y and Ecology 334 (2006) 187–195www.elsevier.com/locate/jembe

Journal of Experimental Marine Biolog

Response of invertebrate larvae to the presence of the ctenophoreBolinopsis infundibulum, a potential predator

Anna Metaxas ⁎, Victoria Burdett-Coutts

Department of Oceanography, Dalhousie University, Halifax, Nova Scotia, Canada, B3H 4J1

Received 7 July 2005; received in revised form 20 January 2006; accepted 31 January 2006

Abstract

Larval loss of marine benthic invertebrates while in the plankton is extremely high, and although several sources of mortalityhave been proposed, the relative significance of each remains unknown. Despite suggestions that predation is a significant sourceof mortality, experimental manipulations using natural densities of prey have measured low predation rates. In part, structural,chemical and behavioural larval defenses may lead to these low rates. In the laboratory, we examined changes in the verticaldistribution of echinoplutei (4- and 6-arm developmental stages) of Strongylocentrotus droebachiensis (Mueller) and veligers ofOstrea edulis (L.) in the presence of the ctenophore Bolinopsis infundibulum (Mueller), a known larval predator. Larvae wereintroduced 2–3 cm above the bottom of experimental plexiglas rectangular columns (60×10×10 cm). The ctenophores were heldin baskets (10×10×10 cm), made of 0.63-μm Nitex mesh, which hung in the water at the top of the experimental columns. Emptybaskets were used in “No predator” treatments. Echinoplutei of both stages, and reared under both high and low food rations,showed a strong response and were found lower in the columns in the presence than the absence of ctenophores. The populationmean height above the bottom of the experimental columns was 12.2–15.2 and 9.4–16.2 cm's lower in the presence than in theabsence of predators (for 4- and 6-arm larvae, respectively). Interestingly, there was little difference in the vertical distribution ofveligers between the two treatments, suggesting that a behavioural defense to predation may not have evolved in all phyla. Abehavioural avoidance of predators, such as the one shown by echinoplutei in our study, may reduce larval mortality and increasethe probability for eventual recruitment to the benthos.© 2006 Elsevier B.V. All rights reserved.

Keywords: Benthic invertebrates; Ctenophores; Larvae; Meroplankton; Predation; Sea urchins

1. Introduction

For most marine benthic invertebrates with complexlife cycles, the highest rate of mortality occurs duringthe larval planktonic stage (Rumrill, 1990; Morgan,

⁎ Corresponding author. Tel.: +1 902 494 3021; fax: +1 902 4943877.

E-mail address: metaxas@dal.ca (A. Metaxas).

0022-0981/$ - see front matter © 2006 Elsevier B.V. All rights reserved.doi:10.1016/j.jembe.2006.01.025

1995). Several different sources of larval mortality havebeen proposed, such as starvation, offshore transport,unavailability of substrate for settlement, and predation(Young and Chia, 1987; Rumrill, 1990; Morgan, 1995).Of these, predation has been considered by someauthors as the most significant (Thorson, 1950; Morgan,1995). However, Morgan (1995) and Pechenik (1999)have cautioned that both the extent and sources of larvalmortality in the plankton remain unknown. Forexample, Lamare and Barker (1999) obtained in situ

188 A. Metaxas, V. Burdett-Coutts / Journal of Experimental Marine Biology and Ecology 334 (2006) 187–195

estimates of high larval loss, by following a cohort of theechinoid Evechinus chloroticus from spawning tosettlement, which they attributed to food limitationrather than dispersal or predation.

