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MARINE PROGRESS SERIES Vol. 40: 115-126. 1987 - Published October 7 Mar. Ecol. Prog. Ser.

Cold seep benthic communities in zones: spatial organization, trophic strategies and evidence for temporal evolution*

S. Kim Juniper", Myriam Sibuet

IFREMER, Centre de Brest. BP 337. F-29273 Brest Cedex. France

ABSTRACT: Submersible exploration of the Japan subduction zones has revealed benthic communities dominated by clams (Calyptogena spp.) around sed~mentporewater seeps at depths from 3850 to 6000 m. Photographic and video records were used to produce microcartographlc reconstructions of 3 contrasting cold seep sites. Spatial and relations of megafauna lead us to propose several hypotheses regard~ng the ecological functioning of these cold seep communities. We dlst~nguish between the likely direct use of reducing substances in venting fluids by Calyptogena- symbioses and indirect usage by accompanying abyssal species not known to harbour symbionts. Microdistribution and known or presumed feedmg modes of the accompanying species indicate 2 different sources of organic matter enrichment within cold seep sites: organic debris originating from bivalve colonies, and enrichment of extensive areas of surrounding surface where weaker, more hffuse porewater seepage may support chemosynthetic production by free-living bacteria. The occurrence of colony-like groupings of empty Calyptogena valves indicates that cold seeps are ephemeral, with groups of living clams, mixed living and dead clams, and empty dissolving shells marlung the course of a cycle of porewater venting and offering clues to the recent history of cold seep activity.

INTRODUCTION al. 1985). One of the bivalve species from this area has been shown to harbour symbiotic bacteria in its gill The discovery of deep- hydrothermal vents has tissue and to oxidise (Childress et al. 1986), recently been followed by the finding of several other confirming that methane, as well as , forms of seafloor emissions of dissolved reducing sub- can serve as energy source for invertebratehacteria stances which fuel -based benthic com- symbioses. Subduction zone cold seeps occur at tecton- munities. Presently the latter appear to be of 3 major ically active continental margins. Kulm et al. (1986) types: brine seeps, oil/gas seeps and subduction zone made the first discovery of this phenomenon on the cold seeps. Deep-sea brine seeps are now known from Oregon continent margin, finding aggregations of a site (3270 m) near the base of the tectonically inactive clams and Vestimentifera associated with seeps of Florida escarpment (USA). Unlike shallow-water brine methane-rich fluids. They proposed that the fluids seeps (Powell et al. 1986) these seeps of sulfide-rich originated as deep porewaters that migrated hypersaline fluid were found to support a fauna to the seafloor surface along fault planes during the remarkably similar to that at hydrothermal vents in the subduction process, possibly as a result of compression East Pacific (Hecker 1985). A taxonomically of subducting sediments. Dissolved methane appears different fauna of bivalves and Vestimentifera to be the energy source for these cold seep com- (Lamellibranchia) has been dredged from 500 m deep munities (Kulm et al. 1986). oil and gas seeps on the Louisiana slope (Kennicutt et A recent Franco-Japanese submersible expedition to the subduction zones in the Japan region (Kai'ko pro- gram) revealed biological exploitation of sediment Contnbution No. 94 from IFREMER,Centre de Brest " Present address: Department of Biology, University of Vic- porewater seeps at depths from 3850 to near 6000 m toria. Victoria, British Columb~aV8W 2Y2,Canada (Bolegue et al. 1985, Cadet et al. 1985, Swinbanks

O Inter-Research/Printed in F. R. Germany 116 Mar Ecol. Prog. Ser 40: 115-126, 1987

