H. L. Sanders

1967. Faunal Diversity in the Deep-Sea. Deep-Sea Research, 14:65-78.

Holme, N. A.

1964. Methods of Sampling the Benthos. Advances in

Marine Biology, 2:171-260.

Hopkins, T. L.

1964. A Survey of Marine Bottom Samplers. Progress in

Oceanography, 2:213-256.

Jansson, B. O.

1967. The Significance of Grain Size and Pore Water

Content for the Interstitial Fauna of Sandy

Beaches. Oikos, 18:311-322.

Krogh, A., and R. Sparck

1936. On a New Bottom Sampler for Investigation of the

Micro Fauna of the Sea Bottom with Remarks on

the Quantity and Significance of the Benthonic

Micro Fauna. Kongelige Danske Videnskabernes

Selskabs Skrifter, Biologiska Skrifter, 13:3-12.

Mclntyre, A. D.

1961. Quantitative Differences in the Fauna of Boreal

Mud Associations. Journal of the Marine Biological

Association of the United Kingdom, 41:599-616.

1964. Meiobenthos of Sub-Littoral Muds. Journal of the

Marine Biological Association of the United Kingdom, 44:665-674.

Mare, M. F.

1942. A Study of a Marine Benthic Community with

Special Reference to Micro-Organisms. Journal of

the Marine Biological Association of the United

Kingdom, 25:517-554.

Mills, A. A.

1961. An External Core Retainer. Deep-Sea Research,

7:294-295.

Moore, H. B., and R. G. Neill

1930. An Instrument for Sampling Marine Muds. Journal of the Marine Biological Association of the

United Kingdom, 16:589-594.

Mortensen, T.

1925. An Apparatus for Catching the Micro-Fauna of

the Sea Bottom. Videnskabelige Meddelelser fra

Dansk Naturhistorik Forening i Kpbenhaven, 80:

445-451.

Muus, B.

1964. A New Quantitative Sampler for the Meiobenthos.

Ophelia, 1:209-216.

Ockelmann, K. W.

1964. An Improved Detritus-Sledge for Collecting Meiobenthos. Ophelia, 1:217-222.

Reineck, H. E.

1963. Die Kastengreifer. Natur und Museum, 93:102-108.

Renaud-Debyser, J.

1957. Description d'un carottier adapte aux prelevements

des sables de plage. Revue de I'Institut Francois

du Petrole, 12:501-502.

Riedl, R.

1960. Ein Kinemeter zur Beobachtung von Dredgen in

beliebigen Tiefen. Internationale Revue der

gesamten Hydrobiologie, 45:155-167.

Sanders, H. L.; R. R. Hessler; and G. R. Hampson

1965. An Introduction to the Study of Deep Sea Benthic

Faunal Assemblages along the Gay Head-Bermuda

Transect. Deep-Sea Research, 12:845-868.

Smidt, E. L. B.

1951. Animal Production in the Danish Waddensea.

Meddelelser fra Kommissionen for Danmarks

Fiskeri-og Havunders0gelser, Serie Fiskeri, 11(6):

1-151.

Smith, W., and A. D. Mclntyre

1954. A Spring-Loaded Bottom-Sampler. Journal of the

Marine Biological Association of the United Kingdom, 33:257-264.

Thiel, H.

1966. Quantitative Untersuchungen iiber die Meiofauna

von Tiefseeboden. Veroffentlichungen des Instituts

fur Meeresforschung in Bremerhaven, Sonderband

2:131-147.

Wigley, R. L., and A. D. Mclntyre

1964. Some Quantitative Comparisons of Offshore Meiobenthos and Macrobenthos South of Martha's Vineyard. Limnology and Oceanography, 9:485-493.

Willimoes, M.

1964. A Ball-Stoppered Quantitative Sampler for the

Microbenthos. Ophelia, 1:235-240.
Robert R. Hessler Problems of

Meiobenthic Sampling

in the Deep Sea

ABSTRACT

The problems of sampling for deep-sea meiobenthos, including those of time and expense, density

of meiobenthos, sampling devices, technical difficulties, and processing, are discussed. Recommendations are given for improvement of the knowledge

of deep-sea meiobenthos.

As is already known, information on the deep-sea

meiofauna is scant. Some descriptions of deep-sea

species and depth records have appeared, but for

groups other than the Foraminifera these, by and

large, are negligible. The Challenger Reports are

deficient in taxa usually regarded as meiofauna.

Only the papers of Wigley and Mclntyre (1964)

and Thiel (1966) have dealt with meiofaunal assemblages as a whole. Essentially, the entire job is

still before us, and, for that reason, a consideration

of the problems one must face in attempting to investigate the deep-sea fauna is in order. The present discussion is based on the author's own experience in investigating the deep-sea macrofauna and

the meiofaunal studies of others.

Basically, there are three general reasons why so

little is known today about the deep-sea meiobenthos. Deep-sea research is expensive. The standing

crop of life in the deep sea is very low. Available

technology is not truly adequate.

The first point requires only a moment's attention. Deep-sea work needs large ships and at least

some sophisticated equipment, and these require a

great deal of money. Many governments, however,

Robert R. Hessler, Scripps Institution of Oceanography,

La Jolla, California 92037.

are releasing money for this type of work, so opportunities for the scientist are improving.

The individual investigator must realize that

such work is very expensive also in terms of time.

In deep-water work only a few samples can be

taken per day, and the time required to sort

through these samples in the laboratory can be

enormous. A side effect of the great amount of

time needed for each sample is that a sampling

program involving many samples is not really

practical. One must design the program very carefully so that a minimum of samples yields a maximum amount of information.

Nearly every study comparing abundance of animals in shallow and deep water has shown that the

amount of life in deep water is as much as several

orders of magnitude less than that occurring in

shallow water. In the northwestern Atlantic, Sanders, Hessler, and Hampson (1965) demonstrated

that the density of benthic macrofauna from the

abyssal plain at 4,000 m to 5,000 m is 20 to 640

times less than on the continental shelf. In the

northwestern Pacific, Soviet investigators have

noted a difference of as much as four orders of

magnitude. Wigley and Mclntyre (1964), in one

of the rare studies of open-ocean benthic meiofauna, documented a definite diminution of

faunal density down to their deepest station at 500

m. Phleger (1964) found that the density of Foraminifera in the Gulf of California was an order

of magnitude less at bathyal-abyssal depths than in

shallow water.

