Deep biological communities in the subduction zone of Japan from bottom photographs taken during “nautile” dives in the Kaiko project

Earth and Planetary Science l.etters, 83 (1987) 329-342

329

Elsevier Science Publishers B,V., Amsterdam - Printed in The Netherlands

[4]

Deep biological communities in the subduction zone of Japan from bottom photographs taken during "nautile" dives in the Kaiko project Suguru O h t a ~ and L u c i e n L a u b i e r 2 i Ocean Research Institute, University of Tokyo, Minamidai 1-15-1, Nakanoku, Tokyo 164 (Japan) 2 IFREMER, 66, acenue d'l~na, 75116 Parts (France) Revised version accepted November 3, 1986 Twenty-seven dives of the submersible "Nautile'" in the subduction zone around Japan conducted in the FrenchJapanese Project Kaiko proved that fairly luxuriant benthic communities dominated by deep-sea giant clams of the genus Calyptogena (family Vesicomyidae) were consistently present on the accretionary prism at abyssal depths. Benthic communities characterized by three hitherto undescribed bivalves of the genus Calyptogena were found between depths of about 3800 and 4020 m at the mouth of Tenryu Canyon and at the top of basement swell of the Zenisu Ridge, both situated in the eastern Nankai subduction zone. Sporadic but discrete patches of organisms characterized by one more undescribed bivalve belonging to the genus Calyptogena were observed and collected between depths of 5130 and 5960 m on the landward wall of the Japan and Kouriles Trenches. Photographic inventories were prepared semiquantitatively using each series of bottom photographs taken in these areas with bow cameras of the submersible "' Nautile". Observations on the sporadic but dense distribution of the clams and other characteristic associated organisms match well with the scheme that communities sustained by chemosynthetic energy sources can be present at connate water seepages in subduction zones. These are to date the deepest record of benthic communities supposedly associated with chemosyntbetic processes.

1. Introduction

2. Material and methods

During the second phase of the French-Japanese Project Kaiko studying the subduction phenomena off Japan using the deep-sea submersible "Nautile", the consistent presence of fairly luxuriant benthic communities dominated by vesicomyid bivalves of the genus Calyptogena was discovered in the subduction-induced deformation areas. These findings are now being analyzed in detail on the working hypothesis that these abyssal communities are sustained by chemosynthetic energy sources squeezed out from the deep subsurface sediments. Biological specimens and images retrieved by the submersible were brought to French and Japanese biologists for closer studies. Both authors were appointed to be the coordinators of the biological studies for each country. This paper gives a preliminary account of the new biological findings and their implications for deep-sea ecology. It deals with the observations and analyses of the pictures taken by bow cameras of the submersible.

Observations were based on the bottom photographs taken with a pair of underwater cameras (BENTHOS model 372) installed on the submersible "Nautile". The cameras were mounted obliquely to the bow of the submersible pointing either anterior left downward or approximately anterior downward accommodated to each dive, Stereoscopic pairs of bottom photographs were not available yet; observations were based on one of the films provided by the Japanese committee of the Kaiko project. Seven strips of film were scrutinized (Table 1) where distinct benthic communities dominated by giant vesicomyid bivalves could be found out of twenty-seven more or less successful Kaiko dives. Analysis was qualitative or, occasionally semiquantitative for the objects of known size in the camera's field of view such as the sampled bivalves. Transparencies were projected on a high precision viewer, sometimes on higher magnification when necessary. Time of shot, heading of the

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© 1987 Elsevier Science Publishers B.V.

330 TABLF 1 List of stations where distinct benthic communities associated with the bivalves (,'alvpto~ena spp. were found in the bottom photographs. Dive No.

Area

Name

(Kaiko Ser.)

(approx. position)

of di ver

Date

Photographic records duration

frames

Depth (m) depth (m)

where

Ca.lvptogena c~curred

KD-3 KD-5 KD-6 KD-14 KD-I8 KD-21 KD-23

Nankai T r o u g h / T e n r y u ('anyon 33°37.2"N, 137°31.6'E Nankai T r o u g h / T e n r y u Canyon 33° 36.9"N, 137 ° 3 2 . 0 ' E Zenisu Ridge sediment swell 33°15.8'N. 1 3 7 ° 2 3 . 0 ' E transect of the Japan Trench 35 °54.2' N. 142° 30.7'E Japan "French landward wall 40°06.3"N, 14A° 10.6"E Kurile Trench landward wall 41°18.5'N, 144°48.3'E Japan Trench landward wall 40 ° 06.5'N, 144°10.0'E

C. Rangin

06-06-1985

A. "l'aira

06-10-1985

J. Charvct

06-11-1985

K. Fujioka

(17-22-1985

J.-P. Cadet

(17-31-1985

J. Aubouin

08-03-1985

N. Niitsuma 08-05-1985

submersible and water depth were read from the data chamber within each frame. Identification of organisms in the photographic frames remains rather tentative, because full-scale biological samplings were beyond the scope of the Kaiko project, and most of the diving sites were so rugged or so steep that remote biological sampling from the surface ships had been greatly restricted. The task, however, was mitigated by informations on the fauna and distribution of benthic organisms compiled to date by the Ocean Research Institute, University of Tokyo, through extensive trawlings and underwater photographic surveys in the Japan Trench and Nankai Trough areas. Detailed topographical and geological settings of the study areas can be found in Le Pichon et al. [1], Cadet et al. [2] and elsewhere in this series of publications. 3. Observations

