QL

155

.S63

no.82-

11.80

Biological Report 82(11 .W

April 1988

TR EL-82-4

Species Profiles: Life Histories and

Environmental Requirements of Coastal Fishes

and Invertebrates (North Atlantic)

SANDWORM AND BLOODWORM

Fish and Wildlife Service

Coastal Ecology Group

Waterwavs ExDeriment Station

U.S. Department of the Interior U.S. Army Corps of Engineers

L

Biological Report 82(11.80)

TR EL-82-4

April 1988

Species Profiles: Life Histories and Environmental Requirements

of Coastal Fishes and Invertebrates (North Atlantic)

SANDWDRM AND BLOODWORM

W. Herbert Wilson, Jr., and R. Eugene Ruff

Manomet Bird Observatory

P.O. Box 936

Manomet, MA 02345

Project Officer

David Moran

U.S. Fish and Wildlife Service

National Wetlands Research Center

1010 Gause Boulevard

Slidell, LA 70458

Performed for

Coastal Ecology Group

U.S. Army Corps of Engineers

Waterways Experiment Station

Vicksburg, MS 39180

and

U.S. Department of the Interior

Fish and Wildlife Service

Research and Development

National Wetlands Research Center

Washington, DC 20240
t

7

DISCLAIMER

The mention of the names of commercial products in this report does not

constitute endorsement or recommendation for use by the Federal Government.

This series may be referenced as follows:

U.S. Fish and Wildlife Service. 1983-19 . Species profiles: life histories

and environmental requirements of coast3 fishes and invertebrates. U.S. Fish

Wildl. Serv. Biol. Rep. 82(11). U.S. Army Corps of Engineers, TR EL-82-4.

This profile may be cited as follows:

Wilson, W.H., Jr., and R.E. Ruff. 1988. Species profiles: life histories and

environmental requirements of coastal fishes and invertebrates (North

Atlantic)--sandworm and bloodworm. U.S. Fish. Wildl. Serv. Biol. Rep.

82(11.80). U.S. Army Corps of Engineers, TR EL-82-4. 23~~.
PREFACE

This species profile is one of a series on coastal aquatic organisms,

principally fish, of sport, commercial, or ecological importance. The profiles

are designed to provide coastal managers, engineers, and biologists with a brief

comprehensive sketch of the biological characteristics and environmental

requirements of the species and to describe how populations of the species may be

expected to react to environmental changes caused by coastal development. Each

profile has sections on taxonomy, life history, ecological role, environmental

requirements, and economic importance, if applicable. A three-ring binder is

used for this series so that new profiles can be added as they are prepared.

This project is jointly planned and financed by the U.S. Army Corps of Engineers

and the U.S. Fish and Wildlife Service.

Suggestions or questions regarding this report should be directed to one of

the following addresses.

Information Transfer Specialist

National Wetlands Research Center

U.S. Fish and Wildlife Service

NASA-Slide11 Computer Complex

1010 Gause Boulevard

Slidell, LA 70458

or

U.S. Army Engineer Waterways Experiment Station

Attention: WESER-C

Post Office Box 631

Vicksburg, MS 39180

iii
Multiply &

millimeters (mm) 0.03937

centimeters (cm) 0.3937

meters (m) 3.281

meters (m) 0.5468

kilometers (km) 0.6214

kilometers (km) 0.5396

To Obtain

inches

inches

feet

fathoms

statute mi

nautical m

square meters (m2) 10.76

square kilometers (km2> 0.3861

hectares (ha) 2.471

square fee L

square miles

acres

liters (1) 0.2642 gallons

cubic meters (m3) 35.31 cubic feet

cubic meters (m3) 0.0008110 acre-feet

milligrams (mg) 0.00003527 ounces

grams (9) 0.03527 ounces

kilograms (kg) 2.205 pounds

metric tons (t) 2205.0 pounds

metric tons (t) 1.102 short tons

kilocalories (kcal)

Celsius degrees ("C)

3.968 British thermal units

1.8('=C) + 32 Fahrenheit degrees

inches

inches

feet (f

fathoms

statute

nautica

t>

miles (mi)

1 miles (nm i>

25.40 millimeters

2.54 centimeters

0.3048 meters

1.829 meters

1.609 kilometers

1.852 kilometers

square feet (ft2)

square miles (mi2)

acres

0.0929 square meters

2.590 square kilometers

0.4047 hectares

gallons (gal) 3.785

cubic feet (ft3) 0.02831

acre-feet 1233.0

ounces (oz) 28350.0

ounces (oz) 28.35

pounds (lb) 0.4536

pounds (lb) 0.00045

short tons (ton) 0.9072

British thermal units (Btu) 0.2520

Fahrenheit degrees (OF) 0.5556 (OF

I

CONVERSION TABLE

Yetric to U.S. Customary

U.S. Customary to Metric

iv

32)

