Cremnoconchus, W. T. BLANFORD, 1869

Reid, David G., Aravind, Neelavara Ananthram & Madhyastha, Neelavara Ananthram, 2013, A unique radiation of marine littorinid snails in the freshwater streams of the Western Ghats of India: the genus Cremnoconchus W. T. Blanford, 1869 (Gastropoda: Littorinidae), Zoological Journal of the Linnean Society 167 (1), pp. 93-135 : 98-103

CREMNOCONCHUS W.T. BLANFORD, 1869

Cremnobates W.T. Blanford, 1863: 184 (type species by monotypy Cremnobates syhadrensis W.T. Blanford, 1863 ; not Cremnobates Swainson, 1855 ; not Cremnobates Günther, 1861 ).

Cremnoconchus W.T. Blanford, 1869: 343 (new name for Cremnobates Blanford, 1863 , not Günther, 1861).

Littorina (Cremnoconchus) – Stoliczka, 1871: 113.

Cremnoconchus (Lissoconchus) Thiele, 1929: 125 (type species by monotypy Cremnoconchus conicus Blanford, 1870 ).

Taxonomic history: Blanford’s (1863) original name Cremnobates was preoccupied ‘for a genus of fishes’ (i.e. Cremnobates Günther, 1861 ; a name used even earlier by Swainson, 1855) and he therefore renamed it Cremnoconchus ( Blanford, 1869) . The genus has been treated as valid at generic rank by all subsequent authors except Stoliczka (1871), who suggested that it should be ranked as a subgenus of Littorina . The subgenus Lissoconchus was introduced by Thiele (1929) for C. conicus and has occasionally been employed for this and other Cremnoconchus species without conspicuously ribbed shells ( Wenz, 1938; Subba Rao & Mitra, 1979; Subba Rao, 1989; Ramakrishna & Dey, 2007).

Diagnosis: Shell: turbinate; smooth or with spiral ribs; protoconch smooth, less than 1.5 whorls (indicating non-planktotrophic development). Operculum: paucispiral; calcified, with proteinaceous layer internally and externally. Male: prostate closed; prostate gland subepithelial; anterior vas deferens closed; penial vas deferens (sperm duct) deeply closed (i.e. no epithelial connection to surface); penial filament retracted into cavity in base; simple penial glands in base, sometimes forming a short protruberance. Female: seminal receptacle absent; oviducal glands subepithelial; egg groove coiled in one spiral. Radula: 5 cusps (plus 2 denticles) on rachidian; 3–5 cusps on outer marginal. Alimentary system: salivary glands anterior to nerve ring. Nervous system: pleurosuboesophageal connective short. (Slightly modified from Reid, 1989.)

Shell: The shell shape lies within the range of that of marine littorinids, being globular, turbinate or highturbinate, of moderate thickness, and sometimes with strong spiral ribs ( Figs 3 , 9, 11). As in many freshwater molluscs, the periostracum is relatively thick. Dissolution of the shell, or radulation by other snails, occurs where the periostracum is damaged, and the apical whorls are frequently eroded away. An umbilicus is present in some species, but is usually absent in juveniles, so it is correctly termed a ‘pseudumbilicus’. The surface is marked by prominent, fine or indistinct spiral microstriae that are visible under low magnification ( Fig. 4 ) and are a useful feature for identification. As in most marine littorinids (e.g. Reid, 1986a, 1996, 2007) the shell shows striking intraspe-

N, sample size; H2/B, shell shape index; H2/LA, relative spire height index; LA/WA, apertural shape index; DS/OL, opercular ratio; SE, standard error of the mean. See Figure 1 for definition of dimensions B, DS, H, H2, LA,OL, and WA.

cific variability. In most species the sampling remains too limited to observe patterns in the shell variation. However, in the most well-studied species, C. syhadrensis , there are clear differences between the range of variation within each of four local populations ( Tables 1 and 2), suggesting possible genetic differentiation. In one population (from Torna; Fig. 3F, J–M ) the shells range from almost smooth to strongly ribbed, so that development of ribs is not a reliable character for identification. Similarly, in C. canaliculatus a sutural rib can be present or absent (Fig. 9P– EE). In both C. conicus and C. canaliculatus the overall shape of the shell (relative spire height and peripheral angulation) and development of the pseudumbilicus are variable (Fig. 9). Shell coloration ranges from pale to dark brown in these three relatively well-sampled species, sometimes with 1–3 indistinct brown bands ( Figs 3 , 9), but does not appear to be polymorphic (i.e. with discrete morphs) within populations. There is slight sexual dimorphism in size, males being smaller (as also noted by Stoliczka, 1871); this phenomenon is usual in littorinids ( Reid, 1986a, 1996). The protoconch is similar in all species in which it has been seen ( Fig. 16C–F ); it is smooth, of 1.3–1.5 whorls, 0.47–0.70 mm in diameter, and therefore similar to the protoconchs of marine littorinids with non-planktotrophic development ( Reid, 1989).

