the role of hoplonemerteans in the ecology of seagrass communities

Hydrobiologia 156: l-11 (1988) P. Sundberg, R. Gibson & G. Berg (eds) Recent Advances in Nemertean Biology 0 Dr W. Junk Publishers, Dordrecht - Printed in the Netherlands

The role of hoplonemerteans in the ecology of seagrass communities

John J. McDermott Department of Biology, Franklin and Marshall College, Lancaster, PA 17604, USA

Key words: hoplonemerteans, seagrasses, Zostera, predation

Abstract

Seagrasses of the world harbor a rich and varied fauna, but a review of the literature revealed that little has been done to evaluate the ecological importance of nemerteans in such communities. Monostiliferous hoplonemerteans are common inhabitants of some seagrasses, e.g. eelgrass (Zostera), but generally they are seldom collected or identified or are apparently absent in other species such as shoalgrass (Halodule) or turtlegrass (Thalassia). Nineteen species of hoplonemerteans (four families) have been identified from eelgrass beds around the world; they exist mainly as epifauna, and all except two species are probably suctorial feeders. Some palaeonemerteans (2 species) and heteronemerteans (4 species) are also associated with eelgrass, but mainly as infauna. Suctorial nemerteans (4 species in 3 families) from eelgrass beds located along the mid- Atlantic coast of the United States feed in the laboratory on a variety of amphipod species that inhabit eelgrass. Tubicolous species (e.g. Corophium) seem to be preferred. Zygonemertes virescens feeds on nine species of amphipods belonging to six families, and is the only species to feed on isopods (3 species). Analyses of field studies on the occurrence of hoplonemerteans in eelgrass beds in Virginia and New Jersey, along with available information on the food habits of these worms, were used as a basis for demonstrating their potential importance as predators of peracarids in seagrass systems. More careful methods for collecting and identifying worms, continued studies on food preferences and rates of predation, and emphasis on the population dynamics of worms and prey, are recommended in order to evaluate the role of suctorial hoplonemerteans in the ecology of seagrasses.

Introduction

Seagrasses are important primary producers in coastal ecosystems throughout the world (Phillips, 1978; Thayer et al., 1975), they function as stabilizers of sediments, serve as bases for distinctive infaunal and epifaunal communties, and are nurseries for ju- venile fishes and decapod crustaceans (McRoy & Helfferich, 1977; Phillips & McRoy, 1980). Fishes and crustaceans along with birds are considered to be the major predators in many of these communities. Numerous studies, especially the more highly quantitative research of recent years carried out over a wide range of latitudes, have shown that the diversity, numbers and biomass of animals within

seagrass communities far exceed that of adjacent areas devoid of these vascular plants (Orth et al., 1984; Virnstein et al., 1984).

Nemertean worms, particularly the hoplonemerteans (Kirsteuer, 1963a; Marsh, 1973), are common inhabitants of seagrass beds, but a review of the literature reveals that they are seldom collected, and if collected, are usually not identified. Certainly the suctorial species are normally well represented in some of these grasses because of the usual abundance of prey, viz. amphipods and isopods (McDer- mott, 1976; McDermott & Roe, 1985).

It is the purpose of the present paper to review research dealing with nemerteans inhabiting seagrasses, to present additional information on

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their occurrence, abundance and food habits, to dis- cuss their potential importance as predators in the communities, and to suggest methods for a more careful evaluation of their role in such communities.

Materials and methods

Suctorial hoplonemerteans were collected and identified from eelgrass (Zostera marina L.) beds located in lagoons behind barrier beaches in Barnegat Bay and Little Egg Harbor, New Jersey, USA, in the summer and fall of 1976 and the summer of 1982, respectively. Some of the worms were subjected to feeding experiments similar to those reported previously from Virginia (McDermott, 1976). Eelgrass beds and their fauna were examined in February 1983 from two estuaries (Sundays River and Swartkops River) in southeastern South Africa. I will also present an analysis of suctorial hoplonemerteans and their potential prey from previously unpublished data eol- lected by G. A. Marsh in conjunction with his published study of eelgrass epifauna in Virginia (1973).

