Predation on Bivalve Veligers by Polychaete Larvae

7 Pages·1998·2.9 MB·English

by  K B Johnson

Reference: Biol. Bull. 194: 297-303. (June. 1998)
Predation on Bivalve Veligers by Polychaete Larvae
KEVIN B. JOHNSON'* AND LAURA A, BRINK"
' Oregon Institute ofMarine Biology, P.O. Box 5389. Charleston, Oregon 97420; and ' Horn Point
Laboratory, Cambridge, Maryland 21613
Abstract. Polychaete larvae from several families are in the guts of the larval polychaete Magelona papilli-
thought to be natural predators upon planktonic bivalve cornis (Magelonidae). Other biologists have also ob-
larvae. However, little direct evidence of interactions be- served bivalve veligers within the guts of field-caught
tweenthesepredators andprey isavailable. Weconducted Magelona sp. larvae (Thorson, 1946; Smidt, 1951; Kuhl,
predator-prey experiments on laboratory roller tables for 1974; Wilson, 1982). Lebour (1922). Smidt (1951), and
five putative predatory polychaete larvae, representing Kuhl (1974) recorded only bivalve larvae as prey for
fourfamilies (metatroch-less larvaeofthe Polynoidae and magelonids, but Thorson (1946) and Wilson (1982) ob-
metatrochophore larvae of the Spionidae, the Mageloni- served that M. papillicornis also consumed other plank-
dae, and the Phyllodocidae). D-hinge veliger larvae of tonic organisms. In spite of these many observations and
the oyster Crassostrea gigas were offered as prey. Preda- thegeneral impressionthatlarvalpolychaetesofthegenus
tion was monitored over a range ofprey densities and in Magelona are specialist predators of bivalve veligers
the presence and absence of background plankton. (e.g., Todd et al. 1996), a natural predator-prey relation-
"Background plankton" are any naturally occurring ship between larval polychaetes and bivalve larvae has
plankton assemblages found in whole, unfiltered seawater yettobe definitively shown. There are problems alsowith
at ambient concentrations. For all polychaete larvae ex- the anecdotal nature of some past observations on wild-
amined, when natural C. gigas densities and background caught plankton: when planktonic predators and prey are
plankton were used, no predation was observed. Magelo- concentrated in the cod-end of a plankton net for several
nids and phyllodocids did not consume any C. gigas lar- minutes or more, as is usually the case when plankton
vae, regardless of conditions. Polynoid and spionid samplesarebeingcollected, it isnotpossibletodifferenti-
trochophores consumed C. gigas veligers at both the ate natural predation from that occurring in the cod-end
"natural" and unnaturally high prey densities in filtered under very abnormal conditions, which we refer to as
seawater.Theadditionofbackgroundplanktoneliminated "artifactual predation."
the predation at all natural prey densities and significantly Predation upon bivalve veligers by polychaete trocho-
reduced the predation observed at high prey densities. phores (metatroch-less trochophores and metatrocho-
phores) has also been observed for representatives of
Introduction other polychaete families, including the Polynoidae (Yo-
kouchi, 1991), the Nephtyidae (Mileikovski, 1959; Yo-
Predation in the plankton is a source of mortality that kouchi, 1991), the Phyllodocidae (Yokouchi, 1991), and
may control the presence and abundance oftheplanktonic the Spionidae (Daro and Polk, 1973; K. B. Johnson, un-
larvae of benthic marine invertebrates (Thorson, 1950). publ. data). These observations of predation are remark-
Observations of predation upon meroplanktonic inverte- able in two ways. First, it is very seldom that a larva has
brate larvae are recorded from as far back as the 1920s. been observed to be the primary food consumed by a
For example, Lebour (1922) noted bivalve veliger larvae planktonic suspension-feeding predator that consumes its
prey one individual at atime. Unlike cases in which pred-
ators {e.g.. some scyphozoans and clupeid fish) indiscrim-
R*eTcoeiwvehdo2m9cJourlryes1p9o9n7d;eanccceepstheodul1d2bMearadcdhre1s9s9e8d.. E-mail; kjohnson inately feed on many planktonic prey, consistent observa-
@oimb.uoregon.edu tions of a given prey item in the gut of such a "single-
297
298 K. B. JOHNSON AND L. A^ BRINK
particle predator" may indicate a strongly specific preda- Using a 100-/./m-mesh plankton net and an on-board elec-
tor-prey relationship and provide insight into predatorbe- tric centrifugal pump, samples were collected for 3 min
havior. Second, bivalve veligers consumed by polychaete at 227.1 1 min"', for a final sample volume of approxi-
larvae are often surprisingly large relative to the preda- mately 680 liters. Between 3 and 5 sampling depths were
tor's body diameter and apparent mouth size (see Fig. 1). chosen at each station, depending upon the station depth.