3.1. Tenryu Canyon and Zenisu Ridge area Tenryu Canyon is a steep-sided submarine valley that cuts into the accreted wedge of sediments being stacked up along the edge of the Eurasian plate, on which the southwestern half of Japanese mainland is situated, as the subducting Philippine plate plunges beneath it. Zenisu Ridge is an up-

12:01'15", 17:47'3g" 13 : 2 3 ' 5 9 " , 17:45'30" 15:11'07". 18: 18'46" 13:47'14", 18:06'44" 13 : 24'32", 17:34'07" 12:49'18". 17: 12'01" 13:02'36". 16: 56'05"'

468

3855 3654

3787-3835

222

3765-3832

383(I

2(17

4216-4026

4021

516

5890-5635

5640 5695

424

5938- 5652

5653 596(I

231

5785-4981

5131-5785

300

5679-5225

5479-5660

lifted basement ridge formed by intraoceanic shortening located about 20 km south of the axis of Nankai Trough [1]. The first clusters of proliferous deep-sea benthic organisms were found by dives KD-3 and KD-5 at the intersection of the front of the Nankai accretional prism and of Tenryu Canyon at a depth around 3830 m [3]. The patches of deep-sea benthic organisms were dominated by three species of giant clams of the genus Calyptogena, serpulid polychaetes and actinians, and contained lesser numbers of buccinid gastropods, a galatheid Munidopsis sp. and a synallactid holothurian (Tables 2 and 3). The colonies were found to be aligned over 800 m length either along northeast-southwest trending flexure and roughly east-west trending probable strike-slip faults [1]. The water temperature inside the colonies at 10 cm depth within the sediment exhibited 0.2 to 0 . 6 ° C positive thermal anomalies compared to the ambient temperature of 1.19°C. The colonies of living clams were oval to circular in outline, up to 60 cm in longer diameter and they contained prodigious numbers of clams. One box core 250 cm 2 in cross-sectional area caught about 40 living clams. Rough density estimate can be drawn to be about 1000-2000 individuals/m 2 in seeming "nurseries" where relatively small and living individuals are densest.

331 TABLE 2 Photographic inventory of the benthic organisms and lebensspuren observed in the bottom photographs duiing dive KD-3 (Nankai Trough/Tenryu Canyon: 3654-3855 m) Organisms

Abundance

Distribution pattern

Xenophyophores (foliaceous type) Umbellula thomsoni K~511iker * Actinians (small, white; attached to holothurians) * Actinians (small, white; attached to rocks and bivalves) * Actinians (medium-sized; cerianthid type) * Actinian (large, brown) * Serpulid polychaete worm tubes Polychaete worm tubes * Calyptogena sp. Type I (undescribed) * Calyptogena sp. Type 1I (undescribed) * Buccinid gastropods Aristeininae penaeid prawn (swimming) * M u m d o p s i s sp. * Synallactid holothurian tiny fishes [? zoarcid] ? Histiobranchus sp.

occasional 1 abundant abundant abundant several abundant abundant abundant abundant 2 1 6 8 6 1

solitary solitary symbiotic gregarious

* V-shaped furrows produced by bivalves Bulldozing tracks produced by buccinid gastropods~ Large mounds t Star-shaped traces produced by echiuran worms

several

solitary

gregarious patchy gregarious gregarious solitary

solitary'

Asterisk denotes the species which are considered as associated with the "'clam colony". TABLE 3 Photographic inventory of the benthic organisms and lebensspuren observed in the bottom photographs during dive KD-5 (Nankai Trough/Tenryu Canyon: 3765-3832 m) Organisms Xenophyophore (foliace,ous type) Branching gorgonian Umbellula thomsoni KiSIliker * Actinian (small, white; attached to holothurians) * Actinian (small, white; attached to rocks and bivalves) * Actinian (medium-sized; cerianthid type) * Actinian (large; brown) Bonellid echiuran proboscis * Calyptogena sp. Type I (undescribed) * Calyptogena sp. Type II (undescribed) * Buccinid gastropods Solenocerininae penaeid prawn * Munidopsis sp. * Synallactid holothurian ? Tunicate Ipnops sp. ? Ilistiobranchus sp. * V-shaped furrows produced by bivalves Bulldozing tracks produced by buccinid gastropods~ Large mounds [ Star-shaped traces produced by echiuran worms ]

Abundance

Distribution pattern

1 1

4 abundant abundant abundant several 1 abundant abundant 10 1 4 2

solitary symbiotic gregarious

gregarious gregarious solitary

1

3 1

several

Asterisk denotes the species which are considered as associated with the "'clam communities".