The seagrasses considered belong to the genera Halodule (shoalgrass), Phyllospadix (surfgrass), Thalassia (turtlegrass) and Zostera (eelgrass).

Results and discussion

Review of nemerteans found in seagrasses

Stoner et al. (1983) and Sheridan & Livingston (1983) recorded, but did not identify, nemerteans from grass beds of Halodule wrightii Ascherson located along the northwestern coast of Florida. Both studies employed cores and 0.5 mm screens for processing the samples, but no distinction was made between the epifauna and infauna. Stoner et al. reported a mean of 417 nemerteans/m2. Sheridan & Livingston recorded even larger numbers of nemerteans. Mean peak values (600- 1 000/m2) occurred from April to June with the lowest values (- 100/m2) from September to December; monthly mean ash-free dry weight (AFDW) values ranged from l-2 104 mg/m2. Although none of these worms was identified, it is probable that large non-

hoplonemerteans from the infauna were included in the tabulations. An abundance of amphipods (especially Ampelisca vadorum, Cymadusa compta, Grandidierella bonnieroides and Gammarus mucronatus) in the seagrass would provide adequate food for suctorial hoplonemerteans that may have been present. That amphipods are abundant in Halodule beds has been adequately corroborated by Nelson et al. (1982) and Stoner (1983).

Fauna associated with turtlegrass (Thalassia testudinum Konig) has received considerable recent attention by Heck (1977, 1979), Heck & Wetstone (1977), Kitting (1984), Lewis & Hollingworth (1982) Lewis & Stoner (1983) and Stoner (1983).,Employing cores and a 0.5 mm screen, only Lewis & Stoner recorded nemerteans (13 unidentified worms in 20 samples) in their samples. They, and others who used sieves with adequate mesh size, found a variety of amphipods to be common in turtle grass. A brief study of a Thalassia hemprichii community in India by Ansari (1984), who used cores and a 0.5 mm mesh seive, revealed a considerable diversity of species, but no nemerteans.

Stricker (1985) recently described a new suctorial hoplonemertean, Tetrastemma phyllospadicola, that lives on the basal parts or the inflorescences of surfgrass, Phyllospadixscouleri Hooker, located in- tertidally on San Juan Island, Washington. It may occur at densities > 50/m2. He observed this worm feeding on Hyale frequens in the field as well as in the laboratory. Two other amphipods, Paracal- liopiellapratti and Aoroides sp. were also consumed in the laboratory (Stricker & Cloney, 1982).

Studies on eelgrass beds (Zostera marina L.) in the United States emphasized their importance as habitats for fishes (Adams, 1976a, 1976b) and invertebrates (Heck & Orth, 1980;-Marsh, 1973; Nelson, 1979a, 1979b, 1980; Orth, 1971, 1973; Orth et al., 1984; van Montfrans et al., 1984). Only Marsh (1973) and Orth (1971) recorded and identified epifaunal and infaunal nemerteans, respectively, from Zostera beds located in Virginia. Brunberg (1964), Friederich (1935), Kirtsteuer (1963a, 1963b) and Reise (1985) identified and estimated the abundance of nemerteans living in European eelgrass, Z. noltii. Gray & Bell (1986) found no hoplonemerteans or amphipods in Australian eelgrass, Z. capricorni Ascherson,

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although their sampling procedures were compatible with procuring these small animals. I did not find nemerteans in beds of 2. capensis Setchell located in estuaries of southeastern South Africa. It was ob- vious to me, even before I carefully examined the eelgrass in the laboratory, that there would be few if any suctorial hoplonemerteans because of the great pau- city of suitable prey, i.e. amphipods and isopods.

Nemerteans and their prey in Zostera beds

As noted above, nemerteans have been identified mainly from Zostera communities. Species collected in North America and Europe are listed in Table 1. Z. marina and presumably Z. noltii (sometimes mixed with Z. marina) are found in these two areas, respectively. Nineteen (76%) of the species are

Table I. Nemerteans reported in the literature as inhabitants of the eelgrass (Zosteru) community.

