QatarUniv. Sci J. (1999), 19: SPONGES (PORIFERA) IN SUBMARINE CAVES By Jean Vacelet Centre d'Oceanologie de Marseille (CNRS-Universite de la Mediterranee, UMR 6540), Station marine d'Endoume. 13007 Marseille, FRANCE

Keywords : Porifera; Submarine cave; Deep-sea fauna; ancient reefs.

ABSTRACT Sponges (phylum Porifera) have the most simple and probably the most ancient body plan of the multicellular animals. They are, however, very successful in most benthic ecosystems. They are dominant in submarine caves, where their study has provided unexpected results.

Submarine caves share several ecological features with deep-sea habitats. The communities living in these habitats depend on allochthonous organic input, and some bathyal species are able to colonize the darkest parts of littoral caves. Some examples will be given, including calcified sponges,«living fossils» of ancient reef builders. Faunal and environmental similarities, however, are limited by the obvious differences in pressure, temperature, habitat size, and by the dispersal abilities of deep water organisms. A recently discovered Mediterranean cave more closely approximates deep-sea conditions, due to the entrapment of a cold water mass resulting in stable temperature conditions throughout the year. Easily accessible to scuba divers, this «bathyal island» in the littoral zone is a natural mesocosm of the deep Mediterranean which offers exceptional opportunities for deep-sea biology. Preliminary results have already provided unexpected insights, which are illustrated.

A large population of Oopsacas minuta, a representative of the bathyo-abyssal hexactinellid sponges, reproduces here year round - making possible the first observations of larval behaviour and ultrastructure to be carried out on this phylogenetically important group of invertebrates, and opening up the poorly known area of larval ecology of these deep-sea sponges. The presence of a species of the deepest known genus of sponges, Asbestopluma (8 840 m in the Central Pacific) is a fascinating opportunity to investigate the biology of the strange deep-sea cladorhizid sponges, which may live in the most oligotrophic abyssal basins. A highly unexpected result is that they are non-filter-feeding sponges with a carnivorous feeding habit. They capture and digest small crustaceans by means of filaments provided with minute hook-shaped spicules. The biology and peculiarities of this carnivorous sponge are illustrated by a video.

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INTRODUCTION : by photosynthesis, display a dramatic Submarine caves have often been consid­ decrease in biomass [5]. In such an ered as interesting natural candidates for environment some invertebrates from the mesocosms of the deep sea, whose access bathyal zone find conditions nearly similar is difficult and expensive, Blind caves and to those of the deep sea and have been deep-sea habitats closely resemble each able to colonize dark caves. Invertebrates other m terms of darkness and normally living several hundred meters hydrodynamic conditions [l ,2]. Both deep have been found at 3 m depth in depend mainly on primary production littoral caves. These features have been elsewhere [3], resulting in some cases in a described in various areas of the world similar amount of trophic resources [4-6]. ocean. A similar habitat is widespread in Similarities have also been described in coral reefs, either in large tunnels from the faunal composition and structure of the outer reef front or in smaller cavities of the assemblages of sessile invertebrates [ 1, 7], reef framework. with several bathyal species living in the darkest parts of sublittoral caves. These Among the bathyal invertebrates able to data concern mainly sponges, which are colonize shallow water caves, most on cave rocky surfaces the dominant remarkable are hypercalcified sponges, group in number of species, biomass and which have, in addition to the usual surface covered. Sponges present a special spicule skeleton, a solid non-spicular interest in caves, due to the preservation of calcareous skeleton. This bears striking hypercalcified «living fossils» which are resemblances to that of various cnidarians, unexpected survivors of ancient reef including the corals which build the builders, and to the presence of deep-sea modem coral reefs, and is able to fossilize. species showing unexpected life strategies, These «coralline sponges» are in fact including carnivory. Such caves have not survivors of enigmatic Palaeozoic and yet been described in the Arabian Gulf. Mesozoic reef-builders, namely stroma­ toporoids, chaetetids «corals» and sphinc­ THE SPONGE FAUNA OF tozoans, which were believed extinct. SUBMARINE CAVES The sponge fauna is remarkably rich and The nature of these organisms has been diverse near the apertures of submarine long debated, and most were classified in caves, in the semi-dark zone [l]. Dim light the Cnidaria a few years ago. Four of these and a good water exchange with the «living fossils» were first found in the productive area outside assure a low bathyal zone at the beginning of the degree of competition with algae and century, but their true existence has been abundant particulate food. Deeper in the disputed. The opinion that they were cave, the benthic communities of the dark chimeras made of calcified organisms zones which depend on allochthonous excavated by sponges, was commonly inputs in the absence of local production accepted. The discovery of a new

