Marine Ecology.

ISSN 0173-9565

ORIGINAL ARTICLE

Unexpected records of ‘deep-sea’ carnivorous sponges

Asbestopluma hypogea in the shallow NE Atlantic shed
light on new conservation issues

1, Thierry Pe
Pierre Chevaldonne
rez1, Jean-Michel Crouzet2, Wilfried Bay-Nouailhat2,
Anne Bay-Nouailhat , Ma€ıa Fourt3, Bruno Almo
2

n4,5, Jacinto Pe

rez5, Ricardo Aguilar6
1
& Jean Vacelet
1 Institut M
editerran
een de Biodiversit
e et d’Ecologie Marine et Continentale (IMBE), UMR 7263 CNRS, IRD, Aix Marseille Universit

e, Avignon
Universit
e, Station Marine d’Endoume, Marseille, France
2 Mer & Littoral, Melgven, France
3 GIS Posidonie, OSU Pyth
eas, Aix Marseille Universit
e, Marseille, France
4 Instituto Espan~ol de Oceanograf
ıa, Canary Islands, Centro Oceanogr
afico de Canarias, Santa Cruz de Tenerife, Spain
5 Grupo de Estudos do Medio Marin ~o (GEMM), A Corun ~a, Spain
6 OCEANA, Madrid, Spain

Keywords Abstract
Carnivorous sponge; Cladorhizidae; deep sea;
marine caves; Mediterranean; NE Atlantic; Marine cave communities have been a continued source of ecological surprises,
Porifera. among other things because of their close ecological and evolutionary ties with
the deep sea. The discovery of cladorhizid sponges, the deepest occurring porif-
Correspondence eran family, in shallow Mediterranean caves in the 1990s was one such sur-
Pierre Chevaldonn
e, Institut M
editerran
een prise, leading to the generally accepted hypothesis that the whole family was
de Biodiversit

e et d’Ecologie Marine et
carnivorous, an unprecedented feeding mode for sponges. The recent observa-
Continentale (IMBE), UMR 7263 CNRS, IRD,
Aix Marseille Universit
e, Avignon Universit
e,
tion of the cave species Asbestopluma hypogea in the Mediterranean bathyal,
Station Marine d’Endoume, Rue de la confirmed the view that some shallow caves can occasionally shelter otherwise
Batterie des Lions, 13007 Marseille, France. deep-dwelling species. Here we present new distribution data of A. hypogea,
E-mail: [email protected] from deep Mediterranean locations, and for the first time from Atlantic loca-
tions. Among the new Atlantic records, the most surprising ones are located in
Accepted: 8 February 2014 three different geographic areas (Ria de Arousa, Groix Island and Cherbourg)
of the NW European coasts, from the Iberian Peninsula to the English Chan-
doi: 10.1111/maec.12155
nel, where A. hypogea reaches SCUBA depths (5–50 m), while not sheltered in
marine caves. The carnivorous sponge however reaches its shallowest occur-
rence (5 m), in a small cave at Groix Island. The ecological significance of
these discoveries, particularly the very patchy distribution and peculiar dynam-
ics, are noteworthy, and the shallow occurrence of A. hypogea, together with
other deep-water or uncommon species, constitute unique assemblages that
must be considered in conservation plans.

sea, this allows carnivorous sponges to live in the hadal

Introduction
zone, whereas other demosponges and hexactinellids,
Whereas unexpected, it recently appeared that sponges although displaying a highly efficient aquiferous system
are able to select food resources to maximize their energy (Leys et al. 2007), do not go beyond the abyssal zone.
uptake in oligotrophic conditions (e.g. Topcßu et al. Carnivorous cladorhizid sponges (Poecilosclerida, Demo-
2010). A sit-and-wait predatory feeding mode can be an spongiae) are therefore generally well represented in the
even more rewarding strategy than the usual filter-feeding deep sea, recorded down to hadal depths (Hajdu & Vac-
mode (Monniot 1979; Gage & Tyler 1991). In the deep elet 2002). Three exceptions, however, have shown that