Despite its potential importance, a clear assessmentof the role of predation in larval mortality remainselusive. Several larval predators have been identified inthe literature, and they include both planktonic andbenthic suspension feeders, such as cnidarians, cteno-phores, chaetognaths, molluscs and crustaceans (forreviews see Mileikovsky, 1974; Young and Chia, 1987;Morgan, 1995). However, the identities of major larvalpredators are most likely still not known (Morgan,1995). Additionally, direct measures of predation ratesunder natural settings are limited to those obtained bytracking short-lived ascidian tadpoles after hatching inthe field (Olson and McPherson, 1987). The potentiallysignificant impact of predation in the field has beeninferred mainly based on limited measures of feedingrates in the laboratory (Pennington et al., 1986; Purcellet al., 1991; Morgan, 1992; Pechenik et al., 2004). It ispossible that these feeding rates may reflect biasedencounter rates, through container effects and unnatu-rally high prey densities (see also Rumrill, 1990).Recent experimental manipulations done both in thelaboratory and in the field using natural prey densitieshave recorded low predation rates on echinoid larvae(Johnson and Shanks, 1997, 2003).

Low predation rates may result in part from thepresence of larval defenses against predation (reviewedin Young and Chia, 1987; Morgan, 1995). Morpholog-ical adaptations, such as the presence of setae and spinesin polychaetes and crustaceans or of a shell in molluscs,can reduce ingestion. Alternatively, chemical com-pounds, which are present in eggs and embryos ofechinoderms and ascidians, can reduce palatability.Behavioural avoidance or escape from a predator, inresponse to physical cues (e.g. photo- and rheotaxis) orupon contact, has been proposed for crustaceans andechinoids (Forward and Cronin, 1978; Rumrill et al.,1985; Morgan, 1995; Johnson and Shanks, 2003). Suchbehaviours may reduce encounter rates and, conse-quently, mortality.

Behavioural responses to the presence of chemicalor physical cues have been recorded for differentlarvae (Metaxas, 2001). For example, we have shownthat echinoid larvae respond behaviourally to featuresin the water column, such as haloclines and foodpatches (Metaxas and Young, 1998a,b,c; Burdett-Coutts and Metaxas, 2004), and that the mechanismof detection that elicits this response is most likelychemo- rather than mechanosensory (Burdett-Coutts

and Metaxas, 2004). We have also shown that thestrength of the response is influenced by larval dietaryconditioning, suggesting that poorly fed larvae are lessresponsive to environmental cues than well-fed ones(Metaxas and Young, 1998a,b,c; Burdett-Coutts andMetaxas, 2004).

In this study, we examined the response of echino-plutei of Strongylocentrotus droebachiensis and veligersof Ostrea edulis to the presence of the ctenophoreBolinopsis infundibulum, a potential larval predator, inthe laboratory. For the echinoplutei, we examinedwhether the response varies with developmental stageand dietary conditioning of the larvae. Studies such asours, done under controlled conditions in the laboratory,can provide a first estimate of the range in behavioursthat have evolved in invertebrate larvae and that may bemanifested under natural conditions in the field.

2. Materials and methods

2.1. Larval rearing

Adults of S. droebachiensis were collected from thesubtidal zone near Halifax, Nova Scotia. Urchins wereinduced to spawn by injecting 2–5 mL 0.55 M KClthrough the peristomial membrane. Females spawnedinto glass beakers containing 0.45-μm filtered seawa-ter, and males dry spawned to prolong spermlongevity. The eggs were rinsed gently through a125-μm sieve, and embryos were obtained by mixingeggs and sperm from 3 pairs of adults. Fertilizationsuccess, determined as the proportion of eggs(n=250–500) with elevated perivitelline membrane,was N95%.

Following fertilization, we combined echinoidzygotes from all pairs and transferred them to 3.5-Ljars containing 0.45-μm filtered seawater with practicalsalinity of 33, at a density of ∼ 1 zygote mL−1. Thecultures were stirred continuously with motorizedpaddles, and we changed the water in the jars andadded microalgae every other day. We reared the larvaeunder high (5000 cells mL−1) and low (500 cellsmL−1) rations of a mixed microalgal diet (Dunaliellatertiolecta and Isochrysis galbana). While the totalnumber of algal cells remained fixed, the ratio for eachalgal species varied through larval development. In thetwo-arm stage, larvae received a combination of 50%D. tertiolecta and 50% I. galbana (by number), whilein the four- and six-arm stages the proportions were66% and 33%, for each algal species, respectively.Larval rearing and experiments were conducted in12 °C.

