Porifera Research: Biodiversity, Innovation and Sustainability - 2007
107
Diversity and evolution of deep-sea carnivorous
sponges
Jean Vacelet
Aix-Marseille Université, CNRS UMR-6540 DIMAR, Centre d’Océanologie de Marseille. Station Marine d’Endoume. Rue
Batterie des Lions, 13007. Marseille, France. [email protected]
Abstract: The carnivorous habit of feeding that has been discovered in a cavernicolous species of Cladorhizidae is probably
general for all the representatives of this deep-sea family, which numbered approximately 90 species at the end of the 20th
century. Recent reports have shown that the number of species is actually considerably higher and that carnivory probably also
occurs in several representatives of other Poecilosclerida families. A few specimens collected by trawling in the Pacific and
Atlantic oceans have been described as new species. A larger sample collected from manned submersibles on rocky substrates
near active hydrothermal sites in the south Pacific has provided a remarkably high proportion of new species. However, it
is at present difficult to determine whether the abundance and diversity of carnivorous sponges in this collection is linked
to the vicinity of hydrothermal sites, which provides solid substrata and general organic enrichment, and also stimulates a
special sampling effort by direct methods. Carnivorous sponges cannot be considered as true members of the hydrothermal
fauna, as they are apparently absent from the rich animal communities that thrive in the immediate environment of active
smokers. The new species from the South Pacific include several representatives of Abyssocladia, previously synonymized
with Phelloderma (Myxillina), increasing the microsclere heterogeneity of carnivorous sponges. Moreover, some other deepsea poecilosclerids, Euchelipluma spp. (Guitarridae) and some Esperiopsis spp. (Esperiopsidae) also appear to be carnivorous.
This may suggest that carnivory appeared independently in several evolutionary lines of poecilosclerids. Conversely, however,
the polyphyly of carnivorous sponges is not supported by a number of shared characters. The two hypotheses are discussed,
but it is suggested, given the important morphological adaptations of these sponges, their ambiguous relationships with extant
families of poecilosclerids and our rapidly increasing knowledge regarding their diversity, that it would be premature to
drastically change the classification before having more information, especially of reproduction and molecular characters.
Keywords: Cladorhizidae, Carnivorous sponges, Evolution, Deep Sea, Poecilosclerida
Introduction
The discovery that a representative of the Cladorhizidae,
Asbestopluma hypogea Vacelet and Boury-Esnault, 1996
was carnivorous (Vacelet and Boury-Esnault 1995) has led
to renewed interest in these strange deep-sea sponges that
were previously only studied from a taxonomic point of view.
Several lines of evidence suggest that this unexpected feeding
habit is general in the Cladorhizidae as defined in Systema
Porifera (Hajdu and Vacelet 2002) with three valid genera,
Cladorhiza Sars, 1872, Asbestopluma Topsent, 1901 and
Chondrocladia Thompson, 1873. It has been shown that in
addition to A. hypogea several cladorhizids contain crustacean
debris in the course of being digested (Kübler and Barthel
1999, Vacelet and Boury-Esnault 2002, Reiswig and Lee
2007). Furthermore, all the cladorhizids display morphological
characters that are seemingly related to carnivory. They
display a peculiar symmetrical shape, generally stipitate with
lateral processes lined by hook-shaped microscleres. Most of
them seem to be devoid of the sponge diagnostic attributes,
i.e. an aquiferous system with canals, ostia, osculum and
choanocyte chambers. An aquiferous system is present only
in the genus Chondrocladia, in which, however, it is modified
and apparently not used for water filtration, but for the inflation
of turgescent spheres at the surface of which prey capture is
performed. Furthermore, recent observations suggest that this
feeding regime also occurs in some other poecilosclerids that
may have other family level affinities.
These carnivorous sponges, which do not concur with the
conventional definition of the phylum as given by Bergquist
(1978) “a sedentary, filter-feeding metazoan which utilizes
a single layer of flagellated cells (choanocytes) to pump
a unidirectional water current through its body”, have
developed an organization that is unique in the Metazoa,
feeding on macro-prey by cells acting individually, without
any digestive cavity (Vacelet and Duport 2004). The evolution,
most likely from “normal sponges”, biology, ecology and
diversity of such a remarkable derivation from a taxon that is
considered as the most basal in the evolution of Metazoa, are
fascinating new topics of research. The aim of this paper is to
examine what is known to date of the diversity, classification
and ecology of the carnivorous poecilosclerid sponges.
How many taxa there are, whether they are monophyletic,
or polyphyletic as carnivorous plants, and whether they are
significant components of the deep-sea ecosystems, will be
the main questions addressed.
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Biodiversity of carnivorous sponges
At the end of the 20st century the Cladorhizidae numbered
approximately 90 species. Most of them were described
without any reference to their histological organization. This
lack of information could be due to the poor preservation
usual for deep-sea animals collected by dredging or trawling.
