Food, Feeding Behavior and Feeding Ecology of Nemerteans

AMER. ZOOL., 25:113-125 (1985)

Food, Feeding Behavior and Feeding Ecology of Nemerteans1

J O H N J . MCDERMOTT

Department of Biology, Franklin and Marshall College,Lancaster, Pennsylvania 17604

AND

PAMELA ROE

Department of Biology, California State College, Stanislaus,Turlock, California 95380

SYNOPSIS. The feeding biology of nemerteans is reviewed, new information is presented,and the role of nemerteans in natural communities is discussed and evaluated. Mostnemerteans are carnivorous, the majority feeding on live, often specific, prey, while someare scavengers. Macrophagous feeding is found in the Palaeonemertea, Heteronemerteaand some of the Hoplonemertea; the more specialized suctorial feeding is limited to fiveof the hoplonemertean families, and suspension feeding (omnivorous diet) occurs only inthe highly specialized symbiotic monogeneric Bdellonemertea.

Feeding adaptations seem to be related to the nature and employment of the proboscis,the dilatability of the mouth, and the structure of the anterior part of the digestive tract.The transport of dissolved organic materials from seawater has been demonstrated, butits role in nemertean nutrition is just being contemplated. Present meager informationon predation has shown nemerteans to have actually and potentially large effects on preypopulations and thus on the communities in which they live. As the feeding biology ofonly a relative handful of species has been studied, much basic comparative research isneeded before we can corroborate or refute our present ideas concerning the ecologicalroles of nemerteans.

INTRODUCTION

The food-catching proboscis apparatusis both a unique and a visibly outstandingfeature of the Nemertea. The feeding biol-ogy of these worms shows them to be ele-gantly adapted in behavior, physiology andmorphology to the particular foods theyeat, and they are consequently integral andpotentially important members of naturalcommunities. In this paper we will relatethese adaptive strategies in four parts:foods, patterns of feeding behavior, the roleof dissolved organic material in nemerteannutrition, and feeding ecology. Finally, wewill discuss areas of research needed beforethe importance of nemerteans in theircommunities can be appreciated.

FEEDING BIOLOGY

Foods of nemerteans

Foods are basically semi-fluid, soft, orpartly digested parts of arthropods, anne-

1 From the Symposium on Comparative Biology ofNemertines presented at the Annual Meeting of theAmerican Society of Zoologists, 27-30 December1983, at Philadelphia, Pennsylvania.

1

lids and other worm-shaped animals, plusa scattering of molluscs, fish, etc., livingand dead (Table 1). Although there is littlepublished information on the food ofpalaeonemerteans, it appears that they feedon annelids compatible with their size. Evi-dence for heteronemerteans indicates thattheir food may be living or dead with apredilection for polychaetes; they also uti-lize molluscs, crustaceans and other ne-merteans. Although scavenging may be away of life for many species, clear-cut evi-dence from nature exists only for Parbor-lasia corrugatus (Dayton et ai, 1970, 1974;Gibson, 1983).

All data continue to show that the free-living marine suctorial hoplonemerteansare primarily predators of live amphipods,especially tubicolous types (Bartsch, 1973,1975; McDermott, 1976a, 1984, unpub-lished), although other crustaceans areeaten by some. Brunberg's (1974) sugges-tion that polychaetes may be in the diet ofNipponnemertes seems to belie all evidence.Insects and myriopods are the only knownprey of the two terrestrial species of Argo-nemertes. Members of the symbiotic familyCarcinonemertidae feed in a suctorial fash-

13

114 J. J. MCDERMOTT AND P. ROE

TABLE 1. Food of Nemertea belonging to the orders Palaeonemertea, Heteronemertea, Hoplonemertea and Bdellone-mertea.'

Nemertean Prey Reference

PalaeonemerteaCephalothricidae and Hubrechtidae

Cephalothrix linearis(Rathke) and C. rufi-jrons (Johnston)1"

Cephalothrix sp.Hubrechtella dubia Bergen-

dalb

HeteronemerteaLineidae

Cerebratulus lacteus (Leidy)b

Cerebratulus sp.Gorgonorhynchus bermuden-

sis Wheelerb

Lineus bilineatus (Renier)Linens desori SchmidtLineus lacticapitatus

WheelerLineus longissimus (Gunne-

rus)b

Lineus ruber (MiiHer)b

Lineus sanguineus (Rathke)

Lineus vegetus Coeb

Lineus viridis (Fabricius)"

Lineus sp.Micrura corallifila CantellMicrura fasciolata Ehren-

bergMicrura purpurea (Dalyell)Parborlasia corrugatus

(Mclntosh)bf

Polybrachiorhynchus dayiGibson

Uchidana parasita Iwata«

HoplonemerteaSuctorial Feeders

AmphiporidaeAmphiporus bioculatus Mc-

lntoshAmphiporus dissimulans

RichesAmphiporus formidabilis

Griffin

Oligochaetes (id. sp. or gen.),nematode (id. gen.); oligo-chaete (id. sp.)

