Polar Biol (2007) 30:1545–1555 DOI 10.1007/s00300-007-0315-x
ORIGINAL PAPER
Antarctic associations: the parasitic relationship between the gastropod Bathycrinicola tumidula (Thiele, 1912) (Ptenoglossa: Eulimidae) and the comatulid Notocrinus virilis Mortensen, 1917 (Crinoidea: Notocrinidae) in the Ross Sea S. Schiaparelli · C. Ghirardo · J. Bohn · M. Chiantore · G. Albertelli · R. Cattaneo-Vietti
Received: 21 February 2007 / Revised: 11 May 2007 / Accepted: 14 May 2007 / Published online: 13 July 2007 © Springer-Verlag 2007
Abstract The Wrst case of parasitic association between an eulimid mollusc (Gastropoda, Ptenoglossa) and a comatulid (Echinodermata: Crinoidea) is reported for Antarctica. The mollusc involved in the association is Eulima tumidula Thiele, 1912, which has now been ascribed to the genus Bathycrinicola Bouchet & Warén, 1986, never recognized before in Antarctica. This genus is present only in the NE Atlantic Ocean and the Mediterranean Sea, and encompass species which are speciWc parasites of the sessile stalked crinoids of the family Bathycrinidae. However, in Antarctica, Bathycrinicola tumidula (Thiele, 1912) exploits the endemic vagile comatulid Notocrinus virilis Mortensen, 1917, and attains the largest known dimensions (»1 cm) for a Bathycrinicola species. The absence of suitable Bathycrinidae host in modern Antarctic benthic assemblages, as well as the long paleontological history of the genus Notocrinus in Antarctica, suggest a possible ‘hostswitch’ phenomenon. This event could reasonably have occurred when many species underwent considerable bathymetric shifts, during the dramatic climatic changes that aVected Antarctica.
S. Schiaparelli (&) Museo Nazionale dell’Antartide (MNA), Università di Genova, C.so Europa 26, Genova I-16132, Italy e-mail:
[email protected];
[email protected] S. Schiaparelli · C. Ghirardo · J. Bohn · M. Chiantore · G. Albertelli · R. Cattaneo-Vietti Dipartimento per lo Studio del Territorio e delle sue Risorse (Dip.Te.Ris.), Università di Genova, C.so Europa 26, Genova I-16132, Italy J. Bohn Zoologische Staatssammlung München, Münchhausenstr. 21, D-81247 München, Germany e-mail:
[email protected]
Introduction The Eulimidae is a large family of gastropods that parasitize echinoderms, with genera speciWcally adapted to feed on Asteroidea, Ophiuroidea, Echinoidea, Holoturoidea and Crinoidea (Warén 1984). Feeding is performed by penetrating the host skin with a proboscis and sucking body Xuids from internal cavities (Warén 1980, 1981a, b, 1984; Warén and Crossland 1991; Rinaldi 1994; Warén et al. 1994). Some species are free-living and can change host specimen, others are permanently attached to the host, while few aberrant species became true endoparasites (Warén 1984). The determination of the host is a very important aspect in the classiWcation of the Eulimidae, since their glossy and transparent shells sometimes oVer too few characters to the taxonomical identiWcation, leading to misidentiWcations. In fact, if the host is unknown, it often results exceedingly diYcult to assign an eulimid species to the proper genus (Warén 1984). Eulimid diversity is greatest at the tropics, and it has been estimated that up to 80% of the sampled species still await description (Bouchet et al. 2002). On the contrary, in Antarctica, notwithstanding the great diversity of echinoderms, where a cumulative number of 305 species has been estimated (Clarke and Johnston 2003), only 13 species of eulimids have been recorded so far (Dell 1990; Hain 1990; Numanami 1996; Engl 2004). Ecology and natural history of Antarctic eulimids are totally unknown and, up to date, notwithstanding eulimids are common in bottom samples, the host has been established only for one endoparasitic eulimid, Asterophila perknasteri Warén, 1994 (Warén and Lewis 1994). This lack of information is the result of technical constraints in sampling activities. In fact, in Antarctica, most benthos samples are obtained by destructive gears as the dredge,
123
1546
which generally does not preserve the association between organisms that live together, such as parasites and hosts. In 2004, Italian, New Zealand, and US researchers operating in the Ross Sea, performed extensive Weld sampling along the Victoria Land coast in the framework of the joint “Latitudinal Gradient Project” (LGP) (http://www.lgp.aq/). During these cruises, particular attention has been turned to the study of associations and, at this scope, potential hosts for parasitic and commensal molluscs have been carefully screened and preserved. In the present contribution, we describe the parasitic association between the eulimid Bathycrinicola tumidula (Thiele, 1912) [Eulima] and the comatulid crinoid Notocrinus virilis Mortensen, 1917. This comatulid was already cited in the literature as infested by ‘parasitic snails’, from samples of the Eltanin cruise collected oV Cape Adare area (Speel and Dearborn 1983), but the association was never described. Bathycrinicol tumidula, was previously only known from the Antarctic Peninsula-Weddell Sea (Hain 1990) and Bouvet Island (Linse 2006), and has never been recorded in the Ross Sea before, although the Speel and Dearborn’s (1983) ‘parasitic snails’ could reasonably be referred to this species. After the original placement in the genus Eulima, this species has been cited as Melanella tumidula (Thiele, 1912) but this ‘catch-all taxa’ genus, widely used for eulimids, which show the most general features of the family (e.g. smooth and glossy conical shells), includes only parasites of holothuroids. In our case, the accurate re-examination of shell features, anatomy and host association of the taxon tumidula, led to the reassignment of this species to the genus Bathycrinicola Bouchet & Warén, 1986. To this latter genus belong deep-water eulimid species that occur in the North Atlantic and Mediterranean Sea.