It may be stressed too that the describers of cladorhizids were
sponge taxonomists expecting a system of apertures, canals
and choanocyte chambers, which in this case was absent or
significantly modified. Several of them, however, such as
Lundbeck (1905, p. 47), expressed their surprise that neither
pores nor oscula have ever been mentioned. Careful observers
such as Ridley and Dendy (1887) wrote “ The Crinorhiza
forms appear to be without oscula and pores, nor have we
succeeded in finding flagellated chambers, although some
of the specimens were in very fair condition. It seems just
possible, therefore, that, as originally suggested by Sars in
the case of the first known species of the genus, Cladorhiza
abyssicola, these sponges have some method of obtaining their
supplies of nutriment which is quite different from that found
in other sponges; this is, however, extremely unlikely”. The
same authors interpreted the lining of hook-like microscleres,
which are now understood to be trapping devices for prey, as
an “efficient protection against parasites and other enemies”.
Recent observations on species that are definitely carnivorous,
Asbestopluma hypogea and Chondrocladia gigantea (Hansen,
1885) have provided new information on their histology and
organization. Moreover, a few recent taxonomic studies and
studies in progress indicate that the diversity of cladorhizid
sponges, and more generally of carnivorous sponges, in the
deep sea is much higher than previously assumed.
Since the beginning of the 21st century, 15 species have been
described as new (Vacelet and Boury-Esnault 2002, Cristobo
et al. 2005, Lehnert et al. 2005, Vacelet 2006, Reiswig and
Lee 2007), increasing significantly the number of known
species and resurrecting the genus Abyssocladia Lévi, 1964
which has been tentatively transferred from Phellodermidae
to Cladorhizidae. The new species were collected in the deep
south Pacific and south Atlantic, with a very high ratio of new
species in the various collections, indicating that these large
areas certainly still contain a large number of undescribed
species. The study that I recently published on specimens from
the deep Pacific (Vacelet 2006) is particularly indicative of the
poor knowledge that we have of this fauna. This collection
includes 9 species, of which 9 are new, although this area
– admittedly very large – has been explored for sponges by
the ‘Challenger’, ‘Vitiaz’ and ‘Galathea’ expeditions (Ridley
and Dendy 1887, Koltun 1958, 1959, 1970, Lévi 1964).
Deep-sea sponges have often been described from very few
specimens, so that their intraspecific variability is poorly
known, possibly wrongly resulting in an exaggerated splitting
of species. This does not appear to be the case, as the new
species are significantly different from any known species,
and variability is low when several specimens are present. An
example is Abyssocladia agglutinans Vacelet, 2006, which is
known by two specimens that are exactly similar although
distant by 557 km.
In this study, such a high proportion of new species could
be ascribed to the collection of the specimens by manned
submersibles on submarine ridges, in deep-sea environments
where active hydrothermal vents favour general fauna
enrichment and where hard substrates are relatively common.
This could provide a higher diversity than the methods that
were used in the deep Pacific by the ‘Challenger’, ‘Vitiaz’
and ‘Galathea’ expeditions during which the specimens
were collected by blind trawling generally on mud bottoms.
However, a preliminary study of cladorhizids collected by
trawling off New Zealand (Kelly and Vacelet, in progress),
including the Kermadec Trench which has been previously
thoroughly explored by the ‘Galathea’ expedition (Lévi
1964), also reveals a high ratio of undescribed species.
Similar results were obtained by Cristobo et al. (2005) for
the genus Chondrocladia in the south Atlantic. A collection
presently under study (Fourt, Vacelet and Boury-Esnault,
unpublished report to IFREMER) from the deep North
Atlantic, an area which has been more thoroughly explored
than the deep Pacific, also contains an unexpectedly high
proportion of new species of Cladorhizidae, although not as
high as in the Pacific. It is thus obvious that the diversity of
cladorhizid sponges in the deep sea is far higher than is known
to date and that many species, possibly genera, have yet to be
discovered. It must be stressed, however, that caution must be
exercised when describing such fragile sponges that are most
often incomplete, in which some spicule categories are often
precisely located, and which often collect pieces of other
sponges due to the adhesive properties of their prey-trapping
surfaces.
None of the new species described in the genera
Asbestopluma, Cladorhiza and Abyssocladia display any
trace of aquiferous system or choanocyte chamber. The best
preserved specimens display a regular arrangement of the
microscleres that line the lateral filaments, with the alae of
chelae or the teeth of sigmancistras outwardly directed, an
arrangement which allows the capture of the thin setae of
crustacean prey. Moreover, a few specimens contain crustacean
debris, especially clear in Abyssocladia huitzilopochtli
Vacelet, 2006, also found in two new Chondrocladia spp.
