Selective Predation by the Zoarcid Fish Thermarces Cerberus at Hydrothermal Vents

Home , Cerberus (snake), Lepetodrilus, Lepetodrilus elevatus, Thermarces cerberus

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Deep-Sea Research I 52 (2005) 837–844 www.elsevier.com/locate/dsr

Selective predation by the zoarcid ﬁsh Thermarces cerberus at hydrothermal vents

G. Sanchoa,Ã, C.R. Fisherb, S. Millsc, F. Michelid, G.A. Johnsone, H.S. Lenihanf, C.H. Petersone, L.S. Mullineauxc

aCollege of Charleston, Grice Marine Laboratory, 205 Fort Johnson, Charleston SC 29412, USA bPennsylvania State University, University Park PA 16802, USA cWoods Hole Oceanographic Institution, Woods Hole MA 02543, USA dStanford University, Hopkins Marine Station, Paciﬁc Grove CA 93950, USA eUniversity of North Carolina at Chapel Hill, Institute of Marine Sciences, Morehead City NC 28557, USA fBren School of Environmental Science and Management, University of California, Santa Barbara CA 93106, USA

Received 12 April 2004; received in revised form 31 August 2004; accepted 3 December 2004

Abstract

This study investigates predation by the vent zoarcid fish Thermarces cerberus through gastrointestinal analyses of 27 specimens collected with the submersible ALVIN at vents at 91500N on the East Pacific Rise. T. cerberus fed most frequently on gastropod mollusks (mainly Lepetodrilus elevatus) and amphipod crustaceans (mainly Ventiella sulfuris). Species found occasionally in high abundance included the swarming amphipod Halice hesmonectes and the snail Cyathermia naticoides. Other items also found in gastrointestinal tracts, but in very low numbers, included polychaete worms, crustaceans and unidentified tissue clumps. The comparison between the size distribution of L. elevatus limpets ingested by T. cerberus and those found attached to vestimentiferan tubes suggest that the fish may selectively prey on large limpets. If the selective removal of large Lepetodrilus spp. limpets by T. cerberus does occur, then it would have potential community-level consequences at hydrothermal vents, since these mobile gastropods appear to inhibit the settlement of sessile vent species, including tube-building worms. Our results suggest possible direct and indirect effects of T. cerberus on benthic community structure at hydrothermal vents on the East Pacific Rise. r 2005 Elsevier Ltd. All rights reserved.

Keywords: Predation; Vent ﬁsh; Deep sea; Hydrothermal vents; Diet; East Paciﬁc Rise

1. Introduction

ÃCorresponding author. Tel.: +1 843 953 9194; Deep-sea hydrothermal vents commonly have fax: +1 843 953 9199. low diversity of physiologically specialized pre- E-mail address: [email protected] (G. Sancho). dators and experience few visits by opportunistic