Materials and methods Sampling Crinoid specimens were collected in the framework of two joint Antarctic cruises held in the Ross Sea from January to March 2004. The R/V Tangaroa (BioRoss Expedition; Mitchell and Clark 2004) sampled between 65 and 75°S, and from 65 to 1,570 m; the R/V Italica explored the area comprised between 71 and 75°S (Ramoino 2004). Biological material was sorted on board into the main groups, labelled and preserved in alcohol or formalin. Laboratory In the laboratory, samples from individual stations were carefully examined for the presence of commensal or para-
123
Polar Biol (2007) 30:1545–1555
sitic molluscs with the aid of a stereomicroscope. Residuals from jars were sieved on a 1 mm mesh in order to obtain also specimens that possibly detached after Wxation. SEM observation was performed with a Leica Stereoscan 440 on critical point dried and gold sputtered specimens. Abbreviations used to describe comatulid ossicles and series of ossicles of arms and pinnules conform with Messing (1997). Map for the distribution of B. tumidula and the diVerent species of bathycrinids has been compiled according to the following sources: Bathycrinicola tumidula: SOMBASE url: http://www.antarctica.ac.uk/BAS_Science/programmes 2000–2005/ABPPF/SOMBASE/, Arntz and Gutt (1999), Gutt et al. (2000), Hain (1990) and present data; Bathycrinus australis: Carpenter (1884), Clark (1977), Döderlein (1912) and Emu database (2006); Bathycrinus sp.: J. Bohn, unpublished data from several expeditions to the Weddell Sea area (ANDEEP I–III, BENDEX). Voucher specimens are deposited in the Italian National Antarctic Museum (MNA) of Genova, Italy.
Results In the framework of the two joint cruises, more than 600 crinoid specimens, belonging to Promachocrinus kerguelensis Carpenter, 1888; Notocrinus virilis Mortensen, 1917; Anthometra adriani (Bell, 1908); Eumorphometra fraseri John, 1938; Phrixometra rayneri John, 1938; Florometra mawsoni A. H. Clark, 1937, have been sampled and examined. Among these, the only crinoid species that was found carrying parasitic snails is N. virilis. The Eulimidae were classiWed as Bathycrinicola tumidula (Thiele, 1912). Some of these parasitic snails were still adhering to the crinoid body with the proboscis inserted between the calcareous plates of the host; other specimens were found detached on the bottom of jars used to store N. virilis specimens (Table 1). Ecological and taxonomical account: host Phylum: Echinodermata Class: Crinoidea Order: Comatulida Family: Notocrinidae Genus: Notocrinus Mortensen, 1917 Notocrinus virilis Mortensen, 1917 (Figs. 1, 2) Material examined: 96 specimens (R/V Italica, cruise IT 04: 62 speciemens from 14 stations; R/V Tangaroa, cruise TAN 04: 34 specimens from 16 stations; see Table 1). Distribution: This species, endemic to Antarctica, probably has a circumpolar distribution (Fig. 6). It has been recorded from the Antarctic Peninsula and its oVshore islands, the South Orkney Islands, oV Enderby Land, from the Adélie Coast, the Balleny Islands and the Ross Sea area,
Polar Biol (2007) 30:1545–1555
1547
Table 1 List of station where N. virilis and B. tumidula were recorded Station
Cruise
Lat South
Long Est
Gear
Depth
Num. spec. N. virilis
Num. Spec. B. tumidula
Hout 4
IT 04
72°17⬘.2
170°23⬘.9
AGT
208
10
2
Hout 3
IT 04
72°17⬘.5
170°26⬘.1
AGT
246
13
2 (attached) + 3 (found in the jar)
Hout 1
IT 04
72°15⬘.5
170°28⬘.3
AGT
537
2
H-out 4ter
IT 04
72°18⬘.2
170°26⬘.0
AGT
218
1
A2
IT 04
71°17⬘.3
170°39⬘.2
AGT + sledge
421
1
A1
IT 04
71°15⬘.5
170°42⬘.2
AGT + sledge
515
1
Hin-3
IT 04
72°17⬘.0
170°13⬘.1
AGT + sledge
316
1
Hin-4
IT 04
72°17⬘.1
170°14⬘.0
AGT + sledge
196
11
H-out 3bis
IT 04
72°17⬘.4
170°26⬘.4
AGT + sledge
258
8
H-out 2bis
IT 04
72°17⬘.1
170°29⬘.9
AGT + sledge
388
2
C2
IT 04
73°22⬘.7
170°06⬘.9
AGT + sledge
410
1
SMN
IT 04
74°43⬘.2
164°13⬘.1
AGT + sledge
366
4
R3
IT 04
74°49⬘.3
164°11⬘.5
AGT + sledge
330
3
R2
IT 04
74°49⬘.0
164°18⬘.1
AGT + sledge
364
4
15
TAN 04
71°43⬘.7
171°44⬘.1
SEL
466
2
18
TAN 04
71°43⬘.6
171°46⬘.9
ORH
522
1
19
TAN 04
71°44⬘.1
171°44⬘.0
ORH
429
3
28
TAN 04
71°43⬘.1
171°30⬘.2
ORH
305
1
33
TAN 04
71°45⬘.3
171°25⬘.0
SEL
282
2
35
TAN 04
71°46⬘.1
171°6⬘.6
SEL
241
3
36
TAN 04
71°46⬘.2
171°8⬘.56
ORH
236
1
39
TAN 04
71°45⬘.3
171°8⬘.9
SEL
250
8
52
TAN 04
72°20⬘.2
170°23⬘.7
SEL
154
2
55
TAN 04
72°18⬘.5
170°21⬘.5
ORH
130
1
63
TAN 04
72°19⬘.3
170°28⬘.7
SEL
303
1
105
TAN 04
71°15⬘.5
170°38⬘.1
SEL
470
2
145
TAN 04
72°1⬘.5
170°54⬘.2
SEL
270
2
186
TAN 04
71°30⬘.7
171°25⬘.5
BEAM
390
3
188
TAN 04
71°32⬘.9
171°6⬘.7
SEL
286
1
269
TAN 04
65°28⬘.3
161°2⬘.5
BEAM
760
1
6
1
Abbreviations for gears: Agassiz Trawl (AGT); Epibenthic Sled (SEL); Rough Bottom Trawl (“orange roughy”, ORH); Beam Trawl (BEAM)
from 80 to 1,120 m (Mortensen 1917; John 1938, 1939; Marr 1963; Clark and Clark 1967; Speel and Dearborn 1983; herein). Remarks: Two closely related Notocrinus species, namely N. virilis and N. mortenseni John, 1937 are widely distributed in the Southern Ocean. The diagnostic features, separating the current species from its congener are according to Clark and Clark (1967, p. 4): centrodorsal truncated and conical, usually higher than wide; centrodorsal bare between interradial columns of cirrus sockets; cirri number less than 50; cirri long and composed of up to 90 segments. Alive, specimens are of a deep red colour, which is already conspicuous in the sessile pentacrinoid larval stage. These stalked larvae (Fig. 1) are quite abundant on mooring structures located oV Terra Nova Bay, in