-47- Jean Vace let main groups of deep-sea sponges, the class consistent with the hypothesis that Hexactinellida and the family Cladorhizi­ sponges are the first step in metazoan dae of class Demospongiae. This allows a organisation, deriving from unicellular direct study of the various feeding and choanoflagellates, To what extent these reproductive strategies of these deep-sea peculiarities may represent a relatively animals, which are poorly known due to recent adaptation to filter-feeding in the difficult access. deep sea, where particulate food is poor, is unknown. SPONGE FAUNA OF THE CAVE As usual in caves, the sponges are the The Mediterranean cave in cold water has dominant group on all the rocky surfaces, been colonized by Oopsacas minuta, an in number of species, biomass and surface hexactinellid sponge which was covered. The percentage of cover, estimat­ previously known from only two minute ed on sampled rocky surfaces of the walls, specimens collected at 924m in depth at decreases from the entrance area with var­ Mediterranean end of the Straits of ying temperature to the homeotherm zone. Gibraltar [24]. Easy access to the cave However the cover does not significantly population of Oopsacas minuta, with decrease though the homeotherm zone up possibility of in situ processmg has to the far end, contrary to what is observed resulted in unusually good preservation of for bryozoans [ 19]. This may be due to the the delicate cytological structures [25]. utilisation by sponges of pulses of parti­ Ultrastructural observations and cles in certain hydrological circumstances. experimental study of the particle uptake [26] by 0. minuta show that the feeding HEXACTINELLID strategy of hexactinellids differs notably Representatives of the class Hexactinellida from that of other sponges. Hexactinellids (glass sponges) are predominantly bathyo­ rely on the extensive development of the abyssal. Due to difficulties in preservation, aquiferous cavities, concurrently with an these sponges remained mysterious for a extreme thinness of the living tissue (less long time. As early as the beginning of than 10 J.lm in most areas of the chamber this century, their histological structure wall). This is very different from a bathyal has been claimed to be very different from dernospongs such as Discodermia other sponges [20, 21]. Recent observa­ pulydiscus living in the same area of the tions have confirmed that their tissues are cave, in which the aquiferous system is mostly syncytial and that their choanocy­ reduced, with small choanocyte chambers tes were anucleate cells wrapped in a spe­ and an extremely dense mesohyl cial tissue, the reticulum. These peculiari­ containing a huge number of symbiotic ties are of special interest in the problem bacteria. In situ or laboratory experiments of early metazoan evolution. Such a struc­ using latex beds, unicellular algae or ture in animals which might be the oldest bacteria have shown that the anucleate known metazoans [22, 23] is not choanocytes of the hexactinellid are

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mostly used for the circulation of water, called «trichimella» [25]. The flagellated and do not trap and digest particles, unlike equatorial zone is made up of in other classes of sponges, Demospongiae multiflagellated mononucleate cells, with and Calcarea. Phagocytosis and digestion up to 50 flagella per cell. The flagellated are performed by the special structure in cells are covered by a thin epithelium which the anucleate choanocytes are pierced by the flagella, which is a unique wrapped, the reticulum, by either its structure in invertebrates. The surprising inhalant or exhalant side depending on the presence of multiflagellated cells, which particle size. are assumed to appear only in the triploblast and Protostomia!Spiralia lines The reproduction of hexactinellids was [28] could indicate that hexactinellids also poorly known, due to difficulty for have acquired multiflagellarity access, and to the fact that deep-sea independently of other metazoans. The specimens rarely reproduce. Although free larva is only 150-180 Jlm long and is many specimens from deep-sea rich in lipids and yolk. Data on the larva hexactinellids have been studied, behaviour would be informative on the embryology and larvae have been dispersal possibilities of deep-sea correctly described only once [27], with hexactinellids. the discovery of the presence of a unique larval skeleton of special siliceous CLADORHIZID DEMOSPONGE spicules. Larval behaviour and ecology The second remarkable example of and dispersal ability are obviously deep-sea sponge in the cave is a unknown. demosponge belonging to the exclusively deep-sea family Cladorhizidae. All the Contrary to deep-sea hexactinellids, the representatives of this family have a cave specimens of 0. minuta sexually strange morphology, stalked with long, reproduce all year round, and stages of thin appendages. Cladorhizids include the embryogenesis have been found in all deepest known sponges, with a species of examined specimens. This is obviously a the genus Asbestopluma found at 8 840 m good opportunity for both embryology and depth in the Pacific [29]. They are able to larval behaviour study, but also addresses live in the most food-poor basins under the problem of seasonality of reproduction low surface productivity [30]. The in deep-sea species. This constant and adaptations and life history traits which active reproduction may be related to a allow them to withstand such extreme higher food input in the cave than in the conditions were unknown. deep-sea. The larva is similar in gross morphology to that previously described The cave species, approximately 20 mm by Okada in another species, but reveals high, is a new species of Asbestopluma, A. interesting ultrastructural characteristics of hypogea [31], belonging to the genus the hexactinellid larva, which has been which holds the depth record for sponges.

