Oases at the bottom of the ocean

Oases at the bottom of the ocean Lucien Laubier and Daniel Desbruykes In the early 1980s biologists were amazed, and sometimes sceptical, to be told of the existence of luxuriant fauna thriving at depths of between two and three thousand metres close to hot water springs. Frequently consisting of hitherto unknown species, these colonies are nothing less than oases, contrasting starkly with the deserts usually to be found at great depths. One of their features is a very short life cycle. But, most strikingly, they are the first discovery on our planet of living systems which survive without solar energy or photosynthesis.

Not more than a few years ago marine biologists specializing in the ocean floor could have been excused for believing that the age of exploration of the great depths was over. In the early 1950s the Danish research vessel Galathea had established that life was present at the greatest depths known, more than 10 000 m below the surface. Since then, it had been established that, though life might have no lower limit in the oceans, the primary characteristic of the fauna of the great depths was its sparse distribution. However, despite popular belief, the almost deserted appearance of the great depths is the result neither of the water temperature, barely above O”C, nor the total absence of light, nor yet the pressure of around 1000 bars - life is scarce for the Lucien Laubier Is s senior scientific adviser in IFREMER (Institut Fran@8 de Recherche pour I’Exploitation de la Mer). which was created as a result of the merger of CNEXO (Centre National pour I’Exploitstion des Mans) and ISTPM (Institut Scientifique et Technique des P&he8 Msritimes). One of the founders of modern French, resesrch into deep ocean ecology, he cooperated with Dsniel Desbruybres on research into hydrothermal populations with a study of the Pompeii worm, one of the strangest of all invertebrates in this very strange world. He is a correspondent of the French Academy of Sciences. Daniel DesbruyBres Is a marine biologist working at IFREMER’s Brest ResearchCentre.Hewaschiefscientistofthefirst two French cruises of research into populations associated with submarine hydrothermalism Biocyatherm, in 1982, and Biocyarise in 1984.

see p. ii Ednvwr, NBW Ados, Volume S. No. 2. 1905. 016o-s327m $0.00 + 50. brwnom Pros& Rlntod in Groat Britain.

simple reason that food is likewise scarce. Biology had, therefore, nothing radically new to expect from the new programmes of deep-water exploration which began in 1977. They were designed to give geologists the opportunity for in situ study of the generation of new crust along the oceanic ridges, which was expected to be accompanied by hydrothermal phenomena resulting from the circulation of sea water within the vast network of fissures and crevasses. These negative expectations proved to be at total variance with reality. During the spring of 1977 the US Navy submersible Alvin, diving over the Galapagos Ridge on the Equator at about 86”W where, one year previously, the American Pleiad Expedition organized by the Scripps Institution of Oceanography had brought back remarkable photographs of the ocean floor showing life flourishing around hot water springs, confirmed the importance of this discovery. Entire animal communities were seen growing around the outlets of hot springs in exuberant colonies of creatures of stunning morphology and size. These were nothing less than oases, in stark contrast to the usual desert of the ocean depths. The first observers, geologists and geochemists, used an evocative range of names to describe them: the clam bake, the mussel bed, the Garden of Eden. Two years later, it was the turn of American biologists to dive over this area for further observations, sampling, and experimental work [l]. In 1978 the French submersible Cyana began exploring a section of the Eastern Pacific Ridge around 21”N. There, some distance from massive polymetallic sulphur structures like anthills, observers discovered a number of zones covered with the abandoned shells of one of the two large bivalve molluscs found at the Galapagos. One year later, the same teams on board the Alvin discovered, only a few kilometres away, the famous black

smokers: jets of superheated black water ejected from chimneys formed from deposits of polymetallic sulphides. Around the smokers, the animal colonies were reminiscent of those of the Galapagos, but extended over even wider areas. American biologists and French researchers made a series of dives in the Alvin over this site during spring 1982. Two years previously, research by Jean Charcot had established that hydrothermal phenomena were widespread along the axis of the Eastern Pacific Ridge, from 21”N over a distance of 2400 nautical miles as far as Easter Island at almost 20%. One of the sites thus identified at 13”N was the scene of the first French research programme organized by biologists (Biocyatherm), in March 1982, where animal populations associated with hydrothermal phenomena proved to be particularly abundant (figure 1) [2]. In another geological environment American biologists were carrying out observations in the Guaymas Basin in the Gulf of California, where basalt bedrock is covered by almost 400 m of sediment, and the ocean floor is covered with a thick layer of filament bacteria of the genus Beggiatoa, with the main species of ‘hydrothermal’ invertebrates likewise being present. During summer 1983 a Canadian team using the Canadian vessel Pisces IV studied a new type of hydrothermal population associated with emissions centred on a volcano on the Juan de Fuca Ridge of British Colombia at 46”N and at a depth of 1570 m. Finally, in March 1984, a French team made a second visit, two years after its discovery, to the Pacific hydrothermal site situated at 13”N. Comparison with the detailed observations carried out in March 1982 showed the scale of fluctuations in the flow of hydrothermal fluids around a single spring, or even a group of springs, and provided original data on the various species’ tolerance of variations in the physico-chemical environment. The animal populations of the various sites 67