solitary solitary

solitary

332

Through cursory measurements of the collected specimens, crude biomass (wet weight including hard parts) of 16 k g / m 2 was obtained, which is similar to the values reported for the biomass of the giant vestimentiferan worm Riftia pachyptila in the eastern Pacific hydrothermal vent communities [4]. Almost all of the living clams bury themselves about four fifths of their long axis in vertical position with posterior tip being exposed. Reddish-purple tint of the short siphons can be observed in close-up photographs. During sample, some clams were crushed in the jaws of the box core releasing clouds of bright red blood containing large amount of haemoglobin-like pigment. Laboratory scrutiny revealed that the bivalve samples collected by the grab contained three hitherto undescribed species of the same genus Calyptogena. The descriptive work is now underway by Japanese and French malacologists * Whereas the surface layer of sediment near the colony is covered by greenish brown soft mud and studded with polychaete tubes other than serpulid worms (terebellids?), the surface sediment within the dense patch of bivalves appears blackish and coarser in grain, similar in texture and colour to the sediment profile dug about 15 cm deep into the sediment by the box corer. Here and there can be found unusual cracks on the sediment surface exposing white materials, supposedly authigenic precipitation of chemicals, and half-buried boulders also with whitish precipitates a n d / o r bacterial films at their skirts (Fig. la). Chalky white conjoined and disarticulated dead shells (several to about 15 cm long, C. Type 1) of the different Calyptogena species are scattered on the ground either fully exposed or half buried, and it is on or around these microhabitats where actinians of several species and serpulid polychaetes are thriving. Galatheid of the genus Munidopsis are roaming around these biocoenoses and thanatocoenoses, but ingestion or attacking of * During the review process of this paper, the results of the morphological studies became available to us: instead of two species (Type I and II in the tables), the specialists now recognize three distinct species. The larger one (length up to 129 ram) corresponds to our C. Type 1, while the two other smaller species (length 45-80 ram) correspond to our ('. Type II. They cannot be distinguished on the pictures.

other organisms by them cannot be witnessed in the bottom photographs. Huge holothurians supposedly of the family Synallactidae with six distinct longitudinal rows of papillae on their lateral and dorsal sides are another conspicuous member of the community (Fig. lb). Each of them carries two to sixteen small actinians on their lateral borders, especially in the anterior half of the body. Recurrent diving (KD-5) four days later on the same spot explored by dive KD-3 found that the same pair of holothurians remained there within the range of I m (Fig. lc). They tended to stay and possibly feed on the sea floor disturbed by manipulators, a water sampler and a grab. In addition to this, comparison of photographic records separated by four days revealed that at least some members of the clams, especially located in the periphery of the cluster, moved around on considerable distance, say more than several tens of centimeters within this period, and the extensive crisscrossing plough marks around the colonies can be ascribed to their frequent horizontal shift. The horizontal movement must be done keeping their vertical position within the sediment with the hinged apex of the shell as leading edge. They leave V-shaped furrows deeply cut into the bottom and contrasting well with the flat-bottomed bulldozing marks produced by the buccinid gastropods. Vertical shift within the same locality seems to be possible. Many lebensspuren correspond with each other between the two photographic records separated in timc, suggesting rather quiet hydrodynamic regimes at the studied area. Far apart form the "colonies" the surface features of the bottom are rather usual as typical abyssal depth with occasional mounds and starshaped feeding traces produced by boneilid worms [5]. Several types of xenophyophores, suspension feeding coelenterates such as gorgonians and the sea pen Umbellula thompsoni, ipnopid and synaphobranchid fishes in the photographic inventories (Tables 2 and 3) are also found in this environment. No vestimentiferan tube worms were found within the communities, while they usually arc dominant in the "subduction-induced seepage communities" off Oregon [6,7] and non-thermal cold vents at the base of the Florida Escarpment [8].

qg. 1. (b) Bottom photograph taken by the submersible Nautile" during dive KD-3 in Tenryu Canyon (3830 m; ,bserver: C. Rangin). Dense bed of Calvptogena spp. (Types I nd II, the later including two different species) and huge ynallactid holothurians bearing actinians on their bodies. Bucinid gastropods can be found here and there.

~'ig. 1. (d) Bottom photograph taken by the submersible 'Nautile" during dive KD-14, eastern landward wall of Japan French (5640 m; observer: K. Fujioka). Dense bed of Calypogena Type III with small holothurians (Peniagone elongata?) :aprellid amphipods and buccinid gastropods. Minute white ,pecks in the clam bed are small rissoacean gastropods.

:ig. 1. (a) Bottom photograph taken by the submersible 'Nautile" during dive KD-3 in Tenryu Canyon (3836 m; ~bserver: C. Rang,in). White stains at the base of an outcropring rock and on the sediment surface may be authigenic ~recipitates of minerals and/or bacterial mats, which suggests rmanation of chemicals from the underlying sediments. Fecal trings, probably of holothurians0 densely scattered over the ;ca floor suggest that the surface sediment is rich in food.

:ig. 1. (c) Bottom photograph taken by the submersible Nautile" during dive KD-5 in Tenryu Canyon (3830 m; ,bserver: A. Taira). The picture covers the same spot explored ,y dive KD-3 four days and one hour before. The same pair of :olothurians are still present. The deep V-shaped furrows are pparently produced by the movement of Calyptogena as it tands upright and ploughs through the .sediment.

