/. Moll. Stud. (1991), 57, 289-300. © The Malacological Society of London 1991

RESEARCH NOTES

Cave-dwelling genezarethensis (, ) from Israel J. Heller, R. Pimstein and E. Vaginsky

Department of Zoology, The Hebrew University, Jerusalem, Israel Downloaded from https://academic.oup.com/mollus/article/57/2/289/1026179 by guest on 30 September 2021

The Ferussaciidae is a small family of land snails In 1989 a karstic cave was accidentally revealed near consisting of twelve genera, some of which are blind Ma'ale Efraim, during extensive road works. The cave and subterranean.u The description and definition of is about 40 m long with its roof about 3-10 m beneath these genera is based mainly upon characteristics of ground level. There is no evidence to suggest that it the shell, except for Cecilioides and Ferussada for was ever previously exposed to the exterior world. A which there is detailed knowledge of the anatomy.3-4 narrow, soil-filled fissure opens through the overlying Data concerning the biology of Cecilioides have been rock into the ceiling of the cave and apparently enables summarised by Frommingp mainly in reference to the minute soil-dwelling to drop onto the floor of earlier work of Wachtler. the cave, some 4 m below. Three species of Cecilioides have been reported A survey of the cave (two days after it was exposed) from Israel.6 The type species, C. acicula (Miller, revealed a small population of C. genezarethensis. 1774); C. judaica (Mousson, 1861), which differs from This is the first live record of this species. C. acicula in its greater height and larger diameter; Several specimens were brought to our laboratory and C. genezarethensis Forcart, 1981, which differs where they were put into petri dishes with damp soil, from C. judaica in its aperture that reaches more than and fed upon aquarium-fish food-flakes ('Tetramin'). half the height of the shell.7 Live specimens of C. Some of them died after about two months, due to a judaica and of C. genezarethensis have not yet been heavy infestation of nematodes. As the three remain- found. ing individuals were also infested, we decided to sac-

Fignre 1. Caecilioides genezarethensis from Maale Efraim: live . Scale bar, 1 mm. 290 RESEARCH NOTES Downloaded from https://academic.oup.com/mollus/article/57/2/289/1026179 by guest on 30 September 2021

8 mm

3 4 mm MH Figure 3. Shell height (SH) as against mouth height (MH) in C. genezarethensis from Maale Efraim, Israel (open circles), as compared to C. genezarethensis from other sites (open circles with horizontal lines) and to C. judaica (full circles); material from the Mollusc Collection of the Hebrew University. Along the diag- onal line, mouth height equals half shell height.

Figure 2. Cecilioides genezarethensis from Ma'ale It is however clear from Fig. 3 that several C. judaica Efraim: shell. also have an aperture that is over half the shell height. Further, one snail of the Ma'ale Efraim population which grew in our laboratory to a shell height of 8 mm, rifice them: one was dissected to examine the had an aperture slightly smaller than the height of the morphology of the radula and reproductive system shell. C. genezarethensis is thus on this character not while the other two served for histological sections. easily distinguishable from C. judaica. A more precise The shell (Figs 1,2) of the live animal is transparent definition of these two species may be achieved when (not translucent, as frequently seen in empty speci- additional material becomes available. mens), thin and fragile. The parietal lamella is present The skin is transparent. Eyes are absent, with no in juveniles, but in adults (shell height of more than pigment epithelium, lens or cornea. The tentacles are 5.5 mm) it is absent or, if present, very weak. Ten long and slender. When both tentacles and foot are empty shells, all undoubtedly adults as they are larger fully extended, the ratio tentacle-length/shell-length than 6.0 mm, were collected within the cave. Their is 0.30; and the ratio tentacle-length/foot-length is dimensions are: 0.29. For comparison, in the chondrinind Rupeslrella rhodia (a snail incidently present in our laboratory during this period; shell height 4.5 mm) the ratio ten- tacle-length/shell-length is 0.32, and the ratio ten- range mean ± SD tacle-length/foot-length is 0.19. In the helicid Monacha crispulata (with a diameter of 7.7 mm), both shell height (mm) 6.0-7.0 6.56 ± 0.307 ratios are 0.44. These very preliminary comparative shell diameter (mm) 1.8-2.4 2.06 ±0.192 observations suggest that tentacles in cavernicolous mouth height (mm) 3.4-4.2 3.69 ± 0.36.1 land snails are not considerably longer than in surface- whorls 5-6 5.7 ± 0.48 dwelling ones, as a compensation for loss of vision.8 shell diameter/shell 0.28-0.36 0.321 ± 0.029 The general layout of the digestive system resembles height that of C. acicula.9 The posterior extremity of the aperture height/shell 0.51-0.64 0.569 ± 0.046 radula sac (Fig. 4) projects beyond the buccal mass height and curves upwards. The narrow salivary glands are joined together towards their hind ends. The minute radula (Fig. 5) has a formula of 10 + 9 + 1 + 9 + 10. The aperture height,.as in C. genezarethensis from The central tooth is small and narrow, with a short some other sites in Israel, exceeds half the shell height. mesocone flanked by a minute ectocone on either side. RESEARCH NOTES 291

