Polar Biol (2000) 23: 11±16
Ó Springer-Verlag 2000
ORIGINAL PAPER
S. Schiaparelli á R. Cattaneo-Vietti á M. Chiantore
Adaptive morphology of Capulus subcompressus Pelseneer, 1903 (Gastropoda: Capulidae) from Terra Nova Bay, Ross Sea (Antarctica)
Accepted: 17 July 1999
Abstract Capulus subcompressus Pelseneer, 1903 (Gastropoda: Capulidae) is a small epibiont gastropod living at Terra Nova Bay (Ross Sea) down to 540 m on the calcareous tubes of its unique host, the serpulid Serpula narconensis Baird, 1865. This polychaete forms bush-like aggregates which host a rich microfauna of crustaceans, hydroids and molluscs. In contrast to all other capulids, C. subcompressus shows an evident oval shell aperture, which is due to an allometric growth that can be imputed to the Serpula tube morphology. Since the allometric growth is detectable in all size classes, it could be deduced that the compressed shape of the C. subcompressus shell is the stable result of a signi®cant evolutionary history which binds tightly these two species in Antarctic waters.
Introduction In Antarctica, only a few data regarding the speci®c interactions occurring among benthic organisms living on hard bottoms are available, and most of these relationships are unknown. In some cases these living assemblages may produce structured communities with a high degree of biodiversity. Among these, the bush-like aggregations of the calcareous tubes of the polychaete Serpula narconensis Baird, 1865 are frequent at Terra Nova Bay (Ross Sea) on rock outcrops and gorgonaceans between 200 and 500 m depth (Di Geronimo et al. 1990; Cantone and San®lippo 1992; CattaneoVietti et al., in press). This microcosm shelters a varied fauna of small crustaceans (scalpellids, ostracods, S. Schiaparelli (&) á R. Cattaneo-Vietti á M. Chiantore Dipartimento per lo Studio del Territorio e delle sue Risorse ± DIP.TE.RIS, Viale Benedetto XV, 5, I-16123 Genoa, Italy e-mail:
[email protected], Fax: +39-10-3538102
amphipods and isopods), hydroids, sponges and molluscs. During the last PNRA expeditions, a study on the structure of these micro-reefs was carried out, with special emphasis on the morphological adaptation of the sessile epibiont gastropod Capulus subcompressus Pelseneer, 1903 (Caenogastropoda), the unique capulid known from all the Antarctic continental margins, except the Antarctic Peninsula where it is absent (Dell 1990; Numanami 1996). The genus has a widespread distribution, with about 25 species living in all oceans, mainly on bivalves. They exploit the strong feeding currents of the host bivalve (Yonge 1938), or steal their accumulated food and/or pseudofaeces (Graham 1988) using a pseudoproboscis. Their shell morphology is quite similar, being the result of an adaptation to grow on ¯at surfaces, and follows a morphological empirical rule, which states that their aperture is generally circular in outline (Morita 1991) and without distinct overlap whorls (Linsey 1977; McNair et al. 1981). Capulus subcompressus showing an evident oval aperture, as its name suggests, represents a singular exception. Several authors (Pelseneer 1903; Powell 1958; Arnaud 1972) have suggested that this form could be due to cidarid spines or an anterior siphonal gastropod canal to which C. subcompressus adheres with its foot, and Numanami (1996) reported a high occurrence of cidarid echinoids at the same stations in which C. subcompressus was collected. However, Hove (1994) reported a personal communication (from H. Zibrowius and P.M. Arnaud) in which C. subcompressus was recorded on tubes, near the mouth, of Serpula narconensis in the Weddell Sea. Within the framework of the ecological studies carried out in Terra Nova Bay (Ross Sea), a signi®cant number of specimens of this quite rare species was collected, allowing the description of its gross anatomy and a partial reconstruction of larval ontogeny. A biometric evaluation of the numerous specimens permitted the identi®cation of substrate constraints (S. narconensis) as the driving force in shell compression.