Marine Ecology (2014) 1–10 ª 2014 Blackwell Verlag GmbH 1

Carnivorous sponges on the NE Atlantic littoral Chevaldonn
e, P
erez, Crouzet, Bay-Nouailhat, Bay-Nouailhat, Fourt, Almo

n, P
erez, Aguilar, Vacelet

the genus Asbestopluma, which holds the deepest record nean endemic, in shallow Northeast Atlantic waters is
for sponges with 8840 m depth (Koltun 1970), also has also a surprising result which is discussed in the overall
relatively shallow littoral representatives. The first one, framework of the implementation of new marine pro-
Asbestopluma (Asbestopluma) hypogea Vacelet & Boury- tected areas.
Esnault, 1996 was discovered in permanently cold Medi-
terranean caves, at 15–26 m depth (Bakran-Petricioli
Study area
et al. 2007), a habitat offering trophic, thermal and
hydrodynamic conditions somewhat analogous to those Two main areas of the NE Atlantic have been the focus
in the deep sea. The carnivorous feeding mode of the of exploratory SCUBA dives to document the occurrence
family Cladorhizidae was evidenced for the first time in of the cladorhizid sponges in situ and to collect speci-
this species (Vacelet & Boury-Esnault 1995). Later records mens: (i) the Island of Groix, Bretagne, France (Fig. 1 #4;
of A. hypogea also came from Mediterranean deep rocks Fig. 2A–D) and (ii) the Ria de Arousa, Galicia, Spain
at 100–700 m depth (Aguilar et al. 2011). The second (Fig. 1 #6; Fig. 2F). One further documented SCUBA
exception, Asbestopluma (Asbestopluma) vaceleti Van Soest record (photograph) was communicated to us from
& Baker, 2011 has been described from 30 m depth in Cherbourg, France (Fig. 1 #5; Fig. 2E; L. Picot, pers.
Antarctica (Van Soest & Baker 2011), from a habitat comm.). Extensive exploration of the French Mediterra-
which, contrary to deep-sea locations and dark Mediter- nean canyons and deep-sea rocks with an ROV, only pro-
ranean caves, cannot be considered oligotrophic and dis- vided one single documented occurrence (video) from
plays more drastic hydrodynamic conditions. The third Western Corsica (Fig. 1 #12). Finally, new ROV sightings
example is Asbestopluma (Asbestopluma) occidentalis obtained by OCEANA around the Iberian Peninsula
(Lambe, 1893), the deepest known sponge, which has also (Fig. 1 #8, 13, 14) were compiled as well as one observa-
been found recently in cold water and dim light condi- tion from Sardinia (Fig. 1 #11; M. Bo, pers. comm.).
tions but at <35 m depth on the Pacific coast of Canada
(Chu & Reiswig 2014).
Material and methods
We here report, besides several new Mediterranean and
near-Atlantic deep-sea locations of A. hypogea, the dis-
Maintenance in laboratory
covery of a sponge identified as the same species in the
NE Atlantic under littoral conditions surprisingly con- Approximately 15 specimens collected with fragments of
trasting with those previously known for this species, and metallic substrate from a wreck at 30 m depth in Groix
more generally for carnivorous sponges. The discovery of were transported alive to Marseille and placed in 1.5–3 l
A. hypogea, which was previously considered a Mediterra- tanks in a temperature-controlled cabinet in the dark and

50°N 5

Fig. 1. Distribution map of all known

Asbestopluma hypogea sightings. Circles
4 represent shallow occurrences (SCUBA) and
squares are deeper observations made with
submersibles (>100 m). Grey symbols are
from Bakran-Petricioli et al. (2007) and
Aguilar et al. (2011). Black symbols are new
2 3
6 1 occurrences. 1:3PP Cave (17–22 m), 2: Jarre
12 Cave (15–17 m), 3: Garmenjak Cave (24–
26 m), 4: Groix Island (5–50 m), 5:
40°N Cherbourg (10 m), 6: Ria de Arousa (28–
9 38 m), 7: Chella Bank (167 m), 8: Ausias
8 11
March Seamount (100–110 m), 9: Enarete
Seamount (660 m), 10: Urania Bank + Linosa
7 13 Slope (625–707 m), 11: Isola del Toro,
14
10 Sardinia (118 m), 12: Les Moines Canyon,
Corsica (460 m), 13: Cabliers Bank, Alboran
Sea (370–400 m), 14: Gazul Mud Volcano
0° 10°E (494 m).

