NOAA Technical Report NMFS 100

Marine Flora and Fauna

of the Eastern United States

Dicyemida

Robert B. Short

u.S. Department of Commerce

February 1991
NOAA Techncial Report NMFS

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Recent~y Published NOAA Technical Reports NMFS

90. Elasmobranchs as living resources: advances in the

biology, ecology, systematics, and the status of the

fISheries, edited by Harold L. PrattJr., Samuel H. Gruber,

and Toru Taniuchi. July 1990, 518 p.

91. Marine flora and fauna of the northeastern United

States-Echinodermata: Crinoidea, by Charles G.

Messing and John H. Dearborn. August 1990, 30 p.

92. Genetics in aquaculture: proc,~edings of the sixteenth

U.S.-Japan meeting on aquaculture; Charleston, South

Carolina, 20-21 October, 1987, edited by Ralph S.

Svrjcek. November 1990, 81 p.

93. Distribution and abundance of juvenile salmonids off

Oregon and Washington, 1981-1985, by William G.

Pearcy and Joseph P. Fisher. Kovember 1990, 83 p.

94. An economics guide to allocation offish stocks between

commercial and recreational fisheries, by Steven F.

Edwards. November 1990, 29 p.

95. Larval fish recruitment and research in the Americas:

proceedings of the thirteenth annual larval fish conference; Merida, Mexico, 21-26 May 1989, edited by

Robert D. Hoyt. January 1991, 147 p.

96. Marine flora and fauna of the Eastern United

States-Copepoda, Cyclopoida: Archinotodelphyidae, Notodelphyidae, and Ascidicolidae, by Patricia

L. Dudley and Paul L. Illg. January 1991, 40 p.

97. Catalog of osteological collections of aquatic mammals from Mexico, by Omar Vidal. January 1991,

36 p.

98. Marine mammal strandings in the United States:

proceedings of the second marine mammal stranding workshop; Miami, Florida, 3-5 December,

1987, edited by John E. Reynolds III and Daniel K.

Odell. January 1991, 157 p.

99. Marine flora and fauna ofthe Northeastern United

States: Erect Bryozoa, by John S. Ryland and Peter

J. Hayward. February 1991, 48 p.

100. Marine flora and fauna of the Eastern United States:

Dicyemida, by Robert B. Short. February 1991,16 p.

101. Larvae of nearshore fishes in oceanic waters near

Oahu, Hawaii, by Thomas A. Clarke. March 1991,

19 p.
NOAA Technical Report NMFS 100

Marine Flora and Fauna

of the Eastern United States

Dicyemida

Robert B. Short

February 1991

u.s. DEPARTMENT OF COMMERCE

Robert Mosbacher, Secretary

National Oceanic and Atmospheric Administration

John A. Knauss, Under Secretary for Oceans and Atmosphere

National Marine Fisheries Service

William W. Fox Jr., Assistant Administrator for Fisheries
Foreword _

This NOAA Technical Report NMFS is part of the subseries "Marine Flora and Fauna

ofthe Eastern United States" (formerly "Marine Flora and Fauna of the Northeastern

United States"), which consists of original, illustrated, modern manuals on the identification, classification, and general biology of the estuarine and coastal marine plants

and animals of the eastern United States. The manuals are published at irregular intervals on as many taxa of the region as there are specialists available to collaborate

in their preparation. These manuals are intended for use by students, biologists,

biological oceanographers, informed laymen, and others wishing to identify coastal

organisms for this region. They can often serve as guides to additional information about

species or groups.

The manuals are an outgrowth of the widely used "Keys to Marine Invertebrates

of the Woods Hole Region," edited by R.I. Smith, and produced in 1964 under the

auspices of the Systematics Ecology Program, Marine Biological Laboratory, Woods

Hole, Massachusetts. Geographic coverage of the "Marine Flora and Fauna of the

Eastern United States" is planned to include organisms from the headwaters of estuaries

seaward to approximately the 200-m depth on the continental shelf from Maine to

Florida, but can vary somewhat with each major taxon and the interests of collaborators.

Whenever possible, representative specimens dealt with in the manuals are deposited

in the reference collections of major museums.

The "Marine Flora and Fauna of the Eastern United States" is being prepared

in collaboration with systematic specialists in the United States and abroad. Each manual

is based primarily on recent and ongoing revisionary systematic research and a fresh

examination of the plants and animals. Each manual, treating a separate major taxon,

includes an introduction, illustrated glossary, uniform originally illustrated keys, annotated checklist (with information, when available, on distribution, habitat, life history,

and related biology), references to the major literature of the group, and a systematic

index.

Manuals are available from the National Technical Information Service, United

States Department of Commerce, 5285 Port Royal Road, Springfield, VA 22161, either

as a paper copy or microfiche, for a charge. Manuals are not copyrighted, and so can

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available in most major libraries and listed at the end of this manual.

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recommend or endorse any proprietary product or proprietary

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an intent to cause directly or indirectly the advertised product to

be used or purchased because of this NMFS publication.

11
Marine Flora and Fauna of the Eastern United States

Dicyemida

ROBERT B. SHORT

Department of Biological Science B-142

Florida State University

Tallahassee, FL 32306-2043

ABSTRACT

This manual treats the six species of dicyemid mesozoans that have been reported in three

species of hosts (Octopus vulgaris, O. joubini, and O. briareus) from the eastern coast of North America

and the Gulf of Mexico, including the Florida Keys. All are parasites of species of Octopus and

are in the genus Dicyema, family Dicyemidae. In the introduction, the life cycle, as known, and

the general morphology of dicyemids are briefly described, and methods are given for collecting

and preparing material for study. These are followed by a key to species and by an annotated

checklist, which includes data, some hitherto unpublished, on their known prevalence in hosts

from various localities including Bimini and Bermuda.

Introduction _

The dicyemid mesozoans are a relatively small group of

minute parasites with a simple yet multicellular structure.