les

iles

liters

cubic meters

cubic meters

milligrams

grams

kilograms

metric tons

metric tons

kilocalories

Celsius degrees
CONTENTS

Page

PREFACE ................................................................... iii

CONVERSION FACTORS ........................................................ iv

ACKNOWLEDGMENTS ........................................................... vii

SANDWORM

NOMENCLATURE/TAXONOMY/RANGE ............................................... 1

MORPHOLOGY/IDENTIFICATION AIDS ............................................ 1

Description ............................................................. 1

Identification Aids ..................................................... 3

Taxonomic References .................................................... 3

REASON FOR INCLUSION IN SERIES ............................................ 3

LIFE HISTORY .............................................................. 3

Gametogenesis ........................................................... 3

Spawning ................................................................ 3

Larval Development ...................................................... 4

Population Structure .................................................... 4

ECOLOGICAL ROLE ........................................................... 4

Feeding ................................................................. 4

Predator-Prey Relations ................................................. 5

Biogeochemical Effects .................................................. 5

ENVIRONMENTAL REQUIREMENTS ................................................ 6

Substratum .............................................................. 6

Salinity ................................................................ 6

Dissolved Oxygen ........................................................ 6

Temperature ............................................................. 6

Adaptability to Laboratory Conditions ................................... 6

Toxicology .............................................................. 7

BLOODWORM

NOMENCLATURE/TAXONOMY/RANGE ............... ............................... a

MORPHOLOGY/IDENTIFICATION AIDS ............ ............................... 8

Description ............................. ............................... 8

Identification Aids ..................... ............................... 10

Taxonomic References .................... ............................... 10

REASON FOR INCLUSION IN SERIES ............ ............................... 10

LIFE HISTORY .............................. ............................... 10

Gametogenesis ........................... ............................... 10

Spawning ................................ ............................... 10

Larval Development ...................... ............................... 11

Population Structure .................... ............................... 11

V
Page

ECOLOGICAL ROLE ...........................................................

Feeding .................................................................

:;

Predator-Prey Relations ................................................. 12

ENVIRONMENTAL REQUIREMENTS ................................................

Substratum ..............................................................

;;

Salinity ................................................................ 12

Dissolved Oxygen ........................................................

Toxicology ..............................................................

;:

LITERATURE CITED .......................................................... 15

vi
ACKNOWLEDGMENTS

We are grateful to Betsy Brown, Battelle Laboratories, Duxbury, MA; Sally

Woodin of the University of South Carolina; Will Ambrose of The Williams-Mystic

Program based in Mystic, CT, and anonymous reviewers for comments on early drafts

of the manuscript. Jack Paar provided photographic assistance for which we are

thankful. Kristian Fauchald of the United States National Museum kindly provided

specimens for our examination.

vii

EVERSIBLE PROBOSCIS

FLESHY PALPS

TENTACULAR CIRRI

DORSAL CIRRUS

VENTRAL CIRRUS

ANTERIOR VIEW

(Left parapodium from

middle of body)

ANTERIOR VIEW

(Proboscis extended)

Figure 1. Sandworm (Nereis virens). - -

SANDWORM

NOMENCLATURE/TAXONOMY/RANGE

Scientific name.... ..Nereis (Neanthes)

virens Sars, 1835 (Figure 1)

Preferred common name.........Sandworm

Other common names...........Clamworm,

ragworm

Phylum........................Annelida

Class.......................Polychaeta

Order.....................Phyllodocida

Family......................Nereididae

Geographic range: Found on both sides

of the North Atlantic as far south

as France off Europe and south to

Virginia off the east coast of the

United States. Figure 2 shows the

distribution of the sandworm in the

North Atlantic region of the United

States. Also recorded in the north

Pacific from Alaska to central California, in the Bering Sea, and off

Japan. Ranges from the high water

mark to about 150 m.

MORPHOLOGY/IDENTIFICATION AIDS

Description

Body elongate, thickened anteriorly

and somewhat flattened posteriorly,

with more than 200 segments. Length

up to 900 mm and width greater than

1
MAINE

i CANADA \

ATLANTIC OCEAN

-c

ii’

MILES

Figure 2. Distribution of sandworm in the North Atlantic region. Heavier

stippling indicates regions of higher abundance.

2
40 mm. Prostomium (head) small,

pentagonal, with a distal pair of

small antennae and two oairs of eyes

in a trapezoidal arrangewnt (Figure

1). Head with a pair of stout,

fleshy palps, each with a small,

rounded palpostyle distally. Eversihle

proboscis with a pair of curved

brownish or black jaws, each with

5 to 10 teeth. Dark, conical,

chitinous paragnaths (teeth) embedded

in the surface of the proboscis. Four

pairs of slender tentacular cirri,

the longest reaching as far as

the ninth seglnent. The first segment

lacking setae, twice the width of an.y

following segrient. Parapodia with

dorsal and ventral lobes (biramous)

with the same shape throughout the

length of the body. Dorsal and

ventral cirri digitifom. Setae from

the dorsal rami (notopodia) consisting

of long, jointed setae (homogomph

spinigers). Setae from the ventral

rami of the parapodia (neuropodia)

consisting of long, jointed setae

(homogomph and heterogomph spinigers)

and jointed setae with short, toothed

blades (heterogomph falcigers).

Identification Aids

The surface of the skin is iridescent, reflecting bright hues in the

light. The body of the male is a dark

blue, blending into green at the base

of the parapodia. The females are a

dull, greenish color. In both sexes,

the parapodia appear orange to bright

red due to the numerous capillaries in

these appendages.