CannibalisticPolychaetes (unid.)

Nereis sp.; Ensis directus

Syndosmya nitidaAtherina harringtonensis (dead);

crustacean exoskeletal remainsPolychaetes (id. sp. or gen.)Polychaetes (id. gen.)Polychaetes (unid.)

Polychaetes (id. sp. or gen.), Asci-dia intestinalts, Anomia sp; poly-chaetes (id. sp., gen. or fam.)

Polychaetes (id. sp. or gen.); liv-ing and dead polychaetes, oli-gochaetes and small crusta-ceans (all unid.); Clitellioarenarius; Littorina saxatilis; dis-solved organics

Polychaetes (id. sp. or fam.), oli-gochaetes (id. gen.),' nemer-tean (id. sp.)c

Liver, dead mussels and shrimpPolychaetes (unid.)

Nephtys sp.Polychaetes (unid.)Polychaetes (id. fam.)

Nemerteans (id. sp.)Acodontaster conspicuous (dead);

Limatula hodgsoni and unid. bi-valve; "almost anything"

Upogebia africana; other crusta-ceans, polychaetes and gastro-pods (unid.)

Mactra sulcataria (gill tissue)

Amphipods (id. sp.)

Amphipods (id. sp.)

Amphipods (unid.); Petrolisthes sp.(claws); isopods (id. gen.)

Jennings and Gibson (1969);McDermott (unpublished)

Mclntosh (1873-74)Hylbom (1956)

Wilson (1900), Coe (1943); Mc-Dermott (1976*), Schneider(1982)

Brunberg (1964)Wheeler (1940); Gibson (1974)

Joubin (1894), McDermott (1984)Beklemishev (1955)McDermott (unpublished)

Mclntosh (1873-74); Pieron(1914), Beklemishev (1955)

Verrill (1892),d Gontcharoff(1948, 1961), Rassmussen(1973), Bartsch (1975); Jen-nings and Gibson (1969); Jen-nings (1960), McDermott (un-published); Muus (1967); Fisherand Cramer (1967), Fisher andOaks (1978)

Jennings and Gibson (1969)

Roe (unpublished)Gontcharoff(1959), Cantell

(1975)Mclntosh (1873-74)Cantell (1975)Cantell (1975)

Riches (1893), Cantell (1975)Dayton et al. (1970, 1974); Day-

ton (unpublished); Gibson(1983)

Day (1974), Branch and Branch(1981); Branch and Branch(1981)

Iwata (1967)

McDermott (1984)

Brunberg (1964),b McDermott(1984)

Strieker and Cloney (1982); Roe(unpublished); Kohn, A. J. (un-published)

NEMERTEAN FEEDING BIOLOGY 115

TABLE 1. Continued.

Prey Reference

Amphiporus imparispinosusGriffin

Amphiporus lactifloreus(Johnston)

Amphiporus ochraceus (Ver-rill)

Zygonemertes virescens (Ver-rill)

CarcinonemertidaeCarcinonemertes carcinophi-

la (Kolliker)sCarcinonemertes epialti

Coe«Carcinonemertes errans

Wickham*

Pseudocarcinonemertes hom-ari Fleming and Gib-son8

CratenemertidaeNipponnemertes pulcher

(Johnston)

ProsorhochmidaeArgonemertes dendyi (Dak-

in)Argonemertes australiensis

(Dendy)

Oerstedia dorsalis (Abild-gaard)

TetrastemmatidaeTetrastemma candidum

(Muller)Tetrastemma elegans (Gir-

ard)Tetrastemma laminariae

(Uschakow)Tetrastemma melanocepha-

lum (Johnston)

Tetrastemma sp.

Macrophagous FeedersEmplectonematidae

Emplectonema gracile(Johnston)

Paranemertes peregrina(Coe)

Nemertopsis gracilis Coe

OtotyphlonemertidaeOtotyphlonemertes brevis

Correab

Amphipods (unid.)

Amphipods (id. sp.)

Amphipods (id. sp.)

Amphipods (id. sp.), isopods (id.sp.)

Host crab embryos

Host crab embryos

Host crab embryos; dissolved or-ganics

Homarus americanus (probablyembryos)

Amphipods (id. sp.); polychaetes(unid.)

