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
from specimens collected with gear operated from
the surface, and assumptions about the ecology of
deep sea forms were deduced from functional anatomy studies (Mironov 1975) or from rare photographs. In the last 20 years, the development of monitored cameras and of research submersibles has
greatly improved our access to reliable ecological observations (e.g. Olu et al. 1997). For example, the
form and function of the so-called "dorsal sacs"
found on the apical side of some echinothuriid species was not accessible from trawled specimens, but
appear to be involved in a defensive function (Emson and Young 1998).
Among deep sea urchins, pourtalesiids (Holasteroida) are characterized by their extreme morphologies as well as by their highly modified plate patterns (Agassiz, 1904, David, 1987, 1990). Because
they are so original, the behavior of these echinoids
cannot easily be inferred by analogy with other irregular echinoids, all the more because recent Holasteroida are exclusively deep-sea. Only Mironov
(1975) has attempted an interpretation of their probable burrowing behavior based on an examination of
their overall morphology.
Cystocrepis is a very rare genus known from a single
species, C. setigera (A. Agassiz 1898). The R/V Albatross collected one complete specimen and a few
fragments during the Panamic deep-sea expedition in
1891, and in 1976, Mironov described another specimen collected in the Northern Pacific. Thus, after
one century of exploration, only two specimens of
this genus were known! Recently, a submersible
survey of the Peru Trench and of the northern Peruvian margin during two geological cruises devoted to
the study of the subduction and of related deformation processes, Nautiperc (1991) and Andinaut
(1999), led to collection of six new specimens, and
to observation in situ of this poorly known pourtalesiid (Fig. 1). During the second cruise, three dives
with the submersible Nautile (AN02, AN04 and
AN11) on the slope of a large mud volcano located
on a platform at about 2500 m deep allowed video
recordings of the sea bottom, providing for the first
time in situ data about the mode of life of a pourtalesiid.
Cystocrepis is a large pourtalesiid of about 100
mm in length accurately described by A. Agassiz
(1904). The ambital outline is elongated. The anterior
extremity of the test is rounded, barely indented by a
notch. The posterior end is more acute. The lateral
copepods
0°
PERU
Lima
20°S
holothuroid
5 cm
40°S
Figure 2. Video frame of a Cystocrepis on the ocean bottom.
3.2 Cystocrepis are covered by ectosymbionts
120°W
100°W
80°W
60°W
40°W
Figure 1. Location of the observation sites.
profile is acuminate anteriorly, sloping abruptly towards the anterior edge, and more gently towards the
rear of the test. The periproct is inframarginal. The
hood makes up the whole posterior part of the test,
and the rostrum (usually large in pourtalesiids) is reduced to a slight projection. This apparently simple
shape actually results from the most complete ontogenetic trajectory seen in pourtalesiids (David 1990),
and Cystocrepis can be viewed as a highly derived
form. This is confirmed by a bizarre architecture
very different from the classical fivefold plate pattern of other echinoids.
3 RESULTS
All Cystocrepis have a rich fauna of associated invertebrates which are particularly conspicuous and
abundant on the apical side of the sea urchins (Fig.
2).
The terminology of interspecific interactions is
still fluctuating (Bronstein 1994). For example, the
term symbiosis is either used for any kind of interactions, or restricted to positive interactions. Here, we
will utilize the original definition (de Bary 1879), encompassing all persisting relationships between
members of different species. For that reason, we
use the term "ectosymbiont" in a general sense to
designate all kind of organisms that may be found on
the test or on the spines of the sea urchin, whatever
the interspecific relation might be: positive, negative
or neutral. The descriptions below are restricted to a
preliminary survey of the fauna carried by
Cystocrepis, they will later be completed by more
precise appraisals of the taxonomy and of the relationships between the symbionts and their host.
3.1 Cystocrepis is an epibenthic dweller
Observation of numerous specimens attests that
Cystocrepis is a ploughing sea urchin, and not an infaunal dweller. This confirms the hypothesis proposed by Mironov (1975) for these large pourtalesiids. Cystocrepis are not evenly distributed on the
sea bottom, but conspicuously aggregated in clusters
recalling "herds of buffalo", a wording used by Fred
Grassle (Grassle et al. 1975) for Phormosoma. Such
a patchy distribution has already been observed for
another large pourtalesiid, Echinocrepis (Lauerman &
Kaufmann 1998), and seems to be quite common in
deep-sea benthic communities (Gage & Tyler 1991).
3.2.1 Echinoderms: holothuroids
The most conspicuously visible ectosymbionts on
Cystocrepis are small holothuroids (about 4 cm in
length). Holothuroids are generally attached on the
lateral sides of the test, their adoral end floating beside the sea urchin. Up to three sea cucumbers have
been recorded on a single Cystocrepis. The same kind
of holothuroids have not been observed on the sea
floor, suggesting a durable interaction. Associations
between sea cucumbers and sea urchins are seldom
reported. A peculiar synaptid has been found on a
Pacific cidaroid (Ohshima 1915), and suspensivore
dendrochirotes are known to live on the test of Antarctic cidaroids (Massin 1992), but this is the first
time that an association between a sea cucumber and
an irregular sea urchin is reported.