Taxonomic References

Refer to Sars 1835; Verrill 1873,

1881; Webster and Benedict 1884, 1887;

Fauvel 1923; Treadwell 1939, 1941;

Pettibone 1963; Imajima 1972.

REASON FOR INCLUSION IN SERIES

The harvesting of sandworms and

bloodworms (Glycera dibranchiata) is a

multi-million dollar industry in Maine

(Dow and Creaser 1970; Dow 1978;

Schroeder 1978). Over 1,200 people

are licensed to dig baitworms in Maine

(Schroeder 1978). Since the early

1970's, the bloodworm populations in

Maine have been declining, leading to

increased harvesting of sandworms.

Nevertheless, there seems to be no

major concern that sandworms are being

overharvested. Creaser et al. (1983)

calculated the Maximum Sustainable

Yield and Optimal Sustainable Yield

for Maine populations. Blake (1979)

suggested that bait-diggers are not

altering the population structure of a

heavily dug mudflat.

LIFE HISTORY

Gametogenesis

Like most polychaetes, the sexes in

N. virens are separate (Bumpus 1898).

In females from Maine populations,

oocytes begin rapid growth in October

or November with oocyte maturation

occurring in the following April or

May, when the oocytes' diameters reach

X$95 pm (Creaser and Clifford

The oogenic cycle requires

12-20' months, depending on when the

oocytes are released into the coelom.

The oocytes synthesize their own yolk

(Fischer and Schmitz 1981). Snow and

Marsden (1974) reported a similar

temporal pattern of oogenesis for a 1.

virens population in the Bay of Fundy,

with maturation occurring in May.

Brafield and Chapman (1967) reported

that oogenesis requires 12-14 months

in a British population and that ripe

oocytes appear in May. Spermatogenesis follows a similar chronology

(Brafield and Chapman 1967; Snow and

Marsden 1974; Creaser and Clifford

1982).

Spawning

Nereis virens is a

species;

semelparous

reproduction results in death

(Bass and Brafield 1972). Mature

males become structurally modified for

3
swimming (epitokous) and swarm in the

water column during times of the new

moon (Brafield and Chapman 1967; Bass

and Brafield 1972; Snow and Marsden

1974; Creaser and Clifford 1982).

Temperatures in excess of 7-8 *C seem

to be a precondition for spawning

(Creaser and Clifford 1982; Goerke

1984a; Yokouchi 1985). Premature

spawning can be induced by increasing

temperature in the laboratory (Bass

and Brafield 1972). Swarming of males

is known to be under hormonal control

as well (Marsden 1971, 1978; Marsden

and Jost 1975; Bell and Marsden 1980).

Females do not become swimming

epitokes and do not swarm; fertilization is presumed to occur in the

burrows of females (Creaser and

Clifford 1982). Fecundity varies between 50,000 and 1,300,OOO eggs, depending on the size of the female

(Creaser and Clifford 1982).

Larval Development

Females of N. virens extrude

fertilized eggs &to the surface of

the mud (Snow and Marsden 1974).

Development apparently occurs on or

near the sediment surface. Snow and

Marsden (1974) believed that

planktonic embryos or larvae are not

found in New Brunswick populations,

although weak spontaneous swimming of

larvae was observed in laboratory

cultures. Bass and Brafie‘ld (1972)

reported that trochophore larvae do

enter the plankton, but never for more

than 15 h. Sveshnikov (1960) and

Yokouchi (1985) reported larvae with

four segments in the plankton.

Juveniles are benthic 12 days after

fertilization and crawl into the

intertidal zone after 16 weeks (Bass

and Brafield 1972).

Population Structure

The demography of the sandworm is

controversial. Brafield and Chapman

(1967) concluded from their sizefrequency data that sandworms mature

in 2 or, occasionally, 3 years. Snow

and Marsden (1974) claimed that Bay of

Fundy worms do not mature until 5 or 6

years of age. They re-analyzed the

data of Brafield and Chapman (1967)

and claimed that British worms mature

after 6 or 7 years. Creaser and

Clifford (1982) reported 5 distinct

modes in a Maine population which

probably correspond to year-classes.

Worms in a Norwegian population reproduce after 3 years (Kristensen 1984a).

As with all other populations, reproduction results in death.

ECOLOGICAL ROLE

Feeding

Sandworms feed by extending a portion of their bodies from an opening

of their mucus-lined burrows. The

burrows consist of a series of interconnected U-shaped sections, generally

in the upper 10 cm of mudflats (Reise

1981). Disagreements over the trophic

status of sandworms span a century.

Nereis virens was regarded as a predatory-ill (1873) and Maxwell

(1897), and as an omnivore by Turnbull

(1876). Gross (1921) concluded that

sandworms are herbivorous and that

they locate their food by chance encounter. His conclusion was challenged by Copeland and Wieman (1924)

who showed that sandworms captured and

ate animals in the laboratory; sandworms also demonstrated a welldeveloped chemoreceptive sense (see

also Retzius 1895; Hamaker 1898; Case

1962). The thorough work by Goerke

(1971a, b) showed that sandworms fed

on both plant and animal material and

that they should be considered omnivores. Recent field experiments have

shown that sandworms feed on amphipods

and polychaetes (Commit0 1982; Ambrose

1984a, b; Commit0 and Schrader 1985).