2 Marine Ecology (2014) 1–10 ª 2014 Blackwell Verlag GmbH

Chevaldonn

e, P

n, P
erez, Aguilar, Vacelet
erez, Crouzet, Bay-Nouailhat, Bay-Nouailhat, Fourt, Almo Carnivorous sponges on the NE Atlantic littoral

A B

C D

F G

Fig. 2. In situ morphology of Asbestopluma

hypogea. A–D, Groix island, Basse Vincent,
22–24 m depth (photos J.-M.C., September
2010). The specimen on (D) is approximately
4 cm high. (E) Cherbourg, 10 m depth,
(photo Laurence Picot, August 2005). (F)
Galicia, Ria de Arousa, 32 m depth (photo
J.P., July 2012). (G) Mediterranean 3PP cave,
20 m depth (photo R. Graille, December
2005).

at a temperature of 13 °C, as described in Vacelet & specimens fixed in 2.5% glutaraldehyde in a buffer com-
Duport (2004). They were maintained with an approxi- posed of 0.4 M sodium cacodylate/seawater 1/1 followed
mately monthly change of seawater and fed with live nau- by postfixation in 2% osmium tetroxide in seawater for
plii of the brine shrimp Artemia sp. 2 h. The specimens were embedded in Araldite and
sectioned as polished sections or semi-thin sections, the
latter after desilicification in 5% hydrofluoric acid for
Spicules and histology
30 min.
The morphological investigations of the samples have
focused on the skeleton architecture made of siliceous
DNA sequencing
spicules. Small pieces of sponges were boiled in a few
drops of nitric acid on a microscopic glass slide. After Specimens for DNA studies were preserved in ethanol
drying, the slide was rinsed with several drops of distilled 95% after sampling. One specimen collected in December
water, then either mounted in Araldite for light micros- 2010 in Groix (Atlantic), four specimens collected in 3PP
copy, or sputter-coated with gold-palladium for observa- cave (French Mediterranean) in 2001, 2004 and 2009,
tion under a Hitachi S570 Scanning Electron Microscope and one specimen collected in August 2008 from Gar-
(Vacelet 2006). Anatomy and histology were studied on menjak cave (Croatian Mediterranean) were used for

Marine Ecology (2014) 1–10 ª 2014 Blackwell Verlag GmbH 3

Carnivorous sponges on the NE Atlantic littoral Chevaldonn
e, P
erez, Crouzet, Bay-Nouailhat, Bay-Nouailhat, Fourt, Almo

n, P
erez, Aguilar, Vacelet

DNA extraction using the QIAmp DNA Mini kit found very abundant on different parts of the wreck since
(Qiagen). PCR amplification of a 658-bp fragment of July 2011. It was also found in September 2011 in lower
the mitochondrial cytochrome oxidase I (mtCOI) was density on the surrounding rocky substrate. Individuals
conducted with universal primers (Folmer et al. 1994). of A. hypogea are typically 2 cm high or smaller, and are
Sequences were obtained after cloning PCR products. primarily found on vertical parts of the wreck, but also
Sequences were edited with BIOEDIT 7.0.9 (Hall 1999) often on horizontal parts. The site is exposed to tidal
and deposited in the European Nucleotide Archive (ENA currents and swell. Visibility as well as light penetration
– EMBL) under accession numbers HG424317– can vary a lot. Temperature can be as low as 9 °C and
HG424322. may briefly reach 17 °C in September on site. Sur-
rounding fauna includes species characteristic of deeper
waters such as Megerlia truncata, the gorgonian Swiftia
Results
dubia (possibly the shallowest record for this species)
among other species such as Phakellia ventilabrum,
Localities and habitat
Raspailia sp., Eunicella verrucosa, Pteria hirundo, Diazo-
Groix Island (Fig. 1 #4) na violacea.

Basse Vincent (47°38.0140 N, 3°30.8160 W) Point 77 (47°35.7940 N, 3°29.8220 W)