Figure 1 Artist’s impression of a submarine site reconstructed from observations made along the East Pacific Rise at 13”N from the French submersible Cyana. Next to the polymetallic sulphide chimneys, which eject a plume of blackish superheated water (350°C). there are other springs which emit a whitish fluid at intermediate temperature (150 to 270°C) and simple flows of tepid water (15 to 40°C). The various animal species are distributed around the springs in concentric rings, depending on their tolerance of heat and the chemical composition of the fluids. The chimneys, which can reach 15 m in height, are frequently colonized by the Pompeii worm, A/vine//a fompeiana, which lives inside whitish tubes. A large crab, Cyanagraea, feeds almost exclusivelyon A/vine//a. Serpulidae, small worms secreting whitish calcareous tubes, are particularly numerous, several hundred to the m*, and form rings ten metres or so in diameter around the base of the chimneys. One of the most typical species the large pogonophoran worm Riffia, which can reach 2 metres in length. It can be recognized by its reddish terminal branchiae extending beyond the end of the tube. Riftia is the main source of food for Bythograea thermydron crabs and zoarcid fish. Also visible are the large bivalves, Calyptogena (white) and Bathymodiolus (yellow). The wealth of fauna around the hydrothermal springs is in stark contrast with the deep ocean desert only a few dozen metres from the spring. Graveyards of bivalve shells and empty tubes (right) are evidence of former hydrothermal activity, whose lifespan, like that of its associated fauna, is relatively short.

have been investigated share five major characteristics. Firstly, they are remarkable for their abundance or, to be more precise, their biomass. Estimates made in the Galapagos for the giant pogonophorous worm Riftia (see below) give figures of the order of 10 to 15 kg/m’, whilst biomass at equivalent depth (2500 m) is normally of the order of 0.1 to 10 which

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g/m2 for the entire regular population of the ocean depths [3]. Secondly, they are closely associated with the presence of active hydrothermal springs. The various species are distributed around the spring in concentric circles dependent upon their tolerance of temperature and the chemical make-up of the fluids. Only a score or so metres from the springs the

deep ocean floor reassumes its habitually deserted appearance. The existence of cemeteries of bivalve shells in areas where hydrothermal activity has ceased confirms that life is impossible for such species in the absence of hydrothermal fluid. Thirdly, they consist of species which were usually previously unknown, and much bigger than their phylogenetic

neighbours. Most of the new species belong to groups whose existence was already known, but at least two examples of ‘living fossils’ have been discovered in these zones. Fourthly, they show a relatively low degree of specific diversity; lower, in any event, than those shown by the creatures more usually found at such depths. Classically, limited specific diversity corresponds to a relatively young ecosystem capable of high productivity in a fluctuating physicochemical environment. Finally, throughout the various sites investigated, their composition remains fairly constant, which is all the more remarkable since man’s knowledge of even the bettter known sites is far from complete. This consistency immediately raises the problem of how the species are propagated from one site to another.

Temperatures

of 350°C

Among the problems raised by the existence of hydrothermal springs, those of the temperature of the water and the composition of the fluids have been widely studied in the search for an explanation for the extraordinary biomass of hydrothermal communities Geochemical research into samples of hydrothermal fluid taken in the Galapagos and in the black smokers of 21”N indicate that the composition of the primary hydrothermal solution for the Galapagos very closely resembles that of the samples taken from the jets of the black smokers at 350°C. Account must, of course, be taken of the widely varying dilution of the primary hydrothermal solution before its arrival at the ocean floor. In the case of both 21”N and 13”N the same site has black smokers producing a virtually undiluted solution whose temperature can reach 350°C; white smokers, also known as diffusers, emitting a more or less diluted solution whose temperature can vary between 150” and 270°C; and systems of fissures emitting highly diluted fluids whose temperature scarcely exceeds a few tens of degrees, but which produce a moire effect linked with their refractive index which differs from that of seawater (figure 1). On other sites, only low-temperatures moire waters are emitted; this is the case at the Galapagos where temperatures recorded by biologists have never exceeded lS”C, although this is considerably in excess of that of the surrounding seawater, at approximately 2°C [4]. Nothing is known of the tolerance of hydrothermal organisms to mineral salts and the metal salts contained in the fluids. The fluid emitted by black smokers is

lean in oxygen and nitrogen but rich in sulphur. Concentrations of several millimoles of hydrogen sulphide per litre have been measured. In the Galapagos the concentrations of oxygen, nitrogen, and sulphur vary, and this indicates the relative degree of dilution of the hydrothermal fluid with seawater before it arrives at the ocean floor. It is the simultaneous availability of these three components which allows the development of primary bacterial production of a most unusual nature. Water samples taken from locations identified precisely by reference to the population are still rare, and the environment is, therefore, defined by reference to temperatures recorded by probes operated by the vessel. In comparison with the ambient temperature (2°C at the Galapagos Islands; 1.7”C at 13”N), the presence of living organisms can be observed up to 35°C but the area showing the greatest abundance of species lies between a degree above ambient temperature and 20°C (21. Certain organisms can tolerate marked temperature gradients, with the dilution limited by a very low degree of permeability; this is the case of the mass of parchment-like tubes constructed by the worm Alvinella pompejana (christened Pompeii worm by the geologists because it can tolerate a permanent shower of metallic particles), through which tubes a whitish fluid escapes on contact with seawater. At their surface, where the plumes of the worm’s four pairs of branchiae develop, the temperature is between 20” and 30°C; it rises to over 100°C when the probe is inserted to a depth of some 12 centimetres in the mass of tubes, and 250°C when inserted to its maximum length, 20 cm! The appearance of hydrothermal fluid emissions varies according to its temperature. Black smokers have one or more outlets some ten centimetres in diameter borne at the top of chimneys whose height can exceed 15 m; on the other hand diffusers, which support abundant colonies of Alvinella, have no orifices of significant dimensions and produce low temperature anhydride inorganic deposits. The appearance and flow of producers of moire water vary with the temperature at emission: in the Galapagos tepid water is emitted from multiple fissures in the basalt sea bed, while at 13”N water is ejected from the foot of sulphur edifices of varying degrees of solidity, or along the walls of the lava lakes which are abundant in the central valley. Animal colonies can also help in the conservation of the nutrient fluid: bushes of Riftia in particular appear able to form a protective cage inside which the fluid conserves its pbysico-chemical properties on a large scale.