Nereis virens feeds by capturing a

foodmwithts eversible proboscis

which is armed with two jaws. The

jaws, especially the distal biting

portions, are hardened with zinc,

which accounts for up to 2.4% of the

total jaw weight (Bryan and Gibbs

4
‘rL_ 1979, 1980). The jaws are powerful

enough to crush small bivalves (Lewis

and Whitney 1968). Food items are

passed into the esophagus, where a

trypsin-like proteolytic enzyme is

9

produced (Michel and DeVillez 1979),

as well as other enzymes (Kay 1974).

Lewis and Whitney (1968) have iden-

,

tified a cellulase which is induced by

the presence of algae in the gut.

Michel and DeVillez (1980) described

striated spines in the esophagus which

apparently triturate food items.

Several workers have estimated

assimilation efficiency and production

of sandworms. Kay and Brafield (1973)

calculated an assimilation efficiency

of 85.2% and annual production of 8.4

g ash-free dry weight/m2. Kristensen

(1984a) calculated the annual production of a Norwegian population as

23.7 ash-free

Neuhoffg (1979)

dry weight/m2.

demonstrated that

Nereis virens has faster growth and

higher efficiency than two congeners,

N. diversicolor and N. succinea.

Sandworm growth and eTficiency is

I.c greater when worms are fed clam tissue

than when fed oyster biodeposits

(feces and pseudofeces) (Tenore and

Gopalan 1974; Tenore et al. 1978).

Sandworms are also capable of taking

up dissolved organic matter. Compounds shown to be absorbed include

glutamic acid and aspartic acids

(Chapman and Taylor 1968; Taylor 1969;

Jorgensen and Kristensen 1980a, b),

leucine (Bass et al. 1969), glycine

(Jorgensen 1980), valine (Jorgensen

1979), and alanine and guanine (Jorgensen and Kristensen 1980a, b). All

of these studies demonstrate that net

influx occurs when worms are exposed

to natural concentrations of free

amino acids (varying from 40 to 2,011

nmol). Jorgensen and Christiansen

(1980a) showed that sandworms can

obtain their total respiratory energy

requirements by absorption of interstitial amino acids. The larvae can

take up to 200 times the amount of

leucine that adult worms take up,

yielding final tissue concentrations

700 times that of the incubation

medium (Bass et al. 1969).

Predator-Prey Relations

Predation by sandworms can have significant effects in marine softsediment communities. Nereis virens

has been shown to reduce significantly the abundance of the amphipod

Corophium volutator, permitting associated infauna to increase in abundance (Commit0 1982; Ambrose 1984a,

b). Commit0 and Schrader (1985)

suggested that N. virens consumes the

predatory polychaete Nephtys incisa

when C-- volutator is not present.

Sandworms are potential prey in

marine food webs. A number of gull

and tern species take spent sandworms

(Spaans 1971; Shklyarevich 1979).

Ambrose (1986) showed that gulls may

take large, nonreproductive individuals. Cantin et al. (1974) showed

that 16%-40% of the diet of Common

Eiders, Somateria mollissima, in late

May and mid-July is composed of N.

virens. Significant numbers of sari&

worms are preyed upon by the polychaete Glycera dibranchiata (Ambrose

1984a, b).

Biogeochemical Effects

The exchange of solutes, such as

nitrate, between the sediment and the

overlying water is strongly affected

by burrow-dwelling infauna like

Nereis virens (Kristensen

1985; Krzen et al. 1985).

1984b,

The

burrows of N. virens have been shown

to increase-the flux of ammonia into

the water column and to be responsible

for 35% of the nitrification and 38%

of the denitrification in an estuarine

habitat (Henriksen et al. 1980).

Nitrification rates are higher in the

burrow walls than on the sediment

surface (Kristensen 1984b, 1985;

Kristensen et al. 1985). Irrigation

of burrows for respiration causes an

increase in the uptake of glycine by

the bacteria living in the burrows

(Jorgensen et al. 1980). Ventilation

5
of the burrow creates a halo of

oxidized sediment along the length

of the burrow. It is not surprising

that small zoobenthos aggregate in

the oxidized regions outside of sandworm burrows; nematode and gnathostomulid abundances were increased by

94% and 200%. respectively. in the

proximity of virens N. bur<ows (Reise

1981).

ENVIRONMENTAL REQUIREMENTS

Substratum

Nereis virens has been reported from

a range ofdiment types, varying

from sandy muds to fine sands (Pettibone 1963; Bass and Brafield 1972;

Snow and Marsden 1974; Reise 1981).

Muddier sediments seem to be preferred.

700/m2,

Highest densities, up to

are found in the lower portions of the intertidal zone (Bass

and Brafield 1972; Rasmussen 1973;

Snow and Marsden 1974). The migration of nonreproductive adults in the

water column in the winter (Dean 1978)

may be a mechanism to allow sandworms

to find more suitable benthic habitats.