about 100 m depth (S. Schiaparelli, unpublished). Adult specimens are large and stout (Fig. 2), and may reach an arm length of up to 20 cm, resulting in a crown diameter of 40 cm or more. Characteristic for the genus is the presence of a brood pouch between the arm and the base of each genital pinnule. Within the brood pouch, the larvae grow to the considerable size of 1.8 mm in length (Mortensen 1920). Ecological and taxomical account: parasite (Fig. 3) Phylum: Mollusca Class: Gastropoda Subclass: Prosobranchia Order: Ptenoglossa Family: Eulimidae Genus: Bathycrinicola Bouchet & Warén, 1986
123
1548
Fig. 1 a, b Pentacrinoid larva of Notocrinus virilis. a Whole pentacrinoid larva, b detail of the crown. Abbreviations: attachment disc (ad); arms (ar); calyx (cl); crown (cw); tegmen (tg); stalk (st). Scale bars: (a) 5 mm; (b) 1 mm
Fig. 2 a–c Adult vagile phase of Notocrinus virilis (Ref# MNA 760, Terra Nova Bay, 2002, 100 m depth). a Oral side of the crinoid, b detail of the arm (oral side). c Lateral view of the same. Abbreviations: anus (an), brachial (br); cirrus (cr); (gd) or brood pouch; mouth (mt); pinnule (pi); tegminal plates (tp)
123
Polar Biol (2007) 30:1545–1555
Bathycrinicola tumidula (Thiele, 1912) [Eulima] new comb. Material examined: 12 specimens (Table 1) Distribution: up to date the species, described from the Gauss-Station, has been reported only from the Antarctic Peninsula and the Weddell Sea (Fig. 6), in 228–673 m (Hain 1990; Engl 2004) and at Bouvet Island (Linse 2006). Description: B. tumidula very closely resembles B. talaena (Dautzenberg & Fischer, 1896) and B. curta (Warén, 1972), which were found in the Atlantic (see Bouchet & Warén, 1986). The shell is broad and conical, transparent, and shows a large aperture with a straight columella, as typical for the genus (Fig. 3a). The protoconch has 2.5 whorls and a diameter of about 790 m (Fig. 3b–c). The operculum is thin and follows the shell aperture outline, although it is smaller than it (Fig. 3d, e). The proboscis is very extensible (Fig. 3a vs. 4) and has a ring fold as is known to occur in B. talaena (Fig. 5c, d) (see Bouchet and Warén, 1986). Gross anatomy of a specimen just extracted from the shell is reported in Fig. 4. Generic placement: In the current check lists of Antarctic molluscs (e.g. SOMBASE url: http://www.antarctica.ac.uk/ BAS_Science/programmes2000–2005/ABPPF/SOMBASE/), Eulima tumidula Thiele, 1912 is placed in the genus Melanella Bowdich, 1822, which encompasses eulimid species that are ecto- or endo-parasite of holothuroids and have a retractile proboscis (Warén 1984). However, it is evident from morphological and host (a comatulid) features, that the taxon Eulima tumidula Thiele, 1912 does not belong neither to Eulima nor Melanella. Among the eulimid genera that are known to parasitize crinoids, Tropiometricola Warén, 1981a, b, Goodingia Lützen, 1972, Crinolamia Bouchet & Warén, 1979, Curveulima Laseron, 1955, Annulobalcis Habe T., 1965 and Bathycrinicola Bouchet & Warén, 1986, this Antarctic species can be reasonably assigned, on a morphological base, to the latter (A. Warén, personal communication, 2006). Up to date, the genus Bathycrinicola is known to occur only in the NE Atlantic Ocean and the Mediterranean Sea (Bouchet and Warén 1986; Peñas and Giribet 2003; CLEMAM database 2006), where it numbers six species (Table 2). So far, Bathycrinicola is absent or has not been recognized yet, from the western Atlantic Ocean south to Argentina (Rosenberg 2005: Malacolog database) from the Indo-PaciWc (OBIS Indo-PaciWc Molluscan Database 2006) and from New Zealand (Bruce Marshall, personal communication, 2006). This represents the Wrst record of the genus for Antarctica, and of the species for the Ross Sea.
Description of the association (Fig. 5) Only two B. tumidula specimens were found still adhering to the body of their host, although many other N. virilis
Polar Biol (2007) 30:1545–1555
Fig. 3 Morphological features of Bathycrinicola tumidula (Ref# MNA 847, Italica cruise 2004, oV Cape Hallett, 258 m depth). a Shell (in frontal and lateral view, respectively), total length 8.8 mm; this is the specimen Wgured on the host in Fig. 5e. b SEM picture of the pro-
1549
toconch, lateral view; the arrow marks the protoconch–teleoconch boundary, scale bar 120 m. c SEM picture of the protoconch, top view; the arrow marks the protoconch–teleoconch boundary, scale bar 120 m. d Operculum in external view. e Operculum in internal view
In both cases, the parasitic mollusc inserts the proboscis between calcareous plates, perforating the perisome, the noncalcareous integument that covers the oral surface and the gonads (Clark 1915). Unfortunately, the preserved material we studied does not allow appreciating any colour matching between the parasite and the host, as crinoid-parasitizing eulimids are known to do in temperate–tropical seas (Potts 1915; Fishelson 1973).
