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Conveying Behavior of the Deep Sea Pourtalesiid Cystocrepis Setigera Off Peru

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Conveying Behavior of the Deep Sea Pourtalesiid Cystocrepis Setigera Off Peru Conveying behavior of the deep sea pourtalesiid Cystocrepis setigera off Peru B. David, F. Magniez & L. Villier UMR CNRS 5561 Biogéosciences, Université de Bourgogne, 6, bd Gabriel 21000 Dijon, France P. de Wever Laboratoire de Géologie, Muséum National d'Histoire Naturelle, 43, rue Buffon 75005 Paris, France ABSTRACT: A submersible survey of the Peru Trench and of the northern Peruvian margin during the ANDINAUT cruise (March 1999) allowed us to observe, and to collect the very rare pourtalesiid Cystocrepis setigera (Agassiz, 1898). Video recordings of the sea bottom (2500 m deep) provide direct data about the mode of life of Cystocrepis. Observation of numerous specimens, generally grouped in clusters, attests that Cystocrepis is a ploughing sea urchin. Cystocrepis individuals thus represent hard islets moving slowly on a very soft, muddy sea bottom. Their aboral side is used by numerous organisms as a support for transport, sheltering… Ophiuroids climb up on the sea urchins and stay grasped between the spines. Numerous small crustaceans dwell on and swim around the spines. Despite being covered by an epithelium, the long and slender aboral spines support tubes (worm ?), foraminiferans, sponges, and amphipods (caprellids)… Several of the observed associations have so far never been described for sea urchins. Keywords. Symbiosis, heart urchin, deep sea, submersible 1 INTRODUCTION 2 MATERIAL Until recently, deep sea organisms were only known Cystocrepis is a very rare genus known from a single from specimens collected with gear operated from species, C. setigera (A. Agassiz 1898). The R/V Al- the surface, and assumptions about the ecology of batross collected one complete specimen and a few deep sea forms were deduced from functional ana- fragments during the Panamic deep-sea expedition in tomy studies (Mironov 1975) or from rare photo- 1891, and in 1976, Mironov described another spe- graphs. In the last 20 years, the development of mo- cimen collected in the Northern Pacific. Thus, after nitored cameras and of research submersibles has one century of exploration, only two specimens of greatly improved our access to reliable ecological ob- this genus were known! Recently, a submersible servations (e.g. Olu et al. 1997). For example, the survey of the Peru Trench and of the northern Peru- form and function of the so-called "dorsal sacs" vian margin during two geological cruises devoted to found on the apical side of some echinothuriid spe- the study of the subduction and of related deforma- cies was not accessible from trawled specimens, but tion processes, Nautiperc (1991) and Andinaut appear to be involved in a defensive function (Em- (1999), led to collection of six new specimens, and son and Young 1998). to observation in situ of this poorly known pourta- Among deep sea urchins, pourtalesiids (Holaster- lesiid (Fig. 1). During the second cruise, three dives oida) are characterized by their extreme morpholo- with the submersible Nautile (AN02, AN04 and gies as well as by their highly modified plate pat- AN11) on the slope of a large mud volcano located terns (Agassiz, 1904, David, 1987, 1990). Because on a platform at about 2500 m deep allowed video they are so original, the behavior of these echinoids recordings of the sea bottom, providing for the first cannot easily be inferred by analogy with other ir- time in situ data about the mode of life of a pourtale- regular echinoids, all the more because recent Holas- siid. teroida are exclusively deep-sea. Only Mironov Cystocrepis is a large pourtalesiid of about 100 (1975) has attempted an interpretation of their prob- mm in length accurately described by A. Agassiz able burrowing behavior based on an examination of (1904). The ambital outline is elongated. The anterior their overall morphology. extremity of the test is rounded, barely indented by a notch. The posterior end is more acute. The lateral Figure 2. Video frame of a Cystocrepis on the ocean bottom. 3.2 Cystocrepis are covered by ectosymbionts All Cystocrepis have a rich fauna of associated inver- Figure 1. Location of the observation sites. tebrates which are particularly conspicuous and abundant on the apical side of the sea urchins (Fig. 2). profile is acuminate anteriorly, sloping abruptly to- The terminology of interspecific interactions is wards the anterior edge, and more gently towards the still fluctuating (Bronstein 1994). For example, the rear of the test. The periproct is inframarginal. The term symbiosis is either used for any kind of interac- hood makes up the whole posterior part of the test, tions, or restricted to positive interactions. Here, we and the rostrum (usually large in pourtalesiids) is re- will utilize the original definition (de Bary 1879), en- duced to a slight projection. This apparently simple compassing all persisting relationships between shape actually results from the most complete onto- members of different species. For that reason, we