These facts confirm that all the sponges presently classified
in Cladorhizidae are very likely carnivorous. Indisputable
general evidence, however, is difficult to provide in these
fragile deep-sea animals, which easily lose the lateral
filaments or appendages on which the prey are trapped
and on which experimentation is not easy. Even in the best
preserved specimens, prey are rarely visible, which is not
surprising, considering that carnivorous sponges are “sit-andwait predators” that very likely do not eat frequently in the
oligotrophic deep sea.
Furthermore, it appears that Asbestopluma, Chondrocladia
and Cladorhiza spp. are not the only carnivorous sponges.
Several deep-sea poecilosclerids that are, or were, classified
in diverse families due to their microsclere spicules, but that
display morphology similar to that of Cladorhizidae, may
also be carnivorous. As already pointed out, Abyssocladia,
previously synonymized with Phelloderma Ridley and Dendy,
1886 (Phellodermidae, Myxillina), is now reconsidered as
a valid genus of Cladorhizidae with seven species (Vacelet
2006) and several new species in the course of description.
A carnivorous feeding habit is highly likely in Euchelipluma
Topsent, 1909, which has been classified in the Guitarridae
109
due to the presence of placochelae similar to those highly
diagnostic of filter-feeding sponges belonging to Guitarra
Carter, 1874. The genus contains three species, E. pristina
Topsent, 1909, E. (Desmatiderma) arbuscula Topsent, 1928
and E. elongata Lehnert et al., 2006. All display a pinnate
shape, with regularly arranged lateral filaments lined by
microscleres with the alae and teeth outwardly directed.
This skeleton organization, the shape of the sponge and
the seemingly absence of aquiferous system suggest a
carnivorous feeding habit, which has been confirmed by the
observation of crustaceans debris in some specimens of E.
pristina (Vacelet 1999, Vacelet and Segonzac 2006). Another
example may be found in the Esperiopsidae, where deepsea Esperiopsis spp. of the group of E. villosa Carter, 1874,
including E. symmetrica Ridley and Dendy, 1886 and E.
desmophora Hooper and Lévi, 1989, have a morphology that
is highly suggestive of carnivorous feeding. The similarities
in shape and skeleton arrangement, including a reinforcement
by desmas which is rather unsual in poecilosclerids, between
Esperiopsis desmophora and the Ordovician sponge
Saccospongia baccata Bassler suggest that carnivory may be
very ancient in poecilosclerid sponges.
It thus appears that there is in fact a very high biodiversity
of carnivorous sponges in the deep sea. There are now more
than one hundred described representatives of Cladorhizidae
which very likely have this feeding habit, but this number is
certainly much higher, and it appears too that carnivory has
been developed in some representatives of other poecilosclerid
families as construed in the present consensual classification.
So far, however, this feeding habit is restricted to the order
Poecilosclerida. A role of exotyles present in diverse orders of
demosponges in trapping large particles has been suggested
by Hajdu (1994), but this does not indicate a carnivorous
feeding habit in sponges possessing exotyles, in which an
aquiferous system has generally been reported. The high
specific diversity and the biogeographical distribution of the
carnivorous sponges are difficult to correlate with peculiarities
in the reproduction mechanisms and to the dispersal ability,
as the reproduction of these species is poorly known. In
the Mediterranean, Asbestopluma hypogea has been able to
colonize several littoral caves most probably from deep-sea
canyons (Bakran-Petricioli et al. 2007), suggesting relatively
high dispersal ability.
Ecology
All carnivorous sponges are deep-sea species that were
previously considered as well adapted to the most foodpoor mid-basin areas (Gage and Tyler 1991). They may be
considered as “sit-and-wait predators”, spending a minimal
amount of energy during long periods between rare feeding
opportunities. Three species of Cladorhizidae have been found
at more than 8000 m depth and Asbestopluma occidentalis
Lambe, 1883 is the deepest known sponge, living in hadal
depth at 8840 m (Koltun 1970). A few cladorhizids, however,
are able to live at only 100 m depth in high latitudes, and the
Mediterranean cavernicolous species, Asbestopluma hypogea,
lives at a few meters depth in a cold-water littoral cave, but
most likely colonizes this habitat from a deep-sea population.
They live either on muddy bottom, where they often develop
rhizoids as an anchoring base, or on rocky bottom where their
diversity has certainly been more seriously underestimated.
However, it remains unknown which is the more favourable
type of bottom. In a few cases, it seems that the same species,
or very close species, may live on both types of substratum,
developing either an enlarged fixation base on rocks or
rhizoids in mud. The high diversity found in collections taken
by manned submersibles from rocky bottom near active
hydrothermal vents might suggest that this previously poorly
sampled environment is their preferred habitat. It would
appear that carnivorous sponges, as generally filter-feeding
sponges, do not take part in the rich oases of life thriving in
the immediate proximity of active hydrothermal vents. One
exception is Cladorhiza methanophila (Vacelet et al. 1995,
1996) which constitutes unusually large populations near
methane sources of a mud volcano in the Barbados because
of symbiosis with methanotroph bacteria. The number and
diversity of carnivorous sponges, however, could be enhanced
at a certain distance from such sites both by the unusual
prevalence of rocky substrates due to volcanic activity,
and by a general enrichment of the deep-sea ecosystem.