Discussion
Fig. 4 Soft part morphology of a dissected specimen; abbreviations: Abbreviations: eye tentacles (et); gonads (g); operculum (op); proboscis (pr); penis (pe)
specimens show evidence of predation, in terms of the presence of predation holes. The Wrst of these was found on the calyx, with the proboscis inserted in the interambulacral area, at the margin of the irregular tegminal plates, between the two radials and basal brachials (Ibr1) (Fig. 5c, arrow). Another predation hole can be seen between the Wrst primibrachial (Ibr1) and the axillary (Fig. 5d, asterisk). The second was attached at the base of the pinnule (P3) of the seventh brachial (br7), where the gonad or the female brood pouch (potentially with embryos inside) is accessible (Fig. 5e, f).
The actual benthic marine fauna of the Southern Ocean is a mixture of taxa with diVering evolutionary histories and biogeographical aYnities (Clarke et al. 1992, 2004), with few relict elements of an autochthonous Cretaceous fauna that evolved in situ for several millions of years after the Gondwana breakage (Knox and Lowry 1977; Clarke and Crame 1989; Crame 1994). In fact, notwithstanding the unique series of climatic and geomorphological events that aVected Antarctica (Clarke et al. 1992; Imbrie et al. 1993; Arntz et al. 1997; Thatje et al. 2005), some of these relicts can still be recognized in few examples of marine genera (e.g. the octocoral Rosogorgia) that show a disjointed distribution, occurring in subtropical and Antarctic waters (see López-González and Gili 2001; Gili et al. 2006). The knowledge of all these dramatic processes has deeply conditioned the ideas about Antarctic Benthos leading, for example, to the general belief that partnerships among marine invertebrates could have not been maintained or developed in Antarctica due to the persistence of a general state of environmental ‘instability’ (AAVV 1977, p. 389).
123
123 Unknown Possibly the crinoid Leptometra phalangium (J. Müller, 1841)
Bathycrinicola media Unknown Bouchet & Warén, 1986
Unknown
Unknown
Unknown
Bathycrinicola nacraensis Peñas & Giribet, 2003
?Bathycrinicola sp
?Bathycrinicola sp.
Rhizocrinus verrilli A. H. Clark, 1908 (=R. lofotensis M. Sars, 1868)
Democrinus sp.
Unknown
Probably Rhizocrinus lofotensis M. Sars, 1868
Bathycrinicola macrapex No snout, foot present, proboscis not Bouchet & Warén, 1986 retracted, operculum present, penis absent
Same as B. talaena, but with head–foot larger, completely retracted proboscis, penis well developed
Bathycrinicola curta (Warén, 1972)
Democrinus parfaiti E. Perrier, 1883
Unknown
No snout, head–foot small, small ring fold on the proboscis, eyes deeply buried at the base of tentacles, operculum very thin and transparent, penis well developed
Bathycrinicola talaena (Dautzenberg & Fisher, 1896)
Crinoid host
Bathycrinicola micrapex Unknown Bouchet & Warén, 1986
Morphological features
Eulimid species
Table 2 Worldwide records of Bathycrinicola species, outside Antarctica Region
NE Brasil OV Nova Scotia
Unknown
Mediterranean (South Spain)
Between Canarie and West Africa
Azores, Bay of Biscay and oV Portugal
Azores, Bay of Biscay and oV Portugal
Norway
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Ectoparasite, attached Azores, Bay of Biscay to the host by the and Ibero-Moroccan proboscis (between Gulf calyx and Wrst arm joint)
Type of infestation
References
Bouchet and Warén 1986
400
1,493
105
500
Clark 1921
Clark 1977
Peñas and Giribet 2003
Bouchet and Warén 1986
1,200–1,900 Bouchet and Warén 1986
1,200–2,400 Bouchet and Warén 1986
315–317
1,000–2,000 Bouchet and Warén 1986
Depth
1550 Polar Biol (2007) 30:1545–1555
Polar Biol (2007) 30:1545–1555
1551
Fig. 5 a–h Bathycrinicola tumidula parasitizing Notocrinus virilis (preserved specimens). a The B. tumidula specimen found on the calyx, with the proboscis inserted in the interambulacral area, at the margin of the irregular tegminal plates of N. virilis (Ref# MNA 848, Italica cruise 2004, oV Cape Hallett, 258 m depth). b–d Closer view of the same specimen; arrow indicates the small ring fold of the proboscis, which is still inserted between the two radials and basal brachials; the asterisk indicates another predation hole where, possibly, another specimen was attached. e, f The second B. tumidula specimen attached
at the base of the pinnule of the seventh brachial, where there can be the gonad or the female brood pouch; arrow indicates the inserted proboscis (f) and the hole on the pinnule after the removal of the specimen (g) (Bathycrinicola Ref# MNA847; Notocrinus Ref# MNA 759). g The same hole after the removal of external tissues, to show the deep aperture drilled by the eulimid proboscis; abbreviations: Wrst primibrachial (Ibr1); primibrachial axillary (Ibr2); radial (rd), seventh brachial (br7); third pinnule (P3)
In recent years however, a growing body of evidence highlighted as these marine symbiotic associations, in the classic De Bary’s deWnition (De Bary 1878), which also encompasses parasitism (see Kutschera and Niklas 2005), do exist in Antarctica, although rarely documented. Among these, several gastropods have been found to be associated with particular hosts/preys, as the kleptocommensal capulid Capulus subcompressus that exploits the serpulid Serpula narconensis (see Schiaparelli et al. 2000), the cerithiopsid Krachia antarctica (Gastropoda) that parasitizes the sponge Haliclona dancoi (see Schiaparelli et al. 2003), and the zerotulid Dickdellia labioXecta which exploits giant pycnogonids (Sirenko 2000; Lehmann et al. 2006), a type of association endemic to Antarctica. In some other remarkable cases, the partnership also involves groups with a possible Cretaceous origin, as the case of the hydroid Sarsia medelae, which lives as a meso-