New species

and living fossils

The first indication that one is approaching an active site is given by species of galathaeid crustacean of the genus Munidopsis, already well represented in the ocean depths. An increase in concentration of Munidopsis, whose white colour stands out clearly against the surrounding basalt, is used by those steering the submersibles to pinpoint springs. The species appears to tolerate quite high temperatures, since it is found even within the bushes of Riftia and on the chimneys (figure 2). The next zone encountered is marked at 13”N by the abundance of two species of bristle worms (Annelida polychaeta) belonging to the family of Serpulidae and not hitherto described, whose calcareous tubes can attain densities of several hundred per m* (figure 2). This ring of Serpulidae is some 10 m across. In this zone was discovered a primitive cirriped crustacean attached to the ocean bed by a peduncle [5]. Given the name Neolepas zevinae, it may be that this creature found refuge against stronger predators in active tectonic zones in shallow tropical waters, and that this ultimately allowed it to descend to greater depths. Also found in the outer part of the ring of Serpulidae is Thermopalia taraxaca , a fragile member of the Siphonophora - close relatives of the jelly fish - which the geologists had already named ‘dandelion’. There is practically no variation in temperature within this zone, apart from individual crevasses from which slightly warmer water (+ 1°C compared with the ambient water) may escape. Next comes an even smaller zone, a few metres in diameter, at the centre of which is found the hot spring. Both in the Galapagos and at 13”N the outer limit of this zone, where the temperature gradually rises a few degrees over ambient temperature, is marked by the presence of a large, yellowish-shelled bivalve of the mussel family, Bathymodiolus thermophilis (figures 3 and 4). Next comes another large white bivalve, Calyptogena magnijica (figure 4), its tissues rich in haemoglobin, and the seething bushes formed by the white, semi-rigid tubes of the giant pogonophorous worm Riftia pachyptila, which can attain a length of 1.5 m and a diameter of 4 or 5 cm (figure 3). The organ closing the tube (obturaculum) and its terminal plume of bright red branchial lamellae extend some 15 cm beyond the extremity of the tube [6]. Its size and brilliant colouring make Riftia by far the most spectacular hydrothermal species. Frequently, the tubes of Riftia support small gastropod molluscs having the form of a Chinese hat (figure 3) including, amongst others, representatives of a new 69

Figure 2 The lushness of the hydrothermal populations is spectacular in comparison with neighbouring basalt lava-beds. Submarine photographs taken at 2160 m on the East Pacific Rise at 13”N. In the foreground are the calcareous tubes of the serpulidae which mark the perimeter of the colony. Galathaeid crabs and zoarcid fish roam in search of food amongst the bushes formed by the giant pogonophorous worm Rifria pachypfila, whose reddish terminal branchiae can clearly be seen. Behind the vessel’s remote control arm a zone of moire water betrays the presence of a tepid hydrothermal fluid vent. (Biocyatherm programme, 13”N. Photo: IFREMER)

species, Neomphalus which, like Neolepas, is a member of a group previously thought to have become extinct. Only one species has been described, but at least 10 different forms have been reported. The temperature in this zone

varies between and 12°C. Within the bushes formed by the tubes of Riftia a number of other species hunt and hide from each other: Pachycara, a fish of the Zoarcidae family (figure 2); a small octopod cephalopod mollusc (figure 5);

Figure 3 In the immediate vicinity of, and at most only a few metres from the hydrothermal fluid vent, the population is particularly well developed. On the tubes of Riftia, visible in the foreground, can be seen the circular greyish marks which are small Chinese-hat shaped gastropods. On the left is a group of yellow-shelled modioli; this bivalve has so far been found only in the Galapagos site and at 13 North. (Biocyatherm programme, 13”N. Photo: IFREMER)

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Figure 4 At the Galapagos site the two great bivalves Calyprogena (white shell) and Barhymodiolus (yellow shell) cohabit along fissures which vent hydrothermal fluid. Between the white valves of Calyprogena can be seen the soft haemoglobin-rich tissue, a feature which is exceptional within this group. A number of empty shells can be seen, and its potential for movement is shown by its retractile foot. Sea anemones are abundant around the fissure zones. (Galapagos programme, 1979. Photo: R. R. Hessler, Scripps Institution of Oceanography.)