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40.5 ± 0.469 41.7 ± 0.43242.2 ± 0.565

27.7 ± 1.8527.3 ± 2.0826.2 ± 1.92

41.4 ± 0.765 41.4 ± 0.383 41.1 ± 0.302

26.2 ± 2.54 28.8 ± 4.18 28.9 ± 2.95

5 10 15 20 5 10 15 20 5 10 15 20

5 10 15 20 5 10 15 20 5 10 15 20

Fig. 1. Strongylocentrotus droebachiensis. Vertical distribution of 4-arm larvae, reared under a high or low food ration, in the presence and absence ofthe predator, Bolinopsis infundibulum, at 15, 30 and 45 min after their introduction into 60-cm experimental columns. Error bars are standard errors ofthe mean (n=4). ZCM values (mean±SE, n=4) are shown within the panel of each treatment combination.

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Adults of O. edulis were obtained from aquaculturefacilities on the South Shore of Nova Scotia, and wereconditioned at the Bedford Institute of Oceanography inan enclosed seawater system at 18 °C for ∼ 5 weeks,

when spawning occurred naturally. Larvae were col-lected immediately after release and transferred to 250 Lcontainers containing 1 μm-filtered seawater andcovered with a lid. The released larvae were reared at

15 min 30 min 45 min

15 min 30 min 45 min

32.7 ± 0.950 32.4 ± 2.9334.7 ± 0.945

20.6 ± 4.8118.5 ± 5.5023.1 ± 6.30

31.0 ± 1.21 33.5 ± 1.80 33.9 ± 1.41

21.6 ± 6.15 20.0 ± 5.55 22.1 ± 4.00

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Fig. 2. Strongylocentrotus droebachiensis. Vertical distribution of 6-arm larvae, reared under a high or low food ration, in the presence and absence ofthe predator, Bolinopsis infundibulum, at 15, 30 and 45 min after their introduction into 60-cm experimental columns. Error bars are standard errors ofthe mean (n=4). ZCM values (mean±SE, n=4) are shown within the panel of each treatment combination.

190 A. Metaxas, V. Burdett-Coutts / Journal of Experimental Marine Biology and Ecology 334 (2006) 187–195

concentrations of∼ 3 larvae mL−1 and were fed a mixedmicroalgal diet of I. galbana, Monochrysis lutheri,Chaetoceros muelleri and Thalassiosira pseudonana at35,000 cells mL−1. Larval rearing and experiments wereconducted in 20 °C.

2.2. Experimental design and statistical analyses

Experiments were conducted in plexiglas rectangularcolumns (60×10×10 cm) marked in 1-cm increments.Baskets (10×10×10 cm), made of 0.63-μm Nitex

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45.6 ± 0.863

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44.3 ± 0.917

42.5 ± 0.85746.6 ± 0.250

Fig. 3.Ostrea edulis.Vertical distribution of 4-arm larvae, in the presence and absence of the predator, Bolinopsis infundibulum, at 15 and 30 min aftertheir introduction into 60-cm experimental columns. Error bars are standard errors of the mean (without ctenophores: n=5; with ctenophores: n=6).ZCM values (mean±SE; without ctenophores: n=5; with ctenophores: n=6) are shown within the panel of each treatment combination.

191A. Metaxas, V. Burdett-Coutts / Journal of Experimental Marine Biology and Ecology 334 (2006) 187–195

mesh, hung in the water at the top of the experimentalcolumns. In treatments where predators were present, B.infundibulum [length: 20.8±3.40 mm (mean± sd,n=24); diameter: 18.8±2.51 mm; biovolume, calculatedfor a cylinder: 5.50±2.43 cm3] were introduced in eachbasket at a concentration of 20 and 25 individuals L−1,for the sea urchin and oyster experiments, respectively.Empty baskets were used in the “No predator”treatments. Ctenophores were collected locally ∼ 4 hbefore the experiments commenced, using a dip net andbucket.