Collembolans, nymphs of del-phacid bugs

Collembola, other small insects,young myriopods (all unid.);myriopods (unid.)

Amphipods (id. sp.)

Artemia nauplii

Amphipods (id. sp.)

Small crustaceans (unid.)

Amphipods (id. sp. or gen.), co-pepods (unid.); amphipods (id.sp.)

Amphipods (id. sp. or gen.)

Barnacles (unid.), acmaeid lim-pets (unid.); injured barnacles(id. sp.), eggs of Nucella emar-ginata; barnacles (unid.)

Polychaetes (id. sp. or gen.); dis-solved organics

Lasaea cistula

Crustaceans (unid.) and setae ofpolychaetes in gut; fresh fish(bait)

Roe (unpublished)

Gontcharoff (1948), Jennings andGibson (1969), McDermott (un-published)

McDermott (1976a)

McDermott (1976a and unpub-lished)

Humes (1942)

Kuris (1978), Roe (unpublished)

Wickham(1978, 1979a, b, 1980),Wickham and Fisher (1977);Roe et al. (1981), Crowe et al.(1982)

Fleming and Gibson (1981)

Brunberg (1964), Berg (1972a),McDermott (1984); Brunberg(1964)

Waterston and Quick (1937)

Hickman (1963); Gibson (1982a)

McDermott (unpublished)

Roe (unpublished)

McDermott (1976a)

Sundberg (1979a)

Bartsch (1973, 1975); Gibson(1982a)

Strieker and Cloney (1982)

Dayton (1971); Glynn (1965); Lel-lelid, N. (unpublished)

Roe (1970, 1976, 1979), Gibson(1970); Roe et al. (unpublished)

Glynn (1965)

Correa(1948)


TABLE 1. Continued.

Nemertean Prey Reference

Ototyphlonemertes pallida(Kerferstein)

TetrastemmatidaeProstoma asensonatum

(Montgomery)Prostoma graecense (Boh-

mig)

Prostoma jenningsi Gibsonand Young

Prostoma rubrum (Leidy)

BdellonemerteaMalacobdella grossa (Mul-

ler)*

Copepods (harpacticoids)

Oligochaetes (unid.)

Insect larvae (id. gen.) Cyclops sp.;oligochaetes (id. sp. or gen.)

Oligochaetes (id. fam.), serologi-cal ident. of oligochaete re-mains

Oligochaetes (unid.), insects, crus-taceans, unicellular organisms,cannibalistic; oligochaetes (id.gen.), insect larvae (id. gen.)

Plankton from mantle cavity ofmany bivalve hosts

Mock (1978)

Child (1901)'

DuPlessis (1893, from Gibson,1972);J Reisinger (1926), Loden(1974)k

Gibson and Young (1976)

Coe (1943); Jennings and Gibson(1969)

Gibson (1968), Gibson and Jen-nings (1969)

* Families and species arranged alphabetically, and hoplonemerteans divided into suctorial and macropha-gous feeders; id. sp., id. gen., id. fam. = items in food groups identified to species, genus and family, respec-tively; unid. = unidentified; semicolon separates references for different food groups.

b Scavenging indicated.c Formerly C. bioculata in Jennings and Gibson (1969).d Called worm L. viridis, but apparently L. ruber (see Coe, 1943).' Eaten by starved worms.' Formerly Lineus corrugatus.8 Symbiotic nemertean.h Called worm A. lactifloreus, but apparently A. dissvmulans (see Berg, 19726).' Originally Stichostemma asensoriatum (see Gibson and Moore, 1976).J Originally Emea lacustris (see Gibson and Moore, 1976).k Originally Prostoma rubrum (see Gibson and Moore, 1976); annelid food supplied in laboratory only.

ion on the embryos of their decapod hosts.Among the marine macrophagous hoplo-nemerteans, polychaetes are importantprey and there is a preference for certainspecies (Roe, 1970, 1976, 1979, for Para-nemertes peregrina). Members of the inter-stitial genus, Ototyphlonemertes, apparentlyfeed on associated small crustaceans andpolychaetes, but our knowledge of thisfamily's biology is meager. All data indi-cate that oligochaetes and worm-like insectlarvae are utilized by species of the fresh-water genus Prostoma.

Patterns of feeding behavior

Two major feeding patterns occur amongthe nemerteans—suctorial and macropha-gous. Both patterns are found in the hoplo-nemerteans, while the palaeonemerteansand heteronemerteans are macrophagous.The scavenging mode of life falls into the

macrophagous category. Suspension feed-ing is found only among the specializedsymbiotic bdellonemerteans. We willdescribe each feeding pattern employinginformation from well-known examples,and will discuss general principles involvedin each behavior.