biont of gorgonians with a non-parasitic relationship (e.g. Gili et al. 2006). Given the above, one of the major challenges in the ecological research relative to Antarctic benthos, examined under a hystorical-evolutive perspective, is to verify in other examples of closely interacting invertebrates, whether or not their ‘symbiotic’ relationships got extinct, or survived to the tortuous changes that aVected Antarctica. In the latter case, one of the most probable adaptations is a ‘host-switch’, as already documented in the case of the kleptocommensal gastropod Capulus subcompressus (Schiaparelli et al. 2000). In this paper, we documented a further case of ‘symbiotic’ association occurring in Antarctica, which involves an eulimid mollusc and its echinoderm host, a comatulid crinoid. These echinoderms, at least in the tropics, are the centre of complex and multispecies series of interactions
123
1552
among diVerent invertebrates, which inhabits/parasitize the crinoid crown of tentacles (e.g. Huang et al. 2005). On the contrary, in Antarctica, only myzostomid infections, which produce calciWed cysts on the upper side of the crinoid arm, have been reported so far (e.g. Jangoux 1987). In our association, it appears that all the basal ecological requirements of Eulimidae are still satisWed and such a relationship could apparently be considered among those that have been ‘maintained’ in time. However, considering the host of the association, it emerges that most probably a ‘host-switch’ phenomenon has occurred. In fact, while all the Bathycrinicola species from the deep Atlantic Ocean (Table 2) parasitize sessile stalked crinoids of the family Bathycrinidae (hence the name of the eulimid genus) (Bouchet and Warén 1986), the Antarctic one, B. tumidula, has adapted to a vagile comatulid. From an autoecological point of view, this fact makes a great diVerence, since stalked crinoids and comatulids have rather diVerent natural histories–ecologies. Bathycrinids predominate in depth levels of 1,500– 3,000 m (Améziane and Roux 1997), where they can migrate along mid-ocean ridges and seamount alignments (Roux 1982). They are generally small, with a total length (from the base of the stalk to the end of the arms) of 120 mm, e.g. in Rhizocrinus lofotensis (see Clark 1970) and about 200 mm in Democrinus parfaiti (see Clark 1977). The comatulids, or ‘unstalked crinoids’, to which Notocrinus virilis belongs, are instead able to crawl and cling onto elevated substrata due to the presence of cirri, or even to swim (Meyer and Macurda 1977); they are generally bigger than stalked crinoids, with a crown diameter of up to 40 cm, and usually occupy much shallower waters, generally not extending deeper than the shelf. Even molecular data underline these diVerences between the two groups, and the sessile Bathycrinus stands as a basal taxon to Comatulida (Cohen et al. 2004). Given the above, it seems that, at a certain stage, in Antarctica, a species of Bathycrinicola switched host, becoming a parasite of a comatulid belonging to the genus Notocrinus, instead of a stalked bathycrinid. To date, in Antarctica, only one small species of Bathycrinus has been sampled, B. australis A.H. Clark, 1907, which is known from the Southern Ocean, the southern Atlantic and the southern PaciWc Ocean (Fig. 6), ranging from 1,730 to 8,300 m depth (Carpenter 1884; Clark 1977; Döderlein 1912; Emu database 2006). Some undetermined Bathycrinus specimens, still at study and collected in the framework of recent Antarctic cruises (ANDEEP I–III, BENDEX) probably also belong to this species (J. Bohn, unpublished data). According to Roux (1987), B. australis was the unique bathycrinid able to migrate in the Southern Ocean, due to its small dimension and an opportunistic life-style. However,
123
Polar Biol (2007) 30:1545–1555
Fig. 6 Distribution of Bathycrinicola tumidula, Notocrinus virilis, B. australis and Bathycrinus sp. around the Antarctic continent. B. australis and Bathycrinus sp. records have been combined in the map under the single name ‘Bathycrinus sp.’ (open triangles); B. tumidula literature records (open circles); B. tumidula present records (Wlled circles); N. virilis distribution (cross symbol)
at the present state of knowledge, is it not possible to ascertain whether or not this genus was also present in Antarctica even millions of year ago, hosting an hypothetic Bathycrinicola ancestor as, up-to-date, no fossils of this group have been discovered yet. Besides the uncertainty about the diVusion of the genus Bathycrinus in Antarctica in the past, it appears however clear that extant Antarctic Bathycrinus cannot represent a suitable host for B. tumidula, as this large eulimid attains the length of 1 cm and, as far as is known, is the largest species in the genus, while Antarctic Bathycrinus are almost of the same size. Therefore, in Antarctica, the absence of a suitable sessile stalked crinoid for this ‘southern’ Bathycrinicola lineage, seems to have represented the crucial selective pressure that determined this possible ‘host-switch’. Notocrinus virilis might instead represent a good ‘candidate’ to be exploited by an eulimid, due to a series of peculiarities that diVerentiate this Antarctic endemic species from the other Antarctic comatulids. For example, its arms and pinnules are smooth, without keels, spines, or ‘ornaments’, all features that are instead present in the majority of other Antarctic crinoids and in those tropical counterparts which face an intense predation pressure (Meyer and Macurda 1977). However, these macroscopic observations cannot be true in the case of a microparasite, as there is also good evidence