Headfoot and locomotion: Externally, the animal is typical of the family, with blunt snout and mobile cephalic tentacles with eyes at their bases (Fig. 2H, I). The head and sides of the foot are commonly pigmented grey to black, but the animal is paler in C. canaliculatus , and in C. syhadrensis some populations are virtually unpigmented. Where head pigmentation is pale, the reddish myoglobin of the buccal mass musculature is visible by transparency (Fig. 2I). The sole of the foot does not show an anterior transverse (propodial) groove, but a small anterior pedal gland is present ( Reid, 1989). No longitudinal division of the sole is visible externally, but locomotion is nevertheless by ditaxic retrograde waves of muscular contraction; one complete wave passes back on one side of the sole of the foot, then on the other.

Operculum: The operculum of Cremnoconchus is paucispiral, but thickened by calcification in between internal and external proteinaceous layers. In species with the thickest calcification (e.g. C. syhadrensis ) the calcified part is inflexible, but an uncalcified flange remains around the margin. Internally, most species show a thickened spiral boss or rib of organic material; this, however, does not show well in SEM images because it is of relatively low relief (Fig. 5). The tightness of coiling, degree of calcification and development of the internal ridge show some variation between species ( Table 1; Fig. 5). The calcification of the operculum was mentioned by several early authors ( Blanford, 1863; Stoliczka, 1871), but without further comment. In fact such calcification is almost unique among littorinids ( Reid, 1989), the only other case being the aragonitic calcareous deposit on the outer surface of the operculum of Tectarius niuensis

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syhadrensis Base – 24 threads 15 developed. 20 threads c developed threads 5 10 – innermost ribs; threads 0 0 Cremnoconchus of Ribs above periphery – 10 8 8 8 5 – at shoulder (2 and; periphery) to or up 8 populations. Max shell height) (mm 9.4 8.3 5.9 9.8

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( Reid & Geller, 1997). The operculum can be withdrawn to a depth of about 0.1–0.2 of the final whorl, but up to 0.4 in C. agumbensis .

Male reproductive system: The anatomy and histology of the reproductive system have been described by Linke (1935) and Reid (1989). A closed prostate with subepithelial glands leads to a tubular anterior vas deferens and to the cephalic penis on the right side of the headfoot. The littorinid penis often bears elaborate glandular structures, but in Cremnoconchus the subepithelial, neutral mucous glands (staining blue in trichrome) are usually simply scattered in parts of the penial base, which appear swollen and opaque. In C. conicus and C. canaliculatus the subepithelial glands are found in a basal drum-shaped appendage, but this is unlike the penial glandular disc or complex mamilliform penial glands present in some marine littorinids ( Reid, 1989). A feature of Cremnoconchus that is unique in the family is the invagination of the penial filament (the intromittent part) into a distal pocket of the muscular base. The filament can be extended to a considerable length and in preserved material is usually fixed in a partly extended state. In the living animal, however, the filament is generally retracted. Dissection reveals that the penial vas deferens (sperm duct) within the base is coiled and folded to allow for extension of the filament during copulation (the duct in Fig. 6F, G is 2.5 times the length of the penial base), and lies within an internal space that is presumably involved in the hydrostatic extension of the filament. Withdrawal of the filament is accomplished by a retractor muscle lying adjacent to the coiled vas deferens and inserted at the junction of the base of the filament with the bottom of the invagination ( Fig. 6G ). Before entering the filament, the vas deferens becomes tightly bound to the retractor muscle. As in most littorinid genera, the form of the penis is an important character for discrimination