This site is the first where Asbestopluma hypogea was rec- Point 77 is located on the southern side of Groix, about
ognized as such in the Atlantic (September 2010). It is halfway between Basse Vincent and Roche Color
ee. This
also the site with the earliest documented record with a 20-m-wide rock head rises from a flat rocky bottom from
posteriori identification of the species from pictures taken 50 to 40 m at its shallowest point. Asbestopluma hypogea
in July 2005. The sponge is still abundant to date. Basse was found in April 2012 on the steep vertical walls at 45–
Vincent is a rock head with the top at 17 m depth, 49 m depth, together with the brachiopods Megerlia trun-
located west of Groix Island, directly exposed to offshore cata and Terebratulina sp.
swell. Visibility can be very low due to the turbidity of
local waters, so most often light is highly reduced below Roche Color
ee (47°35.5890 N, 3°26.4460 W)
20 m, although algae are still present among Asbestoplu- Roche Color
ee is an underwater rock head located near
ma at its upper limit of distribution (about 19 m). Occa- the southeastern tip of Groix, where several Asbestopluma
sionally, water movements on the rock can be intense. hypogea have been observed at 20–24 m depth in July
Asbestopluma hypogea are located on the vertical walls of 2012. Uncommon surrounding fauna includes Homaxi-
a 1–2 m wide fault cut in the middle of the rock, which nella subdola, Pteria hirundo and Doris ocelligera.
reduces light penetration even further, but also reduces
currents. Temperature at 25 m varies from 9 °C in winter Philomel wreck (47°42.4760 N, 3°40.9300 W)
to short peaks at 17 °C in September. Asbestopluma hypo- Off the village of Do€elan, halfway between the Gl
enan
gea is abundant there between 22 and 32 m, displaying archipelago and the island of Groix, lies the ‘Philomel’
all size classes and rather high densities (up to 40 m2). wreck at 40 m depth. Asbestopluma hypogea has been
The biggest individuals reach 4 cm. It is not uncommon found in September 2012 on the wreck (P. Sauleau,
to find neighbouring specimens with fused bodies and pers. comm.). We confirmed this sighting in September
individual stalks. Surrounding fauna includes the forami- 2013.
niferan Miniacina miniacea, the sponges Axinella dissimi-
lis, Homaxinella sp., Raspailia sp., the cnidarians Kervedan cave (47°38.2760 N, 3°30.2950 W)
Parazoanthus anguicomus, Parazoanthus axinellae, Eunicel- On the WSW coast of Groix island, a small cave (7 m
la verrucosa, Leptopsammia pruvoti, Paralcyonium spinulo- long, 3 m wide, 1.5 m high, muddy bottom) sheltered
sum, the brachiopods Megerlia truncata and Terebratulina from the swell opens at 5–10 m depth. More than 20
sp., and the mollusc Doris sticta. Some of these species individual Asbestopluma hypogea have been observed since
are otherwise uncommon in the area. On one occasion, a November 2012 near the end of the cave, in a dark recess
pycnogonid Endeis spinosa was seen captured by A. hypo- at mid-height on the cave wall, occupying three different
gea. spots never exceeding 0.01 m² in surface area. Some indi-
viduals are thriving at 5 m depth. These are the shallow-
U-171 wreck (47°39.4700 N,3°34.8570 W) est A. hypogea and the shallowest carnivorous sponges
Offshore Basse de Groix, WNW of the island, this Ger- ever reported. Surrounding fauna includes Axinella spp.,
man submarine lies on a 38–42 m bottom of large flat Alcyonium hibernicum, Myxicola aesthetica and unidenti-
rocks and silty sand. Asbestopluma hypogea has been fied brachiopods.

4 Marine Ecology (2014) 1–10 ª 2014 Blackwell Verlag GmbH

Chevaldonn

e, P

n, P
erez, Aguilar, Vacelet
erez, Crouzet, Bay-Nouailhat, Bay-Nouailhat, Fourt, Almo Carnivorous sponges on the NE Atlantic littoral