334 TABLE 4 Photographic inventory of the benthic organisms and lebensspuren observed in the bottom photographs during dive KD-6 (Zenisu Ridge sediment swell: 4026-4216 m) Organisms

Umbellula thomsoni Ktilliker * Actinian (small, white; attached to rocks) Actinian (medium-sized) * Actinian (large; with blunt-tipped tentacles) Antipatharian coral (? Bathypathes sp.) * Calyptogena spp. Amphipod Crinoid genus sp. (5-armed, yellow) Freyella pennata Sladen (10-armed) Brisingella armillata (Sladen (7-armed) Ophiurid ophiuroid Small asteroid ? Pseudostichopus sp. ? Psychropotid holothurian Peniagone gracilis (Ludwig) Sargassum sp. (drifted seaweed) Circular sweeps around the antipathan corals

Abundance

ca.

1 25 8 5 6 20 1 1 2 1 6 1 1 1 1

Distribution pattern solitary

solitary solitary gregarious

solitary solitary

1

Asterisk denotes the species which are considered as associated with the "'clam community".

Dive KD-6 surveyed a sedimentary swell of 200 m high to the south of the Zenisu Ridge proper beginning at 4026 m. On average, the fauna and density of benthic organisms are fairly depauperate (Table 4) with all its relatively longer transect line on the silstone layers monotonously inclined to the southeast. Dominance of suspension feeders (the sea pen Urnbellula thornpsoni, deep-sea antipatharian coral Bathypathes sp., crinoid and slender-armed brisingid asteroids such as Freyella pennata and Brisingella armillata ) concomitant with sparse surface deposit feeders like holothurians is well in agreement with the general picture observed in the relatively erosive environment of the oligotrophic to mesotrophic abyssal ocean floor. At the northern extremity of the transect, several clam colonies were found at the top of overhanging wall anticlines (depth 4020 m). The clam colonies observed through bottom photographs are small-scaled ones, consisting of only about twenty living Calyptogena (Type II?) and of small whitish anemones attached to outcropping rocks.

3.2. The Japan Trench and Kurile Trench region The "clam colonies" dominated by the fourth

undescribed species of Calyptogena (Type III) was found throughout the abyssal depths along the landward walls of the Japan and Kurile Trenches [10]. The depth range of occurrence of the "clam colonies" was 5640-5695 m in the dive KD-14 traversing the narrowly constricted axis of the Japan Trench to the west of the Daiichi Kashima Seamount, 5479-5960 m on the landward wall of the Japan Trench at the latitude of about 40 ° N explored by two composite dives KD-18 and KD23, and 5131-5785 m on the north landward wall of the western Kurile Trench surveyed by a single dive KD-21. Although all of the Legs 2 and 3 dives cited above cover essentially the same bathymetrical zonation and biogeographical region from faunistic point of view (see Tables 5-8), minor differences can also be pointed out which may be originating from differences in topographical setting. In dive KD-14, "Nautile" reached the bottom of the northern foot of the western half of the Daiichi Kashima Seamount at a depth of 5820 m. The submersible then started to cross the "axis" of the Japan Trench. The Japan Trench has exceptionally narrow and shallower configuration at the

335

diving site, where the Kashima Seamount is now subducting into the concurrent trench with a great vertical fault cutting the volcano into two halves. The axis is level, though very narrow, filled with debris and the surface is blanketted with fine hemipelagic sediments. Surface deposit feeding organisms dominated by holothurians belonging to the genera Scotoplanes, Peniagone and Elpidia are thriving there (Table 5). Climbing up the foot of the landward wall with pronounced alterations of cliffs and benches, distinct benthic communities were found on the benches filled with debris. At the depth of 5640 m, a sizeable benthic colony was located on a small terrace perpendicular to the general trend of fractures (Fig. ld). The dense clam field occupies an area of about

2 × 0.5 m within a small gulley-like trough of several meters width, and the largest and densest clam cluster contains at least 52 living individuals and measures about 1.3 × 0.2 m in the bottom photographs. The vesicomyid clams of very slender form (Calyptogena Type III, undescribed) keep vertical posture within olive-gray soft mud exposing, on average, only one-third of their length. They sometimes carry small whitish actinians on them, and red-fleshed mantle and short siphons can be observed through the gapes of the bivalves. The modified Ekman-Birge box corer of 15 x 15 cm biting area (225 cm 2) caught nine clams, measuring 150-170 mm in length and weighing 50-75 g (wet weight including the shells). Thus the maxi-

TABLE 5 Photographic inventory of the benthic organisms and lebensspuren observed in the bottom photographs during dive KD-14 (transect of the Japan Trench: 5635-5890 m) Organisms