› Figure 2. Habitats and living animals of Cremnoconchus species. A , 10 km west of Mahabaleshwar on road to Poladpur, Raigad Dist., Maharashtra; altitude 692 m ( C. canaliculatus ). B, 6 km west of Mahabaleshwar on road to Poladpur; 1103 m ( C. conicus ). C, Hulikal Ghat, Udupi Dist., Karnataka; 475 m ( C. cingulatus , C. dwarakii ). D, escarpment of Western Ghats at Mahabaleshwar, Maharashtra; this stream is now polluted and contains no Cremnoconchus . E, C. globulus in flowing water at Lesser Kadambi Falls, Chikmagalur Dist., Karnataka; 967 m. F, Khandala, Pune Dist., Maharashtra; 297 m ( C. syhadrensis ). G, C. syhadrensis aestivating under ledges at Khandala; 297 m. H, living C. conicus , 6 km west of Mahabaleshwar on road to Poladpur. I, living C. syhadrensis, Khandala.

of species and may be a component of the specific mate-recognition system ( Reid, 1996).

Spermatozoa: These have been observed only in C. castanea , by light microscopy. They consist only of euspermatozoa (i.e. parasperm are absent), which are filiform and up to 193 Mm in length. These are among the longest recorded for Littorinidae , exceeded only by those of Bembicium ( Reid, 1989) . The sperm head is 24 Mm long and a distinct helical structure is visible. This may correspond to the helical condensation of chromatin in the nucleus of developing spermatids, reported in SEM studies of sperm development in Littorina species ( Buckland-Nicks & Chia, 1976; Paviour, Mill & Grahame, 1989); however, these reports have not mentioned a helical structure in mature eusperm.

Female reproductive system: The spiral route of the egg groove through the pallial oviduct is a well-known synapomorphy of Littorinidae ( Reid, 1989) . In Cremnoconchus the egg groove forms a single spiral loop of about 3.5 revolutions. Linke (1935) discriminated albumen, capsule and shell glands in the pallial oviduct, but did not explain the spiral structure. Histological examination suggests that the subepithelial glandular material composing the spiral portion of the pallial oviduct is mainly albumen gland, differentiated into two parts staining darker and paler blue in trichrome; these parts can sometimes be distinguished as more and less opaque cream areas in preserved specimens ( Fig. 6C ). The subepithelial lining of the final straight section of the pallial oviduct stains reddish in trichrome and appears to be responsible for the secretion of the outer coating of the egg capsule, which stains similarly; this gland is not, however, homologous with the capsule gland of the Littorininae ( Reid, 1989) . The ciliated cells lining the egg groove do not contain black pigment. There is a large copulatory bursa, opening in an anterior position (Fig. 14C). The seminal receptacle typical of most littorinids is absent; sperm are instead stored in the renal oviduct ( Linke, 1935; Reid, 1989).

Eggs: Mature ova can sometimes be seen in the distal part of the ovarian oviduct. In the pallial oviduct these are coated with albumen and a firm gelatinous covering, to attain a final diameter usually in the range 0.40–0.49 mm. Between 1 and 5 such eggs can be found in the straight section of the pallial oviduct ( Figs 6C , 15J); these are either uncleaved or show only the first cleavage of the embryo, suggesting that they are laid before further development proceeds.

Radula: The radula of Cremnoconchus has been drawn by Troschel (1867), Stoliczka (1871), Annan- dale & Prashad (1919) and Reid (1989), but SEM images are given here for the first time ( Figs 7 , 13 , 16A, B ). The radula is long (length relative to shell height 0.82–4.24) and the radular sac is coiled over the mid-oesophagus. As in all littorinids it is taenioglossate, with all seven teeth in each row well developed and a ‘littorinid notch’ in the base of the lateral tooth ( Reid, 1989). The base of the rachidian tooth is relatively narrow, lacking lateral projections ( Troschel, 1867), but otherwise the radula is of a generalized littorinid form ( Reid, 1989).

Mantle cavity: When the anatomy was first described, Cremnoconchus was said to possess a vascular mantle cavity (a ‘pulmoniferous sac’) with no trace of gills ( Blanford, 1863). Gills were subsequently described ( Stoliczka, 1871; Annandale, 1919; Prashad, 1925). The leaflets are of low triangular outline, continued as ridges (not branched as stated by Stoliczka, 1871) across the roof of the mantle cavity, and number 23–50. Although it has been reported that the opening of the mantle cavity is small and can be completely closed (Annandale, 1919; Annandale & Prashad, 1919), in fact the mantle edge and wide mantle opening are the same as in marine littorinids. The observation may be a reference to the fact that, when active, the headfoot largely occludes the shell aperture. The osphradium is short ( Prashad, 1925), only about one-third of the extent of the row of gill leaflets, but it is not ‘papilliform’ (Annandale, 1919; Annandale & Prashad, 1919). The hypobranchial gland is vestigial ( Prashad, 1925).