1985a, b, Laubier et al. 1986, Le Pichon et al. 1987, mersible Nautile provided a continuous video log of all Ohta & Laubier 1987). These cold seep communities dives. Time, depth and submersible heading were are characterised by the of several species overwritten on the video image, allowing observations of the vesicomyid clam Calyptogena, the absence of to be located on the submersible's dive track. An exter- Vestimentifera and a remarkable local enrichment of nally-mounted 35 mm camera ( Model 372) abyssal benthic organisms (Laubier et al. 1986, Ohta & and strobe, activated from within the submersible, pro- Laubier unpubl.). vided an oblique monocular photographic record. A Apart from the role of chemosynthesis, little is knownof data chamber in the camera added depth and time the ecological functioning of 'seep' communities. Their data, allowing video and photographic information to discovery is very recent, only a handful of sites have been be matched. described, and researchers have tended to be first Examination of video and photo-documentation. All concerned with taxonomic and physiological problems. video and photo-documentation from the 10 dives In addition to symbiotic bivalves and Vestimentifera, reporting the presence of clam colonies were many other organisms representing a variety of feeding examined. In addition, photo records from several dives modes are clearly associated with active seeps: scaveng- not reporhng clam colonies were examined, as a refer- ing and predatory and , deposit-feeding ence to the general character of the abyssal fauna in gastropods and holothurians, suspension-feeding the explored region. Visual information was used to and anemones. The presence of these other assemble an inventory of all observed clam colonies, organisms, as well as the variable presence of bivalves and to identify qualitative differences between fauna and Vestimentifera, invokes questions regarding food accompanying the clams and the surrounding abyssal web structure, faunal requirements, interspecific fauna. This information is reported in another paper interactions, etc. The more than 50 cold seep sites (Sibuet et al. unpubl.). Three of the most well- documented during the course of the 1985 Kaiko diving developed and most differing sites were then selected program have presented an opportunity to observe for detailed analysis of faunal microdistribution. trends in development and organisation and Microcartography. Metre-scale maps of each to study them in detail. Analysis of this component of the selected site were drawn, in overlay, from photo- benthos is necessarily selective. Cold seeps are mosaics to reconstruct the location of individual organ- very small in area and often separated by hundreds or isms, the living/dead condition of visible clams and the even thousands of metres. Traditional random sampling major physical features of the habitat. Living clams techniques are thus an inefficient means of data gather- were identified in the photographs from their upright ing, and sites must be located and selectively sampled by posture and visible mantle tissue, and dead clams by submersible. In this paper we examine the structural and their open valves in various states of dissolution. Scale spatial organization of the megafauna at 3 heavily in the photo-mosaics was extrapolated from the size of colonised sites discovered in the and the clam shells lying horizontally, using size data of clams . The communities of clams Calyptogena taken in samples. Since viewing angle and camera-to- and their accompanying fauna were studied from subject distances were not measurable in the photos, microcartographic reconstruction of each site. Our goal scale estimations were only approximate. This, how- was to use observed microdistribution as a guide to ever, did not detract from the primary purpose of the develop a preliminary picture of the exploitation of cold maps which was to reveal relative spatial organisation seeps by various trophic groups. This approach, similar to of the fauna. that used by Fustec et al. (1987) at hydrothermal vents, has also revealed distlnct patterns of community struc- ture and demography, the latter leading us to consider RESULTS possible patterns of temporal evolution of the biocoenoses following initial colonisation by Calyp- Sites selected for microcartographic analysis (Fig. 1) togena. Another paper (Sibuet et al. unpubl.) examines are located in Tenryu Canyon in the Nankai Trough patterns of cold seep community development in relation (Dives 26 & 28; 33"37'N, 13f032'E; 3830 m depth), in to substratum, faulting and other geological features of the Japan Trench at Kashima (Dive 43; the subduction zone environment. 35"54'N, 142"311E; 5640 m depth) and at another slte in the Japan Trench (Dive 48; 40°06'N, 144" 10'E; 5900 m depth). Geological description and location of ANALYTICAL METHODS these sites in relation to local are given by Sibuet et al. (unpubl.). Substrata at these sites were soft Video and photographic documentation. An exter- sediment (Tenryu Canyon and Kashima Seamount) or nal color video camera and internal VCR on the sub- mudstone (Japan Trench Dive 48). Juniper & Sibuet: Cold seep communities in subduction zones 117