and a quite ordinary-looking crab whose morphology has nevertheless justified the creation of a new family, Bythograea rhermydron [7]. In these creatures the ocular peduncle, where the eyes are located and which is normally developed in the young of the species, gradually atrophies as the crab sloughs its carapace and partially masks it, All three - fish, cephalopod, and crab - are carnivorous and feed principally on the terminal plumes of Riftiu. This grazing, like that of flat fish on inshore bivalves, is not fatal to the animal. Other invertebrates, including shrimps and ringed worms, are also found within the bushes of Ri’ia. The temperature of the hydrothermal fluids exceeds some 30°C at the centre, where colonies of Pompeii worms (Alvinella pompejana) [8] (figure 6), are found, along with another more primitive form for which the genus Paralvinella [9] was created. The latter builds mucous tubes which it nevertheless freely abandons to roam over the substrate; it tolerates lower temperatures and is frequently found within the bushes of Riftia. Alvinella is the most thermophilous species of invertebrate currently known, which is why it is not found at the Galapagos. The creature is found in two distinct forms whose interrelation is still unknown, although from the morphological point of view they appear to belong to one and the same species. Alvinella can tolerate temperatures ranging from 20 to 40°C. It can develop

Figure 5 On several occasions biologists noted a small white cephalopod octopod moving amongst the tubes of Rifha or in the ring of Serpulidae. Not one of these agile little creatures, whose pale arms have only a single row of suckers, has vet been captured. During the March 1984 Biocyarise programme one entered a basket put down by Cyana and was seen inside the basket when it was recovered and placed into the shuttle which was to return samples to the surface. Regrettably, the creature escaped on its way to the surface. (Biocyatherm programme, 13”N. Photo: IFREMER)

into massive colonies covering the white smokers or diffusers, and is also found along the walls of the tall chimneys of polymetallic sulphide which terminate in black smokers. Despite its remarkable tolerance of high temperatures Alvinella is not immune to predators; a large crab closely related to Bythograea lives and feeds on the Afvinella colonies [lo]. The crab, named Cyanagraea praedator (figure 7)) appears from photographs also to be found at 21”N. Despite our somewhat incomplete knowledge of several hydrothermal sites a significant biogeographical pattern is beginning to emerge: whenever the ecological conditions required by any particular species are fulfilled, that species can be expected to be found. For example, during the March 1984 research at 13”N a fragment of shell of Calyptogena was discovered, evidence of its recent presence in the area. The general organization of the population is becoming clearer: a fairly varied group of organisms which can be regarded as primary consumers, since they feed on bacteria at the bottom of the food chain, is exploited by a small number of carnivorous species. The association between predator and prey can become fairly close when, as a result of its exceptional tolerance of the physico-chemical conditions imposed by the hydrothermal emission, the prey manages to colonize an isolated microbiotope. Since 1979 some 60 new spe-

Figure 6 At the top of a chimney some 15 m high the colonies of A/vine//a mark the final level of life only tens of centimetres from the axial vent from which superheated fluid (over 300°C) is escaping. The tubes inhabited by worms can be distinguished by their whitish colour (attributable to anhydride) against the ochres and blues of the hydrothermal minerals. At the mouth on one of the tubes can be seen six of one worm’s eight terminal branchiae. (Biocyatherm programme, 13”N. Photo: IFREMER)

ties have been described, but not all of them are necessarily associated with hydrothermal phenomena. Creatures

with

no digestive

tract

The extraordinary luxuriance of hydrothermal populations is in stark contrast with the poverty of surrounding areas where the low levels of organic matter limit biological production. In 1977 an American geophyicist, P. Lonsdale, put forward two hypotheses which could account for this extraordinary wealth [ll]. The first assumed that organic particles concentrate around the hot spring as a result of the horizontal currents caused by convection with the emission of hot fluid into the surrounding cold water. The second involved bacterial chemosynthesis, with organic matter being synthesized locally by bacteria from the inorganic compounds present in the hydrothermal fluid and from dissolved CO*. Such bacteria are known as autotrophic, in contrast to the heterotrophic organisms whose energy is derived from the breakdown of organic matter. Although the first hypothesis cannot be ruled out totally, there are indications that bacterial chemosynthesis is the more probable origin of the food chain, the more convincing of them are based on the quantities of natural stable nitrogen isoto es in animal protein. The ratio of “N to r4N rises as

Figure 7 One of the zoological discoveries of the March 1982 Biocyatherm programme was the capture of several specimens of a large crab living at the surface of the chimneys colonized by A/vine//a. Examination of these crabs led to the creation of a new genus in the family of Bythograeidae, named Cyanagraea. The crab is large 15 cm shell diameter - and its stomach contents suggest that it feeds almost exclusively on A/vine/la. Cyanagraea is closely associated with active black and white smokers. (Biocyatherm programme, 13”N. Photo: IFREMER)