838 G. Sancho et al. / Deep-Sea Research I 52 (2005) 837–844 predators from surrounding habitats, likely be- communities (Tunnicliffe and Juniper, 1990; Van cause of the toxicity of hydrogen sulfide found at Dover, 1995). But recent predatory exclusion vents to non-specialized organisms (Voight, 2000). experiments at the East Pacific Rise vents (Micheli Zoarcid fishes are specialized predators commonly et al., 2002) suggest that T. cerberus influences the found in sulfide-rich habitats such as hydrother- structure of hydrothermal vent benthic commu- mal vents, cold seeps and whale skeletons (Des- nities by consuming mobile gastropods and bruye` res and Segonzac, 1997; Sibuet and Olu, indirectly reducing their grazing on recruits of 1998; Biscoito et al., 2002). Zoarcids of the genus mobile and sessile invertebrates, including vesti- Thermarces are conspicuous members of deep-sea mentiferans. The present study analyzes the hydrothermal vent communities of the East Pacific composition and size of prey items in guts of T. Rise (Cohen et al., 1985; Rosenblatt and Cohen, cerberus individuals caught using the submersible 1986; Biscoito et al., 2002). The taxonomy of the ALVIN in order to understand the fish’s role as a species inhabiting the hydrothermal vents near predator in potentially structuring hydrothermal 91N at the East Pacific Rise (EPR) has been vent animal communities on the East Pacific Rise. debated among ichthyologists (Rosenblatt and Cohen, 1986; Geistdoerfer and Seuront, 1995; Biscoito et al., 2002), but we will follow the 2. Methods recommendations by Biscoito et al. (2001),and refer to all the specimens we collected at this site as T. cerberus specimens were collected at two Thermarces cerberus. None of the fish collected for hydrothermal vent sites (‘East Wall’ and ‘Biovent’) this study had the dusky brown coloration typical along the axial valley on the East Pacific Rise of the other Thermarces species found at the 91N (9o500N, 1041170W) at depths that ranged between East Pacific Rise site (Biscoito et al., 2001). 2490 and 2520 m. Detailed description of the T. cerberus lives among the vestimentiferan physical and chemical characteristics of this vent worm communities (vestimentiferans are now field can be found elsewhere (Detrick et al., 1987; considered to be members of the polychaete family Haymon et al., 1991; Lutzet al., 1994 ). Fish were Sibloglinidae, but will be referred to herein as caught from among or near megafaunal commu- vestimentiferans to differentiate them from other nities dominated by vestimentiferan tubeworms sibloglinids; Rouse, 2001) and near high-tempera- (mainly Riftia pachyptila) or vent mussels (Bath- ture vents along the East Pacific Rise, in 8–12 1C ymodiolus thermophilus). waters (Geistdoerfer and Seuront, 1995). Geist- A total of 27 T. cerberus specimens was collected doerfer and Seuront (1995) described the diet of T. and analyzed, eight specimens in 1998, 13 in 1999, cerberus as dominated by amphipods, with limpets and six in 2000. Specimens were captured at the as the second most abundant prey items. Frag- ‘East Wall’ (n ¼ 24) and ‘Biovent’ (n ¼ 3) sites. ments of vestimentiferans have been reported in T. Samples were pooled between the two sites for cerberus stomachs (Rosenblatt and Cohen, 1986; subsequent analyses because of the similar inverte- Geistdoerfer and Seuront, 1995), but these reports brate communities and close proximity (800 m) of remain ambiguous because disturbance events these sites (Mullineaux et al., 2003), and the caused by research submersibles could make potentially high mobility of T. cerberus (G. broken vestimentiferan remains available to fish Sancho, personal observation). Fish were captured (Rosenblatt and Cohen, 1986). alive with a multi-chambered suction sampler Though predation has been shown to directly attached to the submersible ALVIN. On reaching and indirectly influence natural aquatic commu- the surface they were transferred immediately to a nities through complex webs of species interactions cold room in order to minimize decomposition of (Paine, 1969; Menge et al., 1994; Hixon and the gut contents. Within 2 h, each fish was Brostoff, 1996), biological interactions have been measured (total length, and when possible stan- generally considered to play relatively minor roles dard length and weight), sexed and dissected, with in determining the structure of hydrothermal vent preservation of the stomach and intestines sepa- ARTICLE IN PRESS