Fig. 1.Bathymetry of the Pacific Ocean in Japan Region showing subduction zones and selected dive sites. Dive 28 (Pl. 28) was located in Tenryu Canyon near its intersection with the Nankai Trough, the subductlon zone off southeastern Japan. Dive 43 (Pl. 43) was made at the site of subduction of Kashirna Seamount in the Japan Trench. Dive 48 (PI. 48) explored the inner wall of the Japan Trench upward from near 6000 m. See Sibuet et al. (unpubl ) for detailed description of these sites

Tenryu Canyon Three species, Calyptogena (Ectenagena) nautilei n. sp., C. (Ectenagena) laubieri n. sp. and C. (Ectenagena) Several fields of Calyptogena colonies were aligned kaikoi n. sp. have been identified from samples taken along thrust faults on the wall of Tenryu Canyon. This at this site (Okutani & Metivier 1986), and a box core is a flat-floored canyon which transects the accretion- taken in the above group contained 2 species. Shell ary prism forming on the landward wall of the Nankai lengths ranged from 114 to 129 mm for C. nautilei, 39 to Trough (Fig. 1) (Sibuet et al. unpubl.). A 1 X 4 m 74 mm for C. laubieri and 46 to 82 mm for C. kaikoi section of the largest observed alignment of clam col- (Okutani & Metivier 1986). The second more widely onies (10 X 2 m) was reconstructed from a photo- spaced colony, in the lower right, was dominated by mosaic (Fig. 2). Limited photographic coverage did not dead but articulated clams (Fig. 3B). Between the 2 permit analysis of the entire site. Two groups of clams clam colonies were a few scattered living and dead can be distinguished in this section. In the upper left of clams. Distinct spatial separation of colonies of living Fig. 3 is a tightly-aggregated colony of 60 - mostly live and dead clams also occurred on a larger scale at this - clams, partially buried in the sediment (Fig. 3A). site, with one region of the 10 X 2 m field of clam 118 Mar. Ecol. Prog. Ser. 40: 115-126, 1987

2 - - m \------I l I I I I

I . . *** I____------__-_--- - . . 0 I , - - , . .. . 0 . . ------Q-- I I

: *OO v

L~ve Gosteropoda A L Colypiogeno sp. I 0 Deod Acflnarla * I 0 Hololhuraideo(Synollaclldae) Q Polychaela I 0 Ov C 0 ~ I 2 3 m

Fig. 2. Microcartographlc reconstruction of the area partially shown in Fig. 3. Zone outside dashed lines not covered by photo mosaic but video records indicate that alignment of depicted colonies is representative of the onentation of the larger clam field from which this section was extracted. Smaller clam symbols represent small-sized individuals. The area shown represents a zone of transition from an area of living clam colonies to an area dominated by dead clams. Substratum is a thick sediment cover