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This is again an opportunity to study the according to the prey size. Complete life history traits of sponges which on digestion of a 7 mm long crustacean is average are deeper than the hexactinellids complete in 10 days. In the cave, prey are and even can reach the hadal zone. mostly tiny crustaceans, such as copepods, ostracods, mysids, but small polychaetes Only one species of Cladorhizidae was or pycnogonids may occasionally be known in the deep Mediterranean, in caught. Specimens have been successfully which the genus Asbestopluma has never raised in aquarium for several month, with been recorded. As for the hexactinellid, it a weekly change of sea water and feeding is likely that the cave species also lives with either living nauplii of Artemia salina under inaccessible overhangs in the nearby or commercially available deep-frozen deep canyon and on rocky surfaces of the Artemia. The characters and behaviour of deep Mediterranean, whose biodiversity this sponge have been illustrated by a seems to be significantly under-evaluated. video [33], a copy of which has been deposited in the Department of Marine We first investigated the aquiferous Sciences of the University of Qatar. system of this deep-sea animal, because the organisation and fine structure of the This unusual mode of life is apparently canal system provide information on the shared .. by the other Cladorhizidae feeding strategy of sponges. Contrary to (approximately 90 species) in deep-sea the hexactinellid in which the aquiferous habitats. The general absence of system is unusually highly developed, the aquiferous system, that intrigued early cladorhizid appeared devoid of any observers, could not be due to poor aperture, canal and choanocyte. It is thus preservation. Small animals are often not a filter-feeder like other sponges. found trapped in the filaments or Subsequent studies demonstrated rather appendages of specimens collected by that it is carnivorous and feeds on small trawls. The hypothesis that the sponge living prey, mostly crustaceans, a highly could feed on the particles collected by the unexpected feeding habit in sponges [32, appendages has been suggested by the first 33]. The long, thin filaments are covered author to describe a cladorhizid [34], by minute hook-shaped spicule disposed at although this unconventional hypothesis right angle to the axis, which give the was considered highly unlikely by filaments a «Velcro»-like adhesiveness. subsequent authors. However, the Once trapped by their appendages, tiny cladorhizids may have other nutrient swimming crustaceans are unable to free sources as well. A cladorhiza sp. from a themselves, although there is apparently deep-sea methane venting, 4900 m deep no toxic or paralysing secretion. After near Barbados, is nutritionally reliant on capture, cells of the sponge migrate methanotrophic symbiotic bacteria [35, towards the prey, which is engulfed in the 36], although also feeding on swimming sponge tissue within a few hours or days prey. This dual source of carbon allows

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the sponge to constitute large aggregations of hundreds of individuals around the The unexpected life history traits which methane source, when deep-sea have been discovered in Porifera appear as cladorhizids usually occur in low densities secondary adaptations to the deep-sea as discrete individuals. conditions, and also address broad problems in biological evolution, such as The organization and biology of A. the ongm of deep-sea fauna, the hypogea, and presumably of the other apparition of multiflagellarity in animal cladorhizid sponges differ widely from cells, or the definition of the phylum those known in other sponges. These Porifera. Significant advances in the organisms lack all the basic sponge knowledge of the poriferan adaptations to attributes, although their spicules are the deep sea have been made or may be similar to those of three different lines of foreseen, such as feeding strategies, evolution in the order Poecilosclerida of seasonality of reproduction, dispersal the Demospongiae. The most likely ability and long-distance fertilization, and interpretation is that in deep-sea habitats, the place of sponges in the deep-sea food where active filter-feeding has a low yield, web has to be reconsidered. Although the these sponges have deviated from the conditions in the cave only approximate filtering organization typical of Porifera the true deep-sea conditions, the life and have developed a new body plan that strategies that have been discovered here resembles no other anatomical design. for sponges are likely the same as for their This may be compared to the emergence deep-sea populations. of macrophagy in abyssal tunicates, but with a more extreme result as the main Dark littoral caves also have an interest as Porifera attributes have disappeared. refuge for invertebrates which had a major Although they are sponges by their role in reef construction during the poriferan spicules, the characteristics and geologic times, and which were long mobility of their cells and the absence of believed extinct. A handful of these organs, the representatives of ancient reef builders survive in the Cladorhizidae do not match the classical precipitous slopes of the continental definition of Porifera, which has to be margin, which are difficult to access, and reinterpreted. in littoral caves, where their study is easier. These «living fossils» provide CONCLUSIONS direct knowledge of the fascinating world The example of sponges shows that of ancient reefs which were previously various general problems of deep-sea known mostly by their fossil remains. biology as well as of history of ancient reefs during geologic times could be successfully addressed in caves.

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