G. Sancho et al. / Deep-Sea Research I 52 (2005) 837–844 839 rately in 95% ethanol. In the laboratory all length (measured along the external side of the recognizable food items from the guts were shell between the anterior and posterior ends) of identified to the species level (or the lowest Sadosky et al. (2002). To compensate, we trans- taxonomic category possible) and measured using formed our total shell linear lengths (Ltot) from a binocular microscope. Total shell length (Ltot) ingested limpets into curvilinear lengths (Lcurv) was measured in gastropods as the maximum using a calibration obtained by measuring both linear length, always with the anterior opening of lengths on 10 specimens covering the relevant size the shell as a reference. Amphipod length was range (3.6–13.5 mm Ltot). The resulting transfor- measured from the frontal edge of the cepha- mation function was lothorax to the most distant point of the curved 2 abdomen, without manual stretching of the speci- Lcurv ¼ 1:16 Â Ltot þ 0:85; R ¼ 0:99. mens. Copepod length was measured from the Differences in shell size-distributions were tested cephalothorax edge to the distal end of the by a Kolmogorov–Smirnov two-sample test (Sokal abdomen. and Rohlf, 1995). In 1998 collections, sub-samples of food items were extracted for isotopic analyses making direct comparisons of prey abundance impossible. In fish collected in 1999 and 2000, all stomach and 3. Results intestinal contents were preserved, identified and measured for analyses of relative prey abundance, The 27 fish analyzed ranged in total length from frequency and size. Because of the extreme 127 to 397 mm (mean ¼ 297 mm, SD ¼ 69 mm). difficulty and high economic cost of capturing The specimens captured included 17 females, six these abyssal fish, the maximum possible numbers males and four immature individuals of indeter- of specimens were included in different analyses minate sex (Table 1). (e.g. calculation of frequency of occurrence of prey The mean number of prey items found in the items employed data from all 27 fish), even though gastrointestinal tracts of T. cerberus (only from the the effects of size, sex, collection site and date 19 fish collected in 1999 and 2000) was 26.4 (range could not be evaluated statistically. 1–118, SD ¼ 59.6) (Table 2). The diet of T. Description of prey items in guts of T. cerberus cerberus was clearly dominated by gastropods followed methods described in Hyslop (1980) and (Cn ¼ 50.1%) and crustaceans (Cn ¼ 47.1%), Costello (1990). Prey items were lumped into four while polychaete worms (Cn ¼ 2.0%) and uniden- general food categories: crustaceans, gastropods, tified tissue clumps (Cn ¼ 0.8%) were much rarer polychaetes and unidentified tissue clumps. The (Fig. 1). The analysis of the frequency of total number of individual items in a certain food occurrence of prey item in gastro-intestinal tracts category was recorded for all fish (Cn; expressed as (f) from all 27 fish specimens also confirmed the the percentage of the total number of items in all dominance of gastropods (f ¼ 66.7%) and crusta- food categories), and the mean number of ceans (f ¼ 77.8%) and the occasional occurrence individual prey per gastrointestinal tract (N). The percentage of all fish that contained one or more Table 1 Total length of the Thermarces cerberus (average, maximum, prey items of a food category (f) was also minimum and standard deviation) used in stomach content employed as a measure of frequency of occurrence. analyses (N ¼ 27) Size distributions of ingested Lepetodrilus elevatus were compared with data from limpet samples Sex N Total length (mm) collected independently (May 8, 1999) from Mean Max Min SD vestimentiferan tubes at ‘East Wall’ by Sadosky (2001) as part of the French cruise ‘HOPE 99’. Female 17 329 397 260 66 Unfortunately, our length measurement of limpets Male 6 304 340 268 51 Immature 4 138 170 127 87 was not directly comparable to the curvilinear ARTICLE IN PRESS

840 G. Sancho et al. / Deep-Sea Research I 52 (2005) 837–844

Table 2 Frequency, abundance and sizes of prey items found in Thermarces cerberus. Percentage of gastrointestinal tracts containing a prey item (f) from all 27 fish collected. Overall total number of prey items (N). and abundance per individual fish (mean and maximum) measured from 19 fish collected in 1999 and 2000. Prey size (mean, standard deviation, maximum and minimum values) measured as stated in Methods section

fNAbundance Prey size (mm)

% Mean Max Mean SD Max–min

ANNELIDA Polychaetesa 22.2 9 0.47 3

MOLLUSCA Lepetodrilus elevatus 59.3 118 6.16 31 7.0 2.8 12.9–0.9 Lepetodrilus pustulosus 14.8 2 0.11 2 9.3 2.8 11.3–7.3 Lepetodrilus cristatus 3.7 1 0.05 1 4.4 Lepetodrilus ovalis 3.7 1 0.05 1 5.6 Cyathermia naticoides 33.3 130 6.84 102 4.0 0.9 6.2–1.3 CRUSTACEA Halice hesmonectes 18.5 117 6.16 91 4.1 1.3 8.8–1.6 Ventiella sulfuris 66.7 108 5.68 19 3.9 1.5 11.2–0.8 Copepods 11.1 6 1.20 3 1.2 0.1 1.3–1.1 Bythograea spp.b 11.1 4 0.80 1 —

Unidentiﬁed tissuec 14.8 4 0.21 2

aDiverse unidentiﬁed polychaete worm remains. bTwo megalopa larvae, one whole crab and a separate pair of claws. cUnidentiﬁed tissue clumps, possibly from Riftia pachyptila.