This low density means that for unit effort numbers of individuals captured in the deep sea will be

significantly lower. In general, it forces the investigator to base his conclusions on data which are less

convincing than those which could be obtained in

shallow water. This difficulty frequently faces the

187
188 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

systematist, who commonly must deal with species

represented by only one or two individuals.

In this problem, the meiobenthologist has an advantage over the student of macrofauna. Wieser

(1960) speculated that meiofauna was about 100

times more abundant than macrofauna. Wigley

and Mclntyre (1964) found meiofauna to be 35 to

770 times more abundant than macrofauna, averaging 223 times. Thiel (1966) collected from 35 to

426 meiofaunal animals per 25 cm2 in depths from

1,000 to 5,000 m. Thus, a sample too small to yield

sufficient macrofauna may have an adequate

amount of meiofauna; however, this advantage

probably will profit only the nematologist. Nematodes dominate the meiofauna in deeper water

(Wieser, 1960). They average 81.5 percent of the

individuals in Thiel's samples and 84.3 percent of

Wigley and Mclntyre's. Students of other groups

may require larger samples.

In the deep-sea benthos, yield has been increased

by using a grab or corer that samples an area

larger than that usually taken in shallow water or

by using a trawl or dredge. The largest grab now

used in deep-sea work is the Cambell grab (Hartman, 1955), which samples 0.55 m2

. The Soviet

Okean grab (Vinogradova, 1962) samples 0.25 m2.

Menzies and Rowe (1968) have developed a promising method for taking 0.25-m2

 cores. The author

has recently modified the Bouma-Marshall box

corer (Bouma and Marshall, 1964) to take 0.25-m2

samples. Most other grabs and corers have been

smaller. Thiel (1966) found a Van Veen grab to

be very effective, and Wigley and Mclntyre (1964)

used a Smith-Mclntyre grab.

All grabs have the disadvantage of offering so

much resistance to the water as they descend that a

"bow wave" may form. This will blow away the

light animals on the surface of the sediment before

the sample is taken unless the grab is properly

modified (Wigley, 1967) or unless great care is

used in lowering the grab the final short distance.

When properly taken, grabs and large-area cores

offer the substantial advantages of being quantitative and of being amenable to subsampling because

they yield undisturbed pieces of the bottom. Wigley and Mclntyre (1964) and Thiel (1966) subsampled their grabs, the former by taking 10-cm2

cores from the sample and the latter by means of a

25-cm2 "Meiostecher." Thiel also subdivided the

subsample vertically and was able to demonstrate

that the majority of organisms live in the surface

centimeter.

Where larger numbers of organisms are desired,

one must use a dredge or trawl. These yield enriched samples by skimming off only the rich, uppermost layer of the sediment and by allowing a

portion of the sediment to pass through the mesh

of the collecting net while retaining the organisms

larger than the mesh opening. The best device of

this sort being used in the deep sea today is the

epibenthic sled designed at Woods Hole Oceanographic Institution (Hessler and Sanders, 1967).

Such a device may yield thousands of individuals,

and single species have been represented by

hundreds of specimens. Unfortunately, such samples are not quantitative; also, the mesh of the collecting net is not small enough to retain meiofauna. Thus, unless there is still mud retained in

the net when it reaches the surface, the meiofauna

will have been washed from the sample.

Finally, in this enumeration of the difficulties in

deep-sea studies is a consideration of our technical

inadequacy. The proof of this deficiency is that in

any deep-sea sampling program there is a depressingly high percentage of failures ranging from no

samples at all to samples which clearly are not representative. Most investigators would be delighted

if they were successful only half of the time. The

high rate of failure can be attributed to three

major factors.

First, benthic sampling in the deep sea requires

good weather, and that condition is fulfilled with

distressing infrequency.

Second, the remoteness of the bottom makes it

difficult to know what the sampling device is

doing. The importance of this factor cannot be overemphasized. The simplest consideration, such as

whether the gear is on the bottom or still in the

water column, is a major problem in the deep sea.

A pinger on the wire (Thiel, 1966) used in conjunction with a PDR is an essential aid in helping

to know when the sampler is on the bottom. A recording tensiometer is more difficult to interpret,

but it can let one know when the gear is sampling

and when it is caught on some obstacle.

Third, the great length of the water column

through which the sample must travel before it

reaches the ship exposes it to the gradual destruc-
NUMBER 76

189

tion of the winnowing process. Few sampling devices are watertight; and with grabs and dredges

there usually is no attempt to have them so. From

the moment the gear leaves the bottom, the current, gravity, ship's surge, and other physical forces

will cause the sampler to leak. The success of shallow-water sampling is based on the fact that the

duration of this leakage is relatively short, so that

only a small portion of the sample is lost. In deep

water, the same amount of leakage per unit time

or distance can result in the complete loss of the

sample by the time the sampling device reaches the

ship. This is probably the single most important

reason for failure in deep-sea sampling. Winnowing is especially difficult to prevent on dredges and

trawls. This is a further reason for employing grab

and core techniques.

Additional problems face those who prefer that

their animals be alive for initial processing.

Usually, deep-sea benthic organisms are dead by

the time the investigator can isolate them. Temperature changes, particularly, and mechanical

damage seem to be the most important factors. Mechanical damage is probably not a serious problem

with individuals of most meiofaunal taxa because

of their small size. Deep-sea animals are stenothermal because the stable cold water in which they

live has not stimulated thermal adaptability. Except in winter at high latitudes, surface waters invariably are significantly warmer, and the resulting

thermal change is immediately lethal. At low latitudes, when the sample consists of a large volume

of sediment, the animals may still be alive when

they reach the ship because the sediment acts as an

insulator, but they die as soon as they are washed

from the sediment by warm surface water.

There are three solutions to this problem: (1)

using techniques that do not require the animals

to be alive, (2) sampling only where and when the

surface temperature is compatible with the organisms' tolerance, and (3) washing the samples

with refrigerated seawater. Ideally, the third solution is the best, but it requires special washing

techniques that use a minimum of seawater because most ships today are not capable of refrigerating the amount of water necessary in our present

routine washing procedures. The bubbling technique of Higgins (1964) meets realistic requirements in that it employs only a small amount

of water; but undoubtedly there are other methods

that will work as well.

To aid in sorting preserved animals in the laboratory, it is useful to bulk-stain the concentrated

sample with Rose Bengal. Thiel (1966) found that

staining properties were improved by adding the

stain to a dilute phenol solution.