Abundance

Distribution pattern

Xenophyophores (foliaceous type) Branching gorgonian Straight gorgonian Actinian (attached to branching gorgonian) * Actinian (small, white; attached to bivalves) * Calyptogena sp. Type Ill * Rissoacean tiny gastropods * Buccinid gastropods Storthyngura-type isopods * Caprellid amphipods (ca. 3 cm long) Amphipods 10-armed crinoid (? Bathycrinus pacificus H.L, Clark) Phrynophiurid ophiuroid (clinging to stalk projection Ophiura bathybia H.L. Clark Amphiurid ophiuroid (disc buried) Porcellanasterid asteroid (? Styracaster sp.) Pterasterid asteroid genus sp Freyella oligobranchia (H.L. Clark) (6 to 7-armed) Spatangoid (moving on the sediment) Peniagone azorica Marenzeller * ?Peniagone elongata (Threi) (swim in sigmoidal fashion) Peniagone rigida (Threl) Peniagone wyoillei Th~el Elpidia longicirrata Belyaev Elpidia glacialis kurilensis Balanova & Belyaev Scotoplanes globosa (Thc~el) Eiasipod holothurian Coryphaenoides sp. (? C. armatus Hector)

common

solitary

abundant innumerous 7 2 abundant several 6 1 fairly abundant 1 6 several 5 1 1 abundant 4 4 several fairly abundant 20 2 4

gregarious gregarious

Subsurface track of pourtalesiid spatangoid Surface track of spatandoid Asterisk denotes the species which are considered as associated with the "clam community".

solitary gregarious solitary solitary solitary solitary solitary solitary

patchy solitary solitary

solitary solitary

336 m u m density of the clams within the cluster can be calculated to be a b o u t 4 0 0 - 7 0 0 i n d i v i d u a l s / m2, a n d crude wet weight biomass to be about 2 4 - 4 2 k g / m 2. Several m e d i u m - s i z e d buccinid gastropods crawl a r o u n d the clam field, and i n n u m e r a b l e small rissoacean gastropods of about 2 m m in shell height are scattered within and just a r o u n d the clam bed. Caprellid a m p h i p o d s of about 3 cm in length are also a b u n d a n t attaching o n t o small m o u n d s , pebbles as well as on the shells of Calyptogena. Small elpidiid holothurians, p r o b a b l y Peniagone elongata, are loosely centered on the clam field (more than 25 individuals within a 3 m 2 field of view), a n d they frequently swim away flexing their bodies in sigmoidal fashion [11]. T e m p e r a t u r e m e a s u r e m e n t s showed a b o u t

0.3 ° C positive thermal a n o m a l y within the cluster c o m p a r e d to the a m b i e n t water. Rather indurated dark greenish-black mud can be observed within the hole just below the paler surface deposits, and a macrourid fish Coryphaenoides armatus feeds in the excavation. Dives KD-18 a n d KD-23 explored the landward wall of the J a p a n Trench between depths of 5225 and 5938 m, where a sinuous escarpment trends subparallel to the trench axis. C o m p a r e d to dive KD-14, b o t t o m photographs reveal more rugged and hard o u t c r o p p i n g s u b s t r a t u m with configurations of the alteration of steep cliff and bench with scarce talus and debris. At least in the deeper half of these two dives, recent s e d i m e n t a t i o n seems to be weak or nearly absent on crust, p r o b a b l y related to rather strong

TABLE 6 Photographic inventory of the benthic organisms and lebensspuren observed in the bottom photographs during dive KD-lg (Japan Trench landward wall: 5652-5938 m) Organisms

Abundance

Distribution pattern

Branching gorgonian Straight gorgonian Actinian (attached to branching gorgonian) * Actinian (small, white; attached to bivalves) Actinian (medium-sized;solitary) Actinian (large, brown) Actinian (huge) * Tubes of polychaetes (shorter type) * Tubes of polychaetes (longer type) * Calyptogena sp. Type III * Buccinid gastropods Pycnogonid Scalpellum sp. Mysids Storthyngura-type isopods Caprellid amphipod Amphipods (including Epimerta-type) t0-armed crinoid (? Bathycrinus pacificus H.L. Clark) Unstalked crinoid 5-armed crinoid (yellow) Freyella oligobranchia (H.L. Clark) Small asteroid ? Ophiacantha batl~vbia H.L. Clark Peniagone azorica Marenzeller Culeolus-type tunicate Other stalked tunicates Small solitary tunicates (attached to boulders) Coryphaenoides sp. (? C. armatus Hector)

5 1 1 5 6 2 1 abundant abundant abundant 8 1 1 5 20 1 2 10 1 1 1 1 1 3 1 2 20 3

solitary

Trail of the walking of Calyptogena

1

Asterisk denotes the species which are considered as associated with the "clam community".

patchy patchy gregarious

solitary solitary

solitary

gregarious solitary

337

southwest-northeast deep-sea current at these depths. The environmental features are reflected in the dominance of suspension feeding and attached fauna in the photographic inventories (Tables 6 and 7). Clam colonies were found throughout these two dives on sediments. Most of the colonies are small-scaled. Larger colonies occur mainly in the lowest part of the surveyed profile, and their size tends to decrease toward the upper part. The largest colony found at a depth of about 5900 m measures 70 × 45 cm in oval outline containing more than 190 living clams in a rosette fashion. Based on the retrieved specimens and the photographic density estimation, the maximum density

was calculated to be 1500 individuals/m 2 and crude biomass to be 51 k g / m 2. It is only around these large colonies that associated organisms such as buccinid gastropods, small whitish actinians and tube-building polychaete worms can be observed. Average-sized colonies consist of only 8-12 Calyptogena clams and no other remarkable organisms were found around or within them. They are "nesting", tightly bundled and buried in coarse sediment on small pocket-like shelves, and in extreme but not rare cases, isolated clams are hanging from pits on a mudstone. In one occasion, a "walking" Calyptogena was found on a relatively flat topography filled with finer sediment. The clam lay on the