No quantitative data are available to date in relation to this
question. The abundance of Chondrocladia lampadiglobus
Vacelet, 2006 on the East Pacific Ridge between 2586 and
2684 m depth has been estimated at 1-2.6 individuals per
km of path by the manned submersible Nautile, but this
estimation was made some hundreds of meters from active
vents and we do not know if this is general on the East Pacific
Ridge. So far hydrothermal sites have been the favorite
targets of exploration from manned submersibles and ROVs,
introducing an evident bias. In a Pacific abyssal plain rich in
polymetallic nodules, the density of Cladorhizidae has been
estimated respectively at 16, 4 and 5 individuals per hectare
for Chondrocladia, Cladorhiza and Asbestopluma (Tilot
1992). Given their relatively small number and small size, it
would not appear at present that carnivorous sponges play an
important role in the deep-sea food chains.
Evolution and classification
The diversity of microscleres and of organization in
carnivorous poecilosclerids raises a puzzling problem of
evolution and classification. It has been pointed out by Hajdu
and Vacelet (2002) that the family Cladorhizidae as construed
in Systema Porifera in the suborder Mycalina lacks a clear
synapomorphy and that it could be polyphyletic. However,
this has to be reexamined, as several shared characters
of Cladorhizidae were also found in other sponges, such
as Euchelipluma, Abyssocladia and Esperiopsis spp. that
now appear to belong to a set of carnivorous sponges. The
three cladorhizid genera Asbestopluma, Cladorhiza and
Chondrocladia display a special shape, generaly stipitate,
pinnate or branching (Table 1), and their megascleres,
although differing in size and shape according to their
localization in the sponge, are referable to a single category
(mycalostyles) with the same skeleton arrangement.
Asbestopluma and Cladorhiza share the general organization,
with a stipitate, often pinnate shape and absence of aquiferous
system, but not Chondrocladia, which has kept the sponge
aquiferous system although its function and organization are
110
Table 1: Characters of the genera of carnivorous sponges (including some unpublished data). +: present in all species. ±: present in some
species only. * present in a single species.
Abyssocladia
Stipitate, pinnate or branching
Stipitate, with inflated spheres
Rhizoids
Aquiferous system
Mycalostyles
Basal substrongyles
Basal desmas
Spinose tylostyles or oxeas
Microtylostyles
Surface lining by microscleres
Palmate anisochelae
Anchorate anisochelae
Anchorate isochelae
Palmate isochelae
Arcuate isochelae
Abyssochelae
Placochelae
Sigmas
Sigmancistras
Forceps
Asbestopluma Chondrocladia
+
+
+
±
+
±
±
±
±
+
+
*
+
*
±
±
+
±
+
±
±
±
significantly modified. The chelae microscleres of the three
genera, however, are different, being palmate anisochelae
in Asbestopluma, anchorate/unguiferate anisochelae in
Cladorhiza and anchorate isochelae in Chondrocladia,
indicating possible polyphyly according to the present
interpretation of chelae (Hajdu et al. 1994). The value
of microscleres, and especially of cheloids in sponge
classification has often been the subject of debate. However,
the most common opinion today for Poecilosclerida is that
summarized by van Soest (2002, p. 518): “Because of complex
morphology, chelae are considered to reflect phylogenetic
relationships both at the family and genus level”. This
seemingly phyletic heterogeneity of sponges conventionally
classified in Cladorhizidae is even more evident for the
whole set of carnivorous sponges with the recent additions.
Carnivorous sponges now very likely include: (i) three species
of Euchelipluma, presently classified in Guitarridae due to the
presence of the diagnostic placochelae; (ii) several species of
Esperiopsis of the villosa group, currently classified in the
Esperiopsidae, with palmate isochelae (Vacelet 2006); (iii)
seven described species of Abyssocladia and several new
species under study from New Zealand and the North Atlantic,
currently classified in the Cladorhizidae although they have
palmate or arcuate isochelae. The case of Abyssocladia is
particularly puzzling because the genus was previously
synonymized, on the basis of possession of special isochelae
(abyssochelae), with Phelloderma Ridley and Dendy, 1886
in family Phellodermidae van Soest and Hajdu, 2002 in the
suborder Myxillina in which the chelae are not palmate, but
arcuate. However, it now appears that the type of isochelae,
arcuate or palmate, is rather uncertain in Abyssocladia as the
genus stands now with the inclusion of the newly described
+
+
+
+
Cladorhiza
+
+
*
*
+
+
±
±
Euchelipluma
+
+
+
±
+
±
*
?