Species References*

Anopla Palaeonemertea

Cephalothricidae Cephalothrix rufifrons (Johnston, 1837)

Tubulanidae Tubulanus pellucidus (Coe, 1895)

Heteronemertea Lineidae

Cerebratulus lacteus (Leidy, 1851) Lineus ruber (Miiller, 1774) Lineus viridis (Miiller, 1774) Micrura fasciolata Ehrenberg, 1831

Enopla Hoplonemertea

Amphiporidae Amphiporus biocularus McIntosh, 1837 - 74 Amphiporus caecus Verrill, 1892 Amphiporus griseus (Stimpson, 1857) Amphiporus lactifloreus (Johnston, 1837) Amphiporus ochraceus (Verrill, 1873) Amphiporus rubropunctus (McGaul, 1963) Zygonemertes virescens (Verrill, 1879)

Emplectonematidae Emplectonema echinoderma (Marion, 1873) Nemertopsis fhzvida (McIntosh, 1873 - 74)

Prosorhochmidae Oerstedia dorsalis (Abildgaard, 1806) Oerstediella tenuicollis Kirsteuer, 1963

Tetrastemmatidae Prostomatelia arenicola Friedrich, 1935 Tetrastemma candidum (Miiller, 1774) Tetrastemma coronatum (Quatrefages, 1846) Tetrastemma elegans (Girard, 1852) Tetrastemma jeani (McCaul, 1963) Tetrastemma melanocephalum (Johnston, 1837) Tetrastemma vermiculus (Quatrefages, 1846) Tetrustemma vittatum (Verrill, 1874)

4

6. 10

10

1, 3 11 1

8, 10 6 2 1, 3, 11 6, 8, 10

7, 8 6, 7, 8, 10

4 4

3, 4, 5, 7, 8, 9 5

11

3, 5, 7 4, 5 2, 6, 7, 8 6, 7 1, 3 6, 7 2

*References: 1. Brunberg, 1964; 2. Coe, 1943; 3. Friedrich, 1935; 4. Gibson, 1982; 5. Kirsteuer, 1963b; 6. March, 1973; 7. McCaul, 1963; 8. McDermott, 1976, present study or general observations; 9. McDermott & Snyder, 1987; 10. Orth, 1971; 11. Reise, 1985.

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hoplonemerteans, existing usually as epifauna, whereas the palaeonemerteans and heteronemerteans are generally infaunal. All of the hoplonemerteans, except members of the Emplectonematidae, are probably suctorial feeders (McDermott & Roe, 1985).

One of the most comprehensive studies of the Zostera epifaunal community was that of Marsh (1973) carried out in the York River estuary of Vir- ginia. His sampling techniques (plastic bag and a 0.5 mm sieve) were conductive to recovering most hoplonemerteans and small peracarid crustaceans. He identified six species of hoplonemerteans and one palaeonemertean (Table l), and recorded the total numbers and incidence of each species. Only Zygonemertes virescens and Tetrastemma elegans were common, each making up - 0.2% of all fauna collected; these occurred in 25 and 31 of the 48 samples, respectively. My non-quantitative observations on a different Zostera bed within the same estuarine system showed dominance of the same species (McDermott, 1976). More recent, non-quantitative studies of eelgrass beds in coastal New Jersey also revealed the dominance of these two species. It was surprising that neither Marsh (1973) nor I recorded Oerstedia dorsalis in the Virginia eelgrass, because McCaul (1963) found this species in eelgrass from the same estuary. Being such a minute species and contracting greatly when preserved, specimens be- come quite nondescript and could easily be over- looked or washed through the 0.5 mm sieve used by Marsh. If it were present during my studies, however, I should have detected it with the procedures I used for collecting living worms (Kirsteuer, 1967). These techniques were effective, nevertheless, in recovering Oerstedia from eelgrass collected in 1976 and 1982 in New Jersey waters (McDermott & Snyder, 1987).