TABLE 7 Photographic inventory of the benthic organisms and lebensspuren observed in the bottom photographs during dive KD-23 (Japan Trench landward wall: 5225-5679 m) Organisms

Abundance

Distribution pattern

Xenophyophores (globular type) Branching gorgonian Straight gorgonian Actinian (medium-sized; solitary) Actinian (large, brown) Branchiocerianthus sp. Tubes of polychaetes (shorter type) * Calyptogena sp. Type III * Buccinid gastropods Mysids Storthyngura-type isopods Sergestid shrimp (swimming) 10-armed crinoid (? Bathycrinus pacificus H.L. Clark) Porcellanasterid asteroid (? Eremicaster crassus (Sladen) Hymenaster sp. Freyella oligobranchia (H.L. Clark) Small asteroid 6-armed asteroid Phrynophiurid ophiuroid Ophiacanthid (mainly Ophiacantha bathybia H.L. Clark) Amphiurid ophiuroid Amphiophiura-type ophiuroid Peniagone azorica Marenzeller Peniagone rigida (Thb,el) Peniagone wyvillei Th~el Scotoplanes globosa (Th6el) Elasipod holothurian Culeolus-type tunicate Other stalked tunicate Coryphaenoides sp. (? C armatus Hector)

abundant 7 16 5 1 2

solitary solitary solitary

abundant 8 12 4 1 17

solitary patchy gregarious

solitary solitary

1

1 7 2 15 1 75 2 2 25 1 3 3 1 2 1 5

Coils and knots of holothurian feces Asterisk denotes the species which are considered as associated with the "clam community".

solitary solitary solitary

solitary solitary

338 TABLE 8 Photographic inventory of the benthic organisms and lebensspuren observed in the bottom photographs during dive KD-21 (Kurile Trench landward wall: 4981-5785 m) Organisms

Abundance

Distribution pattern

Straight gorgonian Actinian (huge) Polychaete worm tubes * Calyptogena sp. Type III * Buccinid gastropods Mysids Ophiacantha bathybia H.L. Clark Freyella oligobranchia (H.L. Clark) Brisingid asteroid (having 10 extremely slender arms) Coryphaenoides sp. (? C. armatus Hector)

2 1 many abundant 1 10 1 1 1 5

solitary

gregarious

solitary solitary

Asterisk denotes the species which are considered as associated with the "clam community".

sediment in horizontal position keeping its hinged edge upward. A 1 m long trail sharply cut into the sediment followed the clam. It is hard, however, to conceive whether or how the hanging clam manage to arrive at a pit in the mudstone via hard substratum with use of its foot. On rare occasions boulders with whitish stains at their feet were found, suggesting authigenic precipitation of chemicals probably welled out from the sediment a n d / o r bacterial mats. However, no moir6 of water or blackish sediment can be found around the colonies and such boulders. As for the north landward wall of the Kurile Trench which was surveyed by KD-21 between 4981 and 5785 m (depth range covered by bottom photographs), the occurrence and situation of clam colonies were essentially the same as in the landward wall of the Japan Trench at 4 0 ° N . Living Calyptogena (Type III) can be observed between depths of at least 5770 m and 5130 m, and even on a small ledge in an almost vertical cliff of siltstone. Only slightest positive thermal anomalies of few hundredths within the colony associated with buccinid gastropods and polychaete worm tubes were reported. Reflecting the steeper topography, seemingly swept by stronger bottom current which produces distinct ripple marks on the debris floor, the photographic inventory embraces scarce organisms, both in number of individuals and in species composition, composed mainly of clinging a n d / o r swimming animals (Table 8). Some kind of holo-

thurians and abundant planktonic organisms were reported to be present by the diving scientist.

4. Discussion From a total number of 27 dives of the submersible "Nautile" in the subduction zones east and south of Japan performed during the FrenchJapanese Kaiko project, the analysis of the bottom photographs proved that fairly luxuriant communities dominated by four undescribed species of giant bivalves of the genus Calyptogena were consistently present on the accretional prism area in the abyssal part of the subduction trenches, at depths ranging from 3787 m in the Nankai Trough to 5960 m in the Japan Trench. At first glance, these animal communities found off Japan recall those previously discovered in the vicinity of hydrothermal vents at ocean spreading centers in the Gulf of California, Guaymas Basin [13,14], in the sulfide-rich hypersaline water seepage at the foot of the Florida Escarpment [8,9,12], in the seepage vent sites along the subduction zone off Oregon [6,7], in the oil and gas seepage bathyal sites on the Louisiana continental slope [15] and in the upper bathyal depth of Sagami Bay, southeast of Hatsushima [16]. Detailed analyses of photographs show that the newly discovered benthic oases differ in several aspects from the five preceding sites. Although the Calyptogena community can be found over rather wide areas, it is composed of a loose set of separate