30 of polychaete worms (f ¼ 22.2%) and unidentiﬁed Cyathermia naticoides 25 Lepetodrilus spp. tissue (f ¼ 14.8%) (Fig. 1). Two mobile species dominated the gastropod Halice hesmonectes 20 Ventiella sulfuris mollusk category, a limpet (L. elevatus, Cn ¼ 23.3%, f ¼ 59.3%) and a snail (Cyathermia 15 naticoides, Cn ¼ 25.9%, f ¼ 33.3%). Other gastropods consumed by T. cerberus included the limpets 10 Lepetodrilus ovalis L. pustulosus L. cristatus Unidentified tissue , and

Number of prey (%) Number Other crustaceans (Table 2). Crustacean prey mainly consisted of 5 amphipods, Ventiella sulfuris (Cn ¼ 21.5%, Polychaetes ¼ ¼ 0 f 66.7%) and Halice hesmonectes (Cn 23.3%, 020406080f ¼ 18.5), and also included copepods and bra- Frequency of occurrence (%) chyuran crabs (Table 2). Polychaete worm remains were easily recogniz- Fig. 1. Relationship between the number (Cn, number of able by characteristic bristles and body structures, individual items in a prey category expressed as a percentage of but were not identifiable to the species level, except all items found) and frequency of occurrence (f, percentage of fish containing prey items of a specific prey grouping) of the for one Archinome rosacea specimen. The uni- prey categories in Thermarces cerberus diet. Only fish collected dentified tissue category consisted of large clumps in 1999 and 2000 were considered. of dark amorphous and partially digested tissue. ARTICLE IN PRESS

G. Sancho et al. / Deep-Sea Research I 52 (2005) 837–844 841

Similar findings in T. cerberus stomach contents (range 1.9–15.8 mm, n ¼ 118), greater than the have been identified as respiratory plume and mean value of 6.9 mm from limpets found on trophosome tissues from vestimentiferan worms, vestimentiferan tubes (range 1.6–12.5 mm, most likely of R. pachyptila (Rosenblatt and n ¼ 476) at the same location (Sadosky, 2001). Cohen, 1986; Geistdoerfer and Seuront, 1995), but a definitive identification was not possible. The size class distribution (Lcurv)ofL. elevatus 4. Discussion found in the gastro-intestinal tracts of T. cerberus collected in 1999 and 2000 was significantly The diet of T. cerberus was dominated by mobile different (Kolgomorov–Smirnov para- gastropod and amphipod species closely associated meter ¼ 1.461; p ¼ 0.028) from the size distribu- with vigorous flow areas, dominated by vestimen- tion of individuals sampled from R. pachyptila tiferan and mussel communities at EPR vents. The tubes at the same vent site in 1999 (Fig. 2). The two most frequent prey species were L. elevatus mean size (Lcurv) for ingested limpets was 9.0 mm and V. sulfuris. This result confirms the limited observations from other studies (Rosenblatt and Cohen, 1986; Geistdoerfer and Seuront, 1995; Geistdoerfer, 1996). Other crustaceans (copepods, 18 Thermarces cerberus adult and larval crabs) and polychaetes were also 16 found, indicating that T. cerberus is a benthic 14 predator feeding on a wide assortment of potential 12 prey. T. cerberus preyed mainly on two gastropod 10 species, the limpet L. elevatus and the snail C. 8 naticoides, which are commonly found on R. Individuals 6 pachyptila worm tubes (Mullineaux et al., 2003). 4 The distribution of gastropods in the diet of T.

2 cerberus varied: L. elevatus was found in the majority of ﬁsh guts (f ¼ 59.3%), as opposed to C. 0 1-2 3-4 5-6 7-8 9-10 11-12 13-14 15-16 naticoides, which was ingested by a third of the ﬁsh analyzed (f ¼ 33.3%), one of which contained 102 100 snails (78% of all C. naticoides counted). The other Vestimentiferan tubes (Sadosky 2001) gastropods preyed upon by T. cerberus (L. 80

pustulosus, L. cristatus and L. ovalis) constituted only 3.3% of the limpets ingested and were all 60 species found mainly within the vestimentiferan faunal zone characterized by vigorous ﬂows and 40 Individuals elevated temperatures (Mullineaux et al., 2003). This clear dominance by L. elevatus within the 20 ingested limpets is similar to the limpet community found on vestimentiferan tubes at the ‘East Wall’ 0 vent site (Sadosky, 2001), where L. elevatus 1-2 3-4 5-6 7-8 9-10 11-12 13-14 15-16 accounted for 99.3% of all limpet species sampled. Curvilinear length (mm) Thus we have no evidence that T. cerberus preferentially selects L. elevatus over other limpet Fig. 2. Size frequency distributions for Lepetodrilus elevatus species found at the vestimentiferan faunal zone of specimens ingested by Thermarces cerberus (n ¼ 118; only from ﬁsh collected in 1999 and 2000) and found on vestimentiferan the EPR vents. tubes collected at the ‘East Wall’ site (re-drawn from Sadosky Focusing on L. elevatus, the distribution of size 2001; n ¼ 476). classes of limpets ingested by T. cerberus was ARTICLE IN PRESS