In order that I might establish some base-lines for the incidence and abundance of hoplonemerteans in Zostera beds, Professor Marsh provided me with unpublished data from which I could calculate the numbers of nemerteans or nemertean prey (amphipods and isopods) per m2 of bottom for the period Feb. -Dec. 1968. All of my calculations (% values) are the result of combining data from Marsh’s (1973) three adjacent collecting stations.

Figure IA shows that the peaks for both 7: elegans

150 (A) NEMERTEANS

100

X

I I I I I I I I I I I I

F A J A 0 D

MONTHS

Fig. 1. The occurrence of selected epifaunal nemerteans and peracarid crustaceans in an eelgrass (Zosteru marina) community from the York River estuary, Virginia, 1968, based on unpublished information from the study of Marsh (1973). Each point is the mean of three samples taken at different depths; two collections were made in March and June. (A) Tetrastemma elegans (solid line) and Zygonemertes virescens (dashed line); (B) common tubicolous amphipods Ampithoe longimana (solid line), Cymadusa compta (dashed line) and the common isopod Erich- sonella attenuata (dotted line).

and Z. virescens in the York River estuary occurred in June (maximum values were 157/m2 and 175/m2, respectively). The biomass of eelgrass (g dry wt/m2) at all three. of Marsh’s stations built up towards peaks in June and then declined in the fall, thus posi- tively correlating with the abundances of these two worms. The correlation coefficients for Zostera bi-

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omass per m2 vs. numbers of 7: elegans and 2. virescens per m2 are 0.82 and 0.80, respectively. Am- phiporus ochraceus was the only other species of sig- nificance; it too peaked in June (maximum 20/m2), but occurred only in April, May and June. A. caecus was found only in July at one of the three stations (8/m2), i? jeani only in May and June (maximum 4/m2), and one specimen of 7: vermiculus was ob- tained in January.

The eelgrass in Virginia yielded 23 species of amphipods (18.5% of all fauna by numbers) and 4 species of isopods (16.7%) (Marsh, 1973). Five species

of amphipods each represented > 1% of the fauna (Ampithoe kmgimana 6.8%, EkzsmOpus kzevis (= E. pocillimanus) 4.69’0, CymQdusQ compta 3.1%, CQprellQpenQntis 2.1% and Gammarus mucronatus 1.3%) as did two isopods (PQrQcerceis candata 10.4% and Erichsonella Qttenuata 6.0%). We have shown in laboratory experiments that all of the above mentioned amphipods and E. QttenuQtQ, as well as the other isopods found in this same study and in New Jersey serve as prey for one or more of the seagrass hoplonemerteans (Table 2). Unfor- tunately, the sphaeromid isopod PQrQcerceis was

Table 2. Species of amphipods and isopods, found in eelgrass (Zostera marina) beds, that have been tested in laboratory experiments as prey for four suctorial hoplonemertean inhabitants of eelgrass.

Amphipods and isopods

Species Species type

Hoplonemertean species

Amphiporidae

Amphiporus Zygonemertes ochraceus virescens

Tetrastemmatidae Prosorhochmidae Tetrastemma Oerstedia elegans dorsalis

Amphipoda Ampeliscidae

Ampelisca vadorum Ampithoidae

Ampithoe longimana Ampithoe valida Cymadusa compta

Caprellidae Caprella penantis

Corophiidae Cerapus tubularis Corophium acherusicum Corophium simile Corophium tuberculatum

Gammaridae Gammarus mucronatus

Melitidae Elasmopus levis Melita nitida

Stenothoidae Stenothoe gallensis

Isopoda Idotheidae

Edotea triloba Erichsonella attenuata Idotea baltica

E, I* X

E E E

F

E

E, 1 X

E, 1 E, I

F

F F

F?

X X X

X

0 X

X

X X

F, B X F X F 0 X

x * X

X

0

0 0 0 0 0

Data are not based on equal numbers of prey-predator encounters. X=consumed, O=tested but not consumed. Prey species type: I=infaunal tube builder; E=epifaunal tube builder; F=epifaunal free living: B=benthic (not tubicolous). Sources: McDermott (1976 and the present study), McDermott & Snyder (1987). *Mainly infaunal.