colonies being dominated by living clams and the other gastropods and an individual clam moving over the by dead clams. The selected section represents the sediment surface and leaving groove-like tracks. Major zone of transition from the region of living to dead features of this and the following 2 sites are summa- colonies. rised in Table 1. The most abundant accompanying species at this site were mainly suspension feeders. Numerous serpulid polychaetes were attached to empty clam valves in the Kashima Seamount second colony (Fig. 2, see also Fig. 3B). No serpulids were associated with the colony dominated by living A single colony of more than 100 living and dead clams, although some were attached to surfaces of clams belonging to a fourth Calyptogena species, C, nearby rocks and bouIders. Actinarians of several (Ectenagena) phaseoliformis n. sp., (Metivier et al. species occurred on a variety of surfaces: living and 1986) was located in a small gully on a steep slope of dead clam shells, boulders and the surface of holothu- the inner wall of the Japan Trench at the site of subduc- nans. Suspended organic concentrations at this tion of Kashima Seamount (Fig. 1). The colony was site appear favorable to suspension feeders, and these aligned along a sediment slide scar. The upslope por- organisms may be limited by the availability of hard tion consisted of nearly 50 living clams which were substrata. A large holothurian (family Synallactidae) closely grouped within the fracture (Fig. 4 A). A similar was the only at this site. Its distribution was number of dead clams comprised the lower portion of rather uneven, and fewer than 5 individuals were pre- the colony, and numerous disarticulated empty shells sent within the l0 X 2 m field of clam colonies. Two were scattered along a line further down the slope, mobile scavenger/ species, a gastropod and a apparently transported by visible slumping of sediment galatheid crab, were present at this site at densities of 1 (Fig. 5). to 2 individuals per clam colony. However, comments Abundant swimming holothurians Peniagone elon- by the scientific observer of Dive 28 suggested that gata were concentrated on the sediment surface near galatheid crabs were more numerous than indicated by the clams. Nearly 60 individuals were counted In the video and photo-documents. There was a remarkable area depicted in Fig. 5 (ca 5 m'). Many swimming density of grooved tracks on the sediment surface at individuals were also visible in the video and photo this and other clam sites in the area, suggesting consid- records during the passage through the area of the erable locomotory activity by some species. Scientific slope where this and several non-living clam colonies observers on the 2 dives at this site report seeing were found. Tube-dwelling polvchaetes (Ohta & Juniper & Sibuet: Cold seep communities in subduction zones 119

Fig. 3. Photographs 01 portions of the studied section of the large Tenryu Canyon Calyptogena field. (A) Colony dominated by living clams, ~ltha large holothurian and few other living clams located nearby. (B) Colony of mainly dead clams with serpulid polychaetes and occasional actinarians attached to empty clam shells; a small galatheid crab is visible on the left 120 Mar. EcoL Prog. Ser. 40. 115-126, 1987

Table 1 Summary of major features of reconstructed cold seep faunal communities from sites in the Japan subduction zones

Isite Calyptogena colonies Accompanying fauna l Tenryu Canyon - Distinct colonies of mainly living clams or ar- - Serpulids and actinarians on dead clams and (Dive 28) ticulated empty valves; clams partially buried other hard surfaces in sehents - Small numbers of galatheids, large holothu- - C. nautilei, C. laubieri and C. kaikoi rians and gastropods on sediment surround - Colony size: 60 to 70 clams clams Kashima Seamount - Single mixed colony of hving clams and articu- - Abundant caprellid amphipods m and around (Dive 43) lated empty valves; clams partially buried in clam colony sediment - Abundant Pen~agoneandtubiculous - C. phaseoLiformis only on sediments around clam colony - Colony size: > 100 clams - Single actinarlan on clam shell, < 5 gastropods - Visit by 2 fish after release of clam blood Japan Trench - Distinct colonies of mainly living clams or ar- - Abundant caprellid amphipods in and around (Dive 48) ticulated empty valves; clams epibenthic on clam colonies mudstone - Extensive area around colonies occupied by - C. phaseoliform.is only tubiculous polychaetes implanted in mudstone - Colony size: 20 to 100 clams - 5 gastropods - No Peniagone