Basse Jean-Mi (47°39.7290 N, 3°34.9270 W) eratum, Alcyonium palmatum, Paramuricea grayi, Spini-
Underwater rock head with the top at 12 m depth, off- muricea atlantica, Swiftia dubia, Eunicella gazella,
shore Basse de Groix, WNW of the island. A vertical wall Eunicella verrucosa, Leptogorgia lusitanica, Monomices pyg-
facing North goes down to 30 m, where it reaches sand. maea, Epizoanthus arenaceus, Savalia savaglia.
Five to six Asbestopluma hypogea have been found in Sep-
tember 2013. Surrounding fauna is rich and peculiar, Gazul Mud Volcano, Gulf of Cadiz (36°33.5590 N,
with the notable occurrence of Axinella infundibuliformis, 6°56.3380 W – Fig. 1 #14)
the gorgonian Leptogorgia sarmentosa (possibly the north- At least two individual Asbestopluma hypogea were sighted
ernmost report for this species), Alcyonium hibernicum, a posteriori on video footage taken by ROV at 494 m
the molluscs Charonia lampas and Okenia mediterranea, depth. They were found on small rocks, on a detritic bed,
and the bryozoan Reteporella sp. with bryozoans, sponges, polychaetes, hydrozoans, deca-
pod crustaceans (Munida sp. and Homola barbata) and
Tombant JM (47°41.5010 N, 3°38.7130 W) the foraminiferans Miniacina miniacea. This is the only
Off the village of Do€elan, a large North–South ‘pass’ Atlantic bathyal observation to date.
cuts through the bed rock. It is 300 m long and
100 m wide, the walls going down from 20 to 25 m Les Moines Canyon, Corsica (41°32.9170 N, 8°44.3830 E –
down to 50 m depth. Asbestopluma hypogea has been Fig. 1 #12)
sighted in September 2013 from 24 to 50 m on the Two large (4 cm?) individual Asbestopluma hypogea
western wall. This is the largest population found in were sighted a posteriori on video footage taken by the
the Groix Island area, possibly with an average of Comex submersible Remora 2000 at 460 m depth on
c. 100 individuals m2 for the whole western wall. The the northern side of the Les Moines Canyon, West Cor-
walls are otherwise rather poor in large benthos, but sica. They were found on slightly overhanging walls
include the noteworthy species Phakellia ventilabrum, made of white indurated marls (Fourt et al. 2013). Sur-
Parazoanthus anguicomus, the gorgonians Eunicella rounding fauna includes the scleractinian Desmophyllum
verucosa and Paramuricea grayi (to our knowledge, the dianthus and sub-fossil deep-sea oysters Neopycnodonte
northernmost report for this species) and the brachio- zibrowii.
pod Megerlia truncata.
Isola del Toro, Sardinia (38°50.9800 N, 8°21.6050 E – Fig. 1
0 0
Cherbourg (49°40.250 N, 1°39.867 W – Fig. 1 #5) #11)
Asbestopluma hypogea was recognized a posteriori on pic- Six individuals (at least 2 cm high) of Asbestopluma hypo-
tures taken in August 2005 by Laurence Picot at 10 m gea were sighted a posteriori on an ROV picture at 118 m
depth on vertical sides of the big rocks between the pier depth off Isola del Toro in SW Sardinia. They were found
and the Chavagnac Fort, Querqueville, west of the city of on vertical or slightly overhanging walls with abundant
Cherbourg (English Channel). Visibility and light level colonies of the red coral Corallium rubrum (M. Bo, pers.
are low due to the high particle load in the water (L. comm.).
Picot, pers. comm.).
abliers Bank, Alboran Sea (35°47.63450 N, 2°15.18570 W;
C^
0 0 0
Ria de Arousa (42º32.570 N, 8º57.070 W; 42º32.580 N, 35°47.70490 N, 2°15.04860 W – Fig. 1 #13)
8º57.3200 W; 42º32.7400 N, 8º57.0500 W – Fig. 1 #6) Two large (3 cm) individuals of Asbestopluma hypogea
Asbestopluma hypogea was found in three different sites of were sighted on an ROV picture taken in June 2011 at
the central part of the Ria, on vertical granitic walls sur- 370–400 m depth on two locations on Cabliers Bank in
rounded by sediment, at 28–38 m depth. Temperature at the Alboran Sea. Both were seen on horizontal substrate
this depth is rather constant year round, around 13 °C among hexactinellid sponges and not far from Lophelia
with brief extremes at 11 °C and 18 °C. Only very dim pertusa and Madrepora oculata reefs.
light reaches this depth, and there is no visible algal cov-
erage. The particle load is high in the water column and Ausias March Seamount, Mallorca Channel (38°44.42970 N,
visibility poor. Current intensity is low but there is a con- 1°49.00680 E – Fig. 1 #8)
stant water circulation. Surrounding fauna is mainly Three more individuals of Asbestopluma hypogea were
composed of large filter feeders, many of them character- sighted on ROV pictures taken in August 2011 at 100–
istic of deeper waters. Among the commonly found fauna 110 m depth on Ausias March Seamount off the Balearic
in the area are the sponges Axinella infundibuliformis, Ax- Islands, next to previous sightings reported by Aguilar
inella dissimilis, Phakellia ventilabrum, Phakellia robusta et al. (2011). They were seen on horizontal substrate in
and the cnidarians Alcyonium coralloides, Alcyonium glom- deep coralligenous beds.

Marine Ecology (2014) 1–10 ª 2014 Blackwell Verlag GmbH 5

Carnivorous sponges on the NE Atlantic littoral Chevaldonn
e, P
erez, Crouzet, Bay-Nouailhat, Bay-Nouailhat, Fourt, Almo