The following recommendations are offered to

those who wish to improve our knowledge of the

deep-sea meiobenthos. Plan the sampling program

with care to obtain maximum benefit from each

sample. Take grab or large-diameter core samples.

Use a pinger and tensiometer to monitor the sampling process. Make every effort to reduce the bow

wave effect and winnowing of the sample. On deck,

be content with dead animals or use a washing

procedure that requires only a minimum amount

of refrigerated seawater. Stain the concentrated

sample with Rose Bengal before sorting. Finally,

be emotionally prepared for a high percentage of

unsuccessful samples. Gleaning facts from the deep

sea is time-consuming, often discouraging work,

but those who make the effort are finding a fertile

field for new discoveries.

Literature Cited

Bouma, A. H., and N. F. Marshall

1964. A Method for Obtaining and Analysing Undisturbed Ocean Sediment Samples. Marine Geology,

2:81-99.

Hartman, O.

1955. Quantitative Survey of the Benthos of San Pedro

Basin, Southern California. Allan Hancock Pacific

Expeditions, 19:1-185.

Hessler, R. R., and H. L. Sanders

1967. Faunal Diversity in the Deep-Sea. Deep-Sea Research, 14:65-78.

Higgins, R. P.

1964. A Method for Meiobenthic Invertebrate Collection.

American Zoologist, 4:291.

Menzies, R. J., and G. T. Rowe

1968. The LUBS, a Large Undisturbed Bottom Sampler.

Limnology and Oceanography, 13:708—714.

Phleger, F. B.

1964. Patterns of Living Benthonic Foraminifera, Gulf of

California. In Symposium on the Marine Geology

of the Gulf of California, Geological Society of

America Memoir, 3:377-394.

Sanders, H. L.; R. R. Hessler; and G. R. Hampson

1965. An Introduction to the Study of Deep-Sea Benthic
190 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Faunal Assemblages along the Gay Head-Bermuda

Transect. Deep-Sea Research, 12:845-867.

Thiel, H.

1966. Quantitative Untersuchungen iiber die Meiofauna

von Tiefseeboden. Verdffentlichungen des Instituts

fur Meeresforschung in Bremerhaven, Sonderband

2:131-147.

Vinogradova, N. G.

1962. Some Problems of the Study of Deep-Sea Bottom

Fauna. Journal of the Oceanographical Society of

Japan, 20th Anniversary Volume, pages 724-741.

Wieser, W.

1960. Populationsdichte und Vertikalverteilung der Meiofauna mariner Boden. Internationale Revue der

gesamten Hydrobiologie, 45:487-492.

Wigley, R. L.

1967. Comparative Efficiencies of Van Veen and SmithMclntyre Grab Samplers as Revealed by Motion

Pictures. Ecology, 48:168-169.

Wigley, R. L., and A. D. Mclntyre

1964. Some Quantitative Comparisons of Offshore Meiobenthos and Macrobenthos South of Martha's Vineyard. Limnology and Oceanography, 9:485-49S.
John s. Gray Sample Size and

Sample Frequency in

Relation to the

Quantitative Sampling

of Sand Meiofauna

ABSTRACT

A comparison is made of the efficiency of three

different-size corers (3.15, 3.75, and 5.95 cm

diameter) in sampling meiofauna of a sandy beach.

The best results were obtained by using a corer

of 3.75 cm in diameter. Frequencies of two, four,

and eight samples per 0.25 m2 were taken. Using

the Index of Dispersion Test the precision of the

estimate of the degree of contagious distribution

increased with increasing sampling frequency. An

analysis of variance showed that only at sampling

frequencies of four and eight samples per 0.25 m2

were there significant differences between areas of

beach.

A number of new core-sampling devices recently

have been described. The efficiency of these devices

usually is assessed by the ease with which an undisturbed deep core is taken. Fundamental to the design of a suitable sampler for sediment-living meiofauna should be a consideration of the sampling

efficiency of cores of different sizes. Sampling

efficiency is held to mean the accuracy of the estimate of population density achieved by the corer.

With the sole exception of the paper by Vitiello

(1968), no investigation has been made to determine the number of samples within a finite area of

sediment needed to establish the distributional pattern of the meiofaunal elements. Many quantitaJohn S. Gray, Wellcome Marine Laboratory, Robin Hood's

Bay, Yorkshire, England.

tive studies on meiofauna have merely quoted

population densities per 50 ml, based on paired

samples, or have even converted and extrapolated

the data obtained to numbers per square meter of

sand. In many cases, such generalizations of faunal

densities are unjustified and grossly oversimplify

meiofaunal distribution patterns.

Thus, an attempt has been made to establish the

most suitable core size for sampling the meiofauna

and the optimal frequency of sampling necessary

to establish the spatial variability of the fauna.

The present study relates only to one beach on the

northeast coast of England; clearly, different

beaches will need different sampling techniques.

The study reported here was made very simple by

intention, and was done as a preliminary to the

author's comparative ecological studies of the meiofauna on a polluted beach and on an unpolluted

beach. It is felt, however, that the problem highlighted here is one which has received too little attention. This paper, therefore, should be regarded

merely as an indication of some factors to be considered when sampling the meiofauna quantitatively. The authoritative works of Cochran (1966),

Greig-Smith (1964), Southwood (1966), and Williams (1964) treat this subject in greater detail.

Methods

A quadrat 0.25 iri2 was divided into sixteen equal

squares. It was decided to test sampling frequencies

of two samples/0.25 m2, four samples/0.25 m2, and

eight samples/0.25 m*. A series of eight random

191
192

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

numbers was chosen, giving four pairs of two

samples/0.25 m2, two pairs of four samples/0.25 iri2,

and one set of eight samples/0.25 m2.

Three plastic corers, each 5 cm in height and

having respective inner diameters of 5.95 cm, 3.75

cm, and 3.15 cm were used. Each corer was fitted

into a wooden guide so that a similar spatial relationship of corers was followed in each sampling

area. The assumption had to be made that faunal

densities and distributional patterns were similar

under each corer.

Two positions were selected on the beach at

Robin Hood's Bay, England. Area 1 was at mean

tide level and was an apparently uniform patch of

bare sand. Area 2 was in a shallow pool within the

sand beach at mean tide level. In each area the

quadrat was thrown randomly onto the sand. The

wooden guide containing the corers was placed on

the sand and the three corers were pushed simultaneously into the substratum. Each core was removed carefully, and the sand contained therein

was placed in separate containers. This process was

repeated for the eight sampling stations within

each 0.25 iri2 quadrat.