339 insular components of small colonies with a diameter of one to two meters. Those components are always characterized by a very dense aggregation of vesicomyid bivalves, which represent the major part of the total biomass. Associated organisms living around the bivalve colonies vary considerably from place to place and depth, which might be related to the size of the bivalves colonies. In a sense, the Calyptogena community off Japan can hardly be considered as a semi-closed ecosystem of fairly complete sets of organisms from primary consumers to higher carnivores, as in the hydrothermal vent communities of the East Pacific Rise [4]. For example, buccinid gastropods, small white actinians and tube-building polychaetes are fairly constant associates to the bivalves colonies, but it is hard to recognize them in very small beds of clams. Rissoacean small gastropods and caprellids were found with certainty only in one large colony in the Daiichi Kashima Seamount area (KD-14), but in tremendous amounts. Munidopsis sp., a possible predator or scavenger in the Tenryu Canyon communities, cannot be found in other localities. The large macrourid fish Coryphaenoides armatus may play a similar ecological role in the latter communities trespassing frequently on the bivalve beds. A stone crab Paralomis multispina present in the Sagami Bay could be the counterpart of Munidopsis sp. from Tenryu Canyon. In some places, holothurians are abundant around the colonies (a large synallactid in the Tenryu Canyon and Peniagone elongata in the Daiichi Kashima Seamount); they are not present in other areas. Consistently, no Vestimentifera could be found throughout the present study, whereas one of us (S.O.) recognized recently what appear to be a Vestimentifera in video records taken recently by the Japanese submersible "Shinkai 2000" in Sagami Bay, at 1300 m depth [10]. Generally speaking, the overall specific composition of the bivalves communities is highly variable, and their specific diversity appears to be very low due to the extraordinarily high densities of the Calyptogena species. There is no specific predator associated with the bivalves; on the contrary, opportunistic suspension and deposit feeders from the abyssal ocean concentrate in the vicinity of the bivalves colonies. Apart from their high biomass, several pre-

liminary results and comparison with existing data from similar animal communities enable us to identify the trophic energy source of these Calyptogena communities. A first set of data comes from the topographic situation of the bivalves colonies. All the diving observers pointed out that the clam beds are arranged more or less parallel to the structural topographies, along the trend of flexures or strike-slip faults in the geotectonically controlled compressive deformation areas. At the same time, they are located in areas of obvious but spatially limited erosion [1]. Such a situation differs markedly from the distribution of Calyptogena pacifica on the sulfide smelling sediments of the Guaymas Basin, where the bivalves are more or less regularly scattered on large areas, with local concentrations [13,14]. Indication of authigenic precipitation just at or below the sediment surface a n d / o r bacterial mats were observed in the Tenryu Canyon (KD-3 and KD-5), in the Kashima area (KD-14) and on the inner wall of the Japan Trench (KD-23). Slight but positive temperature anomalies have been measured within the clam colonies, ranging between 0.2 and 0.6°C, and results of geochemical analyses on the water samples (decrease in pH, high contents of SiO 2 and CH 4, low ratio of methane to ethane plus propane [17], demonstrate the occurrence of seepage of pore water containing thermogenic methane. The pore water flux probably originates from several kilometers depth in the squeezed sediments. Methane carbon isotopic ratios (13C/12C) show ~3C depletion values of -40700, indicating that the methane originates from the reduction of organic matter contained in the sediments under high pressures and temperatures over 4 0 ° C [17]. A second set of data comes from ecological considerations. Estimates of the maximum densities of Calyptogena (400-2000 individuals/m 2) and biomasses (16-42 k g / m 2) represent a striking contrast with the average total biomass evaluations of the order of less than 0.1 g / m E at the equivalent depths of 4000-6000 m in the entire regular deep-sea ecosystem whose energy is sustained primarily by surface photosynthetic production [18]. Such a difference in biomass (several times 100,000 higher), together with the sudden change of biomass at the border of the colonies (occurrence of extremely strong ergoclines) cannot

340 be explained through local concentrations of particulate organic matter originating from the photosynthetic pelagic production nor land vegetation detritus. Such high biomasses clearly involve some kind of local source of energy. We hypothesize that chemicals squeezed from the sediment by subduction forces and carried out by the pore water circulation constitute this energy source. The reason why the pore water seeps occur in very small spots, instead of interesting large areas like in the hydrothermai vents of the Guaymas Basin or the cold seeps of the Oregon subduction zone, remains poorly understood. Some kind of channelization linked with selective erosion of the surface sediment is probably part of the explanation; the bioturbation created by the Calyptogena could also play a role either beginning the process either increasing the surface of the seepage area. The erosion processes play an important role for mid-scale distribution, but do not completely explain the small-scale distribution (distances of the order of 1 m). All four species of Calyptogena contain high concentrations of respiratory haemoglobin type pigment (unpublished results from Japanese laboratory; other species of Calyptogena such as C. magnifica from hydrothermal vents also contain haemoglobin). This fact suggests that the oxygen demand for these Calyptogena is higher than usual for deep-sea bivalves. Some observations of the ultrastructure of the gills of Calyptogena Type III are reported elsewhere in this issue: they have demonstrated the occurrence of numerous endocellular bacteria [19]. Analyses of carbon isotopic ratio in the soft tissues of the same species achieved by the same group of authors record ~3C depletion values of - 4 0 % in all tissues (gills, foot, mantle, viscera), identical to the figures obtained on methane from the water samples. These results strongly suggest that the bivalve utilizes a local carbon source different from photosynthesized organic carbon, and that the carbon used comes from the thermogenic methane through some kind of chemosynthetic processes involving the endocellular bacteria. In the case of the giant mytilid and vestimentiferans living in the cold seeps of the Florida Escarpment, recent results hypothesize a rather complicated model to accommodate low values of ~3C depletion of -75%o in soft tissues of the mytilid and