+
+
+
+
+
*
+
+
±
+
Esperiopsis (pars)
+
±
±
species and of species in the process of description, as will be
explained below in greater detail.
The heterogeneity of the Cladorhizidae, and more generally
of carnivorous poecilosclerids, could be interpreted in two
different ways: (i) carnivory has developed relatively recently
in several different lines of evolution of Poecilosclerida, some
or all of the characters that they share being homoplasies due
to their special mode of life, with the consequence that the
various genera of carnivorous sponges are to be classified
in these different lines, matching up several families of
Mycalina, possibly of Myxillina; (ii) carnivory developed
very early in Poecilosclerida, possibly before the divergence
of Mycalina and Myxillina, the shared characters being
symplesiomorphic, with the consequence that they are to
be classified in a single high level taxon, possibly a distinct
suborder. The present set of data, summarized in Table 1, with
the shared and distinctive characters of carnivorous sponges,
will be examined and discussed below.
Fig. 1: Representatives of four genera of carnivorous sponges
illustrating the diversity of microscleres in sponges with a similar
morphology and organization. All have similar megascleres
(mycalostyles) with or without addition of strongyles. A.
Abyssocladia naudur Vacelet, 2006, paratype, abyssochelae,
sigma and sigmancistra. B. Asbestopluma agglutinans Vacelet,
2006, holotype and paratype, anisochelae 1, anisochelae 2, and
sigmancistra. C. Cladorhiza segonzaci Vacelet, 2006, holotype
and paratypes, anchorate anisochelae, sigma and sigmancistra. D.
Euchelipluma pristina Topsent, 1919, specimen from Barbados,
isochela, placochela and sigmancistra. A, B and C from Vacelet
(2006). D from Vacelet and Segonzac (2006).
111
112
All the presumed carnivorous sponges share a certain
number of morphological characters. They display a special
outer morphology, absence or significant modification of the
aquiferous system, an unusual microsclere arrangement and
the same type of megasclere skeleton. A stipitate shape with
symmetrical lateral expansions is found in all genera. For
instance, the feather-like shape with a more or less laterally
compressed axis bearing symmetrical laterals filaments lined
by prey-trapping microscleres is found in all genera except
Chondrocladia, and species classified in different genera
or families may be remarkably similar in shape (Fig.1).
The absence of canal system and choanocyte chambers
also appears to be general, again with the exception of
Chondrocladia. The main skeleton is always composed of more
or less modified mycalostyles, frequently strongly fusiform,
building longitudinal axes, showing only size differentiation
according to their position in the main or secondary axes,
without an ectosomal differentiation. In several species of
the various genera, the base of the main axis is reinforced by
mycalostyles modified in short strongyles. In three species,
Euchelipluma arbuscula, Asbestopluma (Helophloeina)
stylivarians (Topsent, 1928), Esperiopsis desmophora, again
belonging to various genera and families, these strongyles
are themselves modified in desmas. As far as may be inferred
from the description of often poorly preserved specimens,
most, possibly all species have on their lateral extensions a
lining of sigmoid or cheloid microscleres arranged with teeth
and alae outwardly directed. Carnivorous sponges are the
only poecilosclerids possessing true sigmancistras, which are
sometimes difficult to differentiate from sigmas but most often
clearly distinct. Sigmancistras are recorded in all genera except
Esperiopsis, although their occurrence is not general in all the
species. They have been reported for only two Asbestopluma
spp. and four Chondrocladia spp., but they are more frequent
in Cladorhiza and occur in all species of Abyssocladia and
Euchelipluma. Sigmancistras have been supposed by Hajdu
(1994) to be the primitive condition of development of
diverse poecilosclerid microscleres (cyrtancistra, diancistra,
clavidisc), an hypothesis which may underline the possible
antiquity of carnivory in Poecilosclerida.
An interesting issue for other shared characters of
carnivorous sponges could be the reproductive phenomena.
Reproduction is very poorly known in these deep-sea sponges,
although large embryos have been reported fairly often (for
instance by Lundbeck 1905), but without precise description.