They parasitize cephalopod molluscs and are found

primarily in the fluid-filled renal sacs (renal coelom) or

"kidneys." In decapod cephalopods (squids, sepiolids, and

teuthoids), they have been found also in the reno-pancreatic

coelom and occasionally in the pericardium (Hochberg

1983). Dicyemids were discovered by Cavolini (1787) and

were described by Krohn (1839) and Erdl (1843).

The name Mesozoa was proposed by van Beneden

(1876) to indicate his beliefthat the simple structure ofthese

parasites represents an evolutionary stage between the protozoans and metazoans. There has been considerable controversy regarding their taxonomic position. The dicyemids

have usually been considered to form, together with the

orthonectids (parasites of various invertebrates), the

phylum Mesozoa (e.g., Hyman 1940). Stunkard (1954),

however, has argued that the mesozoans should be included

as a class in the phylum Platyhelminthes. Furthermore,

because of differences between the dicyemids and orthonectids in internal structure and the lack of homologies in their

life-cycle stages, other workers (e.g., Kozloff 1969;

Hochberg 1983) have considered them not to be closely

related. Hochberg (1983) suggested that" it is best to treat

these two assemblages as separate phyla [Dicyemida and

Orthonectida] and to use the term 'Mesozoa' to refer to

their grade of organization only. " In the present manual

this systematic scheme will be followed, and only members

of the phylum Dicyemida will be considered.

Recent accounts of the dicyemids have been published

by Hochberg (1982, 1983, 1990) and Stunkard (1982).

Earlier reviews include those of Hyman (1940), Stunkard

(1954), Czihak (1958), Grasse (1961), and McConnaughey

(1963, 1968).

A total of about 40 species of cephalopods, representing

15 genera, are currently known to be hosts of dicyemids.

The parasites occur mostly in cuttlefishes, sepiolids, and

octopods and less frequently in loliginid squids and have

been reported from temperate, polar, and subtropical

waters in many parts of the world.

This manual deals with the dicyemid mesozoans reported

from off the coast of eastern North America and the Gulf

of Mexico, including the Florida Keys. All hosts reported

herein are species in the genus Octopus.

Morphology and Life Cycle _

In the renal sacs, vermiform stages are the conspicuous

ones. These occur with the anterior ends adhering to, and

more or less embedded in, the renal appendages (venous

appendages) of the host, with most of the body floating

freely in the host urine within the sac. They may also be

seen swimming slowly in the urine, propelled by their cilia.

Vermiform stages have a simple multicellular structure

(Figs. 1, 2). A single elongated axial cell (except in stem
2 NOAA Technical Report NMFS 100 _

Figure :3 (Facing page, top)

Photographs. (A) Dicyema typoides rhombogens. (B) D. hypercephalum rhombogens. (C) D. apalachiensis nematogens. In part

from Short (1962, 1964). Scale in micrometers.

Figure 2

Diagrams of anterior end views of primary and secondary nematogens and rhombogens of the genera Dicyema (A), Pseudicyema

(B), and Dicyemennea (C). Calotte patterns and parapolar cells

shown. Redrawn from Nouvel (1947). Cilia not drawn.

c

o 0

'iC:) c:y o 0

o

B

..

",:..i0 o'~"..

';? 0<;,

A

Figures 4-8 (Facing page, bottom)

Fig. 4. Vermiform embryos ofD. bilobum. (A) Surface view. (B)

Optical section. (C) Optical section of anterior end of Dicyemennea eledones, showing anterior abortive axial cell (arrow). (A and

B) redrawn from Couch and Short (1964); (C) modified from

Nouvel (1947). Fig. 5. Infusorigens within axial cells of rhombogens. (A) Dicyema briarei. (B) D. aegira. (A) redrawn from Short

(1961); (B) redrawn from Short and Damian (1967). Figs. 6-8.

Infusoriform larvae. (6) Dicyema aegira, optical sagittal section (to

same scale as Fig. 5). (7 and 8) Dicyema briarei. (7) Dorsal view

within axial cell of rhombogen. (8) Optical sagittal section. a =

refringent body; b capsule cell; c = urn cell. (6) modified from

Short and Damian (1966). (7 and 8) from Short (1961). Scales

in micrometers. Cilia not shown.

TRUNK

}CALOTTE

DIAPOLAR

CELLS

CEPHALIC

SWELLING

AGAMETES {

(AXOBLASTS)

---#---'1.',

AXIAL CELL -----4'!L-II:.\,~jl

NUCLEUS

VERRUCIFORM

CELL

Figure 1

Generalized drawing of a young dicyemid (Dicyemennea) showing

terms for various parts. Modified slightly from McConnaughey

(1951).

nematogens, which may have two or three axial cells; see

below) is surrounded by a single layer of ciliated peripheral

(somatic) cells. Somatic cells are arranged in groups. The

anterior or "head" group is modified into a calotte consisting (typically) of two tiers of cells, the propolar and

metapolar cells. These cells have shorter, denser cilia than

other somatic cells. Immediately behind the calotte are the

parapolar cells (usually two), then trunk cells, consisting

ofseveral diapolars, and two posterior uropolar cells covering the posterior end of the axial cell. Parapolar and trunk

cells often contain refractive granular material in their

cytoplasm (see Figs. 3, 20). The diapolar and uropolar cells

of certain species become so laden with such material that

they are swollen; if this is the case, they are termed verruciform cells (Fig. 1).

The number and arrangement of somatic cells is rather

constant for a species but may vary within narrow limits.

Somatic cell numbers range among species from 14 to 40.

Lengths of adult vermiform stages vary from about 260

to 10,000 11m, depending on the species.