Laubier 1987), likely , also surrounded the occurring between boulders and rock outcrops. All clam colony. In comparison to that of P, elongata, living C. phaseoliformis at this site were epifaunal on polychaete distribution was more restricted and in the mudstone substratum. At the Kashima site this closer proximity to the clams (Fig. 5). Crustaceans iden- same species occurred partially-buried in soft sedi- tified as caprellid amphipods (not sampled) (Ohta & ment. A few empty clam shells were scattered through- Laubier 1987), up to 5 cm long, were very abundant at out the site, but living clams occurred only within the 3 this site. They were most numerous within and near the defined colonies. Tube-dwelling polychaetes, similar to clam colony, but they occurred as well on the surround- those observed at the Kashima Seamount site, covered ing sediment surface where they occupied approxi- a very extensive area outside of the clam colonies. The mately the same area as P. elongata (Fig. 5). Caprellids polychaetes occupied a surface several times that have seldom been observed in photographs or faunal covered by the 10 or more clam colonies found at this samples from the deep-sea. In coastal waters, cap- site. Approximately 250 polychaetes were visible rellids are omnivorous. The only known abyssal within the area described by Fig. 6, corresponding to a species, collected in the East Pacific Ocean at 3500 to density of near 100 ind m-2. Polychaete tubes were 4000 m, may have browsed upon the associated sessile vertically implanted in the mudstone substratum. fauna (McCain 1966). Only a single actinarian was These polychaetes were similarly abundant at several present, attached to a clam shell. A few gastropods other sites in the Japan Trench. Caprellid amphipods were visible within and near the clam colony. were numerous throughout the site; they were visible resting on the substrata both within and outside the clam colonies (Fig. 6). Numerous actinarians were Japan Trench attached only to clam shells and not to adjacent rock surfaces although a single individual occurred on a The site reconstructed in Fig. 6 represents a portion gravel substrate near Colony A (Fig. 6). Five gas- of a field of more than 10 colonies of Calyptogena tropods were counted within the analysed section. No phaseoliformis n. sp. (Metivier et al. 1986) located on swimming holothurians (Peniagone sp.) were seen. the slope of the inner wall of the Japan Trench between 5940 and 5900 m depth, in a subduction erosion setting (Fig. 1). The 3 colonies of clams in the illustrated DISCUSSION section had rather different general features. The densely aggregated Colony .A (Fig. 6, see also Fig. 4 B) Direct utilisation of porewater: Calyptogenalbacteria consisted of ca 100 clams, nearly all living. Colonies B and C were much smaller: Colony B contained only living clams, numbering slightly less than 20, Colony C The clams are the only found at these sites was a scattered assemblage of mainly dead clams for which there is evldence for direct utilisation of Juniper & Sibuet: Cold seep commumties in subduction zones 121

Fig. 4. (A) Large colony of living and dead clams at the Kashima Seamount site. Note aggregation of Living clams in the upslope portion of the colony and the scattering of empty shells downslope. Accompanying species: polychaetes, swimming holothunans, caprellid amphipods and a gastropod. (B)Largest of the Calyp- togena colorues (Colony A in Fig. 6) studied at the Japan Trench site (Dive 48). Note close aggregation of mainly living clams and the abundance of polychaete tubes on the sediment surrounding the clams reducing substances in venting porewater via sym- most negative reported for marine organisms (-37.8 to biosis with chemosynthetic bacteria. All 4 Kaiko -40.1). species of Calyptogena are associated with sampled Simllar 6C13 values for the Oregon cold seep Calyp- methane-rich cold seeps (Boulegue et al. 1987b). All 4 togena species have been interpreted to indcate that species have blood containing large amounts of haem porewater methane, in addition to providing energy for proteins, suggesting an adaptation to the oxygen trans- symbiotic chemosynthesis, also serves as the clam's port requirements of intracellar symbiosis (Ohta & primary carbon source (Kulm et al. 1986). Ultrastruc- Laubier unpubl.). Values of bC13 in soft tissues of C. tural analyses of gill tissue of C. phaseolifonnis reveal phaseoliformis (Boulegue et al. 1987a). are among the endocellular bacteria (BoulSgue et al. 1987a, A. Fiala 122 Mar. Ecol. Prog. Ser. 40: 115-126, 1987

nutritional contribution from suspension feeding cannot yet be discounted. Kai'ko Calyptogena species examined to date all have functional albeit extremely reduced digestive tracts containing particulate matter including debris (M. Le Pennec pers. comm.). Clarification of the nutritional role of endosym- biotic bacteria in cold seep clams will require phy- siological experimentation. Symbiosis between inver- tebrates and chemosynthetic bacteria remains too poorly understood to permit firm conclusion from car- bon isotope data and the presence of bacteria in gill tissue, particularly in animals anatomically capable of suspension feeding.