Salinity

Nereis virens is euryhaline (Sayles

1935: Jocn and Dales 1957;

Richards 1969; Walmsby 1970; Appy et

al. 1980), tolerating salinities as

low as 0.5 ppt (Larsen and Doggett

1978). Nereis virens is intermediate

in its ability to tolerate low and

high salinity stress relative to three

congeneric species: N. diversicolor,

N. succinea, and N. pelagica (Theede

Zt al. 1973). Reduced salinities

cause an increase in ammonia excretion

(Haberfield 1977) and tachycardia

(deFur and Mangum 1979).

Dissolved Oxygen

Nereis virens has blood containing a

hemoglobinused for oxygen transport

rather than storage (Economides and

Wells 1975). Decreased oxygen tension

results in increased ventilatory

pumping of the burrow to increase

oxygen transport to nonvascularized

tissues (Lindroth 1938; deFur and

Mangum 1979). Hyman (1932) noted that

oxygen intake is independent of surrounding tension within moderate

ranges of tension. The ventilation

amplitude increases with increasing

temperature (Kristensen 1981, 1983a,

b, c>.

When sandworms are exposed at low

tide and oxygen tensions decline, an

anaerobic pathway is utilized (Scott

1976; Scott et al. 1976). The worms

produce large amounts of d-lactate and

later pay an oxygen debt. Under long

periods of anaerobiosis, sandworms

switch to glycogen degradation which

results in the production of succinate

and volatile fatty acids (Schottler

1979).

Temperature

Kristensen (1983b) states that

optimal temperatures are between 11 OC

and 20 OC, although sandworms can

tolerate temperatures as high as 37.5

OC in the laboratory. Richards (1969)

claimed that sandworms are highly

tolerant of changes in temperature.

Adaptability to Laboratory Conditions

Nereis virens is - -

a potentially

valuable research organism because it

can be maintained in healthy culture

in the laboratory (Goerke 1979, 1984b;

Kristensen 1983c). Its adaptability

to the laboratory led to its use in

some of the first studies on conditioned response and habituation in

invertebrates (Copeland 1930, 1934;

Clark 1960; Evans 1963a, b, 1966). A

word of caution is in order for any

who use sandworms as bioassay organisms: sandworms maintained in seawater without sediment, where the

worms cannot form burrows, may show

abnormal metabolism (Pamatmat 1982).

6
Toxicology

Sandworms have been the focus of

many studies on the bioavailability of

heavy metals and organic pollutants.

A significant fraction (30%-40%) of

the total body burden of zinc is

always found in the jaws (Bryan and

Gibbs 1979, 1980), so concentrations

of zinc in sandworms do not closely

follow environmental concentrations,

and sandworms are poor indicators of

zinc contamination. The jaws contribute less than 1% of the total body

burden of silver, cadmium, copper,

iron, and lead. Cadmium uptake increases with increasing concentration

in the environment; uptake, primarily

from interstitial water, is greater in

small worms (Ray et al. 1980). Rice

and Chien (1977) suggested that there

may be a cadmium detoxification

mechanism in the coelomic fluid; body

concentrations may be 1,000 times the

seawater concentration. Biochemical

stress indices have been determined

for sublethal cadmium dosages (Carr

and Neff 1982). Ray et al. (1981)

indicated that the body burden of

copper and zinc did not vary between

clean and contaminated environments

but significantly greater body

burdens of lead and cadmium were

found in worms from contaminated

sites. Pereira and Kanungo (1981)

demonstrated significant effects of

silver on respiration and osmotic

balance.

Among organic contaminants, Eisler

et al. (1972) determined that nitriloacetic acid (NTA) at a concentration

of 5,500 mg/l resulted in 50% mortality of sandworms. Sandworms are

intermediate in tolerance to NTA compared to many other marine species

(Eisler et al. 1972). Sandworms have

been shown to accumulate and metabolize PCB's, w'ith small worms accumulating 10.8 times the environmental

concentration of 0.04-0.58 ppm and

adults 3.8 times (Ernst et al. 1977;

Goerke and Ernst 1977; Goerke 1979;

McLeese et al. 1981). Excretion of

PCB's can be described by an exponential function which varies with temperature; the maximum rate of elimination occurs at 12 OC (Goerke 1984c).

Biochemical stress indices have been

measured in response to pentachlorophenol (Carr and Neff 1981) and to

refined oil products (Carr and Neff

1984). McElroy (1985) showed that a

polycyclic aromatic hydrocarbon (PAH)

was metabolized by Nereis virens.

Sandworms accumulate and metabolize

the insecticide Lindane, reaching

equilibrium in lo-14 days (Goerke and

Ernst 1980). Sandworms are much more

tolerant of organochlorine pesticides

than the shrimp Crangon septemspinosa

(McLeese et al. 1982; Haya et al.

1984).
JAWS

/ ;/ANTENNAE

r

, :

i

ANTEMOR VIEW

(Proboscis extended)

TRAL CIRRUS

POSTERIOR VIEW

(Left parapodium from

middle of body)

Figure 3. Bloodworm (Glycera dibranchiata).