Typical mature vermiform stages encountered are of two

types or phases: nematogens and rhombogens. Besides a

nucleus, the axial cells ofnematogens contain within their

cytoplasm agametes (axoblasts), which are asexual reproductive cells, and vermiform embryos (Figs. 3C, 4) in

various stages of development. Axial cells of young nematogens may contain only agametes (as in Fig. 1). Axial cells

of rhombogens contain one or more of a bisexually reproductive stage (or gonad), the infusorigen (Fig. 5), and also

infusoriform larvae (Figs. 3A, 6-8), which are ciliated when

fully developed. A diagram of the life cycle is shown in

Figure 9.

Vermiform embryos develop within axial cells ofnematogens from mitotic division of agametes. Early in development, they attain the definitive somatic cell number; they
________________________ Short: Dicyemida of the Eastern United States 3

c

o

Q

A B

4

c

A

5

B
4 NOAA Technical Report NMFS 100 _

Primary

RHOMBOGEN

(

Secondary

NEMATOGEN

Stem

NEMATOGEN

(INFUSORIGEN)

c;

j

INFUSORIFORM

?

IN THE

CEPHALOPOD

OUTSIDE THE

CEPHALOPOD ?

Figure 9

Diagram of the life cycle. Single straight

line from primary NEMATOGEN indicates development of vermiform embryos

into primary rhombogens; double lines

indicate transformation of recognizable

nematogens into secondary rhombogens

and of rhombogens into secondary nematogens. From McConnaughey (1951).

then continue to grow in size and, at a certain stage, escape

from the parent nematogen (a process called eclosion).

They further mature to become nematogens and produce

vermiform embryos within their axial cells. By this means,

large numbers of primary nematogens populate the cephalopod kidney. Vermiform embryos of some species of

dicyemids (in the genus Dicyemennea) at eclosion possess,

in addition to the usual single elongated axial cell, a small

"abortive" axial cell located immediately anterior to the

larger axial cell (Fig. 4C). This abortive axial cell degenerates soon after the embryo escapes from the nematogen.

When a large number of primary nematogens have been

built up in the cephalopod kidney by production of vermiform embryos, a change in the population occurs such

that the predominant mature phase becomes the rhombogen. Rhombogens may originate in two ways: 1) from

immature vermiform stages (primary rhombogens) and

2) by transformation of functional nematogens to rhombogens (secondary rhombogens). During this transformation, some transitional stages may have large numbers of

single cells (agametes?) in their axial cells; other transitional

stages may contain both vermiform embryos and infusongens.

The infusorigen (Fig. 5), as mentioned above, is a hermaphroditic individual or stage (probably more properly

called a gonad) that remains within the axial cell of a rhombogen. Each infusorigen is composed of a more or less

spherical "axial" cell, with male reproductive cells inside

and female cells more or less surrounding it. The male cells

consist of spermatogonia, spermatocytes, and tailless spermatozoa; female cells are oogonia and oocytes. Spermatozoa, formed within the "axial" cell, emerge and penetrate

oocytes. When fertilization is completed, the zygote develops into an infusoriform larva (Figs. 6-8), which, when

mature, escapes from the rhombogen and from the cephalopod host with the urine. Rhombogens typically have one

to a few infusorigens (Fig. 3A), and sometimes in larger

individuals a series of developmental stages of infusoriform

larvae extend in opposite directions from each infusorigen.

The infusoriform (Figs. 6-8) is morphologically the most

complex stage in the cycle and is rather similar in structure among a wide variety ofspecies. It is ovoid or pyriform

and has cilia over the posterior region and a large part of

the dorsal and lateral surfaces. A characteristic feature is

the presence of two relatively large "refringent bodies,"

each located within an anterodorsal apical cell and surrounded by a thin layer ofthis cell's cytoplasm. Refringent

bodies are often crystalline. In some species of dicyemids,

however, the bodies are not refractive and are termed

mucoid; in other species bodies are absent or at least not

readily apparent. In the interior of infusoriforms are two

large capsule cells that form the so-called urn. These cells

often contain conspicuous granules and appear in lateral

view relatively thin and more or less C-shaped (Figs. 6,

8); they surround four urn cells posteriorly, dorsally, and

to a large degree laterally. Cytoplasm of the urn cells

usually stains more darkly than that of other cells. Each

urn cell usually contains two nuclei and one smaller cell
___________________________ Short: Dicyemida of the Eastern United States 5

interpreted as a germinal cell. Two germinal cells per urn

cell have been reported in a few species.

As indicated by Figure 9, the life cycle of dicyemids is

not completely known. That part within the host is pretty

well understood, but little or nothing is known about the

mode of entry into new hosts and initiation of infection.

The earliest known stage seen in young cephalopods is

termed the stem nematogen. It differs from other nematogens chiefly in having two or three axial cells instead of

one. Stem nematogens, at first very small, may grow to

be considerably larger than other nematogens. Agametes

in their axial cells develop into vermiform embryos that

emerge and become primary nematogens, each with a

single axial cell. Presumably, the infusoriform larva, which

leaves the cephalopod, is responsible for infecting new

hosts, but whether it infects a cephalopod directly or uses

an intermediate host is not clear, nor is it known whether

infection occurs by means of the entire larva or by only

certain cells (germinal cells?).

Dicyemid Families and Genera _

To date 68 species of dicyemids have been described in the

two families and eight genera listed below.

No. of

specIes

Family Dicyemidae

Dicyema von Kiilliker, 1849 33

Pseudicyema Nouvel, 1933 1

Dicyemennea Whitman, 1883 26

Dicyemodeca Wheeler, 1897 1

Pleodicyema Nouvel, 1961 1

Dodecadicyema

Kalavati and Narasimhamurti, 1980

Pseudicyema: same as Dicyema except that polar cells alternate with metapolar cells (Fig. 2B).

Dicyemennea: 9 polar cells (4 propolar, 5 metapolar) (Figs.

1, 2C).

Dicyemodeca and Pleodicyema: 10 polar cells (4 propolar, 6

metapolar).