842 G. Sancho et al. / Deep-Sea Research I 52 (2005) 837–844 markedly different from the size distribution of cerberus populations strongly targeting large limpets found attached to vestimentiferan tubes. limpets might be effective at reducing the popula- T. cerberus ingested limpets of all sizes, but seemed tions of large limpets through intense predation to preferentially select larger individuals: 39.0% of among the vestimentiferan tubes, especially if large the L. elevatus found in gastrointestinal tracts were limpets are relatively rare in this habitat. larger than 10 mm in curvilinear length, even The higher digestion rates of small crustaceans though individuals this large accounted for only (amphipods and copepods) compared to mollusks 5.7% of this species found on vestimentiferan may result in the underestimation of their im- tubes (Sadosky, 2001). The largest limpet found in portance in the diet of T. cerberus in comparison natural populations sampled from vestimentiferan to gastropod mollusks with thick shells, which tubes at the 9 N1 ‘East Wall’ vent had a maximum likely remain for longer periods in the gastro- curvilinear length of 12.9 mm (Sadosky, 2001). Of intestinal tract. The two amphipod species found the 118 L. elevatus ingested by T. cerberus at the in the gastrointestinal tracts were both abundant same location, 18 limpets (15.25%) were larger prey items, but greatly differed in their distribu- than 12.9 mm and the maximum size recorded was tion: V. sulfuris was homogeneously distributed 15.8 mm. The capture of T. cerberus specimens among the fish analyzed (f ¼ 66.7%), while H. from ‘East Wall’ in 1999 occurred only 7–12 days hesmonectes was found only in five fish before limpets were collected from worm tubes (f ¼ 18.5%), one of which contained 91 indivi- (Sadosky, 2001), negating the possibility that duals (78% of all H. hesmonectes counted). This observed size differences were the result of pattern indicates that T. cerberus regularly preyed sampling at different times. Limpets collected on benthic V. sulfuris, the most abundant amphi- from vestimentiferan tubes at 131N East Pacific pod in East Pacific vents and commonly found Rise vent showed bimodal size distributions close to the substrate in the vestimentiferan zone (Sadosky et al., 2002), and were also smaller (Desbruye` res and Segonzac, 1997). Yet occasion- (maximum length of 13.3 mm) than limpets ally T. cerberus consumed H. hesmonectes, which ingested by fish in our study. form dense monospecific aggregations in the water The discovery of large limpets in T. cerberus column near vent openings (Van Dover et al., guts raises the question of why these sizes were not 1992) and probably constitute an opportunistic, found in tubeworm aggregations sampled by but also important, food resource. Sadosky (2001) or Sadosky et al. (2002).Itis Other prey items found in the gastrointestinal possible that fish are finding the largest limpets in tracts of T. cerberus were rare and did not seem to vent microhabitats that were not sampled by these constitute an important part of the diet of this authors, such as in bivalve beds where L. elevatus predator. All identifiable organisms consisted of densities can be quite high (Van Dover and Trask, vent-associated organisms found in the vestimen- 2000; Van Dover, 2002) or within rock cracks. tiferan zone (Desbruye` res and Segonzac, 1997). Feeding by T. cerberus outside the vent habitat is Vestimentiferans were not definitively detected in unlikely since L. elevatus recruitment is restricted the diet of T.cerberus. If the clumps of ‘unidenti- to vent habitats, with recruits found primarily on fied tissue’ were vestimentiferan remains, their vestimentiferan clumps, with reduced abundances importance in the diet of T. cerberus would still be in bivalve beds and rarely observed in suspension minimal, corroborating previous observations feeder or periphery areas (Mullineaux et al., 2003). (Rosenblatt and Cohen, 1986; Geistdoerfer and Video analysis of T. cerberus feeding behaviors is Seuront, 1995). It has been suggested that the underway to address this issue, but has not yet vestimentiferan R. pachyptila becomes available to yielded conclusive results (G. Sancho, personal the fish only after being ‘‘crushed’’ by submarine observation). A second possible explanation for maneuvering in the vent area (Rosenblatt and these findings is that the random sampling of Cohen, 1986). It is unclear if T. cerberus preys on tubeworms and associated fauna might have live vestimentiferans. Accidental ingestion of missed rare large limpets. Finally, abundant T. Riftia tissue could conceivably occur during ARTICLE IN PRESS