Examining the mechanism underlying particle inges- After pumping was complete, samples were rinsed from
tion by polychaete larvae, Phillips and Fernet ( 1996) fed the cod-ends and preserved with 10% CaCOj-buffered
larvae of the polychaetes Serpula vennlcularis (Serpuli- formalin for later sorting. Plankton samples were sorted
dae) andAictorwe vittata (Polynoidae) polystyrene beads under a dissection microscope with polarized light to aid
and plankton at a range of sizes. S. vermiciilaris larvae in locating bivalves. For a more detailed description of
were apparently not equipped to handle food particles collection and sorting methods, see Brink (1997).
greater than 12 ^m in diameter (Phillips and Pernet. Bivalve veligers were tallied when observed in the guts
1996).A. vittata larvae less than 100 /jm in diameterwere of predatory polychaete larvae. The total density of bi-
observed to ingest large particles (polystyrene beads and valve larvae and polychaete larvae was determined for
phytoplankton) up to 60 /jm in diameter, a common size each sample in which bivalve predation was observed.
for small bivalve larvae. The larvae ofA. vittata, a scale- These densities were considered when deciding upon
worm, likely include relatively large particles in their predator and prey densities to be used in the laboratory
natural diet. Does this diet include larval bivalves? Bi- experiments described below.
valve veligers have been observed in the guts of field-
caught polynoid larvae (Yokouchi, 1991). Like the larvae Culture ofpredators andprey
ofMagelona sp., the larvae ofpolynoids and several other Adult specimens of the scaleworm Arctonoe vittata,
polychaete families maybe natural predators uponbivalve commensal with the keyhole limpetDiodora aspera, were
veligers. collected with their host from the west shore rocky inter-
We examined the potential predator-prey relationship tidal of San Juan Island, Washington. Individuals of A.
between several larval polychaetes and bivalve veliger vittata were spawned and larvae were cultured using the
larvae. The relationship was examined using a combina- methods described by Phillips and Pemet (1996) with the
tion of field observations (plankton samples) and labora- additionofCoscinodiscus radiatus (CCMP310) as afood
tory experiments. In plankton samples, trochophores rep- source. Fertilized eggs were cultured in 600-ml beakers
resenting several families were observed with bivalve ve- at densities of —5001"'. Larvae approximately 21 days
ligers in their guts. More important for this study, old were used as predators in experiments.
however, field samples helped determine densities used All other larval polychaetes used as predators were
inlaboratory experiments. Densities ofpredators andprey collected at high tide near the mouth of Coos Bay, Ore-
reflected field densities from samples in which predation gon, by slowly towing a 150-/im-mesh plankton net
was observed. Laboratory experiments used five types of equipped with a large, blind cod-end (Reeve, 1981). Pi-
larval polychaetes as predators: A. vittata (metatroch-less pettes (3-mm-bore) were used to immediately remove
trochophore, Polynoidae), Magelona sp. (metatrocho- predators from the plankton sample and isolate them in
phore, Magelonidae), and unidentified species from the 250 ml of filtered seawater. Experiments began within
families Polynoidae (metatroch-lesstrochophore), Spioni-
6 hours of predator collection.
dae (metatrochophore), and Phyllodocidae (metatrocho- D-hinge veligers of the oyster Crassostrea gigas. 5 to
phore). D-hinge veliger larvae of the oyster Crassostrea 10 days old (greatest linear dimension 70-90 ^m), were
gigas were offered as prey. Experiments were conducted used as prey in all laboratory experiments. The oyster
at two prey densities and in the presence or absence of larvae were obtained from Whiskey Creek Oyster Farms,
background plankton. The presence ofbackground plank- Tillamook, Oregon, and maintained in 1-gallon jars on a
ton (by which we mean naturally occurring phyto- and diet of Isochrysis galbana and Rhodomonas sp.