BLOODWORM

NOMENCLATURE/TAXONOMY/RANGE MORPHOLOGY/IDENTIFICATION AIDS

Scientific name................Glycera

dibranchiata Ehlers, 1868 (Figure 3)

Preferred common name........Bloodworm

Other common names...........Beakworm,

beak-thrower

Phy?um........................Annelida

Class.......................Polychaeta

Order.....................Phyllodocida

Family......................Glyceridae

Geographic range: Found from low water out to about 400 m along the

Atlantic coast from the Gulf of St.

Lawrence to Florida. Also recorded

in the Gulf of Mexico, and in the

eastern Pacific from central California to Mazatlan, Mexico. Figure 4

gives the distribution of this species in the North Atlantic region.

8

Description

Body elongate, robust, having up to

300 segments. Largest individuals

exceed 370 mm in length and 11 mm in

width. Prostomium (head) conical,

with 14-15 annulations and two distal

pairs of antennae (Figure 3). Indistinct eyes on the basal annulation of

the head, or eyes absent. Eversible

proboscis with four dark, curved,

hollow terminal jawpieces. Proboscis

covered with small, conical proboscidean organs. Parapodia with dorsal

and ventral lobes (biramous), hearing

short dorsal cirri and more elongate

ventral cirri. Paired, nonretractile

gills or branchiae beginning on

segments 15-20 and continuing to near
I

I

I

I

I

I

I

I

I

II

i

I

I/ i CANADA \

&fggi”:: ::‘;. .‘.. .,.. ‘: .;. ‘.

,.,. &. : ., :. .: ,’ .“.

,. ATLANTIC OCEAN

KtLOMETERS

Figure 4. Distribution of bloodworm in the North Atlantic region. Heavier

stippling indicates regions of higher abundance.

9
the posterior of the body; gills

elongate or inflated, exceeding the

length of the parapodia (Figure 3).

Dorsal lobe of parapodia (notopodia)

with simple, elongated, finely

serrated setae. Ventral lobe (neuropodia) with simple and jointed

elongated, finely serrated setae.

Identification Aids

The animals are bright pink. The

species is characterized by the pair

of enlarged gills above and below each

of the middle parapodia. Glycera

dibranchiata can be distinguished from

the similar G. americana in that the

latter has retractile, bush-like gills

above the parapodia.

Taxonomic References

Refer to Ehlers 1868; Verrill 1881;

Webster and Benedict 1884; Arwidsson

1898; Hartman 1940; Pettibone 1963.

REASON FOR INCLUSION IN SERIES

Baitworms (bloodworms and sandworms)

are an important fishery in the

Northeastern United States and Nova

Scotia (MacPhail 1954; Klawe and

Dickie 1957; Dow and Creaser 1970;

Schroeder 1978). Baitworms form the

fourth largest fishery in Maine,

trailing only lobsters, clams, and

total finfish. In the past 30 years,

professional bait-diggers have removed

nearly one billion bloodworms (Dow

1978). Over 90% of the bloodworms in

the United States come from Maine with

the remainder from Nova Scotia (7%)

and Massachusetts (2%). Recent evidence, based on sampling of the worm

sizes of commercial landings, indicates that 2-year old worms, rather

than the larger S-year old worms, are

presently being harvested, suggesting

that the populations are being overharvested (Dow 1978; but see Schroeder

[1978] for an alternative interpretation of the data). Overharvesting of

mudflats in two Maine counties has

eliminated bloodworms (Anonymous

1979). Genetic evidence also indicates that some populations are being

;;;;yarvested (Vatias and Bristow

Dow (1978) believes the only

long-term solution to maintaining

sufficient standing stock to support

present intensities of harvesting is

to culture worms under controlled

environmental conditions. Creaser et

al. (1983) presented models for the

determination of Maximum Sustainable

Yield and Optimal Sustainable Yield.

The imposition of size-limits has been

suggested (Saft 1978). Confounding

attempts at managing stocks is an

inverse correlation between bloodworm

production and mean annual temperature; this relationship may explain

some of the temporal variance in

bloodworm densities (Dow 1978).

LIFE HISTORY

Gametogenesis

Separate sexes are found in bloodworms. Gametogenesis occurs in the

undivided body cavity (coelom) and

requires about 1 year (Simpson 1962a,

b). Oocytes are released into the

coelom when they are about 21 pm in

diameter. Mature oocytes are 151-160

pm in diameter.

Spawning

Populations in Maine and southwestern Nova Scotia reproduce from

mid-May until early June (Klawe and

Dickie 1957; Creaser 1973). Populations from Maryland reproduce in the

fall and possibly in late spring

(Simpson 1962b). Shortly before reproduction, bloodworms undergo radical

morphological changes. Their alimentary tract and musculature atrophy.

Their parapodia and setae elongate.

These sexual forms (epitokes) swarm in

shallow water over a period of 1 to 3

days at high tide in the afternoon

(Simpson 1962a, 1973). Males emit

sperm while swimming. Females

rupture, releasing up to 10 million

10
eggs per individual (Creaser 1973).

Both males and females die after

spawning.

Larval Development

The early development of Glycera

dibranchiata apparently occurs on the

sediment surface (Simpson 1962b).