Indirect utilisation of porewater: classic abyssal species

Aggregation of omnivorous, deposit-feeding, and suspension-feeding species at these cold seeps sug- gests a local increase in food availability (Table 1). and organic debris produced by the clam colonies is one possible source of nutrition for some of the accompanying organisms. Organic matter is scarce at these depths and any significant local source of production is likely to be fully exploited by the abyssal fauna. Two fish quickly arrived at the Kashima site following sampling of clams and the release of clam Colyplogena sp. llve 0 dead Gasteropodo A Holathuro~deal Penlogone sp ) 0 Acl~nor~o* blood. A similar observation was made at the Oregon Arnphtpodal Caprell~dsa) m Polychoeto cold seeps following sampling of clams (Kulm et al. 1986).While these fish may not be regular predators on Fig. 5. Microcartographc reconstruction of cold seep com- the clams, they certainly appear capable of feeding on munity on a steep slope at the Kashirna Seamount site. recently dead individuals. The abundance of colony- Diagonal Line in centre marks position of the slump scar along which the clams were aligned. Arrows in lower left: down- like groups of still-articulated valves seen at these and slope location of dead clam shells. Substratum is sedlrnent other sites suggests that clam colonies are rarely dis- with occasional exposure of underlying rock indicated by turbed by large predators or scavengers (Rhoads et al. shaded areas 1982, Hessler et al. 1985). The omnivorous galatheid crabs seen at the Tenryu Canyon site likely scavenge pers. comm.),which may be responsible for both oxida- dead clams as well as deposit feeding on organic tion of methane and incorporation of methane carbon debris. Galatheids also aggregate around hydrother- into organic matter. Both of these processes have yet to mal vent sites where their omnivorous habit, and pos- be experimentally demonstrated for any species of sibly their tolerance of low oxygen conditions (Burd & Calyptogena. The presence of chemosynthetic activity Brinkhurst 1984, Juniper & Brinkhurst 1986), likely in Calyptogena gill tissue is known from enzymatic permit them to profit from the local production of bio- studies of species found at hydrothermal vents (Fel- mass and organic debris. The few gastropods visible at beck et al. 1981, Cavanaugh 1983).Recent experiments all 3 sites are probably also attracted by the with from seeps in the Gulf of concentration of at cold seeps. Mexico have demonstrated, for the first time, the oxida- The microdistribution of Peniagone and the tube- tion and incorporation of methane in bivalve gill tissue dwelling polychaetes indicates that these organisms containing endocellular bacteria (Childress et al. 1986). exploit surface sediments wthin an extensive zone Cavanaugh et al. (1987) also report the presence of surroundmg the clam colonies (Table 1; Fig. 5 & 6). The endocellular bacteria with methyltroph-like ultrastruc- input of sedimenting organic matter to these depths is ture in gill tissue of mussels from the Florida Escarp- very low, thus suggesting a dependence on the cold ment brine seep sites. While a methane-based sym- seeps. Additional organic debris from the clam colonles biosis seems very likely for these cold seep clams, a may still be insufficient to support such a high biomass. Juniper & Sibuet: Cold seep communities in subduction zones 12:

I , I I I I l I . 1 2 - f --- m 10 i . t I ,-____l I lI Il I0

. ------.