These reports and preliminary observations suggest that
carnivorous sponges could share some peculiarities. In several
genera the embryos have been described as large, including
fascicles of megascleres and a variety of microscleres, and
with a special envelope which suggested to Topsent (1909)
that they were gemmules rather than embryos in Cladorhiza
spp. According to personal unpublished observations in
Asbestopluma hypogea, young embryos have multiflagellated
cells (Fig. 2), a character which is very unusual in sponges
(multiflagellated cells are known only in the trichimella
larva of Hexactinellida). This is confirmed by preliminary
observations in another species of Asbestopluma (Leys, pers.
comm.). The spermatogenesis of A. hypogea also appears
very unusual (Vacelet 1996) (Fig. 2), possibly in relation with
the absence of choanocyte chambers from which the sperm
cells of sponges generally derive. Spermatocysts develop
in the body, and then migrate towards the end of the lateral
processes, where the mature cysts become free. In the mature
cyst, sperm cells are surrounded by two envelopes, the inner
one unicellular, the outer one made by closely intertwined
cells. Two tufts of forceps are diametrically protruding on
the mature cyst, and may serve either as flotation devices for
dispersal of the whole cyst or for capture by the Velcro-like
lining of the filaments of another individual. Preliminary light
microscope observations suggest that similar phenomena
may occur in Cladorhiza methanophila (Vacelet and BouryEsnault 2002), in Chondrocladia gigantea (Hansen, 1885)
(Kübler and Barthel 1999), and in Euchelipluma pristina
(unpublished).
These shared characters of carnivorous sponges, however,
are in contrast with the characters of the chelae microscleres,
which is an important character for the suborder classification
of Poecilosclerida. The chelae are arcuate in the suborder
Myxillina, and palmate in the suborder Mycalina (Hajdu
et al. 1994, Hooper and van Soest 2002). The presence of
palmate anisochelae, anchorate anisochelae and anchorate
isochelae in the three genera of Cladorhizidae as defined in
Systema Porifera, was already rather puzzling. The addition
of Euchelipluma, Abyssocladia and some Esperiopsis spp.,
in which are present placochelae and isochelae grading from
palmate to arcuate, greatly increases the microsclere diversity
of carnivorous poecilosclerids. Moreover, most of the
abyssochelae and isochelae of Abyssocladia, as well as the
isochelae of Euchelipluma are difficult to assign precisely to
the arcuate or palmate type. In several species, isochelae and
abyssochelae may be “palmate to arcuate”, or clearly palmate,
or clearly arcuate (confirmed by Hajdu, pers. comm.). In a
few other Abyssocladia and Asbestopluma, some microsclere
characters do not agree with the present distinction between
microscleres of Mycalina and Myxillina. Abyssocladia
dominalba Vacelet, 2006 has small anisochelae with one end
palmate and the other arcuate, in addition to arcuate isochelae
and “palmate to arcuate” abyssochelae. An Asbestopluma
sp. from New Zealand, in the course of description by Kelly
and Vacelet, has arcuate, possibly anchorate, anisochelae in
addition to the normal palmate anisochelae. An Abyssocladia
sp., which will also be described from New Zealand,
has isochelae intermediate between the arcuate and the
anchorate types. This supports the hypothesis of polyphyly of
carnivorous poecilosclerids, which would mean that several
shared characters were obtained by homoplasic evolution in
several lines of Mycalina, in relationship with carnivorous
feeding. Is that likely?
This feeding mode does not in fact need any aquiferous
system and could induce a certain number of common
features. A plumose or pinnate shape, which is most propitious
for the passive capture of swimming prey, needs strong axes
of fusiform spicules, ideally reinforced at the base of the stalk
by intermingled spicules such as a cover of short vermiform
strongyles or of desmas. Prey capture also requires a lining of
the lateral expansions by hook-like cheloid microscleres, able
to trap the setae or appendages of invertebrate prey. Diverse
shapes of chelae and sigmas are propitious for such a role, and
chelae, sigmancistras and placochelae appear particularly well
adapted. Possible similarities in reproduction processes could
113
Fig. 2: Reproductive stages in Asbestopluma hypogea. A. Semi-thin section through an embryo, showing internal cells with yolk inclusions,
an outer layer of multiflagellated cells (arrow) and a maternal envelope. B. TEM view of a multiflagellated cell of the same embryo. C.
Mature sperm cyst at the tip of a filament, showing sperm cells (Sp), an inner envelope (En) and an outer envelope (Oe) made of closely
intertwined cells, and two tufts of forceps (desilicified) within their sclerocytes (Fo).
also be induced by the absence of aquiferous system and life
in the deep sea. Such a hypothesis of convergent evolution
of different characters linked to a carnivorous feeding habit
from different families of Poecilosclerida cannot be ruled out.
However, it is rather unlikely that the microscleres appeared
independently in several lines of evolution, for instance the
placochelae in Euchelipluma and in Guitarridae. Moreover,
this interpretation would mean the allocation of each genus
to a precise family, which in fact appears difficult. The
affinities of Asbestopluma with Mycalidae, of Esperiopsis
114
with Esperiopsidae and of Euchelipluma with Guitarridae
rely only on a single category of microscleres and on similar
megascleres which, however, are very differently arranged in
filter-feeding representatives of these families. Furthermore,
Cladorhiza, Chondrocladia and Abyssocladia would remain
with uncertain affinities in the present classification system.