In the laboratory the samples of sand were

placed in separate containers and an equal volume

of 6 percent MgCl2 was added. After allowing ten

minutes for anaesthetization the sand was stirred

vigorously and the supernatant liquid poured

through a fine-mesh plankton net (60-/t diameter

pores). The sand was washed and shaken viorously

with three changes of seawater followed by one

change of fresh water. The animals and a little

sand present on the filter were washed off to a

Petri dish and counted under a "low-power binocular microscope.

The sand was further washed with a 10 percent

solution of ethyl alcohol in distilled water and then

with three washes of seawater. It was found that

60 to 70 percent of the animals were removed by

the first treatment and a total of 90 to 95 percent

extraction was achieved by the additional alcohol

treatment. The extraction efficiency was checked by

direct counts of the animals remaining in the sand

residue after the MgCl2 and alcohol treatments.

The nematodes, in particular, were not removed

by MgCl2 treatment alone. Samples were stored at

6° C prior to counting.

1

5

*

9

13

a

2

6

10

14

3

*

7

11

15

4

8

*

12

*

16

1

5

9

13

I

2

6

10

14

3

7

11

•*

15

4

8

12

16

FIGURE 1.—Position of random stations (asterisks) taken from

within a quadrat 0.25 mz at two separate areas of a sandy

beach; a, open beach; b, pool. At each station three samples

were taken simultaneously with cores having diameters of

5.95 cm, 3.75 cm, and 3.15 cm.

Results

Figure 1 shows the stations sampled within the two

0.25 m2 areas investigated. Table 1 lists the combinations of stations used in the frequency analyses.

Table 2 shows the numbers of animals found in

area 1 (open beach) in the different cores and

samples. Table 3 shows the same for area 2 (pool).

Clearly, the population density is higher in the

pool than on the open sand.

Comparison of Efficiency of Core Samples

The ratio of the volumes of the samplers from

small, medium, and large was calculated to be

1 : 1.417 : 3.568. Thus, if the small sampler is as efficient as the other two samplers, one can simply

multiply the mean number of animals found in

the small core by the appropriate ratio to obtain

an expected value for the other tubes, assuming

similar distribution patterns of animals occur

under each corer. If the observed value found for

another core is greater than the value expected,

then that corer gives a better sample when similar

extraction methods are used. Conversely, if the

observed value is less than the expected value, then

the corer gives a poorer sample, with similar extraction methods.

Table 4 shows the results of this experiment for

the total fauna found in areas 1 and 2. The

medium-size corer contained more animals than expected, whereas the large corer contained fewer

animals than expected. On the basis of these data

the medium-size corer seems the most efficient
NUMBER 76

193

TABLE 1.—Combinations of samples used in comparing sampling frequencies

of two, four, and eight/0.25m*

Habitat

Area 1

(open beach)

Area 2

(pool)

21025m*

12. 16

3 , 2

13. 10

5. 8

9. 15

1. 13

11, 16

4, 6

41025m*

12. 16. 3, 2

13. 10, 5, 8

9. 15. 1, 13

11. 16, 4, 6

8/025m*

12. 16, 3, 2. 13. 10. 5. 8

9, 15. 1. 13. 11, 16. 4, 6

It was thought, however, that this evaluation

might hold true for some animal groups and not

for others. For example, the Gastrotricha, being

smaller than the Turbellaria, might be better sampled by a smaller corer. This, however, was found

not to be the case.

Table 5 shows the expected and observed number of Turbellaria, Nematoda, and Gastrotricha

when using the three corers. The medium corer

produced observed/expected ratios in excess of

unity in five of the six samples, whereas the larger

corer produced only two of the six samples in excess of unity.

This evidence suggests that the smaller corer was

TABLE 2.—Numbers of meiofauna in open sand (Area 1) taken simultaneously

in cores of different sizes.

Corer 1Meiofauna

LARGE CORER

Turbellaria

Gastrotricha

Nematoda

Annelida

Mite

Amphipoda

Total

MEDIUM CORER

Turbellaria

Gastrotricha

Nematoda

Annelida

Ostracoda

Amphipoda

Bivalve

Total

SMALL CORER

Turbellaria

Gastrotricha

Nematoda

Annelida

Ostracoda

Amphipoda

Total

2

24

3

23

0

0

0

50

11

3

23

0

1

1

1

40

9

2

18

1

0

1

li

3

31

9

21

0

0

1

~62

15

2

13

0

0

0

0

Id

7

6

9

0

0

0

2~2

5

14

3

61

3

0

0

81

35

0

13

0

0

0

0

48

9

2

9

0

0

0

20

Sample number

8

22

6

59

3

0

0

90

11

4

18

1

0

2

0

16

4

S

19

1

0

0

2~7

10

17

2

18

1

0

0

18

6

2

17

1

0

0

0

~26

13

0

7

0

0

0

Id

12

10

0

31

1

0

0

4~2

9

2

34

0

1

0

0

46

11

0

21

0

0

2

~34

13

30

1

37

0

1

1

Id

15

5

20

0

0

1

0

li

8

3

14

0

2

0

27

16

22

1

27

0

1

0

li

2

2

9

0

0

1

0

77

2

0

11

0

0

1

14
194

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

TABLE 3.—Numbers of meiofauna in a pool (Area 2) taken simultaneously

in cores of different sizes.

Corer j Meiofauna _

LARGE CORER

Turbellaria

Gastrotricha

Nematoda

Annelida

Amphipoda

Harpacticoida

Total

MEDIUM CORER

Turbellaria

Gastrotricha

Nematoda

Annelida

Amphipoda

Harpacticoida

Total

SMALL CORER

Turbellaria

Gastrotricha

Nematoda

Annelida

Amphipoda

Harpacticoida

Ostracoda

Total

1

78

35

25

1

0

0

139

23

98

5

0

0

1

HI

14

53

13

0

0

0

0

~80

4

90

28

28

0

0

0

146

18

38

7

1

0

0

~64

12

30

11

0

0

1

0

14

6

58

75

46

0

0

0

179

26

45

8

0

0

1

Ho

24

71

7

0

0

0

0

102

Sample number

9

96

23

35

1

0

0

155

68

83

27

0

0

0

178

21

23

7

1

0

0

0

~52~

11

102

34

37

0

0

0

w

32

24

15

0

2

0

~73

25

12

6

0

0

0

0

49

13

77

36

67

2

0

1

183

37

50

22

0

0

0

109

23

54

7

0

0

0

0

~84

15

58

18

26

0

2

1

105

32

21

31

0

0

1

~85

14

7

13

0

1

0

1

1 ?