Polar Biol (2007) 30:1545–1555
that eulimids like spiny hosts since they protect the snails from predators (Warén 1984), and the skeletal armour could be used as a defence towards large predators as Wshes. In fact, Antarctic crinoids are commonly exploited by nototheniid Wshes (La Mesa et al. 1997), but no Wne characterization of stomach content has ever been performed and no data about the most exploited crinoid species are available. A plausible explanation could be a diVerent toxicity between the diVerent crinoid species but, also in this case, too few data are about this topic are available (McClintock 1989), so that, at the present state of knowledge, it is impossible to speculate about a greater palatability-minor toxicity of N. virilis in respect to other crinoid species. However, further insights about the possible origin of this association can also be obtained from the palaeontological history of the endemic genus Notocrinus, which appear to have been present in Antarctica since a long time. In fact, a fossil species of Notocrinus, was already present in the late Eocene, as testiWed by fossils from the Meseta formation, Seymour Island (Meyer and Oji 1993), where the species occurred together with an abundant stalked isocrinid crinoid of the genus Metacrinus. At this site, palaeoecological clues suggest that the crinoid beds occupied a shallow water site, during a period of abrupt cooling and expansion of ice sheets, that occurred around 35 million years ago (Meyer and Oji 1993). After this phase, the genus Metacrinus got extinct in Antarctica, while Notocrinus spread to deep-water habitats where they can be found nowadays (Zinsmeister and Feldmann 1984; Meyer and Oji 1993). This fact opens many diVerent scenarios that, however, due to the large gap in the fossil record, especially for the possible ancestors of Bathycrinicola and Bathycrinus, remain in the speculative Weld. On the other hand, it is plausible, that a possible switch between a host of the genus Bathycrinus with one of the genus Notocrinus occurred at this stage, when the shallow water ancestors of Notocrinus, spread into deeper habitats where they could have encountered an unknown Bathycrinicola-carrying host. Notocrinus virilis, or its ancestor, due to its dimensions, could have allowed to a small Bathycrinicola species to exploit more food, attaining a larger size in respect to all other known Bathycrinicola species, that are instead only few millimeters (Bouchet and Warén 1986), leading to the ‘giant’ taxon B. tumidula. A similar host-switch could also have occurred for the unique species of Bathycrinicola described for the Mediterranean Sea, where stalked crinoids are absent (Tortonese 1965). In fact, the recently described Bathycrinicola nacraensis Peñas & Giribet, 2003, has been inferred to parasitize the crinoid Leptometra phalangium (J. Müller, 1841) (Peñas and Giribet 2003), which lives in highly productive areas of the shelf break (Colloca et al. 2004). This association however, needs to be conWrmed with direct proofs.
1553
Unluckily, at the moment, no molecular data about Bathycrinicola and Eulimidae in general are available, preventing the possible reconstruction of timing of host-switch events or, at least, host-based routes of speciation, as sometimes can be tempted for closely interacting groups of predators–parasites (Schiaparelli et al. 2005). Acknowledgments Marine research activities and development of the latitudinal gradient project along Victoria Land, Antarctica, have been jointly supported by Antarctica New Zealand, New Zealand Ministry of Fisheries (MFish), National Institute of Water and Atmospheric research (NIWA), and the Italian Programma Nazionale di Ricerche in Antartide (PNRA). We are extremely grateful to Anders Warén (Swedish Museum of Natural History) for the great help in the classiWcation of B. tumidula and the exchange of ideas about Antarctic eulimids. We wish to thank Bruce Marshall (Te Papa Museum, Wellington, New Zealand) for information about NZ Eulimidae, Kate Neill (NIWA, Wellington) for information about NZ echinoderms and Huw GriYths (BAS, Cambridge) for his invaluable help with SOMBASE and for sharing information about B. tumidula known distribution. This paper is a contribution to the multi-national Latitudinal Gradient Project and contribution #7 to the Census of Antarctic Marine Life (CAML).