zooplankton ever-present in the field but often excluded
in laboratory experiments) is potentially important be- Roller table experiments
cause it may act as a substitute food for predators or
obscure prey from detection (Johnson and Shanks, 1997). One laboratory experiment, with four treatments, was
conducted foreachofthe five species oflarval polychaete
Materials and Methods (Table I). Two densities ofprey were used. The first prey
density (Treatments A and B) was designed to approxi-
Field obser\ations mate natural fieldconcentrations andwas set at 33 bivalve
During August 1994, plankton samples were collected larvae 1' on the basis of the highest value we found in
from within 10 km ofthe shore of Duck, North Carolina. the literature (Carriker. 1951). The second prey density
PREDATION ON BIVALVE VELIGERS 299
Table I
Mean numbero/Crassostrea gigas veligerlarvae in individualguts ofpredatory lan-alpolychaeles according to treatment (prey density and the
presence orabsence ofbackgroundplankton) ± the 95% confidence interval
Treatment
300 K. B. JOHNSON AND L. A. BRINK
these metatroch-less trochophores was often not possible, Discussion
but the following families may have been represented:
Phyllodocidae. Hesionidae. early Nephtyidae. Polynoi- None of the larval polychaete species we tested con-
dae, and Chrysopetalidae. Ofthose metatrochophores that sumed any bivalve larvae when laboratory conditions
had bivalves, 3 were Magelona sp. with 1 bivalve each. were the closest to natural {i.e.. near-natural prey density
The last 2 metatrochophores were likelyeitherphyllodoc- with background plankton present; Table I, Treatment
ids or hesionids; one (380 /vm in length) had 2 bivalves B). We did observe predation in the treatments that used
in its gut, while the other (368 ^m in length) had 1 bi- unnatural prey density or filtered seawater. One explana-
valve. In addition, a single metatroch-less polychaete tion for the lack of predation in Treatment B could be
larva was observed with a gastropod veliger in its gut. that larval polychaetes are notnatural predators ofbivalve
For the 18 samples in which bivalves were observed veliger larvae. In that case, previously published observa-
in polychaete larva guts, densities ranged from42 to 1 193 tions ofbivalve veligers in the guts of larval polychaetes
polychaete larvae sample ' (x = 277.2, SD = 324.3). The might be an artifact of the concentration of predators
range of larval bivalve densities in these same samples and prey in cod-end buckets during plankton tows. Such
was from 419 to 1949 larvae sample"' (x = 1217.6, SD artificial conditions can alter the behavior of predators
= 494.2). Therefore, at least 42 trochophores and 419 and prey and increase the probability of encounters be-
bivalve larvae were concentrated together in the cod-end tween them, resulting in unnatural ingestion. Cod-end
bucket (about 200 ml of seawater) when a sample was predation is well documented for other planktonic preda-
complete. tors, such aschaetognaths (Feigenbaum andMaris, 1984),
and may mislead observers about predator-prey relation-
ships.
Roller table experiments Low encounter rates might also explain the absence of
Table 1 summarizesthe resultsoftherollertableexperi- predation under the most natural laboratory conditions
ments. For the larvae of Magelona sp. and phyllodocid used in this study. Predators and prey may simply not
A, predation on bivalve veligers was not observed in the encounter one another during the experiment. Natural
laboratory under any conditions. The larvae ofArctonoe prey densities, which tend to be relatively low, and the
vittata, polynoid A, and spionid A, however, did consume presence of background plankton can both decrease the
Crassostrea gigas veligers (Fig. 1). These three poly- number ofencounters between predators and prey (John-
chaetes exhibited low levels of predation when veliger son and Shanks. 1997). For example, lack of encounters
larvae were presented at near-natural densities and in fil- may explain the low predation by Arctonoe vittata on
tered seawater (Table I, Treatment A). When background Crassostrea gigas under the most natural conditions (Ta-
plankton was used with this same near-natural prey den- ble I, Treatment B). This explanation is supported by
sity, predation was always absent (Table I, Treatment B). comparisons between observed predation by A. vittata
Predation was most frequent when densities of C gigas and encounter model estimates (K. B. Johnson, unpubl.