n, P
erez, Aguilar, Vacelet

Morphology small end, the alae are serrated and end in two short
lobes, with tooth also serrated and ending in three short
At all Atlantic localities, Asbestopluma hypogea displays a
lobes. Forceps 26.3–40 lm long, localized in spermatic
general morphology similar to that of the Mediterranean
cysts, are present in most of the prepared specimens.
specimens (Vacelet & Boury-Esnault 1996). A long, thin
Their branches are very thin (0.3–0.7 lm), frequently
stalk attached to hard substrate by a small basal plate
broken, and end in a small button.
bears an ovoid body surrounded by numerous filaments
(Fig. 2). The only noticeable difference recorded both
Living tissue
from underwater pictures and from specimens collected
in the shallow Atlantic is that the filaments appear to be Choanocyte chambers and canals are absent. The sponge
generally slightly shorter and thicker than in the Mediter- body of variable density is composed mainly of stellate
ranean. This distinction could be explained by the differ- cells. Bacteriocytes I and II, apparently similar to those
ence in environmental conditions between the type described in Mediterranean specimens, can be recognized
locality in the Mediterranean Sea and the shallow Atlantic on semi-thin sections (Fig. 4). Small micro-organisms are
sites (see Discussion). The colour is always white. The abundant in the denser parts of the tissue, either in bac-
skeleton is a dense axis of closely packed subtylostyles teriocytes I or in the mesohyle. Spermatic cysts in various
(mycalostyles) in the stalk, elongated in the axis of the stages of evolution are present in most specimens. The
body where it diverges into lateral branches toward the spongin of the basal plate contains several dense fila-
filaments. The filaments are cored by a thin spicular axis, ments, which are probably micro-organisms, possibly of
and their surface is lined by a large number of anisoche- fungal nature, boring into the spongin layer. Such
lae anchored by their small ends. filaments were not reported in the original description of
A. hypogea, but have been observed since in this species.
Spicules Remains of crustaceans are often present in the living
tissue (Fig. 4), and a still undigested copepod was
Megascleres observed trapped on one specimen collected in Galicia.
Subtylostyles/mycalostyles, with a faintly enlarged head,
straight or slightly flexuous (Table 1, Fig. 3). 268–
DNA sequences
922 9 2.5–11.8 lm. They are short, often curved and
with a well marked head in the basal plate where they The 658-bp mtCOI sequence obtained from the Groix
can be as small as 120 9 3 lm. These short mycalostyles specimen was strictly identical to that obtained from Gar-
were not reported in the original description of Mediter- menjak (only 611 bp recovered) and to the four
ranean specimens of A. hypogea, but further observations sequences obtained from 3PP (Bakran-Petricioli et al.
have shown their presence in 3PP cave specimens. 2007). They display a 99% identity (BLASTN) with the
partial COI sequence of Asbestopluma hypogea (from 3PP
Microscleres too) deposited in GenBank by Vargas et al. (2012) and
Palmate anisochelae, 10–12.5 lm long, have a central 91% identity with these authors’ Asbestopluma (Asbestop-
tooth of the large end ovoid, 4.5–6.2 lm long. In the luma) obae sequence from New Zealand.

Table 1. Asbestopluma hypogea. Spicule size range (in lm), mean size (bold) and standard deviation, depending on spicule type and on
sampling location.

Style body & filaments Style stalk Style basal plate Anisochelae Forceps

A. hypogea Vacelet & 385–780 350–920 (674  36.1) 9 9–13 25–34

Boury-Esnault 1996; (498  22.6) 9 2–7 3–7 (5.1  0.3) (11.2  0.2) (31.4  1.2)
(4.9  0.3)
Groix, specimen 350–720 10.1–12.2 28–40
collected 18/12/2010 (498.3  60.1) 9 2.8– (11.4  0.6) (34.2  4.1)
7.5 (5.4  1.3) n = 12
Groix, AhypWBN1-1, 370–580 310–720 120–280 10–12 32.5–37.5
coll. 18/12/2010 (493  54.4) 9 4.5–8 (482.8  141.8) 9 2–7 (180.4  57.7) 9 3–4 (10.9  0.6) (34.5  1.5)
(6.8  6.8) (6.1  0.7) n = 20 (3.5  0.6)
Galicia A, complete 268–922 (512.5  157.4) 9 2.5–11.8 (6.3  2.2) 10–12.5 26.3–33.8
specimen (10.9  0.7) (29.7  2.4)
N = 20

N = 50 unless otherwise stated.

6 Marine Ecology (2014) 1–10 ª 2014 Blackwell Verlag GmbH

Chevaldonn

e, P

n, P
erez, Aguilar, Vacelet
erez, Crouzet, Bay-Nouailhat, Bay-Nouailhat, Fourt, Almo Carnivorous sponges on the NE Atlantic littoral

A B E

C D

Fig. 3. Spicules of Asbestopluma hypogea

from different locations. (A) Mycalostyles,
Galicia (left, 524 lm) and Groix. (B) Head of
a mycalostyle (Galicia). (C) Subtylostyles of
the basal plate (Groix). (D) Forceps, Galicia
(top, broken) and Groix. (E) Anisochelae,
from Groix. (F) Anisochelae from Galicia. (G)
Anisochelae from 3PP cave.