We introduced larvae (sea urchins: 100–300;oysters: 50–300) to 2–3 cm above the bottom using aglass tube, and recorded their vertical distribution(number of larvae within each 1-cm increment) after 15,30 and 45 (sea urchins only) min. Two sets ofexperiments were conducted for S. droebachiensis,one in the four-arm stage (6-d old) and one in the six-arm stage (11-d old), and one set of experiments wasdone with straight-hinged veligers (10-d old) of O.edulis.

For each species and stage and for each time interval,we calculated the mean height above bottom (ZCM) forthe entire larval population in an experimental column as

ZCM ¼X

Pi � Zi

where Pi is the proportion of larvae in the 1-cm increment iand Zi is the height above bottom of 1-cm increment i.

For each stage of S. droebachiensis, we examined theeffects of Predator (fixed: present, absent), Food ration(fixed: high, low) and Time (15, 30, 45 min) on ZCMusing 3-way ANOVA with repeated measures on Time.Four replicate columns were used for each Pre-dator×Food ration treatment combination. For O. edulis,we used 2-way ANOVA, with Predator as a fixed factorand repeated measures on Time (15, 30 min). Fivereplicate columns were used for the “Predators present”treatment, and six for “Predators absent”. Datawere ln(x+1)-transformed to successfully remove heterogeneity ofvariances as detected using Levene's tests. Statisticalcomparisons were considered significant at α=0.05.

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Degrees of freedom for Time were adjusted for sphericityusing the Greenhouse–Geisser procedure. All statisticalanalyses were done using SPSS 11.0 for Windows.

3. Results

The magnitude of the larval response to the presenceof predators varied between species, and it was strongerfor S. droebachiensis than for O. edulis. The strength ofthis response was similar between developmental stagesof the sea urchin.

In the absence of predators, 4-arm larvae of S.droebachiensis reared under both food rations ascendedto the top 10 cm's of the experimental columns within15 min of their introduction, and remained there for theduration of the experiment (Fig. 1). In the presence ofpredators, larvae from both food rations did not ascendas high in the water column, although the spread of thevertical distribution was greater for larvae reared underlow than high rations (Fig. 1). ZCM was significantlylower in the presence than in the absence of predators(F1,12=62.5, pb0.001), but did not vary significantlybetween rations (F1,12=0.043, p=0.839) or with time(F1.70,20.4=2.15, p=0.147). The interactions Predator× -Food ration (F1,12=0.107, p=0.750), Time×Predator(F1.70,20.4 = 0.663, p= 0.502), Time ×Food ration(F1.70,20.4=0.007, p=0.986) and Time×Predator×Foodration (F1.70,20.4=0.683, p=0.493) were not significant.

For both rations, the vertical distributions of 6-armlarvae of S. droebachiensis in the absence of thepredator exhibited some aggregation near the surface,but were more even throughout the water column thanthose of 4-arm larvae (Fig. 2). When predators werepresent, larvae remained lower in the water column andpronounced peaks in the distribution emerged that werecentered at 10–20 cm above the bottom (Fig. 2). ZCMwas significantly lower in the presence than in theabsence of predators (F1,12=10.0, p=0.008), but did notvary significantly between rations (F1,12b0.001,p=0.996) or with time (F1.31,15.7=0.123, p=0.797).The interactions Predator×Food ration (F1,12=0.014,p=0.907), Time×Predator (F1.31,15.7=2.63, p=0.118),Time×Food ration (F1.31,15.7=0.867, p=0.396) andTime × Predator × Food ration (F1.31,15.7 = 0.195,p=0.731) were not significant.

The vertical distribution of O. edulis did not changeover the experimental period in the absence of predators,and most larvae aggregated in the top 5–10 cm's of thewater column (Fig. 3). A similar pattern in verticaldistribution was observed in the presence of cteno-phores, at 15 min after larval introduction (Fig. 3).However, in these treatments, there appeared to be a

gradual move of the larval population towards thebottom of the column observed at 30 min, indicating aweak and delayed response to the presence of predators.We did not detect a significant effect of Predator(F1,9 =0.151, p=0.706) on ZCM or a significantTime×Predator (F1,9 = 4.47, p=0.064) interaction.However, ZCM decreased significantly between 15and 30 min (F1,9=16.3, p=0.003).