genetic trajectory seen in pourtalesiids (David 1990), use the term "ectosymbiont" in a general sense to and Cystocrepis can be viewed as a highly derived designate all kind of organisms that may be found on form. This is confirmed by a bizarre architecture the test or on the spines of the sea urchin, whatever very different from the classical fivefold plate pat- the interspecific relation might be: positive, negative tern of other echinoids. or neutral. The descriptions below are restricted to a preliminary survey of the fauna carried by Cystocrepis, they will later be completed by more 3 RESULTS precise appraisals of the taxonomy and of the rela- tionships between the symbionts and their host. 3.1 Cystocrepis is an epibenthic dweller Observation of numerous specimens attests that 3.2.1 Echinoderms: holothuroids Cystocrepis is a ploughing sea urchin, and not an in- The most conspicuously visible ectosymbionts on faunal dweller. This confirms the hypothesis pro- Cystocrepis are small holothuroids (about 4 cm in posed by Mironov (1975) for these large pourtale- length). Holothuroids are generally attached on the siids. Cystocrepis are not evenly distributed on the lateral sides of the test, their adoral end floating be- sea bottom, but conspicuously aggregated in clusters side the sea urchin. Up to three sea cucumbers have recalling "herds of buffalo", a wording used by Fred been recorded on a single Cystocrepis. The same kind Grassle (Grassle et al. 1975) for Phormosoma. Such of holothuroids have not been observed on the sea a patchy distribution has already been observed for floor, suggesting a durable interaction. Associations another large pourtalesiid, Echinocrepis (Lauerman & between sea cucumbers and sea urchins are seldom Kaufmann 1998), and seems to be quite common in reported. A peculiar synaptid has been found on a deep-sea benthic communities (Gage & Tyler 1991). Pacific cidaroid (Ohshima 1915), and suspensivore dendrochirotes are known to live on the test of Ant- arctic cidaroids (Massin 1992), but this is the first time that an association between a sea cucumber and described on diadematid sea urchins (Grygier & an irregular sea urchin is reported. Newman 1991, Grignard et al. 1994), but they be- long to the group of microlepadids. Those micro- 3.2.2 Echinoderms:ophiuroids lepadids are likely to be small parasites settling on A significant number of Cystocrepis are observed in broken spines without epithelium, or fixed directly association with ophiuroids that grasp their aboral on the test and causing deformation. Ascothoracican side. The association involves two different ophiu- barnacles are also known to attach to echinoderms, roids. A small ophiacanthid lives on the test, under and they are highly transformed parasites. Therefore, the canopy of the primary spines, and seems to be a the barnacle observed on Cystocrepis possibly corre- permanent epibiont of Cystocrepis. A large ophiurid sponds to a new kind of crustacean-echinoderm as- is tangled between the primary spines in a more su- sociation. perficial position, but it occupies almost all the abo- ral side. This large ophiurid is not a permanent host 3.2.6 Polychaetes of Cystocrepis as it is also recorded on the sea bot- Mineralized tubes are found on primary spines. tom, and direct observations from the submersible They are slightly conical, 10 mm in length or a bit witnessed one individual attempting to climb up a less, and their aperture is encircled by a thickened sea urchin. rim. At least at their base, these tubes are firmly at- Associations between sea urchins and ophiuroids tached to the spine which does not seem to be dam- seem quite frequent as ophiuroids have already been aged in any way. The distal end of the tube can con- observed on various sea urchins: attached to the abo- tinue its growth free, away from the spine. Only the ral spines of some cidaroids (Mortensen 1928), and spines of the aboral side are colonized, and several in Paracentrotus (Byrne, pers. comm.), and in the spines can be colonized on each specimen. These oral region of Diadema (Grignard et al. 1998), tubes may house polychaetes worms (serpulids ?). Toxopneustes (Mortensen 1943), and some cly- Associations between polychaetes and echinoids peasteroids (Mortensen 1948). So far, only a single have been quite frequently recorded (Hyman 1955 case of a brittle star relationship with an atelosto- for a short review). Polychaetes can live in tubes mate (heart urchin) has been reported, the brittle star fixed on cidaroids spines, as well as free among the being found on the oral region of the spatangoid Li- spines of various other echinoids (Echinus, Astheno- nopneustes murrayi (Stöhr 2001). Generally the as- soma, Spatangus). sociated ophiuroids are quite small or minute com- pared to their host, and the observed association in 3.2.7 Hydrozoans ? Peru departs from those already known. Small soft tubes, ending into polyps, are attached to the spines. These peduncles can be fixed directly 3.2.3 Crustaceans: copepods onto spines or on extremely long stolons (longer than Numerous copepod crustaceans (harpacticoids) are the longest primary spines, i.e.
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