Salivary glands Downloaded from https://academic.oup.com/mollus/article/57/2/289/1026179 by guest on 30 September 2021

Figure 4. Digestive system of C. genezarethensis.

The lateral teeth are tricuspid, with endocones and In the reproductive system (Fig. 6) the ovotestis ectocones that are much shorter than the large meso- (lost in the dissection, but very noticeable in the cones. In the four lateral teeth close to the central histological sections) occupies the uppermost whorls tooth, the mesocone is shorter than in the five more of the visceral mass. It consists of one single large distant ones, which are more hook-like. The marginal lobule containing numerous male gametes in various teeth are short, broad, and their extremely short cusps stages of spermatogenesis and also twenty oocytes, are broken up into serrations. none of which was mature. The upper part of the In our laboratory the snails swallowed soil, and we hermaphrodite gland is slim; its lower convolutions assume that they feed upon soil fungi. Preliminary are swollen, contain sperm and presumably serve as a examinations of the soil of the cave revealed that it vesicula seminalis. The spermoviduct is normal for contains a very low organic content (1.8%); a low that of pulmonates. The free oviduct, between the bacterial concentration (104 bacteria/gram of soil); no spermoviduct and the opening of the receptacle, is algae; and very few fungi. Whatever the precise food short and narrow. The receptacle consists of a small of this cavernicolous population, it is definitely not oval bursa lying against the spermoviduct and borne plentiful. by a broad pedicle, which is positioned as a con- tinuation of the short vagina. In the male system the vas deferens passes forward along the oviduct and vagina, and then bends round and passes backward and upwards beside the penis. It enters the penis at its posterior extremity, near where the penial muscle is also inserted. The penis is broad and muscular at the posterior and slender and thin-walled at the anterior. In the hinder end of the muscular part a series of folds is found, and in the anterior part there are two longitudinal thickenings. Upon these thickenings or near them are two additional thickened structures, which were accidently destroyed in the dissection to such an extent that they cannot, here, be described. The snail is oviparous. Eggs inside the body could be observed through the transparent shell, and seven eggs were laid in the petri dishes. Egg diameter was 0.4-0.58 mm (mean 0.403 ± 0.9 SD). This is less than the smallest pulmonate egg recorded so far (0.6 mm, for Vallonia'"). The eggs were layed singly, into the damp soil or upon it. Four of the eggs hatched. One fifth egg, found with a hole in it but no juvenile, Figure 5. Radula of C. genezarethensis. Scale bar, 10 may indicate that the juveniles could, occasionally, be microns. cannibalistic. 292 RESEARCH NOTES Downloaded from https://academic.oup.com/mollus/article/57/2/289/1026179 by guest on 30 September 2021

Figure 6. Reproductive system of C. genezarethensis.

Table 1 compares C. genezarethensis to C. acicula recorded from Israel is Calaxis (Bourguignat, and to oranensis, both as given in the 1864), described1 as possessing a strongly developed literature.3 In every one of nine features, C. gene- parietal lamella. While most Calaxis in Israel's zarethensis is similar to C. acicula, not to F. oranensis.National Mollusc Collection do have such a parietal Only in one character, the number of laterals in each lamella, in some it is very reduced. This leaves the row of the radula, does C. genezarethensis differ from conchological distinction between Calaxis and Cec- C. acicula. These results lend support for the placing ilioides somewhat vague and emphasizes the need of genezarethensis within the genus Cecilioides, as for live material, to further investigate the precise originally described by Forcart. Another ferussaciid relationship between these two genera.