12 Table 1 Station
Latitude S
Longitude E
Specimen
Depth Device
505 Eolo 506 426
74°51.15¢ 74°40.40¢ 74°52.79¢ 74°54.65¢
164°26.64¢ 164°04.90¢ 164°29.89¢ 163°58.48¢
25 7 20 1
544 177 544 233
Grab Grab Grab Grab
to width and height values of the mollusc shell apertures. The voucher material is deposited at the Museo Nazionale dell'Antartide, Genoa (Italy) (catalogue numbers: MG017/95±96/505; MG017/95±96/Eolo; MG017/95±96/506; MG017/95±96/426).
Results Description of the species and growth patterns
Materials and methods All the specimens of C. subcompressus examined were collected during the 1995/1996 PNRA Italian Antarctic Expedition at Terra Nova Bay, Ross Sea (Table 1). Drawings and sketches were made at a stereo-microscope using a camera lucida apparatus. Protoconchs and radulae were polished with oxygen peroxide, dehydrated in alcohol and then covered with gold for Philips E 515 SEM observations. Morphometrical characters were studied on 40 specimens of C. subcompressus, 9 of which were still adhering to Serpula tubes. A Spearman rank correlation analysis was applied
Capulus subcompressus Pelseneer, 1903 Capulus subcompressus has the Phrygian cap morphology typical of capulids only in the protoconch (Fig. 1a±c), while in the adult, due to the compression of the aperture, the shell tends to be laterally ``squashed'' and loses the typical gastropod coiling (Figs. 1f, 2, 3a, b). The shell surface, except for occasional more marked growth stage lines, is smooth and its colour is dirty-white. The adult
13 Fig. 2a±d Gross anatomy of the soft parts in Capulus subcompressus Peelseneer, 1903. a Whole body removed from the shell, right side. b Left side. c Top view. d Bottom view of the mollusc inside the shell. mg mantle edge; ps pseudoproboscis; ft foot; cm columellar muscle; vs visceral sac; g gills; rct right cephalic tentacle; lct left cephalic tentacle; cs calci®ed shell; ncs not calci®ed shell margin
shell aperture is regularly oval and the peristome is smooth (Fig. 2d). In adult specimens (Fig. 1f) the protoconch is about 1.2 mm in length and is sculptured with spiral cords (Fig. 1g). In some cases a thin but persistent organic ®lm covers the larval shell. In very early juveniles the protoconch is less calci®ed and slightly bigger (up to 1.8 mm in length), being wrapped by a thick organic layer. This covering is yellow-cream in colour and has a sculpture (Fig. 1d) dierent from the ``adult protoconch''. This morphology testi®es that during larval ontogeny two events should occur: (1) a resorption (or b Fig. 1a±h Morphological features in Capulus subcompressus Peelseneer, 1903. a Left side of an early juvenile, with a fractured scaphoconch. b Another specimen, right side. c Same specimen, top view. d Detail of the ornamentation in the organic scaphoconch. e Detail of the fractured scaphoconch (the same as in Fig. 1a); note the porous, unsculptured inner calcareous surface. f An adult specimen. g Same specimen, showing details of the protoconch sculpture. h Middle radular rows of an adult specimen. Scale bars: a±c 1 mm; d, e 0.1 mm; f 1 mm; g, h 0.1 mm
loss?) of the outer organic layer, and (2) a progressive calci®cation of the inner calcareous layer. Both processes are evident in Fig. 1a, e, where a fractured organic conch allows the detection of an unsculptured, porous, calcareous inner layer. In larger adult specimens (maximum recorded shell height: 15 mm), it is possible to detect a progressive clockwise torsion of the shell around the growth direction axis, up to about 30°, indicating slight dextral coiling. The pseudoproboscis, formed from the propodium, seems not to be as long and/or mobile as the C. ungaricus one (Graham 1988) being, in our preserved specimens, shorter than the foot (Fig. 2a±d). The foot is circular in outline in juveniles, while in adults it is markedly oval (Fig. 2a, b, d), being laterally compressed. The muscle is horseshoe-shaped and extends for half of the lateral portion of the body (Fig. 2a, b). In some specimens the ctenidial lamellae protrude the mantle margin (Fig. 2b). No egg masses were recorded from ®xed adults. The radula is taenioglossate (2:1:1:1:2), weak and transparent (Fig. 1h). The shape of the central and