I - -

I ..- L~ve + Fig. 6. Microcartographic reconstruc- Calyptoqena Dead 0 tion of a portion of a large clam field Amphlpoda ( Caprell!dea1 9 in the Japan Trench inner wall (Dive 0 Polychaeta 48).Colonies A, B and C (see text) are Act~narlo * indicated. Shaded areas: rock out- Gasleropoda A crops through the mudstone sub- stratum

A supplementary food source may be localised in sedi- weaker anomalies in adjacent bottom waters (Bou- ments peripheral to the clam colonies. One possibility legue et al. in press b). is that diffuse porewater discharge, too weak to support Deposit feeding is the most likely mode of nutrition clam colonies, supports bacterial productivity in sur- for these unsan~pled tube-dwelhng polychaetes and face sediments surrounding the clams, providing a holothurians. Aprionno other trophic strategy appears local food enrichment for deposit feeders. The clam possible for Peniagone, although the polychaetes could colonies would mark points of more intense fluid dis- have some form of symbiosis. charge, and colonisation of adjacent sediments by deposit feeders would indicate weaker, less localised venting that is utilisable by only free-living sediment bacteria. While sediment bacterial activity at cold seeps Demography of clam colonies remains to be investigated directly, Kulm et al. (1986) report sediment porewaters from the Oregon cold The clam colonies examined here and those seeps to be depleted in NH3 and total CO2. They observed elsewhere during the Kai'ko program (Sibuet interpret this as evidence of CH, oxidation by sediment et al. unpubl.) reveal several demographic features . Aerobic bacterial oxidation of which have interesting ecological implications. Two methane is well known from freshwater sediments (e.g. points arise from the distinction of 4 separate species of Rudd & Hamilton 1975), and there is considerable Calyptogena among the specimens collected by the geochemical evidence for anaerobic microbial submersible: (1) The presence of 3 species of Calyp- methane oxidation in marine sediments (e.g. Devol togena within the same cold seep field, and within the 1983, Alperin & Reeburgh 1985, Whiticar & Faber same colony, in Tenryu Canyon, implies parti- 1986). There is yet no direct evidence for weaker pore- tioning and among 3 species with similar water venting surrounding the clam colonies but dissi- general habitat requirements. (2) The existence of a pation of fluids escaping from underlying rock forma- single, fourth species of Calyptogena at all the deeper tions is likely as they pass upward through the sedi- sites points to possible depth limitations or other ment cover. Temperature measurements made at the specific habitat requirements. This fourth species was Tenryu Canyon site reveal clear thermal anomalies only collected from 2 of the deeper sites, but it is readily above the centre of the clam colonies and occasional distinguished from the other 3 species in photo and 124 Mar. Ecol. Prog. S