Dodecadicyema: 9 to 14 polar cells (4 propolar, 6 metapolar,

plus, in most individuals, 3 (occasionally 2) much smaller

cells forming the anterior tip of the calotte).

An important species character is the peripheral (somatic) cell number. This can be determined accurately for

vermiform embryos and generally for young or small

nematogens because each cell has a single nucleus, which

is easily visible. Care should be taken, however, in determining cell numbers for rhombogens (and sometimes also

large nematogens) because in certain species (e. g. , Dicyema

aegira) peripheral trunk cells sometimes contain accessory

nuclei, i.e., nuclei in addition to the original cell nucleus

(see Fig. 15). Accessory nuclei apparently arise by mitotic

budding that may produce daughter nuclei of very unequal

size (McConnaughey 1951), and their presence may cause

difficulty in obtaining reliable cell counts.

Species are characterized also by the size and general

shape of adult vermiform and infusorigen stages, the shape

of the calotte, the anterior extent and degree of branching

of the axial cell, the presence or absence of verruciform

cells, and the structure of the infusoriform larva.

Only species in the genus Dicyema have been reported

from the coast of eastern North American and the Gulf

of Mexico, and in this genus abortive axial cells have not

been reported nor has branching of the axial cell. As mentioned above, the genus Dicyema is characterized by 4 propolar and 4 metapolar cells.

Family Conocyemidae

Conocyema van Beneden, 1882

Microcyema van Beneden, 1882

4

1

Collection and Preparation of

Dicyemids for Study _

Members of the family Conocyemidae differ from those

ofthe'family Dicyemidae in one major way: peripheral cells

of adult vermiform stages lose their cilia and fuse to form

a syncytium covering the axial cell, whereas in the Dicyemidae peripheral cells of adult vermiform stages retain their

cilia and their individual identity.

Genera in the Dicyemidae have been determined usually

by the number and arrangement of cells in the calottes of

the primary and secondary nematogens and rhombogens.

The situation in the Conocyemidae is not clear, and the

systematics of this group needs revision. The calottes of

genera in the family Dicyemidae have the following

configurations:

Dicyema: 8 polar cells (4 propolar, 4 metapolar), polar and

metapolar cells opposite each other (Fig. 2A).

The following procedure is used commonly for preparation of dicyemids. The octopod host, if active, can be

anesthetized by addition of 70% ethanol to sea water. It

then is laid on its back and a midventral cut of the mantle

is made from its anterior edge posteriorly to expose the conspicuous, fluid-filled renal sacs, which lie at the surface of

the visceral mass. The renal sacs are semitransparent, and

within them lie the renal appendages (see Fig. 39), which

are outpocketings ofthe venae cavae. Vermiform dicyemids

adhere to the renal appendages, often with their calottes

embedded in depressions in the renal epithelium. Smaller

vermiform individuals occur within the folds and crevices

of the appendages, and a few dicyemids may also occur

free in the urine.

The renal sacs are cut open and the appendages removed, en masse or a piece at a time, with the attached
6 NOAA Technical Report NMFS 100 _

dicyemids. Octopods, especially more mature ones, often

harbor heavy dicyemid infections, and the vermiform

stages can be seen easily with the lower powers of a dissecting microscope appearing as "hairs" projecting from

the edges of the renal appendages. Occasionally light infections occur and are more difficult to detect. Smears with

pieces of renal appendage are made on coverslips or slides

and, when fixed, stained, and mounted, are useful for

study. Bouin's fixative is satisfactory and can be followed

by staining with hematoxylin (e.g., Ehrlich's acid hematoxylin or Heidenhain's iron hematoxylin) and, if desired, by

counterstaining with eosin. Care should be taken not to

let the coverslip smears become dry at any time during the

process from fixative to mounting medium.
___________________________ Short: Dicyemida of the Eastern United States 7

Key to the Dicyemid Mesozoa of the East Coast of

North America and the Gulf of Mexico _

Genus Dicyema von Kolliker, 1849

1 Somatic cells of vermiform stages most often 22, varying from 20 to 25 (very seldom 18 and 19) 2

1 Somatic cells fewer than 20 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3

2(1) Adult vermiform stages usually 400 to 1500 JAm in length; somatic cell number 22, seldom 21 to 25; tendency for infusorigens and their products to be located well forward in axial cell of rhombogens causing

a swelling behind the calotte (cephalic swelling); somatic cells not conspicuously charged with granules,

a pronounced tendency to produce accessory nuclei in the posterior diapolar and uropolar cells. Vermiform

embryos 40 to 50 JAm at eclosion. Refringent bodies, in infusoriforms viewed laterally, appearing smaller

than the cluster of 4 urn cells (see Figs. 5B, 6) Dicyema aegiTa (Figs. 10-16)

Hosts: Octopus vulgaris euvier, 1797; Octopus joubini Robson, 1929

15 14

25

16

Figures 10-16

Dicyema aegira. (10) Nematogens, mature, showing general shape. (11) Rhombogens, mature showing general shape.

(12 and 13) Infusoriform larvae, frontal view (12), sagittal optical section (13). (14) Posterior portion of trunk of

young nematogen. (15) Posterior portion of trunk of rhombogen showing fragmentation of nuclei in somatic cells

(16) Anterior end of large nematogen showing calotte and its relation to the axial cell, which contains a vermiform

embryo. (14-16) redrawn from McConnaughey and Kritzler (1952). Scales in micrometers. Cilia not shown on

mature vermiform stages.
8 NOAA Technical Report NMFS 100 _

2(1) Adult nematogens from about 300 to slightly over 1000 Ilm in length; largest adult rhombogens about 1000

Ilm, often smaller; somatic cell number usually 20 to 22, most often 22, seldom 18, 19, 23, 24; body usually

about the same width throughout with no conspicuous cephalic swelling; cytoplasm ofsomatic cells, especially

uropolar and posterior diapolar, characteristically charged with particulate matter variously appearing as

fine granules or small globules of spherical, oval, or irregular shape (Fig. 20); granular material usually

denser and more conspicuous in rhombogens than in nematogens, with tendency toward formation of verruciform cells. Vermiform embryos about 60 to 70 Ilm at eclosion. Refringent bodies, in infusoriforms viewed

laterally, appearing larger than the cluster of 4 urn cells (see Figs. SA, 7, 8) ... Dicyema briarei (Figs. 17-20)

Host: Octopus briareus Robson, 1929

25

19

Figure 20

Dicyema briarci. Posterior ends of rhombogens showing variation in material

in uropolar cells. From published photographs (Short 1961).