G. Sancho et al. / Deep-Sea Research I 52 (2005) 837–844 843 attacks on moving amphipods, and feeding within Acknowledgments the capture chamber of the suction sampler on Riftia remains collected during the capture of fish We thank the pilots and crew of the ALVIN is also a possibility. Group for catching the specimens and keeping the The importance of mobile grazing gastropods suction sampler operational, as well as the crew of in the diet of T. cerberus described in this the RV Atlantis for their support. We also thank study suggests a likely effect on the gastropod Stace Beaulieu, Derk Bergquist, Ewann Berntson, populations through predation-induced mortality. Allison Green, Stacy Kim, Anna Metaxas, Mircea In addition, predation on gastropods by Podar and Craig Young for their help during the T. cerberus can also have indirect consequences cruises and while processing the samples. Scott for other organisms. In the absence of large France graciously identified some of the amphi- predators, i.e. when predators were experi- pods collected, and Franck Sadosky generously mentally excluded with cages, higher abundances shared with us limpet size data from his M.Sc. of limpets and lower abundances of sessile thesis. We also thank Andy Gooday and three benthic invertebrates (including vestimentiferan anonymous reviewers for useful suggestions on the tubeworms, vent mussels and tubiculous poly- manuscript. This work was funded by National chaetes) colonized rocky substrates (Micheli et al., Science Foundation Grants OCE-9315554 and 2002), a finding consistent with the hypothesis OCE-9712233 to L.S. Mullineaux, OCE-9317735 that grazing activities by limpets and snails and OCE-9712809 to C.H. Peterson, and OCE- may dislodge newly recruited organisms and 9317737 and OCE 9712808 to C.R. Fisher. This reduce the effective settlement of larvae. The paper is WHOI contribution number 11139. feeding activity of T. cerberus likely reduces the abundance of limpets, indirectly promoting the successful settlement and growth of juvenile vestimentiferans and other sessile benthic inverte- References brates (Micheli et al., 2002). In the absence of size–frequency data for Biscoito, M., Segonzac, M., Almeida, A.J., 2001. New zoarcid L. elevatus over its entire potential feeding fish species from deep-sea hydrothermal vents of the area (including bivalve beds as well as tubeworm Atlantic and Pacific Oceans. International Ridge-Crest aggregations), it is not possible to be certain Research 10 (1), 15–17. Biscoito, M., Segonzac, M., Almeida, A.J., Desbruye` res, D., that size-selective predation on limpets is Geistdoerfer, P., Turnipseed, M., Van Dover, C., 2002. occurring. Nevertheless, the greater abundance Fishes from the hydrothermal vents and cold seeps—an of large limpets in the guts of T. cerberus than update. Cahiers de Biologie Marine 43, 359–362. in tubeworm aggregations does provide evidence Cohen, D.M., Rosenblatt, R.H., Haedrich, R.L., 1985. Identity that prey are being selected by size. If true, this of thermal vent fishes in the eastern Pacific: an interim report. Biological Society of Washington Bulletin 6, might have significant, direct effects on the 229–230. population structure of these mollusks. For Costello, M.J., 1990. Predator feeding strategy and prey example, it might permit the recruitment and importance: a new graphical analysis. Journal of Fish early growth of small limpets and reduce the Biology 39, 261–263. number of large individuals with the highest Dayton, P.K., 1971. Competition, disturbance and community organization: the provision and subsequent utilization of potential to disrupt the settlement and coloniza- space in a rocky intertidal community. Ecological Mono- tion of benthic invertebrates through ‘bulldozing’ graphs 41, 351–389. (Dayton 1971) while moving and grazing along the Desbruye` res, D., Segonzac, M., 1997. Handbook of deep-sea substrate. The dietary characteristics of T. cerberus hydrothermal vent fauna. Editions IFREMER, Brest, therefore indicate the potential importance of France. Detrick, R.S., Buhl, P., Vera, E., Orcutt, J., Madsen, J., this predator in determining the structure of Brocher, T., 1987. Multi-channel seismic imaging of a vent invertebrate communities through complex crustal magma chamber along the East Pacific Rise. Nature ecological relationships. 326, 35–41. ARTICLE IN PRESS

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