video records by its greater length and elongate form of clam demography in dating cold seeps can be prop- (Metivier et al. 1986). erly assessed, species longevity and rates of new site A study of the digestive tracts of available specimens colonisation and shell dissolution will need to be better revealed that the 3 Tenryu Canyon species, in compari- understood. Analysis of population structure (shell son to the species from the deeper sites, had better lengths) of living and dead clams within colonies and developed digestive tracts which contained greater cold seep fields would be of great aid in understanding quantities of ingested material (M. Le Pennec pers. the history of colonisation and mortal~ty.The proximity comm.). This suggests that proportional contributions of new seep sites to a mother population of clams may of filter feeding and chemosynthesis to meeting nutri- be an important factor in determining the rate of colon- tional requirements may be one character differing isation, although the mechanism of larval dispersal for among Calyptogena species and influencing their dis- these Calyptogena species is unknown. C. magnifica, tribution. from hydrothermal vents, produces large yolk-filled Another notable demographic feature of the clam eggs and Likely has lecithotrophic larvae. It is not clear colonies is variation in the proportions of living and if these lawae develop within egg membranes or are dead clams. Colonies consisting almost entirely of liv- demersal (Berg 1985).The locomotory activity of clams ing or dead clams, and mixed colonies of living and described by Ohta & Laubier (1987) could permit dead clams, were seen throughout the region explored limited colonisation of new sites within an active seep during the Kaiko program. Sampling has revealed that field, although this would be a very risky strategy this aspect is not species specific. The presence of dead where seeps were more than a few metres apart. clams can firstly be attributed to natural senescence Crowding or deterioration of fluid flow is one factor and mortality. In addition, assuming a vital depen- that could stimulate clams to move away from a seep dence of the clams on porewater venting, the presence site, but evidence of unsuccessful forays (i.e. isolated or of groups of mainly dead clams indicates the site of a scattered empty valves) was rare throughout the area recently deteriorated cold seep: in some cases this may explored during the Kai'ko program. Our analyses of indicate a complete cessation of fluid flow. clam microdistribution and demography strongly sug- does not appear to be an important cause of mortality, gest that the clams generally remain within the same since it would presumably result in considerable dis- closely-packed colony until death by senescence or persion of clams from the colonies and disarticulation of deterioration of fluid flow. valves rather than the observed colony-like groups of articulated empty valves. We use the term 'recent deterioration' because the solubility of clam shells at CONCLUSIONS depths of 3850 to 6000 m, at or well below the carbon- ate compensation depth, would prevent their long-term Spatial organization preservation. The duration of dead Calyptogena shells at these depths is likely to be considerably shorter than Calyptogena species are localised around the points the 15 to 25 yr estimated for their complete dissolution of most intense fluid discharge. The fauna accompany- at 2500 m (Roux et al. 1983, Lutz et al. 1985). Signs of ing the clams, while not always constant in composi- dissolutive weathering are even visible on shells of tion, displays distinct patterns of distribution. Suspen- live-collected Calyptogena from the Kalko sites, in that sion-feeding actinanans and serpulid polychaetes are portion of the shell which protruded from the sediment attached to clam shells and nearby hard surfaces. when the was in its living position. Omnivorous and deposit-feeding species occur within Assuming that deterioration of fluid flow and natural and near the clam colonies. These include gastropods, mortality are ihe 2 main processes responsible for the galatheid crabs, caprellid amphipods and a large presence of groups of articulated empty valves, 2 other holothudan. The most abundant accompanying species deductions can be made regarding the duration of are the tubiculous polychaetes and the swimming venting at a cold seep site. Living and dead clams holothurians which occupy extensive areas of the sedi- within a single colony, such as at the Kashima site, ment surface outside of the clam colonies. would indicate that venting has continued long enough to allow the accumulation of empty valves by natural senescence, and perhaps mortality by crowding- Trophic strategies induced displacement away from fluid flow as has been suggested for Calyptogena at hydrothermal vents At least 2 trophic levels are recognizable The clams, (Hessler et al. 1985). Groups dominated by or consist- with their apparent symbiosis, are obvious primary lng entirely of living clams would mark more recently consumers, drectly exploiting porewater fluids. A com- activated and colonised cold seep sites. Before the use paratively smaller biomass of secondary consumers Jun~per8: Sibuet.: Cold seep commun~tlesin subduction zones 125

likely exploits particulate organic matter produced by tremblements de terre dans la region de Tokai (Japon). C. the clam colonies. This group incl.udes serpulids, r. hebd. Seanc. Acad. Sci., Pans, Serie 11, 16: 1217-1219 galatheids, actinarians, gastropods, caprelllds, and Burd, B., Brinkhurst, R. 0. (1984). The distribution of the galatheid crab Munida quadrasplna (Bened~ct1902) in possibly the large holothurian. relation to oxygen concentration in British Columbia The large numbers of swimming holothurians and fjords. J. exp. mar. Biol. Ecol. 81: 1-20 tubiculous polychaetes on sediments surrounding some Cadet. J. P., Kobayashi, K., Aubouin, J., Boulegue. J.. Dubois, clam colonies suggest the existence of a third major J., Von Huene. R., Jolivet, L., Kanazawa, T., Kasahara, J., trophic pathway. We propose that there may be low- Koizumi, K., Lallemand, S., Nakamura, Y., Pautot, G., Suyehiro, K., Tani, S., Tokuyama, H., Yamazaki, T. 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This article was submitted to the editor; it was accepted for printing on July 10, 1987