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organic matter progresses up the food chain, but it is close to that of inorganic nitrogen in the species found close to the most abundant hydrothermal springs, while it is higher in the deepsea creatures whose nitrogen intake is in the form of detritus; that is dead organic matter - animal cadavers, faecal matter, etc. A simple food chain can thus be envisaged: chemosynthetic bacteria living free in the ocean water serve as food for the populations of filter-feeding invertebrates which themselves are the prey of carnivores. A team of American microbiologists working under J. H. Tuttle recently demonstrated that the rate of metabolic activity of the bacteria present in the water emitted by the springs is in fact too low to explain the biomass and high growth rates of the invertebrates [12]. The metabolic energy must therefore have other more complex origins which link the bacteria producers and the primary consumers in a close symbiotic relationship. The most intriguing of the symbiotic associations involves Riftia pachyptila (figure 3). This tubular worm develops bushes one to two metres in height around the vents emitting low temperature (20 to 30°C) hydrothermal fluids. The temperatures decrease from the base of the bush, where they can reach 13°C to the branchiae, at 4 or 5°C. This organ, which terminates in an operculum, is the only part of the worm protruding from the tube and can be rectracted rapidly when conditions become hostile. All known members of the family of the pogonophora have no digestive tube, and they are thus frequently quoted as the classic example of transepidermal nutrition by organic matter dissolved in seawater. Such an explanation may be plausible in the case of the smaller species but is somewhat unconvincing for giants such as these, whose absorption surface is small compared with their volume, The means by which this species feeds was therefore obscure. The first indication of bacterial symbiosis was found in 1981 during research [13] into a highly-irrigated tissue, the trophosome, which fills the trunk cavity of Riftia. The tissue is in fact made up of clusters of intracellular bacteria associated with sulphur crystals. In the same year, H. Felbeck [14] of Scripps Institution of the Oceanography showed that in this tissue there was significant enzyme activity indicative of an autotrophic function in particular enzymes involved in COz fixation (Calvin cycle), and enzymes of the sulphur and nitrogen cycles. The hypothesis of a symbiosis between the worm and chemoautotrophic bacteria deriving their energy from the oxidation of sulphur thus gained weight. 72

phur and therefore to protect the haemoglobin and the intracellular respiratory bacteria from any harmful effects. The worm’s blood is capable of concentrating significant quantities of combined sulphur at the branchiae and of transporting it to the trophosome where the protein with the hydrogen sulphide is transferred to the cells by pinocytosis [18]. The transport of CO2 to the trophosome may be effected directly in liquid form in the liquid blood, since the presence even of high concentrations of CO2 (up to 2 per cent) has only a slight effect on Riftia’s potential for transporting oxygen in its blood. Nevertheless, biochemical and isotopic evidence suggests that the CO2 is in fact transported in the blood vessel in the form of C4 sugar, as in certain plants. Light remains to be cast on a number of questions, in particular the importance of transepidermal absorption of dissolved compounds and the role of the bacteria in the methane and nitrogen cycles. Riftia is, of course, atypical since the absence of a digestive tract in animals is an exception. The study of other species from hydrothermal springs does, however, show that almost all primary consumers in the food chain’ show associations with chemosynthetic bacteria. There is evidence of such associations amongst the giant bivalves where, as in the case of Riftia, a high level of activity of Calvin-cycle enzymes and sulphur metabolism in the branchiae has been discovered. Submicroscopic research [19] has shown high concentrations of bacteria within the cells of the branchial lamellae, and morphologically this symbiosis seems closer in the case of the bivalve Culyptogena magnifica, whose palps around the mouth are much reduced and where stomach contents are inconCar bohydrates compared with mytilid sistent, (horse mussel), where the full digestive Figure 8 Schematic representation of system and annexes are functional. symbiotic relationship between Rifiia and Nevertheless, this morphological and chemoautotrophic bacteria. biochemical evidence does not amount to proof of a symbiotic relationship, since casesof absorption of food substNevertheless, transport of sulphur ances through the branchiae and the compounds by the blood system pre- epithelium had previously been found sents a number of difficulties: they in other bivalves. In areas where hydcombine with haemoglobin to form rothermal activity is falling or dying stable compounds which cannot fix OXY- out the colonies of Riftia and Calypgen; they oxidize spontaneously in the togena appear to be highly sensitive to presence of oxygen and cannot there- the reduced hydrothermal input, while fore be used further by the bacteria; the mytilid survives even in areas where and, finally, they are toxic and inhibit no hydrothermal anomaly has been enzyme reactions in respiration. At detected; that is, after a sharp decrease least one safety mechanism is therefore or even the total disappearance of the needed to provide for the transport of hydrothermal flow. sulphur. Two Californian teams [16, The gastropod Neomphaius fietter171 jointly demonstrated a high- ae feeds by a complex process: analysis molecular-weight protein synthesized of its stomach contents shows that it in the blood vessel which appears to combines branchial filtering with scrapcombine with large quantities of sul- ing by a complex ‘jaw’, the radula. The identical composition of the trophosome and the worm’s muscles as regards certain stable carbon isotopes was disclosed by identical 13C/12Cratios and proved the existence of direct exchanges between the bacteria and the worm [15]. A relatively simple model was then proposed: the worm’s branchiae float in water which is a mix of sulphur-rich hydrothermal fluid and the oxygen-rich seawater, and its circulatory system passes to the bacteria in the trophosome the inorganic components (CO*, sulphurs, etc.) needed by the bacteria for chemosynthesis. The organic carbon thus produced in the trophosome is used by the worm in the form of mobile organic molecules, and the metabolites produced by the worm (spent CO2 and nitrogen compounds) can subsequently be reused by the bacteria (figure 8).