The second hypothesis is more in agreement with the
characters shared by carnivorous poecilosclerids, such as
special morphology, megasclere nature and arrangement,
microsclere arrangement, and the absence or modification
of aquiferous system. Only the genus Chondrocladia
would appear to be distinctive by its morphology and the
preservation of an aquiferous system. However, a taxon
including all the carnivorous sponges, even excluding
Chondrocladia, would not be in agreement with the
present classification of Poecilosclerida. The highly diverse
microsclere complement found in the various genera would
match more or less adequately several families of Mycalina,
possibly also of Myxillina. This could mean that the present
basis of the classification of Poecilosclerida in suborder
is not appropriate. It could also mean that carnivory is
very ancient in sponges – with a possible support from the
similarities between the Ordovician Saccospongia baccata
and Esperiopsis desmophora – and appeared in an early
ancestor of Poecilosclerida with mycalostyle megascleres
and very diverse cheloid microscleres, to be considered as
symplesiomorphies. These microscleres could subsequently
have evolved differently in the diverse lines of Poecilosclerida,
developing a clearer distinction between palmate, arcuate
and anchorate types of chelae. It is interesting to note that in
carnivorous poecilosclerids the cheloid microscleres have an
obvious function, for which both their shape and arrangement
are well designed, while in filter-feeding poecilosclerids they
have no apparent function. Was this function lost in filterfeeding sponges, or was it relatively recently “designed”
by carnivorous sponges from preadapted microscleres of
presently unknown usefulness?
I consider that there is presently not enough strong
evidence for one or another of these hypotheses, which rest
on morphological and spicule characters. As suggested by the
surprising specific diversity found in the recent collections, we
may in the near future expect the discovery in the deep sea of
a large number of undescribed species, which will bring new
information. The data on reproduction are still very incomplete
and poorly understood, but the uniqueness of preliminary
observations in a few species suggests that they will provide
significant information. Furthermore, indications from gene
sequences will certainly become available soon and will bring
new data on the molecular phylogeny of Poecilosclerida,
which is at present insufficiently achieved and includes very
few exploitable data for carnivorous sponges. My feeling is
that it would be preferable to wait for this new information
before offering an interpretation of the phylogeny or a formal
proposal for the classification of carnivorous Poecilosclerida.
However, in predictive mode, the present set of data appears
to me more in agreement with the hypothesis of monophyly
or paraphyly of carnivorous poecilosclerids, possibly to be
considered as a distinct suborder of Poecilosclerida, rather
than with a polyphyletic interpretation.
Acknowledgements
I am grateful to Michel Segonzac (Ifremer) and Michelle Kelly
(NIWA) for entrusting me with the study of deep-sea specimens.
I also acknowledge the technical help of Chantal Bézac, Centre
d’Océanologie de Marseille. This paper benefited from fruitful
discussions and comments from Nicole Boury-Esnault and Eduardo
Hajdu.
References
Bakran-Petricioli T, Vacelet J, Zibrowius H, Petricioli D,
Chevaldonné P, Rada T (2007) New data on the distribution of the
“deep-sea” sponges Asbestopluma hypogea and Oopsacas minuta
in the Mediterranean Sea. Mar Ecol Evol Persp 28(suppl. 1): 1023
Bergquist PR (1978) Sponges. Hutchinson & Co, London
Cristobo FJ, Urgorri V, Rios P (2005) Three new species of
carnivorous deep-sea sponges from the DIVA-1 expedition in the
Angola Basin (South Atlantic). Organisms Diversity & Evolution
5: 203-213
Gage JD, Tyler PA (1991) Deep-sea biology. Cambridge University
Press, Cambridge.
Hajdu E (1994) A phylogenetic interpretation of hamacanthids
(Demospongiae, Porifera), with the redescription of Hamacantha
popana. J Zool 232: 61-77
Hajdu E, Vacelet J (2002) Family Cladorhizidae. In: Hooper JNA, van
Soest RWM (eds). Systema Porifera: a guide to the classification
of sponges, vol. 1. Kluwer Academic/Plenum Publishers, New
York. pp. 636-641
Hajdu E, van Soest RWM, Hooper JNA (1994) Proposal for a
phylogenetic subordinal classification of poecilosclerid sponges.
In: van Soest RWM, van Kempen TMG, Braekman JC (eds).
Sponges in time and space: biology, chemistry, paleontology.