Suctorial feeding. Suctorial behavior isfound in five of the seven families withinthe Monostilifera (Table 1). It has beenconfirmed for only 19 species in 8 generaamong the estimated 260 species in 53 gen-era (Gibson, 19826) in the five families.Only members of the genus Tetrastemma(~80 species) within the Tetrastemmati-dae are herein considered suctorial.

The description of the general feedingbehavior of free-living suctorial species thatfollows, is based on laboratory observationmade primarily with Amphiporus lactiflo-reus, A. ochraceus, Nipponnemertes pulcher,


Oerstedia dorsalis, Tetrastemma elegans, T.melanocephalum and Zygonemertes virescens(Jennings and Gibson, 1969; Bartsch, 1973,1975; McDermott 1976a, 1984, unpub-lished). The pattern, which involves var-ious species of amphipods as prey, isremarkably similar for these and relatedspecies.

As the nemertean makes contact with anamphipod, the proboscis is everted withconsiderable force (still unmeasured), sothat its tip strikes the prey on the morevulnerable ventral side at the base of theappendages. It may strike this locationdirectly or by coiling halfway around theprey before the tip makes ventral contact.The thin exoskeleton of the sternal plateis pierced by the stylet and a toxin is intro-duced into the body. The everted probos-cis may remain apposed to the plate fromseveral seconds to 2 min. Usually, however,the prey is immobilized and apparentlykilled (McDermott, 1976a) in <1 min aftereversion of the proboscis. Following inver-sion of the proboscis, the nemertean usesits head to probe among the appendagesseeking to penetrate one of the sternalplates. The proboscis may be everted oneor more times onto the ventral side of theamphipod before the head penetrates.Worms may move away from the preybefore penetration, but they apparentlymaintain contact by means of a mucus-trail.The head is eventually wedged past thepartially dislodged sternal plate (usually onthe peraeonal section of the body), and theanterior gut (esophagus-stomach complex)is everted into the opening as a shallowcup-like structure.

As the suctorial action begins, due toperistaltic movements of the body wall, theprey's fluid, tissues and organs flow intothe gut of the nemertean. Eventually theprey is completely evacuated leaving theotherwise intact exoskeleton. Internalfluids and organs are obviously partiallyreplaced with fluid from the externalmedium because the exoskeleton does notcollapse from the vigorous suctorial action.

The entire feeding sequence (initial pro-boscis eversion to the end of feeding) takesfrom 3 to > 40 min depending on a varietyof conditions particularly related to pre-

penetration behavior. Once a worm pen-etrates, the evacuation process proceeds ata more uniform rate (McDermott, unpub-lished).

Jennings and Gibson (1969) suggestedthat the sternal plates are subjected to his-tolytic action by glandular secretions fromthe anterior proboscis prior to penetrationby the head, and that proteolytic enzymesmay be forced through the stylet-producedhole in the exoskeleton and thus begin someinternal digestion of the body parts priorto suctorial action. While these ideas maybe true (still not proven) for A. lactifloreusand also for N. pulcher (McDermott, 1984),it is unlikely to be the case for other speciesthat hold the proboscis against the prey foronly a few seconds (McDermott, 1976a).

Free-living marine suctorial species arefood specialists. Laboratory experimentshave shown that they feed primarily onamphipods (Table 1), especially the tubic-olous Ampeliscidae and Corophiidae(Bartsch, 1973; McDermott 1976a, 1984,unpublished). A notable exception is Z.virescens which may also utilize the abun-dant isopods in its eelgrass habitat(McDermott, 1976a, unpublished).Attempts to feed them other small crus-taceans, polychaetes and molluscs havebeen negative (Jennings and Gibson, 1969;Bartsch, 1973; McDermott, 1976a). Littleis known about specialization in terrestrialspecies (Table 1).

The diet of the suctorial symbiotic Car-cinonemertidae is as might be expected,very specialized, i.e., it feeds on the host'sembryos. However, Roe (unpublished) hasshown that Carcinonemertes spp. from thewest coast of the U.S. will feed and repro-duce on both natural and unnatural hostcrab embryos.

Free-living suctorial feeders probablyfind food by chance contact with their oftenabundant prey. Jennings and Gibson (1969)showed that A. lactifloreus apparently doesnot detect food from a distance. It seemslikely that in comparison to some of themacrophagous scavengers, distance che-moreception is poorly developed, but thishas yet to be demonstrated experimentally.