16

84

13

22

0

0

0

Jl9

35

8

29

0

1

0

~73

13

1

4

0

1

0

0

~19

sampling only part of clumps of animals, whereas

the medium corer was sampling complete clumps.

In support of this hypothesis the variance of

samples taken with the small corer showed wider

fluctuations than the variance of samples taken

with either the medium corer or large corer. With

the large corer the fauna may have been extracted

less efficiently with the methods used, thus producing a lower observed number of animals than expected. Therefore, for die beach sampled and when

using the extraction methods outlined, a corer

3.75 cm in diameter is the optimum size. It must

be emphasized, however, that this size may not be

appropriate for other areas or beaches (see Mclntyre, in the present volume).

Number of Samples Per Unit Area

If beaches or areas of a beach are to be compared,

then the variation in density of the meiofauna

TABLE 4.—Mean numbers of animals taken simultaneously in cores of different

sizes on open beach (Area 1) and in pool (Area 2).

Habitat

Area 1

Area 2

Small corer

(1.0)

24.37

59.50

Medium corer

(1.417)

Expected

3454

84.31

Observed

34.87

98.62

Obs./Exp.

1.01

1.17

Expected

86.97

21259

Large corer

(3.568)

Observed

6050

149.87

Obs./Exp.

0.69

0.76
NUMBER 76 195

TABLE 5.—Mean numbers of Turbellaria, Nematoda, and Gastrotricha taken in

cores of different sizes on open beach (Area 1) and in pool (Area 2).

Meiofauna

Turbellaria

Area 1

Area 2

Nematoda

Area 1

Area 2

Gastrotricha

Area 1

Area 2

Small carer

7.87

1855

13.50

8.50

2.00

31.37

Medium corer

Expected

11.16

25.86

19.13

12.04

2.83

44.46

Observed

13.00

33.87

18.37

18.00

2.50

45.87

Obs./Exp.

1.16

1.31

0.96

1.49

1.13

1.03

Expected

28.10

65.12

48.17

30.33

7.14

111.95

Large corer

Observed

2155

80.37

34.62

35.75

3.12

32.75

Obs./Exp.

0.76

1.23

0.72

1.18

0.44

059

within a given area must be known. If too few samples are taken, the size of variations within a given

area will in all probability be greater than any

differences between areas.

Sampling frequencies of two, four, and eight

samples were taken within 0.25 m2 of the two areas

investigated. The variance and mean were calculated for each sample at the different frequencies

and at both areas. Using the Index of Dispersion

(/), where / = S2(n-\)x and where S2 = variance,

n = number of samples, and x = mean (GreigSmith, 1964, p. 63), the pattern of contagious or

noncontagious distribution could be assessed. The

significance of the values of / was assessed by reference to the chi-square table (Fisher and Yates, 1963)

for n-1 degrees of freedom. Deviation from random

expectation towards a contagious distribution is

significant if the values of / exceed p = 0.05.

Table 6 shows the results of this analysis on the

total fauna data. At a sample frequency of two

samples per 0.25 m2 only eight of twenty-four samples showed contagious distribution, whereas at a

frequency of four samples per 0.25 m2 seven of

twelve showed contagious distribution, and at a

frequency of eight samples per 0.25 m2 five of six

showed contagious distribution. In addition, the

precision of the estimate of the degree of contagious distribution (lowering of the significance

level to p = 0.01) increased with increasing sampling frequency.

Clearly, therefore, if beaches or areas of beaches

are to be compared quantitatively in terms of total

meiofauna (= biomass), a sampling frequency of

TABLE 6.—Index of Dispersion (I) for total fauna data using different

sampling frequencies.

Corer /Area

LARGE CORER

Area 1

Area 2

MEDIUM CORER

Area 1

Area 2

SMALL CORER

Area 1

Area 2

0.44

4.81 •

8.14f

16.44f

4.17*

1.45

2/025m*

0.64

3.01

0.71

0.69

0.76

0.05

4.74

459

1.98

0

052

4.64

Sampling frequency

• 054

• 1.67

0.86

0.89

052

• 9.0f

41025m*

2.97

16J9f

lSjO4f

28.07t

7.33

18.81f

16.61f

11.06#

5.62

1.33

156

56.87t

81025m*

35.17*

32.73f

2250-

91.00f

1059

87.12f

•p = 0.05; fP

 = ° 0 1
196

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

upwards of eight samples per 0.25 m2 gives the

greatest precision. For area 2 (Table 6) a sample

frequency of four samples per 0.25 m2 gave a reasonably accurate estimate of density, but this was

not true for area 1.

This method of predicting the number of samples needed can be used for total fauna (= biomass) comparisons or in comparing numerically the

major faunal elements. In another method used by

macrofaunal workers the number of new species

found in each successive sample are totalled. At

first, each successive sample adds a large number to

the cumulative species total. After a certain number of samples the number of new species added

with each additional sample falls to almost zero.

The number of samples needed to include 90 percent of the available species is taken as the sampling frequency needed. This method is unlikely

to be applicable to meiofaunal sampling procedure

unless one has access to a large number of systematists and technicians, as the number of species of

meiofauna present in one sediment sample are very

large.

Comparison of Two Areas of Beach

The variance of the samples taken was found to be

proportional to the mean; therefore, the raw data

was transformed to logn in order to stabilize the

variance. (Williams, 1964, and South wood, 1966,

have extensive reviews of transformation procedure.) Analyses of variance were conducted on the

transformed data obtained by the medium corer at

the three sampling frequencies used. Table 7 shows

the results of these analyses. At a sampling frequency of two samples per 0.25 mz

 the F ratio was

insignificant. However, at sample frequencies of

both four and eight samples per 0.25 m2 the F ratio

was significant at p = 0.01 (i.e., the between-area

variation was greater than the within-area variation) . The areas, therefore, were significantly different from each other in terms of total fauna.

Significance of Results

For the sand sampled in this investigation (for

both areas 75 percent of the grains were in the

range 125 to 250 p. diameter) and for the animals

found (size range 1 to 15 mm), a corer 3.75 cm in

diameter was found to be the most suitable with

the extraction procedure used. Mclntyre (in the

present volume) has found that, for mud, a corer

10 cm in diameter is necessary to prevent loss of

surface floe. Thus, sample size should vary according to the environmental and faunistic conditions

being investigated.