high percentage of recent ~4C in the total organic carbon: the hydrogen sulfide a n d / o r ammonia could be utilized by free bacteria living in the sediment, giving birth to organic matter; this organic matter could then be reduced by anaerobic methanogenic free living bacteria and the methane produced used as an energy source by chemosynthetic bacteria living in invertebrates cells [ 12]. Similar and more recent data come from the bivalves living near oil and methane seeps found at 600 m on the Louisiana continental slope [15]. Calyptogena ponderosa and Lucinoma atlantis show 13C depletion of respectively - 3 5 and - 3 1 to -33c/~, while the oil and methane have respectively values of - 2 6 . 5 and -45%c. These isotopic values provide supporting evidence that the food source of the bivalves is sulphur or hydrocarbon oxidizing bacteria in this hydrocarbons/sulfide rich environment. On the Oregon subduction sites, 13C depletion values of -51.6%o have been reported for the gills of Calyptogena sp. (probably C. magnifica), which suggests that CH4, usually strongly enriched in u C , is venting from the accretionary complex and sustains the macrobenthos via microbial symbionts capable of oxidizing CH4 [7]. Chemical analyses performed on the water sampled during the dives just above the Calyptogena communities do not reveal either hydrogen sulfide or ammonia. This in fact do not imply that these chemicals are not present in pore water and consumed by chemolithotrophic bacteria within the last layers of bioturbated sediments. Anyhow, present results suggest that methane could be directly used as energetic substrate oxidized by endocellular chemosynthetic bacteria, which in turn transfer their metabolites and organic content to the bivalves without changes in 13C depletion. However, it is impossible to determine the detailed pathways of the trophic energy: there could well be some biogeochemical differences between the pore water 10 cm below the sediment surface and the water sampled by the submersible. The situation of the living bivalves buried about four-fifths of their length in the sediment may also imply some kind of mixotrophic mechanisms. In the case of Calyptogena magnifica. evidences come from enzymological studies and from the fact that the very reduced digestive tract appears empty on all presently examined specimens. We know nothing about the anatomy of the

341 digestive tract of the new species of Calyptogena from Japan, a n d no enzymological studies have yet been achieved. However, the aggregation of s u s p e n s i o n feeders a n d p l a n k t o n i c organisms near the clam colonies shows a local increase of the density of available particulate matter a p p a r e n t l y c o m i n g from the bivalves colonies. A l t h o u g h much work remains to be done, the distribution, disposition a n d densities of the bivalves colonies can only be explained in the context of chemosynthetic m e c h a n i s m s using chemical sources squeezed out from the deep sediments a n d carried to the surface by the pore water circulation. O n e can predict that the long-term persistence at a worldwide scale of the seepage c o m m u n i t i e s along the s u b d u c t i o n zones of the ocean and passive margins and c o n t i n e n t a l $lopes where hypersaline solutions or h y d r o c a r b o n s seeps occur, will involve the evaluation of their possible c o n t r i b u t i o n to the deep-sea ecosystem as a whole, through exportation of organic matter by active p r e d a t i o n a n d particulate organic matter p r o d u c tion. It must be u n d e r l i n e d that cold seeps comm u n i t i e s have a wider geographical spread than the hot or warm waters [20]. The m o v i n g ability of the clams in the b o t t o m sediments presents a n o t h e r interesting aspect. Whereas the clams can move a b o u t r a t h e r freely w i t h i n the s e d i m e n t s , graveyards or thanatocoenoses of clams can be observed within or at the CCD. D o those graveyards come from the local i n t e r r u p t i o n of pore water seepage, or do they result from intense p r e d a t i o n pressure? T o what extent does the possibility of adult migration c o n t r i b u t e to the geographical d i s t r i b u t i o n of these species, a n d to their adaptive strategies for survival in the supposed u n s t a b l e e n v i r o n m e n t locating new c o n d u i t s of seepage? This is one of the questions to be answered through detailed analyses of the b o t t o m p h o t o g r a p h s together with the elucidation of the reproductive biology of the clams.

Acknowledgements The authors wish to express their sincere gratitude to the Kaiko scientific c o m m i t t e e ' s chief scientists of each relevant leg a n d all p a r t i c i p a n t s of the project for placing the biological samples, image records of the u n d e r w a t e r camera a n d TV

together with o t h e r i n v a l u a b l e i n f o r m a t i o n s a t t h e i r disposal.

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