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never tested in feeding experiments. Figure 1B shows the seasonal distribution of three

representative peracarids from the Virginia eelgrass. The occurrence of these species was similar to all others, in that the main peaks occurred after June and decreased after October. The decrease in biomass of Zostera which began in June is negatively correlated with the occurrence of amphipods, unlike the positive correlation seen with the abundance of nemerteans.

Many questions arise as to the interaction of these predators and prey in this Zostera community. Why were numbers of nemerteans and amphipods correlated differently with the eelgrass biomass? Were these at all related? Was nemertean predation a fac- tor in the occurrence of relatively small numbers of amphipods during the spring months? If amphipods in eelgrass are breeding mainly in the spring months (Nelson, 1980), are they more susceptible then to predation, or are the recently released young more susceptible, so that this might be the season when nemerteans have the greatest effect on the dynamics of susceptible populations?

We know (from laboratory studies) that certain species of amphipods from eelgrass are preferred by suctorial nemerteans (McDermott, 1976; McDer- mott & Snyder, 1987). Corophium acherusicum, a tubicolous species, was notable in this regard. Marsh (1973) showed that C. acherusicum was only the eight most abundant amphipod in his year-long study (306 collected compared to > 10500 Ampithoe longimana), making up 0.2% of the fauna, and oc- curring in < 50% of the samples. It was found spo- radically and in relatively small numbers throughout the study period, with a relative void during the nemertean peak in June, and a slight increase in the fall. We might ask, was this distribution pattern in- dicative of the Corophium population being more influenced by nemerteans than other less-preferred amphipod populations? Bartsch (1973) has shown that Corophium volutator is a potentially very important prey for Tetrastemma melanocephalum in non-seagrass areas, with the potential for killing > 10000 corophiids/m2/month.

The amphipods tested in the laboratory as prey for hoplonemerteans (Table 2) belong to seven families, and species from all families except one (Stenothoi-

dae) were consumed by at least one species of worm. Of the amphipods belonging to the other six families, some species are tubicolous and others are non- tubicolous. The Ampeliscidae, Ampithoidae and Corophiidae contain seven tubicolous species that were consumed, and the others (4 species) are non- tubicolous.

Table 3 summarizes feeding experiments with Zygonemertes carried out in New Jersey subsequent to my studies in Virginia (McDermott, 1976). This study added to the list of potential natural prey the tubicolous species Ampelisca vadorum and Cymadusa compta, and the non-tubicolous species Elasmopus levis. It also confirmed that Corophium acherusicum was a preferred species. Furthermore two other isopods commonly found on eelgrass, Edotea triloba and Idotea baltica, were added to the list of prey consumed by this worm. An experiment was performed in 1982 to determine if starvation of Z. virescens might induce predation on Idotea. Specimens of the isopod were placed individually with eight starved worms (starved for approximately one month and kept at 10 “C; x length 12 mm) and eight worms (x length 15 mm) collected at the start of the experiment. The pairs were checked several

Table 3. Summary of feeding tests with 160 Zygonemertes virescens, involving one worm with one specimen of prey in each test; based on laboratory observations made in 1976 and 1982 with worms and prey collected from eelgrass; worms ranged in length from 9-40 mm.

Species of prey’ Number presented

Number killed (%)

Amphipoda Ampelisca vadorum * 32 Ampithoe longimana 9 Cerapus tubularis 2 Corophium acherusicum 68 Cymadusa compta* 22 Eiasmopus levis* 3 Gammarus mucronatus 26

Isopoda Edotea triloba* 5 Erichsonella attenuata 27 Idotea baltica* 64

8 (25.0) 3 (33.3) 0 ( 0.0)

15 (22.1) 1 ( 4.5) 1 (33.5) 2 ( 7.1)

1 (20.0) 3 (11.1)

15 (23.4)

*New prey record for Zygonemertes.

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times during a 35 h period, and killed isopods were replaced with new ones. The 26 isopods used during this period had a x length of 3.9 mm (range 2.6-5.1 mm). Starved worms killed 57.1% of the isopods (8 of 14) and the fresh worms killed 41.7% (5 of 12). The difference is not significant (Contin- gency x2 = 0.155, P = >0.5).