3.2.2 Echinoderms:ophiuroids
A significant number of Cystocrepis are observed in
association with ophiuroids that grasp their aboral
side. The association involves two different ophiuroids. A small ophiacanthid lives on the test, under
the canopy of the primary spines, and seems to be a
permanent epibiont of Cystocrepis. A large ophiurid
is tangled between the primary spines in a more superficial position, but it occupies almost all the aboral side. This large ophiurid is not a permanent host
of Cystocrepis as it is also recorded on the sea bottom, and direct observations from the submersible
witnessed one individual attempting to climb up a
sea urchin.
Associations between sea urchins and ophiuroids
seem quite frequent as ophiuroids have already been
observed on various sea urchins: attached to the aboral spines of some cidaroids (Mortensen 1928), and
in Paracentrotus (Byrne, pers. comm.), and in the
oral region of Diadema (Grignard et al. 1998),
Toxopneustes (Mortensen 1943), and some clypeasteroids (Mortensen 1948). So far, only a single
case of a brittle star relationship with an atelostomate (heart urchin) has been reported, the brittle star
being found on the oral region of the spatangoid Linopneustes murrayi (Stöhr 2001). Generally the associated ophiuroids are quite small or minute compared to their host, and the observed association in
Peru departs from those already known.
3.2.3 Crustaceans: copepods
Numerous copepod crustaceans (harpacticoids) are
sheltered among the aboral spines of Cystocrepis.
They are generally about a dozen, but up to 25 copepods have been observed resting on a single sea
urchin. Harpacticoids swim actively, and they may
not be permanently associated with the sea urchin.
They move away rapidly when the sea urchin is
collected by the arm of the submersible, and none
has been caught.
3.2.4 Crustaceans:amphipods
Highly atypical amphipods, apparently caprellids,
have been observed on Cystocrepis. Caprellids live
generally attached to seaweed or branching colonial
animals on rocky shallow habitats. Their association
with echinoderms is already known from several sea
stars (Wirtz & Vader 1996), and, very rarely, from
the sea urchin Echinus esculentus (Comely & Ansell
1988).
3.2.5 Crustaceans: cirripedes
A small cirripede has been found attached to a primary spine. It displays the usual aspect of a goose
barnacle. The spine that supports it is not broken,
nor damaged. Some barnacles have previously been
described on diadematid sea urchins (Grygier &
Newman 1991, Grignard et al. 1994), but they belong to the group of microlepadids. Those microlepadids are likely to be small parasites settling on
broken spines without epithelium, or fixed directly
on the test and causing deformation. Ascothoracican
barnacles are also known to attach to echinoderms,
and they are highly transformed parasites. Therefore,
the barnacle observed on Cystocrepis possibly corresponds to a new kind of crustacean-echinoderm association.
3.2.6 Polychaetes
Mineralized tubes are found on primary spines.
They are slightly conical, 10 mm in length or a bit
less, and their aperture is encircled by a thickened
rim. At least at their base, these tubes are firmly attached to the spine which does not seem to be damaged in any way. The distal end of the tube can continue its growth free, away from the spine. Only the
spines of the aboral side are colonized, and several
spines can be colonized on each specimen. These
tubes may house polychaetes worms (serpulids ?).
Associations between polychaetes and echinoids
have been quite frequently recorded (Hyman 1955
for a short review). Polychaetes can live in tubes
fixed on cidaroids spines, as well as free among the
spines of various other echinoids (Echinus, Asthenosoma, Spatangus).
3.2.7 Hydrozoans ?
Small soft tubes, ending into polyps, are attached to
the spines. These peduncles can be fixed directly
onto spines or on extremely long stolons (longer than
the longest primary spines, i.e. > 25mm). In this
later case, individuals branch alternatively on each
side of the stolon. A third type of putative hydrozoan observed forms club-shaped colonies fixed at
the tip of the spine. All these animals are provisionally referred to hydrozoans, but some may turn out
to be bryozoans or kamptozoans.
3.2.8 Sponges
At least two species of sponges have been observed
on the primary spines. They are encrusting sponges,
sometimes bulbous, showing a rather loose meshwork. Sponges are also very frequent on cidaroid
spines that are free of epithelium above the Prouho's
membrane.
3.2.9 Foraminifera
Two kinds of foraminifera have been found, fixed on
primary spines. One belongs to the encrusting polymorphinids, and the other is an unidentified spirally coiled form.
3.2.10 Miscellaneous ectosymbionts
Several other ectosymbionts have been observed on
the primary spines. They are not yet fully identified,
and may correspond to bryozoans, other sponges,
worms, gastropods, etc. The total number of species
so far identified on the test of Cystocrepis is 17, and
the total is likely to be more than 20.
entific help and discussions. This work is a contribution of the UMR CNRS BIOGÉOSCIENCES.
6 REFERENCES
4 DISCUSSION
Among sea urchins, cidaroids are the most prone to
host ectosymbionts. The shaft of the primary spines
of cidaroids is bare and lacks an epidermis, therefore
allowing settlement of various epibionts including algae, foraminiferans, sponges, bryozoans, bivalves,
polychaetes, holothurians… (Hyman 1955). On the
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of stability on the very soft deep sea bottom.
Pourtalesiids, and particularly Cystocrepis, are
not only extraordinary by their shape and architecture, they are also quite original in their behavior and
in their relationships with other deep sea organisms.
5 ACKNOWLEDGMENTS
We first would like to thank J. Bourgois, chief scientist of Nautiperc and Andinaut, as well as all the scientific participants to those cruises. We also thank
the crew of the R/V Atalante, and the Nautile group
for their invaluable help while at sea. We are indebted to M. Segonzac for providing us with the
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