References AAVV (1977) The structure and function of marine benthic ecosystems. Discussion of Part II: Adaptations within the Antarctic Marine Benthic Ecosystem. In: Llano GA (ed.) Adaptations within Antarctic ecosystems. Proceedings of the third SCAR symposium on Antarctic Biology. Smithsonian Institution, Washington Améziane N, Roux M (1997) Biodiversity and historical biogeography of stalked crinoids (Echinodermata) in the deep sea. Biodivers Conserv 6:1557–1570 Arntz WE, Gutt J, Klages M (1997) Antarctic marine biodiversity: an overview. In: Battaglia B, Valencia J, Walton DWH (eds) Antarctic communities, species, structure and survival. Cambridge University Press, Cambridge, pp 3–14 Arntz WE, Gutt J (1999) The expedition ANTARKTIS XV/3 (EASIZ II) of RV “Polarstern” in 1998. Ber Polarforsch 301:1–229 de Bary AH (1878) Vortrag: Über Symbiose. Tagblatt der 51. Versammlung Deutscher Naturforscher und Aerzte in Cassel. Baier & Lewalter, Kassel, pp 121–126 Bouchet P, Warén A (1986) Revision of the northeast Atlantic bathyal and abyssal Aclididae, Eulimidae, Epitoniidae (Mollusca, Gastropoda). Boll. Malacol Suppl. 2:297–576 Bouchet P, Lozouet P, Maestrati P, Heros V (2002) Assessing the magnitude of species richness in tropical marine environments: exceptionally high numbers of molluscs at a New Caledonia site. Biol J Linn Soc 75:421–436 Carpenter PH (1884) Crinoidea. 1. The stalked crinoids. Rep Sci Res Challenger Zool. 11:1–442 Clark AH (1915) A monograph of the existing crinoids, vol 1. The comatulids. Part 1. Bull US Natl Mus 82:1–406 Clark AH (1921) A monograph of the existing crinoids, vol 1. The comatulids. Part 2 Bull US Natl Mus 82(i-xxv):1–795 Clark AM (1970) Echinodermata Crinoidea. Marine invertebrates of Scandinavia, 3. Universitets Forlaget, Oslo, pp 1–55 Clark AM (1977) Notes on deep-water Atlantic Crinoidea. Bull Brit Mus (Nat Hist) Zool 31:159–186 Clark AH, Clark AM (1967) A monograph of the existing crinoids. Volume 1. The Comatulids. Part 5 - Suborders Oligophreata (concluded) and Macrophreata Bull US Natl Mus 82(i-xiv):1–860
123
1554 Clarke A, Aronson RB, Crame JA, Gili JM, Blake DB (2004) Evolution and diversity of the benthic fauna of the Southern Ocean continental shelf. Antarct Sci 16:559–568 Clarke A, Crame JA (1989) The origin of the Southern Ocean marine fauna. In: Carme JA (ed) Origins and evolution of the Antarctic biota. Geol Soc Special Publ 47:253–268 Clarke A, Johnston NM (2003) Antarctic marine benthic diversity. Oceanogr Mar Biol Ann Rev 41:47–114 Clarke A, Crame JA, Stromberg J-O, Barker PF (1992) The Southern Ocean benthic fauna and climate change: a historical perspective [and discussion]. In: Drewry DJ, Laws RM, Pyle JA (eds) Antarctica and environmental change. Phil Trans R Soc B 338(1285): 299–309 CLEMAM (2006) Check list of European marine Mollusca. Available at http://www.somali.asso.fr/clemam/ (accessed September 2006) Cohen BL, Améziane N, Eleaume M, Richer de Forges B (2004) Crinoid phylogeny: a preliminary analysis (Echinodermata: Crinoidea). Mar Biol 144:605–617 Colloca F, Carpentieri P, Balestri E, Ardizzone GD (2004) A critical habitat for Mediterranean Wsh resources: shelf-break areas with Leptometra phalangium (Echinodermata: Crinoidea). Mar Biol 145:1129–1142 Crame JA (1994) Evolutionary history of Antarctica. In: Hempel G (ed.) Antarctic science: global concerns. Springer, Heidelberg, pp 188–214 Dell RK (1990) Antarctic mollusca: with special reference to the fauna of the Ross Sea. Bull Roy Soc NZ 27:1–311 Döderlein L (1912) Die gestielten Crinoiden der deutschen TiefseeExpediton. Wiss Ergeb Dtsch Tiefsee-Exped 17:1–34 Emu database (2006) USNM Invertebrate collection database. Available at http://goode.si.edu/webnew/pages/nmnh/iz/DtlQuery.php (accessed Mar. 2006) Engl W (2004) Antarctic mollusks: Part 5: Revision of the Antarctic Eulimidae with the description of three new species. La Conchiglia 36(310):11–18 Fishelson L (1973) Ecology of the crinoids of the northern Red Sea, with emphasis on epi- and endozoic fauna associated with them. J Mar Biol Assoc India 15:461–473 Gutt J, Sirenko BI, Arntz WE, Smirnov IS, De Broyer C (2000) Biodiversity of the Weddell Sea: macrozoobenthic species (demersal Wsh included) sampled during the expedition ANT XIII/3 (Easiz I) with RV Polarstern. Ber Polarforsch 372:1–103 Gili JA, López-González PJ, Bouillon J (2006) A new Antarctic association: the case of the hydroid Sarsia medelae (new sp.) associated with gorgonians. Pol Biol 29:624–631 Hain S (1990) The benthic seashells (Gastropoda and Bivalvia) of the Weddell Sea, Antarctica. Ber Polarforsch 70:1–181 Huang HD, Rittschof D, MingShiou J (2005) Multispecies associations of macrosymbionts on the comatulid crinoid Comanthina schlegeli (Carpenter) in southern Taiwan. Symbiosis 39:47–51 Imbrie J, Berger A, Boyle EA, Clemens SC, DuVy A, Howard WR, Kukla G, Kutzbach J, Martinson DG, McIntyre A, Mix AC, MolWno B, Morley JJ, Peterson LC, Pisias NG, Prell WL, Raymo ME, Shackleton NJ, Toggweiler JR (1993) On the structure and origin of major glaciation cycles. 2. The 100,000 year cycle. Paleoceanography 8:699–735 Jangoux M (1987) Diseases of Echinodermata. III. Agents metazoans (Annelida to Pisces) Dis Aquat Organ 3:59–83 John DD (1938) Crinoidea. Discovery Rep 18:121–222 John DD (1939) Crinoidea. Rep BANZ Antarct Res Exped 1929– 1931, Ser B (Zool Bot) 4:191–212 Knox GA, Lowry JK (1977) A comparison between the benthos of the Southern Ocean and the North Polar Ocean with special reference to the Amphipoda and the Polychaeta. In: Dunbar MJ (ed) Polar oceans. Arctic Institute of North America, Calgary, pp 423–462
123