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lateral teeth resemble C. ungaricus (Bandel 1984), except perhaps for a less marked denticulation of the cusps. The marginal teeth are not denticulate, as in other capulids (Thiele 1929). Ecological remarks C. subcompressus is a member of a complex microcosm (reconstructed in Fig. 3d±e), constituted by the calcareous tubes of S. narconensis, which has an average external diameter of 3.07 0.4 mm (n 20). These bush-like aggregations shelter a varied fauna of small crustaceans (ostracods, amphipods and isopods) and hydroids (Fig. 3h). Often the tubes are bound by an encrusting unidenti®ed sponge which includes long spicules belonging to other sponge species (Fig. 3f ) and hosts numerous specimens of the cirriped Litoscalpellum
Fig. 3 Reconstruction of a portion of the microcosm living on the Serpula narconensis tubes. a Specimen of Capulus subcompressus, partially covered by a sponge, adheres to the serpulid tube near its aperture. b Specimen of C. subcompressus with a living young S. narconensis settled on its shell. c A young capulid lodged far from serpulid aperture is completely covered by sponge tissues. d A S. narconensis specimen with protruded tentacle crown during feeding activity. e A S. narconensis retracted in the tube. f The unidenti®ed sponge which binds Serpula tubes (the spicules protruding from its body are extraneous to the skeleton of this species). g Two specimens of Litoscalpellum sp. h Hydroid colonies
sp. (Fig. 3g). Among the vagile mollusc fauna, the small limpet Iothia coppingeri (Smith 1881) occurs frequently at the base of the microcosms. C. subcompressus is found close to the Serpula tube aperture (Fig. 3a, b), in accordance with Hove's (1994) report. This underlines the cleptocommensalistic behaviour (Bavestrello et al. 1996) of this species, which, as other capulids, uses its pseudoproboscis to steal mucous particles collected by the serpulid. A young specimen was found at the crossing of two Serpula tubes (about 2 cm away from the tube aperture), partially embedded by sponge tissues (Fig. 3c); it was probably collecting water-carried particles in the space delimited by two thin sponge-tissue layers. Sometimes the larger specimens are embedded by the tubes of newly settled serpulids (Fig. 3b) and/or covered by the encrusting sponge (Fig. 3a). This suggests a sedentary life-style and a slow growth. The Spearman rank correlation analysis applied to height and width shell aperture data evidences a clear allometry, more evident when the mollusc size approaches that of the serpulid host (Fig. 4), although the correlation for these larger records is not statistically signi®cant due to the paucity of larger specimens examined (with shell aperture height over 5 mm, corresponding to shell height larger than 1 cm) as these are very rare. No ``home scars'' (Vermeij 1987) were observed on Serpula tubes, as sometimes occurs on the shell that the boreal C. ungaricus inhabits (Sharman 1956); this could be due to the miniaturisation of the Antarctic species
Fig. 4 Spearman rank correlation applied to height and width measurements of 40 Capulus subcompressus shell apertures. It is clear that the asymptotic abrupt change around the 3-mm value corresponds to the maximum external diameter of the Serpula narconensis tube
15
and to the environmental paucity of CaCO3, which makes both shells weak.