The heavily folded walls of the stomachin suctorial feeders appear to be an adap-


tation for their mode of feeding (Jenningsand Gibson, 1969; Berg, 1972a), allowingthe worms to consume prey larger thanthemselves. In all species studied to date,the esophagus-stomach complex is evertedinto the body of the prey after the headhas penetrated the sternal plate; it thenexpands to form the cup that collects thesoft parts of the prey.

Macrophagous feeding. In this type, thenemertean consumes the entire preyorganism rather than taking fluids andorgans from inside the prey. Macropha-gous feeders may be divided into twogroups: 1. those hoplonemerteans that usethe stylet of the proboscis to immobilizethe prey—Monostilifera of the familiesEmplectonematidae, Ototyphlonemerti-idae and some members of the Tetrastem-matidae; and 2. anoplans in which the pro-boscis may or may not be used to captureprey. Scavenging occurs in members of theAnopla, some species showing evidences ofboth predatory and scavenging behavior(Table 1).

Feeding has been observed in only 9 (5genera) of an estimated 95 species (Gibson,19826) in the three hoplonemertean fam-ilies. Approximately 30 of the 110 knownspecies of Tetrastemmatidae are hereinconsidered potentially of the macrophagoustype, although this has been demonstratedonly in four species of Prostoma.

Paranemertes peregrina is a typical exam-ple of a hoplonemertean macrophagousfeeder (Roe, 1970). Upon contact of theanterior edge of the nemertean's head withthe polychaete prey, the nemertean retractsits head, everts its proboscis, wraps itaround the prey and punctures the preyseveral times with the stylet. After the preyis paralyzed, the nemertean retracts theproboscis, losing contact with the prey, thencrawls to the prey and engulfs it whole.Peristaltic waves can often be seen passingalong the body apparently to help the wormgain traction or to move the food into thedigestive tract. As with suctorial feeders,some prey selectivity occurs, e.g., nereidpolychaetes are preferred (Roe, 1970,1976).

Jennings and Gibson (1969) gave a sim-

ilar description of feeding for the fresh-water species Prostoma rubrum, and showedthat oligochaetes and chironomid larvaewere acceptable prey while the crustaceansGammarus and Asellus were not attacked oreaten.

An example of a typical anoplan macro-phagous feeder is Lineus ruber (Jennings,1960; Jennings and Gibson, 1969; Bartsch,1975). The nemertean everts the proboscisin a spiral coil around the prey when itcomes within range (prior contact is notrequired as in the hoplonemerteans). Asticky mucus released by the proboscisseems to help bind the prey. As the pro-boscis retracts it pulls the prey toward theventral mouth. The body anterior to themouth is raised and curls downward overthe prey, even gripping the prey, thusgradually forcing it into the highly expand-able mouth. The ingestion process may takeminutes to hours depending on the size ofthe prey. Non-living foods in this and otherspecies are ingested without the aid of theproboscis.

The genus Cephalothrix uses its proboscisin the same manner as Lineus. Jennings andGibson (1969) suggested that the barbs inthe proboscis epithelium (proboscidialrhabdoids—see Strieker and Cloney 1983)may be used both to paralyze and grip theoligochaete prey. They hypothesized thata toxin is introduced into the holes pro-duced by the barbs. Recent observationswith C. rufifrons (McDermott, unpub-lished), however, showed that oligochaetesdo not become paralyzed and may continuetheir writhing activity even when fullyingested. Although Cerebratulus uses itsproboscis to capture worms (Wilson, 1900;Coe, 1943) it seems unlikely that this organis used in attacking Ensis in its burrow(McDermott, 19766).

Unlike the suctorial species, macropha-gous feeders do not have an enlarged,folded stomach nor a distinct esophagus(Jennings and Gibson, 1969; Gibson, 1970).The size of prey is generally limited to thenemertean diameter or dilatability of themouth; therefore prey is usually of worm-like proportions (annelids, elongatedaquatic insect larvae, Ensis). Having worm-


shaped prey is probably an adaptation tomaximize the amount of food per preydiameter.

Distance chemoreception is not welldeveloped in the enoplan P. peregrina (Roe,1970), but Amerongen and Chia (1982)showed that the cerebral organs of thisworm function in close-range chemorecep-tion for prey detection and recognition. Aswith free-living suctorial species, prey tendto be abundant, and are captured whencontacted by the nemertean.

Scavengers are apparently limited pri-marily to the orders Palaeonemertea andHeteronemertea. Lineids provide the moststudied laboratory examples of scaveng-ing, but their feeding behavior differs frompredatory behavior mainly in that the pro-boscis is not used in the process, certainlyan energy conserving behavioral adapta-tion.