Figures 17-19

Dicycma briarci. (17) Nematogens (to same scale as Fig.

18). (18) Rhombogens. (19) Infusoriform larva, side

view, showing refringent bodies and urn cells (stippled).

(17-19) redrawn from Short (1961). Cilia not shown on

vermiform stages.
___________________________ Short: Dicyemida of the Eastern United States 9

3(1) Somatic cells usually 14 4

3(1) Somatic cells usually 16 to 18 5

4(3) Lengths of mature nematogens 254 to 264 JAm, mature rhombogens 438 to 657 JAm. Somatic cell number

almost invariably 14. Calotte markedly elongate; in young vermiform individuals often 30 to 50% of total

length, in largest vermiforms 14 to 20% oftotal length. Parapolar cells usually shorter than calotte. Vermiform embryos about 40 to 50 JAm long at eclosion. Refringent bodies, in infusoriforms viewed laterally,

appearing larger than cluster of urn cells (see Fig. 3B) D. hypercephalum (Figs. 21-24)

Host: Octopus joubini Robson, 1929

24

23

L--=25"-__-'

o

Q

Figures 21-24

Dicycma hypercephalum. (21) Nematogens. (22) Rhombogens. (23) Anterior ends ofrhombogens. (24) Infusoriform

within axial cell ofrhombogen, sagittal optical section. All figures from Short (1962). Scales in micrometers.

Cilia not shown on vermiform stages.
10 NOAA Technical Report NMFS 100 _

4(3) Largest mature nematogens 299 to 645 JAm long, seldom longer than 350 JAm; rhombogens unknown. Somatic

cell numbers usually 14, sometimes 15, very occasionally otherwise. Calotte not markedly elongate; parapolar

cells usually as long as or longer than calotte. Vermiform embryos about 20 to 25 JAm long at eclosion

(see Fig. 3C) D. apalachiensis (Figs. 25-27)

Host: Octopus joubini Robson, 1929

26

27

50

o

2

Figures 25-27

Dicyema apalachiensis. Nematogens. (26) Anterior end only. All redrawn from Short (1962).

Scales in micrometers. Cilia not shown.
____________________________ Short: Dicyemida of the Eastern United States 11

5(3) Largest nematogens 432 to 610 !-1m; largest rhombogens 514 to 802 !-1m; somatic cells 16 to 18, occasionally

15 or 19. Calotte large and conspicuous in older vermiform stages, appearing ellipsoidal to bilobed, often

with a constriction between propolar and metapolar cells, anterior end of calotte in older vermiforms

sometimes rather blunt with propolar region as broad as metapolar. Vermiform embryos 40 to 60 !-1m long

at eclosion. Refringent bodies, in infusoriform viewed laterally, appearing about same size or only slightly

larger than cluster of urn cells (see Fig. 4, A and B) Dicyema bilobum (Figs. 28-33)

Host: Octopus vulgaris Cuvier, 1797

33

31

32 30

Figures 28-33

Dicyema bilobum. (28 and 29) Nematogens. (30-32) Rhombogens. (32) Anterior ends

only. (33) Infusoriform, optical sagittal section. All figures except 31 from Couch and

Short (1964), mostly redrawn. Scales in micrometers. Cilia not shown on vermiform

stages.
12 NOAA Technical Report NMFS 100 _

5(3) Largest nematogens 193 to 414 jAm; largest rhombogens 450-689 jAm; somatic cells almost always 18. Calotte

relatively smaller than that of D. bilobum and with no tendency toward constriction between propolar and

metapolar cells; often with cephalic swelling in parapolar region; in older rhombogens propolar and metapolar

cells sometimes alternately arranged (in contrast to usual opposite arrangement in this and most other species

of Dicyema). Vermiform embryos about 35 JAm long at eclosion. Refringent bodies of infusoriform appear

considerably larger than the cluster of urn cells viewed laterally (see Fig. 3A) . Dicyema typoides (Figs. 34-38)

Host: Octopus vulgaris Cuvier, 1797

38

35

34

1

Figure 39 (right)

Octopus vulgaris, ventral view. Dissected to show renal appendages (dotted outlines) within semitransparent renal sacs.

Figures 34-38

Dicyema typoirks. (34) Nematogens. (35) Anterior end of nematogen. (36) Rhombogens. (37) Infusoriforms in axial cell of

rhombogens: (A) Frontal view; (B) Sagittal optical section.

(38) Infusoriform side view. Urn cell stippled. Note unusually

large refringent bodies. Except for (36), all from Short (1964).

Scales in micrometers. Cilia not shown on vermiform stages.
___________________________ Short: Dicyemida of the Eastern United States 13

Annotated Systematic List _

In addition to the six species in the genus Dicyema (family

Dicyemidae) that have been reported from off the coasts

of eastern North America and the Gulf of Mexico, Aldrich

(1964) recorded a single dicyemid in a single specimen of

the squid Illex illecebrosus from Newfoundland, and in 1989

I recovered an as yet unidentified species of Dicyemennea

from a specimen of Bathypolypus arcticus (furnished by Professor M.D.B. Burt) from off Grand Manan Island, south

of St. Andrews, N.B., Canada.