The meiofauna in beaches or in areas of beaches

often have been compared quantitatively by using

a single pair of samples. The present study has

shown that, for the meiofauna at the beach investiTABLE 7.—Analysis of variance tables after transformation to logn of the total

fauna data obtained from the medium corer (see Tables 2, 3). Sample frequencies

of two, four, and eight samples per 0.25m* are based on the random numbers

shown in Figure 1.

Samples per 025m* Source of variation

Sum of Degrees of

squares freedom Mean square F ratio

Two samples

Four samples

Eight samples

Between areas

Within areas

Total

Between areas

Within areas

Total

Between areas

Within areas

Total

0.4764

0.1801

0.6565

0.7470

0.2099

03569

0.8265

0.3792

12057

1

2

3

1

6

7

1

14

15

0.4784

0.0900

0.7470

0.0350

0.8265

0.0271

5.293

21.34»

S0.495*

•Significant at less than p = 0.01.
NUMBER 76 197

gated, the variation within a single pair of samples

was larger than the variation between areas of a

beach. Upwards of four samples per 0.25 m2 were

found to be necessary to render the variation for

the total meiofauna between areas of beach greater

than that within an area. However, four samples

per 0.25 m2 did not give a reliable estimate of the

dispersion pattern of the fauna in one of the two

areas investigated. Upwards of eight samples per

0.25 m2 were found necessary to encompass the variations in spatial distribution patterns in both

areas.

Since truly quantitative sampling techniques are

being established for the meiobenthos (see Hulings

and Gray, 1971), sampling procedure should be

given more attention. It must be reemphasized that

this investigation was intentionally made simple.

This paper is intended merely to focus more attention on this important subject, which has been neglected by meiofaunal workers.

Literature Cited

Cochran, W. G.

1966. Sampling Techniques. 413 pages. New York: John

Wiley.

Fisher, R. A., and F. Yates

1963. Statistical Tables for Biological, Agricultural and

Medical Research. 146 pages. Edinburgh: Oliver

and Boyd.

Greig-Smith, P.

1964. Quantitative Plant Ecology. 256 pages. London:

Butterworths.

Hulings, N. C, and J. S. Gray

1971. A Manual for the Study of Meiofauna. Smithsonian Contributions to Zoology, 78:1-83.

Southwood, T. R. E.

1966. Ecological Methods. 391 pages. London: Methuen.

Vitiello, P

1968. Variations de la density du microbenthos sur une

aire restreinte. Recueil des Travaux de la Station

Marine d'Endoume, 43:261-270.

Williams, C. B.

1964. Patterns in the Balance of Nature. 324 pages.

New York: Academic Press.

R. Williams A Technique for

Measuring the

Interstitial Voids

of a Sediment

Based on Epoxy

Resin Impregnation

ABSTRACT

A vacuum impregnation technique for sand and

gravel sediments using unsaturated polyester and

epoxy resins is described. Simple methods are given

for the measurements of porosity and particle and

void dimensions, from the thin sections obtained

by the above method. The technique enables the

interstitial fauna to be related directly to the

dimensions of the interstices of sand and gravel

sediments rather than to their grain size composition.

Many attempts have been made to relate animal

types to the deposits in which they occur. The influence of the particle size composition of a beach

on the distribution of certain organisms has been

suggested by Davis (1925), Prenant (1932),

Holme (1949), Jones (1950), Wieser (1956), and

Ganapati and Rao (1962). Wieser (1959) illustrated a correlation between particle size and the

interstitial fauna.

The aim of this investigation, which utilizes the

impregnation technique, is to enable one to relate

the faunal components directly to the dimensions

of the interstices of sand and gravel sediments

rather than to their grain size composition. AlR. Williams, Oceanographic Laboratory (SM.BA.), Edinburgh, Scotland.

though the interstitial system is influenced by the

size, shape, and spatial relationships of the grains

of the deposit, it is the labyrinth of channels between the sand grains that forms the real habitat

for the fauna. Because the limitations of the interstices constitute the actual barrier to the interstitial

animals, the percentage of voids exceeding a certain dimension will probably determine the suitability of the habitat for a given species. If the

percentage of the interstices exceeds a certain value

the voids may form a system which will be continuous for colonization by the animal. A technique

was devised so that the dimensions of this habitat,

i.e., the voids of the sediment, could be measured

and a comparison made to those of other sediments. It is based on an established method for the

preparation of thin sections of soil. In this method

an air-dried sample of soil is fully impregnated

with a hard-setting liquid, and is cut, mounted,

and ground to the point at which the structure

may be recognized.

In the past, materials used as impregnants had

limitations. Materials used prior to 1940 are summarized by Volk and Harper (1939), and the more

advanced materials and techniques are reviewed by

Jongerius and Heintzberger (1963). In recent

years, Hagn (1953), Alexander and Jackson (1954),

Altemuller (1956, 1962), and Wells (1962) have

attained a high degree of success by using cold and

thermosetting, unsaturated polyester and epoxy resins. Although these resins make the complete im199
200

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

pregnation of gravel and sands relatively simple,

the preparation of sections still requires specialized

equipment.

Preparing Thin Sections

Undisturbed samples of the sediment are collected

with the use of brass rectangular samplers with

double sliding lids (10 by 5 by 2.5 cm). The sampler is pressed into the surface of the deposit and

when the sediment around the sampler has been

cut away the lower lid can be slid into place. The

sampler then is marked appropriately with orientation, tidal height, and date. The brass samplers are

allowed to drain, leaving the minimum amount of

water in the sample, and then are air-dried and

impregnated with resin. The crystallized salt in the

dried sample does not hinder impregnation or

lessen, to any extent, the quality of the finished

slides. In fact, a small amount of salt tends to

maintain the structure of the sediment in the dry

state before the resin sets in place.

The resins used for impregnation are Crystic

28C (Alexander and Jackson, 1954) and Araldite

MY750 (Wells, 1962). When using Araldite for

impregnation the inner surface of the sampler

should be treated with Araldite Release Agent

QZ12 to aid the release from the sampler of the

hardened impregnated sample. A fluorescent dye,

Uvitex SWN, is mixed with the resin following a

technique outlined by Werner (1962). Under ultraviolet light, this dye in the pore system fluoresces reddish pink; the quartz fraction, red, and

the calcium carbonate, blue. This coloration

greatly assists in the identification and measurement of the interstices.