Few lineids have been observed to scav-enge in nature. Dayton et al. (1974), how-ever, showed that large numbers of Par-borlasia corrugatus moved onto and fed onrecently killed Antarctic sea stars, Acodon-taster conspicuous.

Scavenging species tend to have well-developed distance chemoreception andlittle food selectivity. Specimens of Lineusvegetus will congregate on pieces of mussel,shrimp or liver from scattered places in a200 liter aquarium within several minutesafter their introduction (Roe, unpub-lished). Jennings and Gibson (1969)reported that Lineus sanguineus and L. ruberlocate food up to 8 cm by chemotaxis. Day-ton (personal communication) found Par-borlasia corrugatus to have effective che-moreception of 10-20 m. Fisher andCramer (1967) listed a variety of organiccompounds that attract L. ruber (cellobiose,glucose, histidine, n-acetyl-glucosamine,proline and taurine).

Suspension feeding. This specializedmechanism has evolved only in Malacob-della (Bdellonemertea), symbiotic inbivalves (Gibson, 1972). The followingaccount is from Gibson and Jennings(1969). Malacobdella grossa is primarily anunselective plankton feeding omnivore thatutilizes the mollusc's incurrent water.

Associated with this behavior are uniquemorphological characteristics of the diges-tive tract: the rhynchodaeum and buccalcavity are incorporated into a large papil-late, ciliated, distensible pharynx. In feed-ing, the worm closes off its esophagus andexpands the pharynx, thus drawing inwater. Then the pharnyx is contractedslightly, causing the papillae to form ameshwork that prevents particles fromescaping. Further pharyngeal contractionforces the water back out, and food is car-ried via cilia into interpapillate ciliary tractsthat lead to the esophagus. The sameauthors showed that the digestive enzymesof Malacobdella are carbohydrases in con-trast to the proteases of typically carnivo-rous nemerteans.

Role of dissolved organic uptake

Many soft-bodied marine invertebratesabsorb dissolved organic material (DOM)directly through the epidermis (Stephens,1982). Absorption of DOM by nemerteanshas been shown in Lineus ruber (Fisher andCramer, 1967; Fisher and Oaks, 1978),Paranemertes peregrina (Roe et al., unpub-lished) and Carcinonemertes errans (Roe etal., 1981; Crowe et al., 1982). Fisher andOaks (1978) presented strong evidence thatepidermal cells of L. ruber are the primarysite of uptake, and that DOM is used in anutritional sense, both in providing energyand in protein synthesis. In addition, Jen-nings and Gibson (1969) found nonspe-cific esterases and exopeptidases in the epi-dermis (L. sanguineus) and blood vascularsystem of most species studied. They sug-gested that these enzymes are concernedwith extracorporeal digestion of simpleproteins or polypeptides, and that theproducts of this digestion supplement thenormal diet.

The role of DOM in nutrition of free-living marine organisms is only beginningto be realized (Stephens, 1981, 1982), andits quantitative role in nutrition of nemer-teans has not been established. However,some information on its importance in thesymbiotic Carcinonemertes is available. Indi-viduals of C. errans on male and non-ber-ried female crabs (9 months/yr) appar-


ently do not feed. Roe et al. (1981) andCrowe et al. (1982) not only snowed thatnon-feeding individuals absorb dissolvedamino acids, but also demonstrated thatthe crab hosts leak amino acids acrossarthrodial membranes in excess of sur-rounding water levels. These amino acidsare the same ones most readily absorbedby the worms, and there is net influx atconcentrations found in this worm habitat.

Roe (unpublished) also isolated non-trophic worms in fingerbowls in sea waterwith and without amino acids. She wasunable to get long-term maintenance ofworms with the amino acids. However,worms kept in sea water subjected to ultra-violet light and passed through a 1 /urn filterplus a charcoal filter to remove organicmaterials shrank from an average weightof 4.5 Mg/worm (800 worms in 4 samples)to 3.1 /jg/worm (480 worms in 1 sample)in 22 days. These results, coupled with thelack of any obvious mechanism of feedingby the worms, and the fact that little organicmaterial besides the small molecules leakedby the crab is present in arthrodial mem-brane areas, lend support to the hypothesisthat absorption of DOM is the primarymethod of nutrition for C. errans duringmuch of its life span.

Nemerteans in community ecology

Three topics will be discussed withrespect to feeding ecology of nemerteansand the community: a) the adaptive strat-egies of nemerteans as optimal foragers; b)the effects of nemerteans on communitystructure; and c) the role of nemerteans asprey.