were high in filtered seawater (Table I, Treatment C). data): the estimates produced by two models (Gerritsen
Notably, the polynoid larvae, A. vittata and polynoid A, and Strickler, 1977. and a simple clearance rate model)
consumed the greatest numbers of veligers in Treatment were statistically indistinguishable from the minimum
C. The most extreme was polynoid A, averaging 6.17 known encounters of A. vittata with C. gigas {i.e.. ob-
bivalve veligers gut ' with twoofthe individualsconsum- served predation events). This bolsters the argument that
ing 8 veligers each. Presenting prey at high densities in larval polychaetes naturally prey upon bivalve veligers
the presence ofbackground plankton (Table I, Treatment during relatively infrequent encounters. Indeed, the many
D) reduced, but did not eliminate, the predation observed published observations ofpredation {e.g., Thorson, 1946;
at the same densities in Treatment C. Smidt, 1951: Kuhl, 1974; Wilson, 1982) may reflect rela-
Polynoid trochophores, which consumed numerous ve- tively rare field encounters rather than artifactual cod-end
ligers in Treatment C, voided their gut contents through predation. Predator-prey encounters in these previously
a large posterior rupture. This rupture quickly heals and published studies can. however, be difficult to estimate.
the unburdened trochophore suffers no obvious perma- Fielddensities, swimming speeds, andencounterradiuses,
nent damage. Veliger valves sometimes remain attached essential components of encounter rate models, are often
at the hinge after passage through the gut. Intact veligers unknown. Finally, the hypothesis that these polychaetes
that passed through the guts of larval polychaetes were may, upon infrequent encounters, be natural predators of
isolated in filtered seawater, but no consumed veligers bivalve larvae is also supported by an observation of a
revived. Thus, although digestion by trochophores can be spionid larva with one C. gigas veliger in its gut (K. B.
incomplete, predation does appear to result in mortality Johnson, unpubl. data). This metatrochophore larva was
for bivalve larvae. fixed only seconds afterbeing collected in a 120-1 sample
PREDATION ON BIVALVE VELIGERS 301
Figure 1. (A) D-hinge veliger ofthe oyster Crassostreagigas. (B)Trochophore larva ofthe polynoid
Arctonoe viihiia with a vehger of the oyster C. gigas in its gut. (C) Metatrochophore larva of spionid A
with a C. gigas veliger in its gut. (D) Trochophore larva of polynoid A with two C. gigas veligers in its
gut. A, C, and D are viewed with cross-polarized light. Scale bar = 100 /jm.
of seawater. No plankton net was towed: the water was ner, 1980: Ueda et al.. 1983) or the accumulation of
collected in a plastic bag, then immediately concentrated plankton in a front (Stommel, 1949: Bray. 1953: George
and fixed. This method allowed little time for artifactual and Edwards. 1973). A net towed through such a patch
predation. and then through a sparsely populated region would col-
The true frequency of encounters between predators lect a sample with an apparent density lower than the
and prey in the field may, however, be far greater than actual density within the front or aggregation. Further-
estimated by models or from laboratory experiments if more, bivalve veligers are known to associate with marine
natural densities are greater than those recorded by inves- snow (Green and Dagg. 1997: Shanks and Walters, 1997),
tigators. The effect of plankton patchiness on sampling creating localized high larval densities. Larval poly-
accuracy has received some attention (Hamnerand Carle- chaetes can also be strongly associated with marine snow
ton, 1979; Omori and Hamner. 1982) and could cause (Shanks and del Carmen. 1997) and, as a result, may
underestimation offield densities.—Plankton can be highly encounter potential prey items such as bivalve veligers
concentrated in a localized area for example, through more frequently. Published observations of predation
behavior-related aggregation (e.g., Alldredge and Ham- upon bivalve veligers by larval polychaetes may thus re-
302 K. B. JOHNSON AND L. A, BRINK
fleet natural predation in concentrated patches of preda- space, andWhiskey CreekOysterFarms (Tillamook, Ore-
tors and prey. gon) for supplying oyster larvae. The manuscript bene-
In spite of the fact that we never observed predation fited from the input of B. Pemet, S. S. Rumrill, A. L.