In tests with 7: elegans, eleven worms were presented with 15 Corophium acherusicum and 6 (40%) were consumed, thus confirming similar observations with Virginia worms and prey (McDer- mott, 1976). Lastly, we showed that Oerstedia dorsalis also readily consumed C. acherusicum as well as the tubicolous species A. vadorum (McDermott & Snyder, 1987).

All evidence to date then indicates that the tubicolous amphipods of eelgrass may be the preferred, or merely the more susceptible prey of suctorial worms. The reasons for this remain obscure, but may be related to the more sedentary habits of the tubicolous species which make them easier to stalk than the swifter moving free-roaming species. The problem is certainly adaptable to laboratory ex- perimentation.

It is difficult to categorize some amphipods as either epifaunal or infaunal on eelgrass. Ampelisca vadorum, for example, may be found in both locations, but probably is more prevalent infaunally at the base of eelgrass as I have found in New Jersey and Orth (1973) has shown in Virginia. The same way be said for Corophium acherusicum, and although certainly not limited to eelgrass it attaches its tube to the blades as well as the shallow roots of eelgrass (Nelson, 1980). The isopod Edotea triloba also exists in both locations (Marsh, 1973; Orth, 1973). The suctorial hoplonemerteans of eelgrass seem to prefer the leaves as a habitat, but they also live at the base of the grass along with the peracarids mentioned above.

There is little quantitative information in the literature on the abundance of hoplonemerteans in eelgrass with which to compare the present data. Bar- nard (1970) reported that nemerteans (unidentified, but likely hoplonemerteans) amounted to lOUrn or 10% of the total individuals from Zostera in Baja California. Many species of amphipods were also found there, including Corophium acherusicum

(112/m2). R. W. Virnstein (pers. comm.) reported that unidentified nemerteans in Zostera beds of northeastern Florida ranged from 20 to 70/m2. Both Barnard’s and Virnstein’s figures for these worms (if they are mostly hoplonemerteans) are generally lower than the data from Virginia (Fig. lA), but since seasonal components are lacking it is difficult to make meaningful comparisons.

Reise (1985, Table 5.3) found the two hoplonemerteans Amphiporus lactifloreus (epifaunal) and Pro- tomatella arenicola (an interstitial form) in Zostera beds along the North Sea at densities of 25 and 6/m2, respectively. Lineus viridis was recorded at 88/m2. In benthic enclosure experiments, Reise detected A. lactij7oreus at 47/m2 and 147/m2 in the control versus the caged condition, respectively, in 1974, and 13/m2 versus 53/m2 in 1978. In the same experiments, L. viridis was found at densities of 20/m2 and loo/m2 in 1974 and 33/m2 and 67/m2 in 1978. Asmus & Asmus (1985), working in the same location as Reise, showed that A. lactifloreus made up only 0.03% of the total biomass (g AFDW/m2/year), and L. viridis only 0.07%. This particular seagrass location had a scarcity of amphipods, prey that are required by at least Amphiporus (McDermott & Roe, 1985).

Estimated interaction of nemerteans and prey in eelgrass

Combining the meager information available on the rate of amphipod consumption by the suctorial hoplonemerteans of eelgrass (McDermott, 1976) with the quantitative data on amphipods living in eelgrass from the York River estuary of Virginia, it is possible to suggest some potential effects of nemertean predation. Table 4 shows the estimated monthly predation of amphipods/m2 of eelgrass based on two calculations: (A) the A number of each species of nemertean/m2 for eleven monthly samples; (B) the x maximum number of each nemertean/m2 calculated from the highest monthly values. Employing A, the mean number of amphipods consumed/m2/year would be > 50000. During the peak of nemertean abundance in June (Fig. lA, Ta- ble 4B), these nemerteans may be capable of con-

8

Table 4. Estimated predation of amphipods by the three most common suctorial hoplonemerteans found in eelgrass beds, based on rates of predation on Corophium determined in the laboratory (McDermott, 1976) and previously unpublished information on the incidence of worms in eelgrass from Marsh’s (1973) study in the York River estuary, Virginia. Predation rate for each species is estimated at 3 prey/d.

it values Nemertean species Totals

Amphiporus ochraceud Tetrastemma elegans Zygonemertes virescens

A.2 No. worms/m2 1 18 20 39 No consumed/m2/month prey 90 1620 2700 4410

B.3 Max. no. worms/m2 11 88 84 183 No consumed/m2/month prey 990 7920 7560 16470

‘Experimental data on rate of predation not available, but based on information for other two species, a value of 3 amphipods/d is assigned.