The vacuum apparatus used for impregnation

(Figure 1) is a modification of the method used

by Wells (1962). This apparatus can be constructed easily by using "Quick-Fit" glassware. A

number of samples located around the periphery

of the desiccator can be impregnated in succession

by rotating the upper part of the apparatus in its

socket. Sufficient vacuum for complete impregnation of cohesionless sediments, sands and gravels

possessing a single grain structure, can be obtained

with the use of a water pump. Water vapor is prevented from entering the vacuum apparatus by a

FIGURE 1.—Impregnation apparatus: a, vessel containing

resin; b, desiccator containing anhydrous CaCl2 and the

sample (c) for impregnation; d, inlet for air into a and b;

e, suction by water pump via a silica gel vessel inserted

into the vacuum line.

vessel containing calcium chloride or silica gel introduced into the vacuum line.

Thin sections are prepared parallel to and at

right angles to the surface of the deposit following

the pattern outlined by Dalrymple (1957) and by

Jongerius and Heintzberger (1963). For convenience, the hardened impregnated blocks of sediment

(10 by 5 by 2.5 cm) are sawn into three blocks

measuring 3 by 5 by 2.5 cm. Thin sections cut

from these blocks are ground, polished, and

mounted on slides. From each large block approxi-
NUMBER 76 201

mately three to six sections are cut vertically and

six sections are cut horizontally to the original surface of the deposit. During grinding, the thicknesses of the sections on the slides are checked frequently by use of a polarizing microscope to

observe the interference colors of the quartz grains.

For sand deposits it is essential that mechanical

grinding of the sections does not proceed beyond

50 (i because further grinding may crack the sand

grains. The final thickness of the slides will vary

with the different types of sediment and may vary

with each sediment.

The ideal section thickness for measurement of

the voids and particles is obtained when the maximum dimensions of the majority of particles still

can be observed through the transparent embedding resin. Grinding is then finished by hand,

using varying grades of carborundum powder.

Sometimes, especially when the constituent grains

are smooth, the samples need reimpregnation after

grinding and polishing because the particles have

been dislodged from the resin matrix. Coverslips

are then placed over the thin sections, using Araldite AY 103 as a mountant. When carrying out this

procedure care must be exercised so that all the air

bubbles are excluded. If not excluded the air bubbles show up clearly in transmitted light and interfere with the measurement of the sections. The

slides are then set aside overnight for the mountant to cure, after which they are ready for microscopic examination.

Measuring Sections

Two different sets of measurements are obtained

from the thin sections of sediment: one series for

porosity determinations and the other for void and

particle measurements.

The porosity measurements are taken when the

microscope is focused on the surface plane of the

sections. When the voids and particles are measured the complete thickness of the sections can be

utilized. This is possible because the embedding

resins are transparent and a three-dimensional

view is obtained by the packing of the particles.

Because the maximum dimensions of the particles

are measured, there is no need to apply a conversion factor to the particle size data (Williams and

Crisp, in preparation).

Measuring Porosity

Methods for the micromorphometric analysis of

soil structure have been developed by Kubiena,

Beckmann, and Geyger (1961, 1962, 1963), Jongerius (1963), Beckmann (1964), and Geyger (1962,

1964), but all of these methods require specialized

equipment. One of the sophisticated techniques for

measuring the porosity of photomicrographs utilizes the Zeiss Particle Size Analyser, which has 48

diameter classes (Jongerius, 1963). Its lower limit

for measurement is 10 p..

A similar but simpler method, developed by

Rosiwal and adapted by Swanson and Peterson

(1940), is used for the measurement of the percentage volume of pore space in thin sections ot

undisturbed soil. The microscope is focused on the

surface of the section and measurements are taken

in this plane only. The slide is traversed across a

mechanical stage parallel to the direction of the

graduated scale incorporated in the eyepiece, and

the distance is measured between the intercepts

made by each successive void and each successive

particle (Figure 2). The traverses are repeated

over the entire section following a grid system.

The complete procedure is duplicated in a direction at right angles to the first series of measurements. Further measurements are made on the

other sections horizontally cut from the three

blocks. The total void measurement for the sample

then is expressed as a percentage of the total measurement of void and solid. It has been assumed

(Holmes 1930; Swanson and Peterson, 1940) that

this value is equivalent to the porosity of the sediment defined as the fraction of the total volume

occupied by the voids. An independent test, which

FIGURE 2.—Cross section of a model spherical system to illustrate the method of measuring porosity. Measurements are

taken along the grid line. The solid outlines represent the

plane in which the slide has been focused.
202

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

will be given in a later paper (Williams and

Crisp, in preparation) has shown this assumption

to be justified.

From Figure 2 an estimate of the porosity (P) is

given by

P =

a+b+c+d

A+a + B + b + C+c+D + d

The technique may be used directly on the slides

or it can be adapted for measurement of photographs taken from the slides by direct projection.

The views in Figure 3 are magnifications of

small areas of sections of two shell gravels obtained

by projection. Photographs obtained by this

method are useful for making combination figures

with accurate scale silhouettes of interstitial animals (Williams, 1969).

Sections of deposits from beaches having sand of

small grain sizes are first projected to obtain a negative, which then is enlarged to give a positive at a

magnification of about fifty times. Satisfactory photographs are not always obtained from sections of

very fine sands because the thin sections of quartz

transmit as much light as the voids, making the

peripheries of the voids indistinct. In such cases

the porosities are measured directly from the slides

under ultraviolet light, which causes the voids to

fluoresce characteristically.

Measuring Particles and Voids

Particle and void measurements are made only on

the slides; however, instead of measuring intercepts, particles and voids are systematically located

by utilizing a grid system. The grid is formed by

traversing the mechanical stage of the microscope

through a specified number of divisions between

each series of measurements. The maximum dimensions in two directions at right angles of each

particle and void so located are measured. The

above method of measurement, utilizing the complete thickness of the section, is illustrated in Figure 4. The grain measurements are given by AjA.,,

B^a, etc., and the void measurements by a^ , bxb2,

etc. The procedure is carried out for the sections

which are taken parallel to and vertically to the

surface of the deposit. The four sets of values thus

obtained represent the maximum dimensions of the

voids in three directions in the deposit, with a duplicate measurement of one of the directions parallel to the surface. From these measurements the

possibility of directional orientation of the pores

or the particles can be checked by analyzing the

data statistically. The measurements of particle

and void dimensions then can be plotted against a

Log10 or Log_2 scale and the relevant statistical

parameters, such as the mean, median, standard deviation, etc., can be obtained from the cumulative

curves.