Development proceeds to swimming

stages in 14-20 h after fertilization,

giving rise to unspecialized,

planktotrophic larvae (Simpson 1962a).

The larvae are not found in plankton

tows, suggesting that their planktonic

life is short or that they are

demersal (living just above the

bottom).

Population Structure

Klawe and Dickie (1957) and Creaser

(1973) found that Glycera dibranchiata

has a maximum life span of 5 years.

The most rapid growth occurs during

the second and third years. Most

bloodworms reproduce and die at 3

years of age although some postpone

reproduction until the fourth or fifth

year.

ECOLOGICAL ROLE

Feeding

There has been much debate about

whether bloodworms are deposit-feeders

or predators. Sanders et al. (1962)

suggested that Glycera dibranchiata is

a deposit-feeder, based on gut contents. Frankenberg and Smith (1967)

and Adams and Angelovic (1970) demonstrated significant utilization of

dead organic matter by bloodworms in

the laboratory. Such findings are

puzzling in light of the formidable

feeding apparatus of G. dibranchiata.

These worms possess an eversible proboscis which contains four terminal

jaws (Wells 1937). The jaws are

strengthened, particularly distally,

by accumulation of copper; 13% of the

distal tip is composed of copper

(Gibbs and Bryan 1980). Each jaw is

coursed by a canal with numerous pores

to the exterior through which a

secretion from associated glands can

flow (Michel 1966; Wolff 1976, 1977).

The secretion is a neurotoxin, especially effective

(Michel and Keil 1975yn

crustaceans

It is therefore not surprising that bloodworms

have been found to feed on amphipods

(Dubois-Laviolette 1985) and polychaetes (Ambrose 1984a, b).

A congeneric species, G. e, has

been shown to maintain -a permanent

gallery of burrows (Ockelmann and Vahl

1970). Prey are detected by mechanoreception and ambushed at the sediment

surface. Glycera dibranchiata

occupies burrows (Klawe and Dickie

1957), but their exact configuration

has not been observed. Anecdotal

evidence for G. dibranchiata as an

ambush predator derives from the

foraging behavior of Black-bellied

Plovers (Pluvialis squatarola),

specialized predators G.

dibranchiata (Dubois-Lavio1et.T: 1985j.

To bring bloodworms near the sediment

surface, these plovers engage in foottrembling behavior, setting up

vibrations at the sediment surface.

Bloodworms apparently mistake these

vibrations for the vibrations of a

potential prey item. Stolte (1932)

described the complex innervation of

the mechanoreceptive sense organs of

bloodworms. Bloodworms refused to eat

dead prey in the laboratory, indicating the importance of mechanoreception in prey location (Klawe and

Dickie 1957; Fauchald and Jumars

1979).

Several features make it likely that

Glycera dibranchiata is primarily a

predator: the proboscis armed with

neurotoxin-injecting jaws, mechanoreceptive abilities, lack of a complete gut (Ockelmann and Vahl 1970),

and the presence of proteolytic

enzymes in the gut (Vahl 1976). Evidence does exist indicating that

bloodworms can successfully utilize

detritus (Frankenberg and Smith 1967;

Adams and Angelovic 1970). It seems

11
likely that detritivory is manifested

only in the absence of suitable animal

prey.

Bloodworms are capable of utilizing

dissolved organic matter. Stephens et

al. (1965) showed that bloodworms take

up creatine opportunistically.

Stevens and Preston (1981a, b, c)

showed that alanine can be concentrated against a concentration gradient. Preston and Stephens (1969),

Preston (1970) and Chien et al. (1972)

indicate that a number of other amino

acids can be concentrated.

Predator-Prey Relations

Bloodworms can significantly affect

populations of other infaunal organisms. Wilson (1979) showed a correlation between bloodworm abundance

and the number of maldanid polychaetes

regenerating their anterior ends and

argued that bloodworms were browsing

on the maldanids. Ambrose (1984a, b)

showed that bloodworms consume significant numbers of the sandworm,

Nereis virens. Dubois-Laviolette

(1985) reported that bloodworm guts

contained the amphipod Corophium

volutator.

Predators on G. dibranchiata seem to

be few. They-were rarely found in

fish guts (Klawe and Dickie 1957).

Dubois-Laviolette (1985) reported that

bloodworms are the major prey of

Black-bellied Plovers (Pluvialis

squatarola) in the upper Bay of Fundy.

The striped bass, Morone saxatilis,

and the sand shrimp, Crangon septemspinosa, consume large numbers of

spent, dead bloodworms.

ENVIRONMENTAL REQIJI REMENTS

Substratum

Bloodworms live in a range of substratum types, but seem to be most

abundant in very fine muds with high

organic content (Klawe and Dickie

1957; Creaser 1973; Dubois-Laviolette

1985). Bloodworms are conspicuous in

the water column during the fall and

winter (Dean 1978b; Graham and Creaser

1979). Such swimming worms are not

reproductive; they may be searching

for more suitable benthic habitat.