Table 1. Cecilioides genezarethensis as compared with two other ferussacuds, Ferussacia oranensis3 and Cecilioides acicula3. Feature F. oranensis C. genezarethensis C. acicula

Shell light brown transparent transparent Body colour yellow unpigmented unpigmented Eyes present absent absent Radula marginalia cusps tricuspid serrated serrated marginalia shape elongate broad broad marginalia number 19-22 10 10 laterals number 12 9 5 Ovotestis lobules several one one Penis complex simple simple Receptacle base thick, muscular not muscular not muscular Reproduction ovoviviparous oviparous oviparous RESEARCH NOTES 293 REFERENCES opaischen landgastropoden. Dunker & Humbolt, Berlin. 1. ZILCH, A. 1959 (1959-1960). , Euthy- 6. MffiNis, H. 1982. Lcvantina, 39: 457-565. neura. Handb. Palaozool. 6. Gebruder Borntra- 7. FORCART, L. 1981. Basteria, 45: 97-108. ger, Berlin. 8. VANDEL, A. 1965. Biospeleology, Pergamon, Lon- 2. KERNEY, M.P. & CAMERON, R.A.D. 1979. Afield , don. guide to the land snails of Britain and north-west 9. TUXIER, S. 1989. Malacologia, 30: 1-303. Europe. Collins, London. 10. TOMPA, A. 1984. Land snails (Styloramatophora). 3. WATSON, H. 1928. /. Conch., 18: 305-306. In: The (A.N. Tompa, H. Verdonk & 4. WATSON, H. 1929. /. Conch., 18: 305-306. J.A.M. van den Biggelaar, eds.) 7: 48-141. Aca-

5. FROMMING, E. 1954. Biologic der mittelew- demic Press, NY. Downloaded from https://academic.oup.com/mollus/article/57/2/289/1026179 by guest on 30 September 2021

Faeces collecting and sitting in heiicid snails: a previously undescribed behaviour M.M. Bleakney Department of Agricultural Zoology, Faculty of Agriculture and Food Science, The Queen's University of Belfast, Belfast BT9 5PX, U.K.

Pulmonates display a limited range of stereotyped conveyor-belt (Fig. la). Sometimes the anterior pel- behaviour. Courtship and mating behaviour has been matic margins enfold the faecal string, almost forming described for a number of species and other forms of a tube down which it passes. Adhesion is maintained purposeful behaviour include: nest-digging, homing, by the viscosity of the foot mucus and the mucoid huddling, foraging, trail following and possibly shell- faecal wrapping. The posterior half'of the pelma cleaning. The small movements observed by Bailey1 experiences no muscular waves and remains stationary and construed as shell-cleaning activity, may in fact throughout. When the faecal string reaches the have been a mixture of shell-cleaning and the behav- stationary region of the foot in contact with the sub- iour described in these notes. Both involve recurving stratum it begins to pile up and form loops. Phase four of the anterior headfoot to the mantle region and are begins when defaecation is complete; the pedal sole difficult to distinguish on a video image. returns to the substratum, trapping the contorted fae- During casual observations of a variety of heiicid snails, kept in transparent plastic lunch boxes (270 x 150 x 100 mm) and fed mainly on an artificial diet (lab-chow, similar to that used by Cowie and Cain2), it was noticed that snails habitually spent the day resting, upside-down on the lid, with their foot on a contorted pile of faeces. The sequence of behaviour, shared by several helicids, whereby a resting snail M deposits a faecal string up to 80 mm in length under its foot and then rests or 'sits' on it for several hours is described below. Although the following description refers to Helix aspersa Muller, similar behaviour has been observed in H. pomatia, H. texta, Hemicycla bidentalis, Theba pisana, Eobania vermiculata, Otala lactea and Cepaea nemoralis. The behaviour may be divided into four separate phases, beginning and ending with a resting phase. During phase one the snail is either at, or comes to rest, and gradually contracts its body until the 'head' and 'tail' portions of the headfoot are close to the shell. In phase two the faeces collecting behaviour is initiated; the snail raises and recurves the front part of the headfoot so that the pedal sole is uppermost F8 and in contact with the anal pore in the mantle. To accomplish this the head is drawn under the mantle B with only the tentacles protruding from behind the lip of the shell. Defaecation then commences (phase three); a faecal string is gradually expelled and fed onto the upturned anterior pelma. Immediately retro- Figure 1. Faeces collecting (A) and sitting (B), see grade waves appear on the uplifted pelma and the text for explanation. Abbreviations: A, anus; Fs, faecal string is drawn along, the sole acting like a faeces; Ft, foot; M, mantle; S, shell.