on bivalve veligers by Magelona larvae in laboratory ex- Shanks, and two anonymous reviewers. Field work was
periments, published observations of this predator-prey supported by NSF grant #OCE-9123514 to A. L. Shanks,
relationship are numerous and should not be summarily Oregon Institute ofMarine Biology. Laboratory work was
dismissed. Wilson (1982) mentions that three species of funded by NSF grant #OCE-9521093 to ALS and by an
Magelona are known to be carnivorous in later stages and award from the Lerner-Gray Fund for Marine Research
includesdescriptionsoflate-stagemetatrochophorelarvae to KBJ.
> 4 mm in length. TheMagelona—metatrochophore larvae
used in our experiments were 2 3 mm long. At a later Literature Cited
stage, with larger palps and mouths, these larvae may be Alldredge, A.L., and W.M. Hamner. 1980. Recurring aggregation
more effective at capturing bivalve larvae. It should be of zooplankton by a tidal current. Estiiarine Coastal Mar. Sci. 10:
noted, however, that a larva of Magelona papillicomis. 31-37.
lacking long palps and only 1 mm in length, is depicted Bhaud, M., and C. Cazaux. 1987. Description and identification of
polychaete larvae; theirimplications in current biological problems.
by Todd et al. (1996) with a bivalve veliger in its gut. Oceanis 13: 596-753.
Experiments analogous to ours should be conducted with Bray, B.M. 1953. Sea-water discoloration by living organisms. N.
later stage Magelona larvae to clarify the relationship of Z.J. Sci. Technol. B 34: 393-407.
this predator with potential bivalve prey. Brink,L.A. 1997. Cross-shelftransportofplanktoniclarvaeofinner
shelfbenthic invertebrates. M. S. Thesis,University ofOregon, Eu-
Summary gene.
Carriker, M.R. 1951. Ecological observations on the distribution of
Certain larval polychaetes may be significant natural oyster larvae in New Jersey estuanes. Ecol. Monogr. 21: 19-38.
predators upon bivalve veligers. This investigation, how- Daroa,lonMg.tHh.e,BaenldgiPa.nPcoolaskt..1N9e7t3h.. J.ThSeeaauRetse.co6l:og1y3o0f-1P4o0l.ydora ciliaia
ever, provides laboratory evidence that natural predation Feigenbaum, D.L., and R.C. Maris. 1984. Feeding in the Chaeto-
on bivalve larvae by polychaete larvae is absent or un- gnatha. Oceanogr. Mar. Biol. Annu. Rev. 22: 343-392.
common, possibly because the predators and prey have George, D.G., and R.W. Edwards. 1973. Daphnia distribution
fewencounters in the field(assuming thatpublished larval within langmuir circulations. Limnol. Oceanogr. 18: 798-800.
bivalve densities accurately reflect natural densities). Gerrciotmsmenu,niJt.,yasntdrucJt.uRre.iSntrziocokpllearn.kt1o9n7:7.amaEtnhceomuanttiecralprmoboadbeill.it/iesFiasnh.d
Published reports of bivalve veligers in the guts of Res. Board Can. 34: 73-82.
larval polychaetes suggest a natural predator-prey rela- Green, E.P.. and M.J. Dagg. 1997. Mesozooplankton associations
tionship and are seemingly incongruous with our results. with medium to large marine snow aggregates in the northern Gulf
One possible explanation is that polychaete larvae con- ofMexico. J. Plankton. Res. 19: 435-447.
sumed the veligers while in the cod-end of a plankton Hambnuetres,aWn.d Hro.l,eainndcoJr.alH.reCeafrelceotsoyns.te1m9s7.9.LimCnoolp.epOocdeasnwoagrrm.s:24:attr1i--
net. making the predation an artifact of the collection 14.
method. Johnson, K.B., and A.L. Shanks. 1997. The importance of prey
When polychaete larvae consumed bivalve veligers in densitiesandbackgroundplanktoninstudiesofpredationoninverte-
our laboratory experiments, the use of near-natural prey brate larvae. Mar Ecol. Prog. Ser. 158: 293-296.