2Based on eleven monthly samples. 3Based on samples from one month (June) when maximum numbers of worms occurred.

suming > 16000 amphipods/m2. In this particular community, however, the greatest amphipod abundance occurred after June (Fig. 1B). Nevertheless, we may ask the question - what effect did the peak of worms in June have on the subsequent buildup of each vulnerable amphipod population? The consumption of adult females or ovigerous amphipods, if they were present in the early summer, should have had some measurable effects on each population. Although developing embryos on an ovigerous amphipod are not consumed by some suctorial nemerteans (McDermott, 1976,1984) it is unlikely that they would continue development to hatching while at- tached to an evacuated exoskeleton. On the other hand, if females are carrying hatched young, it is likely that some of these will also be consumed along with the mother (McDermott, 1976).

One might argue that the daily feeding rates used in these calculations (derived from less than full day laboratory experiments with starved worms) may be higher than would be expected under natural conditions. Observations of Nipponnemertes p&her feeding on Haploops spp., for example, showed that after the first 24 hours the rate of consumption declined to - 25% or less of the original rate (McDermott, 1984). This reduction probably reflects a degree of satiation, and may be more typi- cal of natural conditions. If, for the sake of further discussion, we use this 25% value to reduce the experimental feeding rates for each species in Table 4

to 0.75 prey/d, the potential number of amphipods consumed would be reduced to a mean monthly rate of - 1 000/m2, and 4000/m2 during the June peak in nemertean abundance.

I have calculated the X number of amphipods/m2 in the Virginia eelgrass, based mainly on six of the most numerous species, which in turn are known to serve as nemertean prey in the laboratory (Ampithoe longimana, Cymadusa compta, Elasmopus levis, Gammarus mucronatus, Caprella penantis and Corophium acherusicum). Data for the whole year show - 2 000 amphipods/m2, and potentially > 8000/m2 during peak periods (e.g. late summer and fall, Fig. 1B). Therefore, the calculated annual mean consumption of 1000 amphipods/m2/month is one-half of the mean standing crop. Likewise, during peak periods of amphipod abundance, when the standing crop averages > 8000/m2, the potential consumption by nemerteans would also be about one-half. These calculations tell us nothing about the dynamics of the pre-predator interaction in this situation. The reproductive potentials of prey and predator are needed to arrive at production esti- mates, and there is virtually nothing known of such potentials for the hoplonemerteans in question. More is known about production in amphipods. Those living in eelgrass and other seagrasses may produce several broods a year (Fredette & Diaz, 1986; Nelson, 1980; Stoner, 1983).

It has also been demonstrated that amphipods in-

9

habiting seagrasses are continually subjected to predation, particularly by fishes and decapod crustaceans (Kikuchi, 1966; Kikuchi & Peres, 1977). Nelson’s (1979a, 1979b) experimental work with amphipods from eelgrass communities of North Caroli- na has demonstrated that certain fishes (e.g. the pin fish, Lagodon rhomboides (L.)) may be important in determining the relative abundance of different species of amphipods, and may effect seasonal changes in species diversity because of their selective feeding. At times when fishes are not abundant, decapods, such as the grass shrimp Palaemonetes vulgaris, may exert similar influences. Stoner (1983), comparing the ecology of amphipod species in seagrass beds composed of Thalassia, Halodule and Syringodium, concluded that “relationships among plants, prey, and predators are highly complex and should be studied concurrently, particularly where all the components demonstrate temporal and spatial variation in abundance”. This, of course is the message of the present discussion. Hoplonemerte- ans must be evaluated as predators in seagrass systems.