4. Discussion

Both echinoplutei stages of the sea urchin S.droebachiensis showed a strong response to thepresence of ctenophores. The larval population attaineda lower overall position in the experimental columns inthe presence than in the absence of B. infundibulumwithin the first 15 min of introduction and maintained itfor the duration of the experiment.

Ctenophores are voracious predators of zooplankton(ranging from ciliates to copepods) and ichthyoplanktonand, consequently, play an important role in theregulation of planktonic assemblages (Purcell et al.,1994; Martinussen and Båmstedt, 1999; Purcell andDecker, 2005). They are known to prey on a range oflarval types such as echinoplutei, molluscan and bivalveveligers, annelid trochophores, bryozoan cyphonautes,and decapod zoea (Young and Chia, 1987; Morgan,1992), although their impact on the populations of theseprey is mostly unknown. Consumption rates measuredin the laboratory vary among ctenophore and larvalspecies. For example, Pleurobachia bachei consumed20–30 larvae of the polychaete Sabellaria cementariumin 24 h (Pennington and Chia, 1984), but only ∼ 10plutei (15% of total) of Dendraster excentricus(Pennington et al., 1986). However, B. infundibulumconsumed ∼ 25 (sd: ∼±18, n=3) plutei (∼ 45±35% oftotal) of the sand dollar within 24 h (Pennington et al.,1986).

It has generally been assumed that most of the N90%larval mortality between release and settlement is theresult of predation (Young and Chia, 1987; Rumrill,1990; Morgan, 1995). However, several studies both inthe field and in the laboratory have measured extremelylow predation rates on echinoplutei and gastropod andmolluscan veligers at natural prey densities, which theyattributed to low encounter rates (Bingham and Walters,1989; Johnson and Brink, 1998; Johnson and Shanks,1997, 2003).

Our results suggest that encounter rates may bereduced as a consequence of larval behaviour. Animmediate reversal in direction of swimming has beenrecorded for 4- and 6-arm plutei of D. excentricus upon

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contact with the carapace of predatory zoea of Cancerproductus (Rumrill et al., 1985). Additionally, Penning-ton et al. (1986) attributed the lower predation rates onechinoplutei than on earlier developmental stages of thisspecies to controlled swimming. Bingham and Walters(1989) suggested that settling larvae might be able toavoid the inhaling siphons of ascidians by sensingsuction and responding through negative rheotaxis.Crab larvae exhibit a shadow response to the perceivedpresence of a predator, manifested as a downwardswimming movement in response to a change in lightintensity (Forward, 1977). A downward movement(such as the one we observed) would also be the mosteffective behaviour to escape ctenophores, whichgenerally reside in surface waters (Young and Chia,1987).

Holoplankters, such as calanoid copepods, areknown to alter their swimming patterns in the presenceof the predator to decrease frequency of encounter(Viitasalo et al., 1998; Kiørboe and Visser, 1999). Forexample, nauplii of six species of copepods exhibitedescape jumps away from the flow in fluid deformations(meant to simulate the presence of a predator) above acertain threshold (Titelman and Kiørboe, 2003). Bothswimming behaviour and encounter rate in theseholoplankters can be greatly affected by turbulence(Kiørboe and Saiz, 1995).

In our experiments, the mechanism of detection of B.infundibulum by the echinoplutei was most likely chemo-rather than mechanosensory. Calanoid copepods usemechanoreception to detect fluid deformation by foragingpredators (Viitasalo et al., 1998; Visser, 2001). Theseorganisms can detect velocity differences between thebase and the tip of the setae on their antennae (Yen et al.,1992), which allows for great sensitivity to hydrome-chanical signals. Although not as elaborately equipped,echinoplutei may be able to detect fluid deformation byB.infundibulum through mechanoreception using theirciliary band. To evaluate this possibility in our experi-mental setting, we injected fluorescein dye in holdingbaskets, with andwithout ctenophores. In both treatments,dye penetrated through the baskets into the water columnwithin 1 min of injection and reached the bottom of theexperimental columns within 20 min. We did not observeany turbulence, eddy formation or any other fluiddeformation associated with the presence of ctenophores.We, thus, concluded that detection of mechanical cuesfrom the predator, while constrained from swimming, wasunlikely.