Kuhl,H. 1974. Ubervorkemmen undnahrungderlarvenvonMagel-
densities with natural background plankton completely onapapillicomisO. F.Muller(PolychaetaSede^taria)lmMundungs-
eliminated predation. This lack of predation may be due gebiet von Elbe. Weserund Ems. Ber. Dt.sch. Wiss. Komm. Meeres-
to a reduction in the number of encounters with prey forsch. 23: 296-301.
(published data indicates that natural densities of bivalve Larson,E.T.,andA.L.Shanks.1996. Consumptionofmarinesnow
larvae are relatively low) or to the role of background bytwospeciesofjuvenilemulletanditscontributiontotheirgrowth.
Mar. Ecol. Prog. Ser. 130: 19-28.
plankton as a substitute food for predators or a screen to Lebour,M.V. 1922. The foodofplanktonic organisms.J. Mar. Biol.
obscure prey from detection. In short, our results suggest Assoc. U.K. 12: 644-677.
that a natural predator-prey relationship between poly- Mileikovski, S.A. 1959. Interrelations between the pelagic larvae of
chaete larvae and bivalve veligers may not exist. If a Nephrys ciliata (O. F. Mullen, Macoma baltica and Mya arenaria
relationship does exist, then the frequency of interaction ofthe White Sea. Zool. Zh. 38: 1889-1891.
Omori, M., and W.M. Hamner. 1982. Patchy distribution of zoo-
and its ecological importance may be less than expected plankton: Behavior, population assessment and sampling problems.
on the basis of published observations. Mar. Biol. 72: 193-200.
Omori, M., and T. Ikeda. 1984. Methods in Marine Zooplankton
Acknowledgments Ecology. John Wiley. New York, 332 pp.
Phillips, N.E., and B. Pemet. 1996. Capture of large particles by
We thank Bruno Pemet for valuable culture assistance, suspension-feeding scaleworm larvae (Polychaeta. Polynoidae).
Friday Harbor Laboratories for providing cold room Biol. Bull. 191: 199-208.
PREDATION ON BIVALVE VELIGERS 303
Reeve, M. R. 1981. Large cod-end reservoirs as an aid to the live larvae in the sound (Oresund). Medd. Dan. Fisk.-Havunders. Serie:
collection of delicate zooplankton. Limnol. Oceanogr. 26: 577- Plankton 4: 7-523.
580. Thorson,G. 1950. Reproductiveandlarvalecologyofmarinebottom
Shanks.A.L.,and K.A.del Carmen. 1997. Larval polychaetes are invertebrates. Biol. Rev. Camb: Philos. Soc. 25: 1-45.
strongly associated with marine snow. Mar. Ecol. Prog. Ser. 154: Todd,C.D., M.S. Laverack,and G.A.Boxshall. 1996. CoastalMa-
211-221. rine Zooplankton. 2nd ed. Cambridge University Press, New York.
Shanks, A.L., and K. Walters. 1997. Holoplankton, meroplankton, Ueda,H.,A.Kuwahara,M.Tanaka,andM.Azeta.1983. Underwa-
and meiofauna associated with marine snow. Mar. Ecol. Prog. Ser. ter observations on copepod swarms in temperate and subtropical
156: 75-86. waters. Mar. Ecol. Prog. Ser. 11: 165-171.
Smidt, E.L.B. 1951. Animal production in the Danish Waddensea. Wilson,D.P. 1982. ThelarvaldevelopmentofthreespeciesofMage-
Medd. Dan. Fisk.-Havunders. 11(6): 151 pp. lona (Polychaeta) from the localities near Plymouth. / Mar. Biol.
Stommel, H. 1949. Trajectories of small bodies sinking slowly Assoc. U.K. 62: 385-401.
through convection cells. / Mar. Res. 8: 24-29. Yokouchi, K. 1991. Seasonal distribution and food habits ofplank-
Thorson, G. 1946. Reproduction and larval development of Danish tonic larvae ofbenthic polychaetes in Volcano Bay. Southern Hok-
marinebottominvertebrates,withspecialreferencetotheplanktonic kaido, Japan. Ophelia 5: 401-410.