Filter-feeding is however acquired late, the branchiae of the juvenile mollusc not being fully developed, while the jaw is prominent. The main source of food for such animals is without doubt the bacterial populations which develop on most of the substrates [20]. With another species of the same group, found on the Juan de Fuca site, M.deBurghof theUniversityofVictoria, Canada, observed that a number of filament bacteria are fixed to the branchiae and that cases are frequently found of intracellular capture and digestion (endocytosis) of the bacteria by the epithelial surfaces, and it is therefore possible that the system of filtering and scraping is supplemented by endocytosic nutrition. The most puzzling case is undoubtedly that of the bacteria associated with Alvinella pompejana. Both variants of the Pompeii worm have at their surface a large number of filament, cocciform, or spiral bacterial attached along the cuticuiar axes in the creases between adjoining segments of the worm. In addition, other associations are specific to each of the two variants: hirsuta has dorsal expansions composed of filament bacteria linked with a secretion from the creature. The appendages of the posterior part of caudata are highly elongated and their hypertrophied epidermis shows lateral digitations; a number of filament bacteria are present under the cuticle in these areas, forming mats in which the reduced minerals are imprisoned. Lastly, bacterial develop attached to the internal wall of the tubes secreted by the worm on the hydrothermal chimneys. These are chemosynthetic bacteria of the sulphur cycle whose thermal optimum is around 25°C. No internal bacterium has been found, the digestive tract being only slightly different from that of neighbouring species, and apparently functional. High intracellular concentrations of various elements (S, As, Zn, etc.) have been identified in the epidermis, but it has not yet been determined whether these are metabolites excreted by the bacteria or the result of direct contamination by the hydrothermal fluid [21]. The role of the bacteria in nutrition is unclear, but it can be imagined that the worm and its tube, taken together, form a microenvironment which is highly favourable to bacterial chemosynthesis temperature between 20 and 4O”C, abundant sulphurs, high concentrations of products of the worm’s metabolism, etc. The bacteria can, therefore, enrich the fluid in the tube in dissolved organic compounds and thus contribute to transepidermal absorption. In certain coastal annelidae - tube-dwelling worms - transepidermal absorption of small organic molecules can provide up

to 80 per cent of the creature’s energy requirements for respiration. Only radioactive tracer experiments will provide any estimate of the role of bacteria in nutrition. Though attractive, in situ experimental work using the remote-control arm of the submersible presents a number of technical problems. One technique frequently used at present is on-board recompression of the creatures, but the influence on their physiology of decompression and recompression has not yet been fully investigated. To summarize, the first link in the food chain consists of chemosynthetic bacteria which use inorganic compounds reduced from the hydrothermal fluids. These bacteria can live either freely in the seawater or on inert surfaces, or be associated with animal tissue. Such associations between primary producers and consumers can be of varying degrees of closeness, ranging from the obligatory symbiosis of Riftia to the wide-open systems of the mytilid or the Pompeii worm. The one feature common to these associations is that they operate only in the immediate springs. vicinity of hydrothermal Although symbiosis would seem to be the most profitable nutrition strategy, it does call for the existence of large-scale detoxification processes since the zones most favourable to chemosynthesis are also those in which a number of toxic compounds are precipitated (As, Pb, Cu, etc.), and where the concentration of sulphur compounds, and the shortage of oxygen are most extreme. Nothing at all is known of how symbiosis is transmitted from one generation to the next. Since the importance of associations between chemosynthetic bacteria and primary consumers in hydrothermal systems was highlighted, a number of researchers have turned to the inhabitants of other reducing environments such as the sediment of ‘shallow-silled deep fjords, the sea outfall of major carriers of urban waste, mangrove swamps, etc. In all these cases, the, interface between the reducing sediment and the seawater contains invertebrates which sustain symbiosis with chemosynthetic bacteria, such as certain inter-tropical bivalves (Codakia orbicularis) or an oligochaet annelida (annelid worm with few bristles) living at the interface of the reduced zone in the Bermuda sediments. Examples of such associations are becoming more and more numerous and indicate that the importance of chemosynthesis in the biological economy of the marine environment has undoubtedly been underestimated in the past. Vast graveyards