Conclusions

Although the method requires specialized cutting

and grinding equipment, very reliable results can

be obtained, even with little experience.

In recent years the development of water-soluble

resins has made possible in situ impregnation of

marine sediments. The development of this technique will overcome the use of the sampler for obtaining "undisturbed" samples and will eliminate a

source of error and criticism of the method.

The accuracy of the technique was tested by impregnating various model systems of "Ballotini,"

which are uniform glass beads (Williams and

Crisp, in preparation). Porosity, void, and particle

measurements were made from the slides and excellent correlations were observed with results obtained from sieving and displacement methods for

porosity estimates.

The resin impregnation method enables direct

measurement and visual examination to be made

of the interstitial habitat. The measurements of

the interstices together with the other physical

data from the sediment create a set of interwoven

factors, the interplay of which will affect the distribution of the fauna. The information acquired

from this technique is a further measurable character which will contribute towards a better understanding of this extremely complex biocoenosis.

Acknowledgments

This paper was originally presented at the Third

European Marine Biology Symposium at Arcachon,

France, September 1968, but owing to uncertainty

of publication has been included in these Proceedings of the First International Conference on

Meiofauna.
NUMBER 76 203

FIGURE 3.—Projections of thin sections of shell gravel. The angularity of the sediment is due to

the plates of barnacle shells.
204

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

FIGURE 4.—Cross section of a model spherical system to illustrate the method of measuring voids and particles.

I express thanks to Professor D. J. Crisp, under

whose supervision this work was carried out, and

to all members of the Marine Science Laboratories

staff for their help and interest. I am especially

grateful to Professor W. C. Evans and Dr. D. A.

Jenkins of the Department of Soil Science,

U.C.N.W., Bangor, for the use of their sectioning

facilities.

This work was carried out during tenure of

a N.E.R.C. Research Student grant held at the

Marine Science Laboratories, U.C.N.W., Menai

Bridge, Anglesey.

Literature Cited

Alexander, F. £. S., and R. M. Jackson

1954. Examination of Soil Micro-Organisms in Their

Natural Environment. Nature, 174:750-751.

Altemuller, H. J.

1956. Neue Moglichkeiten zur Herstellung von Bodendunnschliffen. Zeitschrift fur Pflanzenernahrung,

Dungung, Bodenkunde, 72(117):56-62.

1962. Verbesserung der Einbettungs- und Schleiftechnik

bei der Herstellung von Bodendunnschliffen mit

VESTOPAL. Zeitschrift fur Pflanzenernahrung,

Dungung, Bodenkunde, 99(144): 164-177.

Beckmann, W.

1964. Zur Ermittlung des dreidimensionalen Aufbaues der

Bodenstruktur mit Hilfe mikromorphometrischer

Method. In A. Jongerius, editor, Soil Micromorphology, pages 429-444. Amsterdam: Elsevier.

Dalryraple, J. B.

1957. Preparation of Thin Sections of Soils. Journal of

Soil Science, 8(1):161-165.

Davis, F. M.

1925. Quantitative Studies on the Fauna of the Sea

Bottom. Part II. Fishery Investigations, London,

8(4): 1-50.

Ganapati, P. N., and G. C. Rao

1962. Ecology of the Interstitial Fauna Inhabiting the

Sandy Beaches of Waltair Coast. Journal of the

Marine Biological Association of India, 4(l):44-57.

Geyger, E.

1962. Zur Methodik der mikromorphometrischen Bodenuntersuchung. Zeitschrift fur Pflanzenernahrung,

Dungun, Bodenkunde, 99(144): 118-129.

1964. Mikromorphometrische Untersuchungen iiber den

Einfluss bestimmter Pflanzengemeinschaften auf die

Strukturbildung im Boden. In A. Jongerius, editor,

Soil Micromorphology, pages 445-457. Amsterdam:

Elsevier.

Hagn, H.

1953. Polestar, ein Hilfsmittel fur die Herstellung orientierter Diinnschliffe kleiner Objekt. Mikrokosmos,

43:68-72.

Holme, N. A.

1949. The Fauna of Sand and Mud Banks near the

Mouth of the Exe Estuary. Journal of the Marine

Biological Association of the United Kingdom,

28:189-237.

Holmes, A.

1930. Petrographic Methods and Calculations. New York:

D. Van Nostrand.

Jones, N. S.

1950. Marine Bottom Communties. Biological Reviews,

25:283-313.

Jongerius, A.

1963. Optic-Volumetric Measurements on some Humus

Forms. Proceedings of a Colloquium on Soil Fauna,

Soil Microflora and Their Relationships, Amsterdam, pages 137-148.

Jongerius, A., and G. Heintzberger

1963. The Preparation of Mammoth-Sized Thin Sections.

Soil Survey Papers, 1:1-37. Netherlands Soil Survey

Institute, Wageningen.

Kubiena, W.; W. Beckmann; and E. Geyger

1961. Zur Methodik der photogrammetrischen Strukturanalyse des Bodens. Zeitschrift fur Pflanzenernahrung, Dungung, Bodenkunde, 92(137): 116-126.

1962. Zur Untersuchung der Feinstruktur von Bodenaggregaten mit Hilfe von Strukturphotogrammen.

Zeiss Mitteilungen, 2(7):256-27S.

1963. Mikromorphometrische Untersuchungen an Hohlraumen im Boden. Anales de Edafologia y Agrobiologia, 22(ll-12):551-567.

Prenant, M.

1932. L'Analyse mlcanique des sables littoraux et leurs

qualites ecologiques. Archives de Zoologie Expertmentale et Generate, 74:581-595.

Swanson, C. L. W., and J. B. Peterson

1940. Differences in the Microstructure of Profiles of the

Marshall and Shelby Silt Loam. Proceedings of the

Soil Science Society of America, 5:297-303.

Volk, G. W., and H. J. Harper

1939. A Revised Method for the Microscopic Examination

of Natural Structure and Pore Space in Soils. Journal of Soil Science, 48:141-145.

Wells, C. B.

1962. Resin Impregnation of Soil Samples. Nature,

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NUMBER 76 205

Werner, J. 1959. The Effect of Grain Size on the Distribution of

1962. Ober die Herstellung fluoreszierender Bodenan- Small Invertebrates Inhabiting the Beaches of Puget

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