Evaluating the role of nemerteans in seagrass communities

Suctorial hoplonemerteans apparently dominate other types of nemerteans in seagrasses (Table 1). The first step in a program designed to elaborate their role in such communities is to correctly identify the species present and to determine their relative abundances. Seagrasses should be collected in plastic bags rather than mesh bags. The latter should not be used because young worms and the adults of very small species such as Oerstedia dorsalis may escape through the mesh. In the laboratory each sample should be poured into a suitable container and al- lowed to gradually stagnate, whereupon worms will generally move to the surface of the water around the sides of the container, from which they may be har- vested (Kirsteuer, 1967). All of the worms in a sample may not emerge by this method, but generally the relative abundance of the species may be established.

Investigators must carefully record characteristics of the living worms, particularly color, color pat-

terns and stylet apparatus, so that identifications can be made with the use of books such as Gibson’s (1982), which is particularly designed for the non- specialist. Since eventually the absolute number of worms per unit area has to be determined, it will be necessary to sort the contents of preserved samples. Identification of preserved worms is a problem. In this regard, species that were identified in the living condition should be preserved with the same preser- vative used in quantitative sampling in order to de- tect preservation characteristics that may aid in identification. Shapes peculiar to contracted worms of a particular species, the amount of color or the re- mains of certain patterns may be constant enough to be used for identification purposes.

I recommend the procedures used by Marsh (1973) for determining the numbers and biomass of epifauna on eelgrass. He ascertained the standing crop biomass (dry wt) of Zostera per m2 for each month of his study period. Smaller study samples of eelgrass collected at the same time, from which the fauna had been extracted, were also weighed and compared with the standing crop biomass. The numbers of epifauna/m2 is calculated from this comparison.

Determining the ecological role of suctorial nemerteans presents a problem unique to the group, i.e. the prey making up the gut contents of freshly collected worms cannot be identified in the usual microscopic manner. The food of macrophagous monostiliferous hoplonemerteans such as Paranemertesperegrina for example, is easily determined by examining the intestinal contents or feces of freshly collected or preserved worms (Roe, 1970, 1976, 1979). Hard secreted structures such as the se- tae and jaws of the various polychaetes in the diet of Paranemertes allow for specific identification even in well-digested material. With suctorial nemerteans it is necessary to conduct feeding experiments in the laboratory with a variety of potential prey found in the seagrass community. From such experiments it is possible to learn which species of prey are accepted, which are preferred, and the rate of consumption of each. It is evident, however, that it is still not possible to determine the percentage of each type of prey naturally ingested by suctorial forms as Roe (1976) has done with Paranemertes. The immunological techniques employed in recent years for

10

the identification of amorphous gut contents, while laborious, may eventually be used to help solve this basic problem (Davies, 1969; ‘Davies et al., 1978, 1979; Feller et al., 1979; Feller & Gallagher, 1982; Feller, 1986; Gibson & Young, 1976).

Combining the necessary laboratory observations with the usual field sampling techniques, and determining the reproductive potentials of predators and prey, it should be possible to eventually gain an ap- preciation of the role played by hoplonemerteans in seagrass communities. Perhaps we may be able to de- fine their role in seagrasses with some of the preci- sion determined by Roe (1970, 1976, 1979) for Paranemertes peregrina in the intertidal regions of the Pacific northwest.

Acknowledgements

I am indebted to J. B. Durand, Director of the Rut- gers University Marine Field Station, Tuckerton, New Jersey, and to A. McLachlan, Department of Zoology, University of Port Elizabeth, South Afri- ca, for providing research facilities. I thank J. R. Orchardo, R. L. Snyder and T. Wooldridge for as- sistance in the field, and Franklin and Marshall Col- lege for financial support. I am particularly grateful to G. A. Marsh, Florida Atlantic University, Boca Raton, Florida, for providing me with unpublished information on the epifauna of eelgrass beds in Vir- ginia. Presentation of this paper was supported by NSF grant #BSR-8603561.

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