Original living systems in their own

right, the oases of the great depths also have the particularity of being ephemeral. Considered on the scale of a hydrothermal spring, the physicochemica1 environment is marked by its short lifespan. Lead 210 dating of samples of polymetallic sulphide from a spent smoker at 21’N gave an age of 23 to 61 years only. The survival of hydrothermal populations is, therefore, strictly associated with short-span physicochemical phenomena distributed discontinuously in space. What is known of the lifespan of giant bivalves allows us to assert the lifespan of the physicochemical environment is on the same scale as that of the hydrothermal species. This, from the ecological point of view, is totally original and must inevitably seriously affect thinking on the mechanisms for the survival and propagation of the species. In the shorter term, there are also large variations in the flow of hydrothermal springs, which naturally have their effect on the general metabolism of the creatures, particularly their growth. Microstructural analysis of the shell of Calyptogena shows alternate rapid and slow rates of growth which may be explained by changes in the physicochemical environment or, less easily, by the movement of the animal itself. The growth rate of these giants has been estimated in a number of ways: radiosotope measurement using the decay of radium 228 into thorium 228, then radium 224, microstructural analysis on samples taken at several years’ interval on the same site, or direct measurement by physical marking and recapture some 10 months later. An average value of the order of 1 cm per year is accepted as reasonable estimate for Bathymodiolus and a slight underestimate for Calyptogena, and gives a maximum age of 15-25 years. Such values are comparable with the growth rates of the larger bivalves of coastal waters. The degree of medium-term variation is one of the principal results of the recent Biocyarise research programme, which involved returning two years after their first discovery to three hydrothermal sites: Pogonord, Actinoir, and Pogosud, situated at 12”50’N in the axial trough of the East Pacific Ridge, and spaced regularly over a distance of approximately 1 km [2]. During this short period of time (24 months) reduction in hydrothermal activity at Pogonord produced a dramatic effect on the associated population. In 1982 Pogonord was an active white smoker some 5 m in height with one lateral vent. At the base of the structure with a zone venting tepid water through the fissures. The population of Riftia covered a surface of some 73

not hard to image the consequences of this collapse in the ecosystem, and certain other dead sites discovered during the same research programme give a glimpse of the future of Pogonord (figure 10). Only a few lean mytilids and the occasional Jericho worm remain amongst the collapsing polymetallit sulphur structures as evidence that only a few years previously the site had supported several hundred kilograms of brilliant-red life. Colonization

Figure 9 The most spectacular discovery from the ecological point of view was that made during the Biocyarise programme at 13”N in March 1984, concerning the dynamics of the hydrothermal population in the event of the reduction or total cessation of hydrothermal activities. A/vine//a and Rifiia are the first to disappear when the spring on which they depend dies, along with their associated fauna, and in this photograph there remain onlythe modiolus (yellow shell) and a medium-sized pogonophoran worm with a characteristically-ornamented sinuous tube, tentatively named Jericho worm. At the centre, the yellowish spherical creature supported on short tentacles at the base of the fissure is Thermopalia taraxaca, one of the siphonophora and a relative of the jellyfish. (Biocyatherm programme, 13”N. Photo: IFREMER)

12 m2, and the fish population (Puchycura) had been estimated at 350 specimens. Two years later, the white smoker had become inactive and the only emissions which continued were of moirC water at a temperature not exceeding 40°C. Most of the Riftia were dead and their empty tubes, detached from their support, lay at the bottom of a lateral fault. The fish had disappeared totally. On the other hand, whilst practically no specimens of B&ymodiolus had been noted in 1982, two years later they were abundant and apparently prospering in the crannies of the sulphur deposits, whereas previously they had been concealed by the dense growth of Riftia. Another form of pogonophoran worm, the Jericho worm, whose morphology is reminiscent of a pagoda roof and whose tube is decorated with a series of interlocking mouthpieces, is apparently more tolerant of lower temperatures than Riftia, and remained alone in certain zones (figure 9). The ring of skrpulids had likewise suffered, and most of the tubes were empty; their colour had changed from pure white to brown, evidence of ferro-manganese deposits. The central zone closest to the spring was the least changed and the colony of Pompeii worms was still being exploited by the Cyanugruea crabs. It is 74

of new sites

Such ecological disasters certainly form part of a continuous process, as evidenced by the vast graveyards of Culyptogena valves, three-quarters dissolved and badly holed, observed at 21”N. Quite apart from the basic ecological interest of the dynamics of such systems, both terms of which - living and non-living - have approximately equal life-spans, such observations give rise to a second fundamental question: how do such relatively sessile organisms manage to colonize other springs and other hydrothermal fields? The problem is that the question of propagation arises in a different manner according to the space-time scale being considered: in a single field such as that researched at 13”N the distance between springs barely exceeds 500 m over a total distance of several tens of kilometres. Nonetheless, geophysicists

spring the fauna has Figure 10 Within a few years of the death of a hydrothermal totally vanished, save for the accidental presence of zoarcid fish, which are frequently found several hundred metres from hydrothermal springs, and very occasionally a galathaeid crab.) In the foreground, a series of solid sulphur chimneys are evidence of earlier activity at the site. Behind can be seen the fossilized tubes of A/vine//a. The cylinder (upper centre) is a titanium bottle for sampling high-temperature hydrothermal fluids, which are aspirated through the elbow tube on the left of the bottle. (Biocyatherm programme, 13”N. Photo: IFREMER)