Nemerteans as optimal foragers. We haveseen that several features of behavior, gutmorphology, prey detection, etc., functiontogether to result in each nemertean beinghighly adaptive with respect to feeding. Arelatively large body of ecological litera-ture exists which describes optimal forag-ing patterns for different types of preda-tors under different conditions (e.g., Pykeet al., 1977). For predators that pursue rel-atively large prey, the most adaptive strat-egy is to specialize when preferred food isabundant, but become less specialized whenthat food becomes scarce (Ivlev, 1961,

Emlen, 1966 and MacArthur and Pianka,1966 in Roe, 1976; Pyke et al., 1977). Par-anemertes peregrina pursues its prey (Roe,1976) and prefers nereid polychaetes (Roe,1970). Studies of its diet in several studysites that differed in abundances of pre-ferred nereid food, showed that P. pere-grina was most selective in the area wherepreferred nereids were most abundant.Nereids comprised a higher proportion ofthe diet where they were most abundant,and more polychaete families were repre-sented in the nemertean diet where nereidswere less abundant (Roe, 1976, 1979).These studies indicate that P. peregrina isan optimal forager, emphasizing again theadaptive nature of nemertean feeding biol-ogy-

Effects on community structure. Some pred-ators have a large effect on communitystructure and diversity {e.g., Paine, 1966;Dayton, 1971). Predators that have thegreatest effect on their communities arethose that eat abundant, competitivelydominant prey (Paine, 1966) and those thatcause a moderate level of disturbance(Connell, 1978). Although such effects areless clear-cut in soft-sediment communities(Peterson, 1979; Dayton and Oliver, 1980)than in rocky intertidal communities(Paine, 1966) some evidence exists forcommunity structural changes as a conse-quence of predation (reviewed in Peterson,1979; Dayton and Oliver, 1980). On inter-tidal mud flats on San Juan Island, Wash-ington, P. peregrina prefers and eats pri-marily Platynereis bicanaliculata. The latteris not only one of the most abundant poly-chaetes on these mud flats, but its presencenegatively affects at least the polychaetesArmandia brevis and Axiothella rubrocincta(Woodin, 1974). By feeding mainly on thisnumerically and biologically importantpolychaete, P. peregrina has much potentialsecondary effect on community structure.Although questions of community effectwere not tested, Roe (1976) did show thatP. peregrina feeds on a substantial portionof the nereid population. At one mud flatthe nereids averaged 819/m2 and P. pere-grina was estimated to eat approximately38% of the population. At a similar areathe nereids averaged 3,240/m2 and the


nemerteans ate about 15% of the popula-tion. Although diversity indices were notcalculated nor other factors considered, thefirst community appeared qualitativelymore diverse, having more polychaetespecies than the second. It appears that P.peregrina may, therefore, by feeding heavilyon a prey that is important, affect structureand diversity of these soft-sediment com-munities.

From her studies on the biology ofTetrastemma melanocephalum, Bartsch (1973)was able to calculate the effect of this ne-mertean on a population of Corophium vol-utator. Applying a laboratory-determinedfeeding rate of 3 corophiids/da to a con-centration of 116 nemerteans/m2 on a par-ticular mud flat, she calculated that thepotential predation was over 10,000amphipods/m2/mo in a population esti-mated at 118,000 corophiids/m2. She alsosuggested (Bartsch, 1977) that T. melano-cephalum is not a serious food competitorof the more opportunistic feeder Nereis di-versicolor, whose tubes it occupies simulta-neously with impunity. Commito (1982)showed that Nereis virens regulates num-bers of C. volutator in Maine, and wherepopulation levels of C. volutator are low,other infaunal species show increasednumbers. Heavy predation by T. melano-cephalum of C. volutator could produce sim-ilar results in the C. volutator community.

Cerebratulus lacteus, in feeding on razorclams, feeds on larger prey than most ofthe macrophagous nemerteans. Its preda-tion has the added effect of making indi-viduals it misses more susceptible to epi-benthic predators and desiccation. In theirescape response the clams project much ofthe body above the surface, or may evenleave the burrow altogether (McDermott,19766). Schneider (1982) also found thatthe naticid snail Polinices duplicatus com-petes with Cerebratulus for the same prey.

Wickham's studies (1979a, 1980) of Car-cinonemertes errans have demonstratedadverse effects on its host Cancer magister.With a population averaging 43,000worms/crab near San Francisco, and eachworm eating about 70 crab embryos dur-ing the 30 day crab brooding season, theworms are consuming about 55% of the

total egg production of central Californiadungeness crabs. C. errans is obviously asignificant predator, and has been impli-cated in the collapse of the central Cali-fornia dungeness crab fishery.