Behaviour in aquarium Discussion

The specimens collected from the U-171 wreck in Groix The identification of the shallow NE Atlantic specimens
island have survived in the temperature-controlled cabi- as Asbestopluma hypogea, previously believed a Mediterra-
net at 13 °C in the dark for more than 21 months so far, nean endemic, appears certain, despite the differences in
with a monthly change of seawater and a monthly feeding life conditions. The general morphology, spicule size and
with live nauplii of brine shrimp. Their behaviour was characters, histology and cytology are exactly the same.
slightly different from that of specimens from the Medi- This morphological identification appears to be con-
terranean 3PP cave, which were maintained at the same firmed by the sequences of mtCOI, all of which are iden-
time in the same cabinet. After a long period of starva- tical from Croatia to Groix. The mtCOI data alone do
tion, the filaments of 3PP cave specimens tend to become not provide proof that the species is the same in the
very thin and elongate. However, the Groix specimens Atlantic and Mediterranean as this molecular marker is
displayed filaments that remained shorter than those of known to be slowly evolving in Porifera (W€ orheide et al.
3PP cave. Starvation caused a higher mortality in Groix 2005), but it brings significant support to the morpholog-
specimens, the sponge senescence usually being indicated ical evaluation. The filaments are generally slightly shorter
by the loss of their filaments and their body becoming and thicker in the shallow Atlantic specimens, but this
roundish. character can be highly variable in a given population

Marine Ecology (2014) 1–10 ª 2014 Blackwell Verlag GmbH 7

Carnivorous sponges on the NE Atlantic littoral Chevaldonn
e, P
erez, Crouzet, Bay-Nouailhat, Bay-Nouailhat, Fourt, Almo

n, P
erez, Aguilar, Vacelet

A B

C D

Fig. 4. Anatomy and histology of

Asbestopluma hypogea from Groix Island. (A)
section of a specimen from Groix (fixed
several hours after collection, with reduced
filaments). (B) Enlargement of the insert of
E (A), showing the surface lining of anisochelae
and debris of a partially digested copepod
(arrow). (C–E) Semi-thin section of desilicified
tissue, specimen from Groix; (C) bacteriocyte I
(stellate) and bacteriocyte II (round); (D)
sperm cyst; (E) group of bacteriocytes II
(vertical arrow) and one bacteriocyte I
(horizontal arrow).

and is related to water movements and to the feeding higher-salinity Mediterranean seawater. Iron oxidation
stage. Such a difference in the filament length was to be and more probably salinity conditions could explain the
expected owing to the higher hydrodynamic conditions behavioural differences observed and the higher mortality
and greater food availability encountered by the Atlantic of specimens from Groix.
specimens. This difference, however, remained for a long The surprise discovery of A. hypogea in the Atlantic
time even when both Atlantic and Mediterranean sponges first of all shows that it is not a Mediterranean endemic.
were maintained in the same laboratory conditions. The However, it should be stressed that the Gulf of Cadiz, the
environmental conditions in the temperature-controlled Galician coast and even South Brittany are known to be
cabinet, with no water movement at all, are more similar biogeographical areas still influenced by the Mediterra-
to those in the 3PP cave than to those of the Groix sta- nean biota (Borja et al. 2004). In that respect, the Cher-
tions, exposed to currents, tides and swell. However, the bourg observation appears the most unexpected. The
filaments of the captive Groix specimens never assumed other unexpected conclusion is that A. hypogea is not
the shape observed in Mediterranean caves. Iron debris limited to the bathyal zone, or to its shallow-water mim-
collected as a substrate to the Groix specimens has under- ics, cold-water dark caves. The species first appeared to
gone continued oxidation in the aquarium. Moreover, be confined to a very stable cave or bathyal environment,
water changes were provided to the Groix specimens with with low water movements, constant cold temperature,