Polar Biol (2007) 30:1545–1555 Kutschera U, Niklas KJ (2005) Endosymbiosis, cell evolution, and speciation. Theor Biosc 124:1–24 La Mesa M, Vacchi M, Castelli A, Diviacco G (1997) Feeding ecology of two nototheniid Wshes, Trematomus hansoni and Trematomus loennbergii, from Terra Nova Bay, Ross Sea. Polar Biol. doi:10.1007/s003000050105 Lehmann T, Gailer JP, Melzer RR, Schwabe E (2006) A scanningelectron microscopic study of Dickdellia labioXecta (Dell, 1990) (Gastropoda, Littorinoidea) on Colossendeis megalonyx megalonyx Fry and Hedgpeth, 1969 (Pycnogonida, Colossendeidae): a test for ectoparasitism. Polar Biol. doi:10.1007/s00300-0060178-6 Linse K (2006) New records of shelled marine molluscs at Bouvet Island and preliminary assessment of their biogeographic aYnities. Polar Biol 29:120–127 López-González PJ, Gili JM (2001) Rosgorgia inexspectata, new genus and species of Subergorgiidae (Cnidaria, Octocorallia) from oV the Antarctic Peninsula. Polar Biol. doi:10.1007/ s003000000176 Marr JWS (1963) Unstalked crinoids of the Antarctic shelf. Notes on their natural history and distribution. Phil Trans R Soc B 246:327–379 McClintock JB (1989) Toxicity of shallow-water Antarctic echinoderms. Polar Biol 9:461–465 Messing CG (1997) Living comatulids. In: Waters JA, Maples CG (eds) Geobiology of Echinoderms. Paleontol Soc Pap 3:3–30 Meyer DL, Macurda DB Jr (1977) Adaptive radiation of comatulid crinoids. Paleobiology 3:74–82 Meyer DL, Oji T (1993) Eocene crinoids from Seymour Island, Antarctic Peninsula: paleobiogeographic and paleoecological implications. J Paleontol 67:250–257 Mitchell J, Clark M (2004) Voyage Report Tan04–02. Western Ross Sea Voyage 2004. Hydrographic and biodiversity survey of the RV Tangaroa, 27 Jan–13 March 2004. Cape Adare, Cape Hallet, Possession Island and Balleny Islands, Antarctica. National Institute of Water and Atmospheric Research (NIWA) Publication, Wellington, pp 1–102 Mortensen T (1917) Notocrinus virilis n.g., n.sp., a new viviparous crinoid from the Antarctic Sea. Vidensk Medd fra Dansk naturh Foren 68:205–208 Mortensen T (1920) Studies in the development of crinoids. Pap Dep Mar Biol Carnegie Inst Wash 16:94 Numanami H (1996) Taxonomic study on Antarctic Gastropods collected by Japanese Antarctic research expeditions. Mem Natl Inst Polar Res Ser E 39:1–245 OBIS Indo-PaciWc Molluscan Database (2006) Available at http:// data.acnatsci.org/obis/ (accessed September 2006) Peñas A, Giribet G (2003) Additions to the malacological fauna of El Garraf (NE of the Iberian Peninsula). Iberus 21:177–189 Potts FA (1915) The fauna associated with the crinoids of a tropical coral reef: with especial reference to its color variations. Pap Dep Mar Biol Carnegie Inst Wash 8:71–96 Ramoino MC (2004) Rapporto sulla Campagna Antartica Estate Australe 2003–2004. Diciannovesima spedizione. P.N.R.A. Programma Nazionale di Ricerche in Antartide, Progetto Antartide, Final Report, Roma Rinaldi AC (1994) Frequency and distribution of Vitreolina philippi (De Rayneval and Ponzi, 1854) (Prosobranchia, Eulimidae) on two regular echinoid species found along the southern coast of Sardinia. Boll Malacol 30:29–32 Rosenberg G (2005) Malacolog 4.0.1: A Database of Western Atlantic Marine Mollusca. Availabele at http://www.malacolog.org/ Roux M (1982) De la biogéogaphie historique des oceans aux reconstitutions paléobiogéographiques: tendances et problèmes illustrés par des exemples pris chez les Echinodermes bathyaux et abyssaux. Bull Soc Geol Fr Sér 7 24:907–916
Polar Biol (2007) 30:1545–1555 Roux M (1987) Evolutionary ecology and biogeography of recent stalked crinoids as a model for the fossil record. In: Jangoux M, Lawrence JM (eds) Echinoderm studies, vol 2. A.A. Balkema, Rotterdam, pp 1–53 Schiaparelli S, Cattaneo-Vietti R, Chiantore M (2000) Adaptive morphology of Capulus subcompressus Pelseneer, 1903 (Gastropoda: Capulidae) from Terra Nova Bay, Ross Sea (Antarctica). Pol Biol 23:11–16 Schiaparelli S, Albertelli G, Cattaneo-Vietti R (2003) The epibiotic assembly on the sponge Haliclona dancoi (Topsent, 1901) at Terra Nova Bay (Antarctica, Ross Sea). Pol Biol 26:342–347 Schiaparelli S, Canapa A, Barucca M, Boyer M (2005) Phylogenetic relationships within the Ovulidae (Gastropoda: Cypraeoidea) based on 16S rRNA gene. Mar Biol 147:411–420 Sirenko BI (2000) Symbiosis of an Antarctic gastropod and pantopod. Ruthenica 10:159–162 Speel JA, Dearborn JH (1983) Comatulid crinoids from R/V Eltanin cruises in the Southern Ocean. In: Kornicker LS (ed) Biology of the Antarctic Seas XIII. Antarct Res Ser 38:1–60 Thatje S, Hillenbrand CD, Carter R (2005) On the origin of Antarctic marine benthic community structure. Trends Ecol Evol 20:534–540 Thiele J (1912) Die antarktischen Schnecken und Muscheln. In: Drygalski E von (ed) Deutsche Südpolar-Expedition 1901–1903. Band XIII, Zoologie V. Georg Reimer, Berlin, pp 183–286, pls 11–19
1555 Tortonese E (1965) Echinodermata. Fauna d’Italia, vol 6. Edizioni Calderini, Bologna Warén A (1980) Revision of the genera Thyca, Stilifer, Scalenostoma, Mucronalia and Echineulima (Mollusca, Prosobranchia, Eulimidae). Zool Scr 9:187–210 Warén A (1981a) Eulimid gastropods parasitic on echinoderms in the New Zealand region. NZ J Zool 8:313–324 Warén A (1981b) Revision of the Genera Apicalia A. Adams and Stilapex Iredale and description of two new genera (Mollusca, Prosobranchia, Eulimidae). Zool Scr 10:133–154 Warén A (1984) A generic revision of the family Eulimidae. J Moll Stud Suppl 13:1–96 Warén A, Crossland MR (1991) Revision of Hypermastus Pilsbry, 1899 and Turveria Berry, 1956 (Gastropoda: Prosobranchia: Eulimidae), two genera parasitic on sand dollars. Rec Aust Mus 43:85–112 Warén A, Lewis LM (1994) Two new species of eulimid gastropods endoparasitic in asteroids. Veliger 37:325–335 Warén A, Norris DR, Templado JT (1994) Description of four new eulimid gastropods parasitic on irregular sea urchins. Veliger 37:141–154 Zinsmeister WJ, Feldmann M (1984) Cenozoic high latitude heterochroneity of Southern Hemisphere marine faunas. Science 224:281–283
123