Discussion and conclusions C. subcompressus shows many features that may also be found in other capulid species: (1) the radula is in fact reduced to a sort of conveyor-belt, used to pull and guide the mucous collected by the pseudoproboscis, as occurs in most of the Crepiduloidea, due to epibiotic and ®lter-feeding habits (Bandel 1984); (2) its protoconch seems to possess an ``organic conch'', probably related to a late scaphoconch of the echinospira larva (Graham 1988; Bandel et al. 1997), which is also known in C. ungaricus (Lebour 1937; Graham 1988). In C. subcompressus, however, a rework occurs during larval ontogeny, and the internal calcareous shell is probably moulded following the inner surface of the scaphoconch which works as a matrix. In this way it attains the shape observed in the ``adult protoconch'' (Fig. 1g). Similar processes are known only for some other gastropod taxa not related to Capulidae (Bandel et al. 1994; Bandel et al. 1997). In contrast to other capulid species, in C. subcompressus, the shell aperture does not show the typical circular outline, being laterally compressed. It is known that in gastropods with a sessile lifestyle (Savazzi 1996), physical environment conditions may in¯uence the shell shape, triggering changes in allometric growth patterns or regulating the body size (Savazzi 1990; Pansini et al., in press). In fact, as the mollusc mantle works as a ``pneu'', it can approximate to any shape of the substrate by opportunely tethering and/or strutting its membrane and thus the shell re¯ects the surrounding topography (Savazzi 1990; Morita 1991). This behaviour occurs also in Capulidae which, being epibionts and ®lter feeders, have the shape and dimension of the shell in¯uenced by the host morphology. Most species live mainly on ¯attened surfaces, such as bivalve shells or rocks (Yonge 1938; Jones 1949; Graham 1954; Sharman 1956; Dell 1964; Abbott 1974). In the Mediterranean Sea, C. ungaricus (L. 1758), the unique capulid whose feeding physiology was studied (Yonge 1938), reaches the maximum possible dimension and maintains a regular circular outline when it lives on Atrina pectinata (L., 1767) or Pinna nobilis L., 1758 (personal observations). These two large pinnids are in fact able to move a great amount of water, favouring the feeding activity of their epibionts. For C. subcompressus, cidarids were inferred to be the possible host (Pelseneer 1903; Powell 1958; Arnaud 1972; Numanami 1996), but they represent only a potential poor food source and, moreover, they are absent at Terra Nova Bay. However, the most common Antarctic pectinid, Adamussium colbecki (Smith 1902) lives, in comparison to C. subcompressus, in shallower water and probably has too high a mobility (Ansell et al. 1998) for a non-
cemented epibiont. These species have probably constrained C. subcompressus to ®nd a new but, ecologically speaking, analogous niche in S. narconensis. This serpulid represents a suitable and stable over time substratum and probably shares with C. subcompressus very slow growth rates. This kind of living substratum is not new for capulids, which are in fact sometimes found on serpulids (Sharman 1956; Graham 1988) such as Protula intestinum (Lamarck 1818) and Pomatoceros sp. in the case of C. ungaricus. This behaviour, however, should represent only a sub-optimal solution, adopted by young Capulus when no bivalves are available as de®nitive substrata. In contrast, in Antarctica, since no C. subcompressus with rounded shell apertures have ever been recorded, this choice seems to be obligatory and so all the adaptive changes occurring in this species must be related to the morphology of its unique host, the serpulid S. narconensis, whose calcareous tube has a maximum diameter of 3 mm. A similar phenomenon of ``compression'' also occurs in the archaeogastropod genus Lepetella (Mollusca: Lepetellidae) whose members, living on the outside or inside of the chitinous tubes of the polychaete Hyalinoecia in deep water, show compressed shell apertures (Dantart and Luque 1994). This is, however, to be considered only a phenomenon of evolutive convergence, because the two families are not related and present very dierent feeding habits. Clearly, adaptive allometric patterns due to selective pressure are rare in molluscs (Savazzi 1990). As the allometric growth is evident in all size classes (Fig. 4), it is possible to state that the compressed shape of the C. subcompressus shell is the stable result of a signi®cant evolutionary history which binds tightly C. subcompressus and S. narconensis in Antarctic waters. Acknowledgements This work was done at the Study Centre of the National Antarctic Museum of Genoa (Italy). The work was supported by Italian PNRA (Programma Nazionale di Ricerche in Antartide) funds.
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