Salinity

There are no published data on

tolerance limits of bloodworms to

salinity stress. Costa et al. (1980)

demonstrated that bloodworms are osmoconformers. Bloodworms use free amino

acids to decrease intracellular solute

concentrations during hypo-osmotic

stress. Machin (1975) found that

these animals equilibrated to 50% and

150% seawater after lo-25 h, producing

a urine that is iso-osmotic to the

coelomic fluid. The volume of coelomocytes changes rapidly in response to

different osmotic pressures (Machin

and O'Donnell 1977).

Dissolved Oxygen

Glycera dibranchiata is called a

bloodworm because its hemoglobin

imparts a reddish color to the body.

The hemoglobin is found in cells in

the body cavity (coelom); a circulatory system is lacking. No data

exist on the minimum dissolved oxygen

concentration needed for survival.

The hemoglobin of bloodworms consists

of two different molecules, differing

greatly in molecular weight and oxygen

affinity (e.g., Weber et al. 1977;

Harrington et al. 1978; Parkhurst et

al. 1981). The two hemoglobin types

allow for the storage of oxygen under

conditions of low oxygen tension and

for the transport of oxygen under conditions of high oxygen tension. Mangum (1970) and Hoffman and Mangum

(1970) showed that much of the oxygen

transport in bloodworms continues

after experimentally blocking the

hemoglobin, implying that the storage

capability of hemoglobin is the more

important use. In addition to hemoglobin, the muscles of the proboscis

contain a myoglobin which facilitates

12
transfer of oxygen (Terwilliger and

Terwilliger 1981).

Toxicology

Limited information is available on

the effect of heavy metals and organic

pollutants on bloodworms. In contaminated sites, copper may increase in

the body but not in the jaws; 67% of

the body burden of copper is in the

jaws (Gibbs and Bryan 1980). Zinc

concentrations remain reasonably

constant in both the jaws and body for

worms exposed to different levels of

environmental zinc. Rice and Chien

(1979) showed that cadmium accumulates

through both the body surface and the

intestine. They argued that the

coelomic fluid may act like mammalian

metallothioneins to bind the metal

ions. Medeiros et al. (1981) showed

that mercury uptake is very rapid,

with 75% of the equilibrium value

being attained after only 2 h of

exposure. PCB's do not produce

increased mortality in bloodworms but

may affect the ability of coelomocytes

to phagocytize pathogens (Anderson et

al. 1984).

13

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23
50272 -IO1

1 REPORT DOCUYENlATlON ) k .“‘““. No._ _ _ _ ,_ _ __ \ _I_ I= 3. ROClPIWIt’l keosslon No.

I

I PAGE Itiiological Keport 82(11.8u)" 1 I

I Species Profiles: Life Histories and tnvironmental Kequlrements oT ( April 1988

I

Coastal Fishes and Invertebrates (North Atlantic) - Sandworm and 6 1

Bloodworm

1. -r(9)

Herbert Wilson, Jr., and R. Eugene Ruff

9. hrformi~ O~nhtlon Nwne and Addnss

Manomet Bird Observatory

P.O. Box 936

Manomet, MA 02345

12. Sponsoring Organlutlon Name and Address

10. ?~i.MT~sh/Work Unit No.

11. Contract(C) 0, Grant(G) NO.

(G)

National Wetlands Research Center U.S. Army Corps of Engineers

Fish and Wildlife Service Waterways Experiment Station

U.S. Department of the Interior P.O. Box 631

Washington, DC 20240 Vicksburg, MS 39180

*U.S. Army Corps of Engineers Report No. EL-82-4

Species profiles are literature summaries of the taxonomy, morphology, range, life

history, and environmental requirements of coastal aquatic species. They are prepared to

assist in environmental impact assessment. The sandworm (Nereis virens) is a commercially

valuable baitworm, reaching lengths of 30 cm. Most wormsliVe or 5 years. Males swarm

in the water column before spawning in the females' burrows. Both males and females die

after spawning. A planktonic larval phase is either brief or lacking. Sandworms are

omnivorous. They can significantly reduce the abundance of smaller infaunal organisms.

Predators on sandworms include bloodworms and gulls. Physiological tolerances are broad

although most worms are found in fine sand with water of high salinity. Sandworms have

been the subject of much toxicological research and readily adapt to laboratory

conditions. The bloodworm (Glycera dibranchiata), attaining lengths of 40 cm, is also an

important baitworm. Its maximum life span is 5 years. Spawning occurs in the water

,column with both males and females dying after spawning. Bloodworms are primarily

predators, preying on certain species of polychaetes and crustaceans, although they are

capable of digesting detritus. Bloodworms appear to have few predators. Bloodworms

possess at least two types of hemoglobin, permitting them to tolerate a wide range of

oxygen tensions.

17. Docunmnt Analysis a. Desctipton

Fisheries Annelids

Salinity Life cycles

Temperature Oxygen

Feeding habits Contaminants

b. IdwMi~n/O$?en-Endad Terms

Nereis virens Salinity requirements

eaxnchiata Temperature requirements

Sandworm Oxygen requirements

Bloodworm Toxicology

Life history

Spawning

c. COSATI Fiald/Gmup

1C. Availability Statement

Unlimited distribution

19. Security Class CThis Report) 21. No. of PaSo

Unclassified 23

20. Socuriw Class CThls Pace) 22. price

I

(Se. ANSl-239.11))

1 Unclassified I I

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