As indicated above, the dicyemids are here considered

to represent the phylum Dicyemida. In this system to my

knowledge no class or order names have been assigned in

the literature and it seems inappropriate to designate them

in this manual. The species in this list are arranged alphabetically. Except for type host and locality, the locality and

prevalence records summarize published and unpublished

data (mostly from the present author's records). These records should not, of course, be interpreted as representing

the true range of the parasites. It is my impression that

octopods have not been examined systematically for

dicyemids over most ofthe eastern and Gulf coasts of North

America, and it is expected that at least some of the

dicyemid species range much more widely than here indicated and that undescribed species remain to be

discovered. Hochberg (E. Hochberg, Curator, Dept. oflnvert. Zoology, Santa Barbara Mus. Nat. History, 2559

Puesta del Sol Rd., Santa Barbara, CA 93105, pers. commun., 1990) has pointed out that apparently unexamined

potential octopod hosts in the region include Octopus macropus, O. burryi, O. defilippi, O. cardinensis, and O. mercatoris.

Family DICYEMIDAE E. van Beneden, 1882

Dicyema aegira McConnaughey and Kritzler, 1952-

(Figs. 5B, 6, 10-16).

Stages Known-nematogen (primary), rhombogen,

vermiform embryo, infusorigen, infusoriform larva.

Type Host and Locality-Octopus vulgaris Cuvier, 1797.

Western North Atlantic Ocean, oflshore from St. Augustine,

Florida.

Additional Host-Octopus Joubini Robson, 1929 (Short

1957).

Additional Localities-Octopus vulgaris, Western North

Atlantic Ocean, coast of North Carolina, near Cape Lookout; Northern Gulf of Mexico, coast of Florida, Apalachee

Bay west to Pensacola Bay. OctopusJoubini, Northern Gulf

of Mexico, coast of Florida, Apalachee Bay, near St.

Teresa.

Prevalence (in Octopus vulgaris)-Of26 hosts from the

type locality examined, 25 were infected with dicyemids.

The species of dicyemid was determined in 22. Dicyema

aegira was in 17, 6 of which also harbored D. typoides ( =

D. typus of McConnaughey and Kritzler, 1952, see below).

Two hosts from the North Carolina coast near Cape

Lookout were examined. Both were infected with D. aegira.

From the northern Gulf of Mexico off Florida, 147 hosts

were examined; 144 were infected with dicyemids. The

dicyemid species was determined in 122 hosts; D. aegira

was present in 93, 18 of which also harbored D. typoides.

Prevalence (in Octopusjoubim)-Four hosts from Apalachee Bay were examined; 2 harbored dicyemids that appeared to be D. aegira.

Other Reports-Austin (1964) reported on gametogenesis and Short and Damian (1966, 1967) on morphology

of the infusoriform larva, oogenesis, fertilization, and first

cleavage. Transmission electron microscopical studies were

published by Ridley (1968, 1969).

Dicyema apalachiensis Short, 1962-(Figs. 3D, 25-27).

Stages Known-stem nematogen, nematogen (primary), vermiform embryo. The stem nematogen was

described from an entire small specimen and part of a larger

one.

Type Host and Locality-OctopusJoubini Robson, 1929.

Northern Gulf of Mexico, off Franklin Co., Florida, about

6 miles south of Light House Point.

Additional Hosts-none.

Additional Localities-none.

Prevalence-From the type locality, 13 hosts were examined; 12 were small, immature specimens, and all were

infected with D. apalachiensis. One additional, larger specimen from the same locality was negative for D. apalachiensis but harbored D. hypercephalum.

DU:yema biwbum Couch and Short, 1964-(Figs. 4, A and

B, 28-33).

Stages Known-nematogen (primary), rhombogen,

vermiform embryo, infusorigen, infusoriform larva.

Type Host and Locality-Octopus vulgaris Cuvier, 1797.

Northern Gulf of Mexico, off Pensacola Florida.

Additional Hosts-none.

Additional Localities-Northern Gulf of Mexico off

Panama City, Florida.

Prevalence-Ten hosts from the type locality were examined; all were infected with dicyemids. In 2 hosts the

species of parasites were not determined; of the remaining 8, 5 had D. bilobum alone and 3 D. typoides alone.

Other Report-Ridley (1968) reported transmission

electron microscopical studies.

Dicyema briarei Short, 1961-(Figs. 5A, 7,8, 17-20).

Stages Known-nematogen (primary), rhombogen,

vermiform embryo, infusorigen, infusoriform larva.

Type Host and Locality-Octopus briareus Robson,

1929. Gulf of Mexico, inshore near Long Key, Florida

Keys.

Additional Hosts-none.

Additional Localities-none.
14 NOAA Technical Report NMFS 100 _

Prevalence-Two of 16 adult octopuses from the type

locality were infected in 1958. From 1959 to 1963, the

following numbers of O. briareus from other locations were

found not to be infected: 43 from areas in the Florida Keys;

12 from Bear Cut, Biscayne Bay, near Miami; and 3 from

Bimini.

Dicyema hypercephalum Short, 1962-(Figs. 3B, 21-24).

Stages Known-nematogen (primary), rhombogen,

vermiform embryo, infusorigen, infusoriform larva.

Type Host and Locality-Octopusjoubini Robson, 1929.

Northern Gulf of Mexico, off Franklin Co., Florida, about

6 miles south of Light House Point.

Additional Hosts-none.

Additional Localities-Northern Gulf of Mexico, off

Franklin Co., Florida, south of Dog Island.

Prevalence-From the type locality, 13 hosts were examined; 1 harbored D. hypercephalum alone, 12 had D.

apalachiensis, and 7 of these also had an unidentified species

of dicyemid.

From south of Dog Island, 2 hosts were examined; both

were infected with D. hypercephalum.

Dicyema typoides Short, 1964-(Figs. 3A, 34-38).