Part of the adaptive feeding strategy forboth macrophagous and suctorial feedingtypes, especially among hoplonemerteans,is to utilize only a few species as food (theyspecialize or show preference althoughcapable of feeding on a greater variety).Such food is often abundant enough thatthe worm finds the prey by simple contactrather than having well-developed long-distance chemoreception. Since moststructural and macrophagous hoplonemer-teans do specialize on abundant prey, ifthey themselves are abundant, these wormshave high potential for affecting commu-nity structure through their feeding activ-ities. That nemerteans are important totheir communities as predators seemsobvious, but supporting data are meager.

Nemerteans as prey. Little informationexists indicating that nemerteans are eatenby other animals. Cerebratulus lacteus maybe consumed by Cyanea capillata (Coe,1943), Limulus polyphemus (Shuster, 1982)and the black-bellied plover, Pluvialissquatarola (Hicklin and Smith, 1979;Schneider and Harrington, 1981). Somenemerteans will feed on other nemerteans,e.g., Micrura purpurea has been observedfeeding on the related nemertean Micrurafasciolata (Cantell, 1975) and Emplectonemaneesii (Riches, 1893). Starved Lineus san-guineus will feed on Amphiporus lactifloreus(Jennings and Gibson, 1969). Small speci-mens oi Paranemertes peregrina are preyedupon by the cephalaspidian gastropodAglaja diomedea, and worms are sometimesconsumed by black-bellied plovers (Roe,1976, 1979). The gastropod Tricolia hasbeen observed to eat Carcinonemertes errans(Wickham, personal communication).

Nemerteans (rarely identified) occasion-ally occur in the diet of fishes, polychaetesand crustaceans (e.g., Feller et al., 1979;Jewett and Feder, 1980; Hacunda, 1981;Lasiak, 1982). Limited experimental stud-ies have shown, however, that nemerteanswere rejected by various species of pred-atory fishes and decapod crustaceans (Gib-


son, 1970; Kern, 1973; Prezant, 1979;Sundberg, 1979*; Prezant et al, 1981;McDermott, 1984). Kern (1971, 1973) sug-gested that toxins of the nemertean bodywall must serve as antipredatory adapta-tions. Such information is not in harmony,however, with the fact that C. lacteus andthe large South African heteronemertean,Polybrachiorhynchus dayi, are commonlyused, and often prized, as bait for sportfishing (Branch and Branch, 1981;McDermott, unpublished). These limiteddata suggest that nemerteans are moreimportant as predators than prey.

FUTURE STUDIES ON FEEDING BIOLOGY

Effects of nemerteans on communitystructure are almost completely unknown,often misinterpreted and often ignored.The studies discussed herein, however,indicate that nemerteans are potentiallyimportant predators and perhaps influen-tial scavengers in a variety of communities.Recent research, indicating the importantrole that Nipponnemertes pulcher may haveon the Haploops community in the Danish0resund, further emphasizes this point(McDermott, 1984).

Before the ecological relationships ofthese worms can be properly evaluated,more work is necessary in taxonomy. Inaddition, the feeding biology of many morespecies, especially with respect to quanti-tative information on trophic interactionsbetween nemerteans and prey, needs to beinvestigated, so that the patterns wedescribed can be tested and modified andhopefully become more predictive. Noattention has been given to the whole sub-order Polystilifera.

Although the suctorial nemerteans pres-ent greater difficulties for analysis, somequantitative studies have begun in the Zos-tera community (McDermott, unpub-lished). By investigating feeding rates inlaboratory situations and by determiningdensities of nemerteans and prey in nature,one can estimate the potential feedingimpact of suctorial species. Laboratory datacan be verified and enhanced by employingserological analysis on entire mud flat com-munities (Feller et al., 1979) and on theamorphous gut contents of freshly col-

lected specimens, as have been donerecently for Prostoma (Gisbon and Young,1976) and Paranemertes (Feller etal, 1979).

The role of nemerteans as prey is a vir-tually untouched area for study. Finally,the ecological role of prey or host metab-olites in attracting nemerteans, needs con-siderable attention.

ACKNOWLEDGMENTS

Financial assistance received from theAmerican Philosophical Society (JohnsonFund) and Franklin and Marshall College,and the many kindnesses provided by thepersonnel of the Marine Biological Labo-ratory, Helsingor, Denmark, the Univer-sity of Port Elizabeth, South Africa, andthe University of North Wales, Bangor, toJ. J. McDermott are greatly appreciated.Research on Carcinonemertes reportedherein by Roe (unpublished) was sup-ported in part by NOAA, National SeaGrant College Program, Department ofCommerce (Grant No. NA80AAD00120,Project No. R/F-75B).

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Food, Feeding Behavior and Feeding Ecology of Nemerteans