Balkema, Rotterdam. pp. 123-140
Hooper JNA, Lévi C (1989) Esperiopsis desmophora n. sp. (Porifera:
Demospongiae): a desma-bearing Poecilosclerida. Memoir Queensl
Mus 27: 437-441
Hooper JNA, van Soest RWM (2002) Order Poecilosclerida Topsent,
1928. In: Hooper JNA, van Soest RWM (eds). Systema Porifera:
a guide to the classification of sponges, vol. 1. Kluwer Academic/
Plenum Publishers, New York. pp. 403-408
Koltun VM (1958) Cornacuspongida of sea waters washing the South
Sakhalin and the South Kurile Islands region. Issled dalvenost Mor
SSSR 5: 42-77
Koltun VM (1959) Corneosiliceous sponges of the northern and far
eastern seas of the USSR. Zoological Institute of the Academy of
Sciences of the USSR, Moscow-Leningrad
Koltun VM (1970) Sponge fauna of the north-western Pacific from
the shallows to the ultra-abyssal depths. Inst Oceanol Acad Sci
USSR 86: 165-221
Kübler B, Barthel D (1999) A carnivorous sponge, Chondrocladia
gigantea (Porifera: Demospongiae: Cladorhizidae), the giant deepsea clubsponge from the Norwegian trench. Memoir Queensl Mus
44: 289-298
Lehnert H, Watling L, Stone R (2005) Cladorhiza corona sp. nov.
(Porifera: Demospongiae: Cladorhizidae) from the Aleutian Islands
(Alaska). J Mar Biol Assoc UK 85: 1359-1366
Lévi C (1964) Spongiaires des zones bathyale, abyssale et hadale.
Galathea Rep 7: 63-112
115
Lundbeck W (1905) Porifera. Pars II: Desmacidonidae (pars).
Danish Ingolf-Exp 6(2): 1-219
Reiswig HM, Lee WL (2007) A new species of Cladorhiza (Porifera:
Cladorhizidae) from S. California (USA). In: Custódio MR, LôboHajdu G, Hajdu E, Muricy G (eds). Porifera research: biodiversity,
innovation, sustainability. Série Livros 28. Museu Nacional, Rio
de Janeiro. pp. 517-523
Ridley OS, Dendy A (1887) Report on the Monaxonida collected by
H.M.S. ‘Challenger’ during the years 1873-1876. Rep Sci Res Voy
H.M.S. ‘Challenger’, Zool 20(59): 1-275
Tilot V (1992) La structure des assemblages mégabenthiques d’une
province à nodules polymétalliques de l’Océan Pacifique tropical
Est. Thesis, Université de Bretagne occidentale, Brest
Topsent E (1909) Étude sur quelques Cladorhiza et sur Euchelipluma
pristina n. g. et n. sp. Bull Inst océanogr Monaco 151: 1-23
Topsent E (1928) Une mycaline productrice de desmes Desmatiderma
arbuscula n. g., n.sp. Bull Inst océanogr Monaco 519: 1-8
Vacelet J (1996) Deep-sea sponges in a Mediterranean cave. In:
Uiblein F, Ott J, Stachowitsch M (eds). Deep-sea and extreme
shallow-water habitats: affinities and adaptations, 11. Austrian
Academy of Sciences, Vienna. pp. 299-312
Vacelet J (1999) Outlook to the future of sponges. Memoir Queensl
Mus 44: 27-32
Vacelet J (2006) New carnivorous sponges (Porifera, Poecilosclerida)
collected from manned submersibles in the deep Pacific. Zool J
Linn Soc 148: 553-584
Vacelet J, Boury-Esnault N (1995) Carnivorous sponges. Nature
373: 333-335
Vacelet J, Boury-Esnault N (2002) A new species of carnivorous
deep-sea sponge (Demospongiae: Cladorhizidae) associated with
methanotrophic bacteria. Cahiers Biol Mar 43: 141-148
Vacelet J, Boury-Esnault N, Fiala-Médioni A, Fisher CR (1995) A
methanotrophic carnivorous sponge. Nature 377: 296
Vacelet J, Duport É (2004) Prey capture and digestion in
the carnivorous sponge Asbestopluma hypogea (Porifera:
Demospongiae). Zoomorphology 123: 179-190
Vacelet J, Fiala-Médioni A, Fisher CR, Boury-Esnault N (1996)
Symbiosis between methane-oxidizing bacteria and a deep-sea
carnivorous cladorhizid sponge. Mar Ecol Prog Ser 145: 77-85
Vacelet J, Segonzac M (2006) Porifera. In: Desbruyères D, Segonzac
M, Bright M (eds). Handbook of deep-sea hydrothermal vent
fauna, 18. Denisia. pp. 35-46
van Soest RWM, Hajdu E (2002) Family Phellodermidae fam. nov.
In: Hooper JNA, van Soest RWM (eds). Systema Porifera: a guide
to the classification of sponges, vol. 1. Kluwer Academic/Plenum
Publishers, New York. pp. 621-624
van Soest RWM (2002) Suborder Myxillina Hajdu, van Soest &
Hooper, 1994. In: Hooper JNA, van Soest RWM (eds). Systema
Porifera: a guide to the classification of sponges, vol. 1. Kluwer
Academic/Plenum Publishers, New York. pp. 515-520