Previous studies have suggested that echinoplutei usechemical cues to detect quality of food particles. Forexample, Metaxas and Young (1998a,b) have shown

that echinoid larvae aggregate in algal food patches.These aggregations depend on the food quality of thepatch and occur in response to chemical rather thanmechanical cues (Burdett-Coutts and Metaxas, 2004).Echinoid and asteroid larvae are known to preferentiallyingest both algal cells to polystyrene algal mimics(Rassoulzadegan et al., 1984; Okaji et al., 1997) andflavoured to non-flavoured algal mimics (Appelmans,1994). It is possible that the ctenophores were detectedwith the same sensory mechanism. In zoea of Rhithro-panopeus harrisii, the presence of kairomones andmucus from the ctenophore Mnemiopsis leidyi reducedthe threshold of induction of a shadow response (Cohenand Forward, 2003). These chemicals may also havebeen detectable by the echinoplutei in our study.

Behavioural avoidance of B. infundibulum wasshown by plutei reared under both high and low foodrations. In previous studies, we have shown that thestrength of a behavioural response to the presence of afood patch depends on larval dietary conditioning(Metaxas and Young, 1998a,b; Burdett-Coutts andMetaxas, 2004). We have suggested that larvae rearedin low rations either are unable to control their verticalposition or they respond to stronger environmental cuesthan larvae reared in high rations. Our results support thelatter explanation by indicating that the presence of apotential predator provides a sufficiently strong cue tostimulate a response even in poorly fed larvae.

Indirect evidence indicates that larval O. edulisshowed an extremely weak, delayed response to thepresence of B. infundibulum. Given the prevailing flowregimes in coastal waters, it is unlikely that the relativepositions of oyster larvae and their predators would besustained for as long as 30 min, making such a responseinsignificant. It is possible that larval bivalves do notexhibit behavioural predator avoidance, but may still beable to reduce mortality from predation. It has beensuggested that the presence of a shell may providebivalve larvae with protection against ingestion anddigestion (Young and Chia, 1987; Morgan, 1995). Forexample, Purcell et al. (1991) found that only 1% ofingested oyster veligers were actually digested bymedusae of Chrysaora quinquecirrha. More than 70%of egested veligers survived for at least 24 h, followingan ingestion period of up to 6 h (Purcell et al., 1991).However, in the same study, 96% of veligers capturedby M. leidyi were digested (Purcell et al., 1991).

This study is the first to show a behavioural avoidanceresponse of larvae of benthic marine invertebrates to thepresence of a potential predator, manifested as a modi-fication in vertical distribution. This avoidance behaviourcan provide a possible mechanism for the low levels of

194 A. Metaxas, V. Burdett-Coutts / Journal of Experimental Marine Biology and Ecology 334 (2006) 187–195

predation observed for some invertebrate larvae. Thepresence of such a behavioural response, when observedunder controlled conditions in the laboratory, can serve asan indicator of an evolved adaptation to respond to apotentially harmful cue in the environment. However, themanifestation of this behaviour may occur only undercertain conditions in the field. For example, in areas ofhigh flow, where larvae cannot regulate their position, butrather behave like passive particles, such behaviours maynot be effective. In contrast, in quiescent, strongly stra-tified embayments, where aggregations of ctenophoresare frequently observed near the surface, larval avoidanceof such aggregations may be possible. The ecologicalimplication of such amechanism is increased survival andprobability of eventual recruitment to the benthos.

Acknowledgements

Bernita Giffin assisted with urchin larval rearing andexperiments, and Ivy Whitehorne with oyster experi-ments. Barry MacDonald (Invertebrate Division, Bed-ford Institute of Oceanography, Fisheries and OceansCanada) provided oyster veligers. Dr. R. Scheibling readan earlier version of this manuscript. Funding for thisstudy was provided by a NSERC Discovery Grant to A.M. [SS]

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