8 Marine Ecology (2014) 1–10 ª 2014 Blackwell Verlag GmbH

Chevaldonn

e, P

n, P
erez, Aguilar, Vacelet
erez, Crouzet, Bay-Nouailhat, Bay-Nouailhat, Fourt, Almo Carnivorous sponges on the NE Atlantic littoral

oligotrophic conditions and low levels of light and inter- depths in the NE Atlantic and the Arctic, most of them
specific competition (Vacelet & Boury-Esnault 1995, from the Norwegian sea (Lundbeck 1905), and this area
1996; Vacelet 1996). However, it was later found that can be considered to be relatively well sampled. None of
total darkness was not required, as at 3PP, but mostly at these species can be confused with A. hypogea. The near-
Garmenjak in Croatia, light conditions were semi-dark est species, Asbestopluma (Asbestopluma) hydra Lundbeck
(Bakran-Petricioli et al. 2007). It was also found that the 1905 (Arctic, 1847 and 2394 m), also of the ‘lycopodina’
predator sponge benefitted from some degree of water type, differs in that it has thicker and shorter megascleres
movement, as all three previously known occurrences and slightly larger anisochelae with a larger frontal tooth.
showed an increased density where currents were higher However, relatively few species have been reported from
(Bakran-Petricioli et al. 2007). Temperature seems to be the Lusitanian region. A recent review of the NE Atlantic
a key factor controlling their distribution. Although Cladorhizidae did not record the presence of A. hypogea
A. hypogea appears to withstand temperature variations in this area (Hestetun et al. 2014). Here we have reported
better than originally expected (e.g. brief extremes at a single possible occurrence in Atlantic bathyal depths
23 °C), it is consistently found in places where average based on one in situ picture, in the Gulf of Cadiz, still
temperatures are cooler (i.e. cold-water lenses trapped in very close to the Mediterranean. A more extensive sam-
descending caves; Vacelet 1996; Bakran-Petricioli et al. pling may reveal its presence in the deep Atlantic further
2007). In all Atlantic populations here reported, tempera- away from the Mediterranean.
ture is unlikely to ever exceed 20 °C, so this requirement These new records are not likely to be the last surprise
is met even at the shallowest depths reported in Kervedan provided by the ‘deep-sea’ carnivorous sponge A. hypogea.
or Cherbourg, whereas in the Mediterranean shallow Regarding its amazing scattered distribution, from very
waters, the sponge is likely excluded by high temperature shallow waters to the deep sea, and from oligotrophic and
conditions in summer, when not in cold-water caves. calm waters of Mediterranean caves to eutrophic waters
Whereas the deep sea is a preferred habitat for carnivorous subject to the powerful swell and tides of the Brittany
sponges, A. hypogea is able to develop thriving populations shore, this charismatic sponge appears to be an ideal model
in shallow waters when conditions of temperature, inter- for research in evolutionary ecology, such as studies of the
specific competition and food availability are met. This connectivity between shallow and deep habitats or of adap-
also seems to be the case for the Antarctic cladorhizid tive processes in response to environmental changes.
Asbestopluma (Asbestopluma) vaceleti (Van Soest & Baker
2011) and the newly found populations of Asbestopluma
Acknowledgements
(Asbestopluma) occidentalis in the shallow (18–35 m)
Canadian Pacific (Chu & Reiswig 2014). We gratefully acknowledge the assistance of the SUBAG-
Our knowledge of A. hypogea distribution so far both REC diving club facilities in Groix. We wish to thank
in the Mediterranean and the Atlantic is still very partial Pierre Sauleau for sharing his observation on the ‘Philo-
and limited. It seems to be a sturdy species when envi- mel’ wreck, and Laurence Picot for her observation and
ronmental requirements are met, but its very patchy geo- picture taken in Cherbourg. We thank Pilar R
ıos L
opez
graphic distribution is an indication that its populations and Marcos Gonz
alez Porto for their advice and orienta-
might not be very resilient or that they are unable to set- tion. Marzia Bo provided information on photographic
tle in most available habitats. Despite intensive explora- evidence acquired off Sardinia. Thanks are also due to
tion conducted in Spain, Italy and France in recent years, Jackson Chu and Henry Reiswig for exchanging with us
deep-water occurrences of A. hypogea in the Mediterra- on the discovery of Asbestopluma occidentalis in shallow
nean are very scarce and sponges rarely occur in great waters. Caroline Rocher at IMBE-SCBM and Pierre-Alex-
numbers. Instead, single individual occurrences are more andre Rastorgueff provided much appreciated assistance
common (Corsica, C^abliers Bank, etc.) indicating an unu- in obtaining DNA sequences of the Groix specimen. The
sual population dynamic. For this reason, their listing on Corsican observation was obtained from ROV videos of
the Bern and Barcelona conventions appears justified. the CORSEACAN expedition thanks to the GIS Posido-
Shallow-water occurrence of this species is usually con- nie, the Comex Team and the French Agency for Marine
comitant with that of other deep-water or uncommon Protected Areas (AAMP).
remarkable species, constituting unique assemblages where
shallow- and deep-water species meet and interact. Such
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