have reason to believe that the hydrothermal phenomenon itself is propagated like a wave along any particular section of ridge isolated by two systems of transforming faults, over distances of several hundred kilometres, with undoubtedly widely varying time constants. Little is yet known about the process adopted by the organisms to maintain their existence in such a random environmental context. It is possible to predict quite simply that changes will be the greater the more closely the species is associated with hydrothermalism and the more sessile its habits. Various observations from Cyana have shown that certain species such as the fish Pachycara are capable of movement several hundred metres from a spring. Such possibilities of migration in the adult state are probably less than usual. It is more likely that, as is usual in the case of marine invertebrates, the larval stage is the best adapted to dissemination. The microstructure of the shell of juvenile Galapagos mytilid reveals, as with inshore mussels, that the species has a larval form with a long plankton stage of development. Although the mytilid larva has not yet been identified, it is estimated that it is capable of drifting with water massesfor periods ranging from several weeks to several months [23]. Some deep-water currents can attain speeds of 10-20 cm/s at only 50 m above the sea floor at the ridge, and even higher values have been recorded at comparable depths elsewhere in the Pacific. Under these conditions the larvae could travel several hundred kilometres before returning to the sea floor. Their chances of encountering an active hydrothermal site are extremely slim. Preliminary results of research into the genetic variability of mytilid populations suggest that the colonization of a new hydrothermal site tends to be undertaken by the population of the neighbouring spring, immediately account being taken of the general direction of the currents. Isolated populations consist as a rule of genetically very similar individuals accompanied by a few rarer specimens which differ as much from each other as from the majority of the population. The latter may be evidence of the sporadic individual migration of larvae from more distant sites. The problem of propagation is different when it concerns species without pelagic larval stages capable of floating. This is the case with the Pompeii worm. The Ampharetidae, the family of polychaet worms in which it is classified, do not produce a pelagic larva: eggs are spawned inside the mother tube and develop into larvae which crawl on the sea bed for a period of only a few hours to a few days before

constructing their own tube and becoming sessile. And if the larvae of Alvinella require the same high temperatures as the adult population it is difficult to see how such a species can colonize new springs or new fields of hydrothermal activity. Observations made by geologists have given rise to the hypothesis that the adult worm leaves its tube to swim actively in the open water and thus ensure the propagation of its species. No biologist has yet been able to confirm this observation, and despite Alvinella’s ability to move rapidly in and out of the tube the worm does not seem enthusiastic to venture into the hostile icy waters which surround it. Yet the species exists in three sites along the Pacific ridge spread over some 2400 nautical miles: 21”N, 13”N, and 19%. Can we compare terrestrial biogeography and surmise that juvenile worms are transported from one site to another by a larger, mobile species? Support for this hypothesis came with the finding of galaspecimens of Amphisamytha pagensis, an Ampharetidae recently discovered in the Galapagos, on the branchial lamella of the crab Bythograea. Paradoxically, as our knowledge increases it becomes increasingly clear that the species which are best adapted to the precarious life of this environment and which are unable to survive in ordinary deep-ocean water are also those which are the most widely distributed. The origin of the fauna associated with hydrothermalism still remains unclear. Two of the species just described. Neolepas and Neomphalus, are of course known to be prehistoric types, and have for that reason been called living fossils. The same is far from the case, however, for the other creatures which represent new genera or families. Curiously, the Bythograeidae crabs constitute an isolated family amongst the crabs, and that isolation is perhaps explained by our own imperfect knowledge of their phylogeny. Very recently, palaeontologists have provided the first evidence of the existence of fossil hydrothermal populations: worm tubes l-5 mm in diameter have been discovered in massive polymetallic sulphide deposits of the Cretaceous system (Mesozoic era approximately 95 m.y.) in the ophiolites of Samail in Oman [24] rocks which are evidence of a former oceanic crust. These are the first fossils to have been discovered in such deposits. Tbe existence of mesozoic remnants in current hydrothermal populations, together with the discovery of these fossilized tubes which appear to have belonged to forms closely related to the present day Pompeii worm, leads us to the conclusion that the

hydrothermal populations are in fact very ancient. Research for analogous traces in Paleozoic deposits would also be of great interest. Exploring

other regions

It is a commonplace that one of the factors governing scientific progress in oceanography has been the development of technology. This holds true for marine geosciences, and a fortiori for marine life sciences; without the submarine, detailed observations, sampling, and experimental work on hydrothermal populations would not have been possible. Marine biologists were almost the only French scientists to use the first-generation deep-sea submersibles - the heavy and unwieldy bathyscaphe - and, following the example of their marine geologist brethren they have for some years now turned to lightweight submersibles such as Cyana and Alvin. The discovery of hydrothermal populations has provoked a remarkable acceleration in this trend in France, the USA and Canada, and, in the near future, Japan. Submersibles are the only vehicles which allow serious study of populations such as these, which are concentrated in very small areas. The still-controversial discovery of bacteria capable of surviving at temperatures in excess of 250°C and pressures of 250 bars has also opened up new perspectives in the study of hydrothermal populations. A question of such magnitude cannot be left long without an unequivocal answer, regardless of whether it relates to the origin of the organic matter to be found in hydrothermal sites, or to the origin of life on our planet [25, 261. Exploration of new hydrothermal sites in zones where the Earth’s oceanic crust is being formed must be one of the objectives for future programmes, made all the more important by a recent major discovery. In March 1984, at a depth of 3270 m in the Gulf of Mexico off Florida, Alvin discovered a population of the hydrothermal type, including large pogonophorous worms and two large bivalves. The hydrothermal fluid had little apparent similarity with the more or less dilute fluids emitted by the black smokers of the Eastern Pacific; this was a supersaline ammonia-rich fluid which resulted in the deposition of sediments rich in iron sulphide. No temperature anomaly was observed. Apart from the exploration of typical areas of ocean crust formation such as high-expansion ocean ridges, this fortuitous discovery confirms the value of further exploration in areas of potential hydrothermal activity such as the arcs which mark the limits of archipelagos, which may reveal hydrothermal sites of a different variety. 75

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