Stages Known-nematogen (primary), rhombogen,

vermiform embryo, infusorigen, infusoriform larva.

Type Host and Locality-Octopus vulgaris Cuvier, 1797.

Northern Gulf of Mexico, offshore about 3 miles from

Panama City, Florida.

Additional Hosts-none.

Additional Localities-Northern Gulf of Mexico: Pensacola Bay; St. Joseph's Bay; Apalachee Bay-off Panacea,

Alligator Point, Dog Island, St. George Island. Western

Atlantic Ocean: offshore from St. Augustine, Florida;

Bimini, Bahama Is., Bermuda Is.

Prevalence-From the northern gulf coast of Florida,

144 of 147 hosts were infected with dicyemids; ofthese 144,

the species of dicyemid present was determined in 122

hosts. Dicyema typoides occurred in 48 hosts, 18 of which

also harbored D. aegira.

From offSt. Augustine, Florida, 12 of 13 hosts were infected; dicyemids were identified in 9; D. typoides occurred

in 7, 3 of which also had D. aegira. McConnaughey and

Kritzler (1952) reported Dicyema typus van Beneden, 1876,

sensu Nouvel, 1946, from Octopus vulgaris offshore from St.

Augustine, Florida. I believe that these authors were dealing with D. typoides, at that time (1952) not described. Four

of 13 hosts were reported infected with "D. typus"; 3 of

the 4 also had D. aegira.

Bimini. Of 24 hosts examined, 13 were parasitized by

dicyemids; in 11 the species was determined; all harbored

D. typoides.

Bermuda. Of 3 hosts examined, all harbored D. typoides.

Other reports-Ridley (1968, 1969) reported transmission electron microscopical studies of this species.

Citations _

Aldrich, F.A.

1964. Observations on the Newfoundland bait squid (Itlex illecebrosus

LeSueur, 1821), and the netting of squid in Newfoundland

bays. (Ms.) Spec. Rpt. Canad. Fish Indust. Develop Branch,

Ottawa, p. 1-22.

Austin, C.R.

1964. Gametogenesis and fertilization in the Mesozoan Dicyema

aegira. Parasitology 54:597-600.

Cavolini, F.

1787. Memoria sulla generazione dei pesci et dei granchi. Napoli

(cited after Nouvel, 1948).

Couch, j.A., and R.B. Short.

1964. Dicyema bilobum sp. n. (Mesozoa: Dicyemidae) from the northern Gulf of Mexico. j. Parasitol. 50:641-645.

Czihak, G.

1958. Morphologie und Entwicklungsgeschichte der Wirbellosen.

Forschritte der Zoologie 11:1-34.

Erdl, Professor.

1843. Ueber die beweglichen Fiiden in den Venenanhiingen der

Cephalopoden. Arch. Naturgesch. 1:162-167.

Grasse, P.-P.

1961. Classe des dicyemides. In Traite de zoologie: anatomie,

systematique, biologie, vol. IV (P.-P. Grasse, ed.), p. 707-729.

Masson, Paris.

Hochberg, F.G.

1982. The "kidneys" of cephalopods: a unique habitat for parasites.

Malacologia 23:121-134.

1983. The parasites of cephalopods: a review. Mem. Natl. Mus.

Victoria 44:109-145.

1990. Diseases of Mollusca: Cephalopoda. Diseases caused by protistans and metazoans. In Diseases of marine animals, vol. III

(0. Kinne, ed.). Biologisches Anstalt Helgoland, Hamburg.

Hyman, L.H.

1940. Phylum Mesozoa. In The invertebrates: Protozoa through

Ctenophora, p. 233-247. McGraw-Hili, New York and

London.

Kozloff, E.N.

1969. Morphology of the orthonectid Rhopalura ophiocomae. j.

Parasitol. 55:171-195.

Krohn, A.

1839. Uber das Vorkommen von Entozoen und Krystallablagerungen in den schwammigen Venenanhiingen einiger Cephalopoden. Froriep's "Neue Notizen" 11 :213-216.

McConnaughey, B.H.

1951. The life cycle of the dicyemid Mesozoa. U niv. Calif. Publ.

Zool. 55:295-336.

1963. The Mesozoa. In The lower Metazoa: comparative biology

and phylogeny (E.C. Dougherty, ed.), p. 151-165. Univ. California Press, Berkeley and Los Angeles.

1968. The Mesozoa. In Chemical zoology, Vol. II: Porifera,

Coelenterata, and Platyhelminthes (M. Florkin and B.T. Scheer,

eds.), p. 557-570. Acad. Press, New York.

McConnaughey, B.H., and H. Kritzler.

1952. Mesozoan parasites of Octopus vulgaris, Lam. from Florida.

j. Parasitol. 38:59-64.

Nouvel, H.

1947. Les Dicyemides. Ire partie: systematique, generations vermiformes, infusorigene et sexualite. Arch. BioI. 58:59-219.

Ridley, R.K.

1968. Electron microscopic studies on dicyemid Mesozoa. I:

Vermiform states. j. Parasitol. 54:975-998.

1969. Electron microscopic studies on dicyemid Mesozoa. II:

Infusorigen and infusoriform stages. j. Parasitol. 55:779-793.
____________________________ Short: Dicyemida of the Eastern United States 15

briarei .

Systematic Index _

hypercephalum .

typoides .

Short, R.B., and R.T. Damian.

1966. Morphology of the infusoriform larva of Dicyema aegira

(Mesozoa: Dicyemidae). J. Parasitol. 52:746-751.

1967. Oogenesis, fertilization, and first cleavage of Dicyema aegira

McConnaughey and Kritzler, 1952 (Mesozoa: Dicyemidae). J.

Parasitol. 53: 186-195.

Stunkard, H.W.

1954. The life-history and systematic relations of the Mesozoa. Q.

Rev. BioI. 29:230-244.

1982. Mesozoa. In Synopsis and classification of living organisms,

vol. 1 (S.P. Parker, ed.), p. 853-855. McGraw-Hill, New York.

van Beneden, E.

1876. Recherches sur les dicyemides. Bull. Acad. Roy. Belg., A.

Sci., (ser. 2) 41:1160-1205 and 42:35-97.

Dicyema

aegZTa 7

apalachiensis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 10

bilobum 11

8

9

12

Acknowledgments _

Preparation ofthis manual was supported in part by a grant

from the National Science Foundation to the Editorial

Board of the "Marine Flora and Fauna of the Eastern

United States."

Thanks are given to Drs. F.G. Hochberg and Eugene

N. Kozloff for critically reading the manuscript and making

helpful suggestions. Especial appreciation is expressed to

Dr. Hochberg for helpful discussions and aid with literature. Anne Thistle's preparation of the manuscript and

Arthur K. Womble's help in preparing Figure 8 and in

labeling the figures are acknowledged with gratitude. Also

much appreciated is the contribution of many students and

colleagues for their help over the years with collection and

preparation of material for study.

Preparation of manuals in the "Marine Flora and Fauna

of the Eastern United States" subseries is coordinated by

the following Board.

Coordinating Editor

Melbourne R. Carriker, College of Marine Studies, University of Delaware, Lewes, DE 19958.

Editorial Advisers

A. Ralph Cavaliere, Department of Biology, Gettysburg

College, Gettysburg, PA 17325.

Arthur G. Humes, Boston University Marine Program,

Marine Biological Laboratory, Woods Hole, MA 02543.

David L. Pawson, Department of Invertebrate Zoology,

National Museum of Natural History, Smithsonian Institution, Washington, D.C. 20560.

Kenneth P. Sebens, Marine Science and Maritime Studies

Center, Northeastern University, East Point, MA 01908.

Ruth D. Turner, Museum ofComparative Zoology, Harvard University, Cambridge, MA 02138.

Robert T. Wilce, Department of Botany, University of

Massachusetts, Amherst, MA 01002.

In addition to establishing the format for the "Marine

Flora and Fauna of the Eastern United States," the Board

invites systematists to collaborate in the preparation of

manuals, review manuscripts, and advise the Scientific

Editor of the National Marine Fisheries Service.

Coordinating Editor's Comments _

Publication of the "Marine Flora and Fauna of the Eastern United States" is most timely in view of the growing

universal emphasis on work in the marine environment and

the crucial need for precise and complete identification of

organisms related to this work. It is essential, if at all possible, that organisms be identified accurately to species.

Accurate scientific names of plants and animals unlock the

great quantities of biological information stored in libraries,

obviate duplication of research already done, and often

make possible prediction of attributes of organisms that

have been adequately studied.

Robert B. Short received the M.S. degree in' biology

from the University of Virginia in 1945 and the Ph.D.

degree in zoology, with emphasis on parasitology, in

1950 from the University of Michigan. He was on the

faculty of Florida State University from 1950 to 1990

and is now Professor Emeritus. His research interests

have included the schistosomes as well as the dicyemid

mesozoans.
16 NOAA Technical Report NMFS 100 _

Published Manuals

Marine Flora and Fauna of the Northeastern United States

Annelida: Oligochaeta Cook, David G., and Ralph O. Brinkhurst

Protozoa: Ciliophora Borror, Arthur C.

Higher Plants of the Marine Fringe Moul, Edwin T.

Pycnogonida McCloskey, Lawrence R.

Crustacea: Stomatopoda Manning, Raymond B.

Crustacea: Decapoda Williams, Austin B.

Tardigrada Pollock, Leland W

Cnidaria: Scyphozoa Larson, Ronald J.

Higher Fungi: Ascomycetes, Deuteromycetes, and Basidiomycetes

Cavaliere, A. R.

Copepoda: Harpacticoida Coull, Bruce C.

Sipuncula Cutler, Edward B.

Echinodermata: Holothuroidea Pawson, David L.

Copepoda: Lernaeopodidae and Sphyriidae Ho, Ju-Shey

Copepoda: Cyclopoids Parasitic on Fishes Ho, Ju-Shey

Crustacea: Branchiura Cressey, Roger F.

Protozoa: Sarcodina: Amoebae Bovee, Eugene C., and Thomas K. Sawyer

Crustacea: Cumacea Watling, Les

Arthropoda: Cirripedia Zullo, Victor A.

Cnidaria: '" Scleractinia Cairns, Stephen D.

Protozoa: Sarcodina: Benthic Foraminifera Todd, Ruth, and Doris Low

Turbellaria: Acoela and Nemertodermatida Bush, Louise F.

Lichens (Ascomycetes) of the Intertidal Region Taylor, Ronald M.

Echinodermata: Echinoidea Serafy, D. Keith, and F. Julian Fell

Echinodermata: Crinoidea Messing, Charles G., and John H. Dearborn

Erect Bryozea Ryland, John S, and Peter J. Hayward

Marine Flora and Fauna of the Eastern United States

Cephalopoda Vecchione, Michael, Clyde F. E. Roper, and Michael J. Sweeney

Copepoda, Cyclopoida: Archinotodelphyidae, Notodephyidae, and

Ascidicolidae Dudley, Patricia L., and Paul L. Illg

Dicyemida Short, Robert B.

NOAA Tech Rep.

NMFS Circular no.

374

378

384

386

387

389

394

397

398

399

403

405

406

409

413

419

423

425

438

439

440

446

NMFS no.

33

91

99

73

96

100

NTIS no.

COM 73 50670

73 50888

74 50019

7450014

7450487

7451194

PB 257 987

261 839

268 036

268 714

273 062

274999

280040

281 969

222 923

285 538

296 460

297 676

124 520

225 053

219 387

124 735

PC A03/MF AOl

PB 86 156 395

PB 89 189 583