Range: Endemic to the northern and central Western Ghats of India, in the states of Maharashtra and Karnataka ( Fig. 8 ) .

Habitat and ecology: The habitat is highly specific, restricted to streams and waterfalls on the basaltic cliffs of the western escarpment of the Western Ghats (Fig. 2D), between altitudes of 297 and 1125 m (and potentially up to 1400 m, from localities of museum specimens; Supporting Table S1; see also Blanford, 1863, 1870; Annandale, 1919; Prashad, 1925). During the heavy rain of the south-western monsoon season (June–September) these streams become torrents. However, when collections were made by the authors during October 2010 the snails were mostly to be found crawling over rocks wetted by spray, or where water was flowing in a shallow film, usually in abundance (Fig. 2E). Cremnoconchus conicus also occurred in shallow pools with moving water, while C. syhadrensis and C. dwarakii were sometimes found on moss and wet vegetation beside the streams. In the northern part of the range (Maharashtra state) the surrounding vegetation in the stream gullies consisted of fern and balsam ( Impatiens ), with adjacent woodland or cloud forest, depending upon altitude (Fig. 2A, B). In the southern part (Karnataka state) the streams ran through rainforest (Fig. 2C). During the dry season, small streams may disappear and C. syhadrensis is known to aestivate in clusters in crevices and shaded pits in the rock ( Blanford, 1863; Annandale, 1919; Hora, 1926, 1928). At Khandala (October 2010) C. syhadrensis was observed in tight clusters of up to 1000 individuals under overhangs on shaded cliffs, where they would presumably aestivate as the rock surface dried out (Fig. 2G).

The behaviour of C. syhadrensis at Khandala was described by Annandale (1919: 119). At this locality it was abundant on cliffs, shaded from the midday sun, which ‘supported a growth of the peculiar dull green filamentous alga on which it feeds’. The animals became inactive and closed the operculum tightly when dry. When submerged, the snails crawled out of the water but, if prevented from reaching the surface, drowned after 24 h. The mantle cavity was said to be filled with water (‘never filled with air’) in snails that were crawling in air, but this was not the case in animals observed during the present study, in which the mantle cavity was air-filled. Stoliczka (1871) noted that the stomach of this species contained ‘minute algae’. In the present study the faecal pellets of C. hanumani were found to consist almost entirely of elongated diatoms.

The breeding season has not been recorded, but is presumed to be during the monsoon season. In October 2010, at the end of the monsoon, some specimens of all the species collected were mature (i.e. seminal vesicle with sperm and/or eggs in ovarian or pallial oviduct), but some were spent, suggesting that the breeding season was coming to an end. Samples of C. castanea collected in March and June also included some mature individuals (BMNH). Stoliczka (1871) recorded eggs in a mature female of C. syhadrensis in March. Since the eggs in the final section of the oviduct were always either uncleaved or at the twocelled embryonic stage, it is predicted that the large eggs are deposited and not retained until hatching. There is no evidence for ovoviviparity, as occurs in some marine littorinids ( Reid, 1989). Eggs are probably laid either singly or in small numbers, and presumably on the rock surface, where development and hatching take place.

The prevalence of parasitism by trematodes was very low, being observed only in C. canaliculatus from a single locality.

Remarks: At present there is no strong evidence for the subgeneric division of Cremnoconchus . The recognition of Lissoconchus as a subgenus based only on the smooth shell of C. conicus ( Thiele, 1929) is unwarranted, in view of the variability of shell ribs in C. syhadrensis .

Figures

Figure 1. Measurements and terminology of shell and operculum (illustrated by Cremnoconchus syhadrensis). Abbreviations: B, breadth; DS, diameter of spiral part of operculum; H, height; H2, height of last two whorls; LA, length of aperture (in apertural plane); OL, opercular length (excluding flexible flange); p, periphery; U, width of pseudumbilicus; WA, width of aperture (in apertural plane). Shape indices: shell shape = H2/B; apertural shape = LA/WA; opercular ratio = OL/DS.

Figure 3. Shells of Cremnoconchus syhadrensis. A, Cremnobates syhadrensis W.T. Blanford, 1863, neotype, no locality (BMNH 1906.1.1.2247). B, C, Matheran, Raigad Dist., Maharashtra (two views of same specimen; ZSI/WGRS/IR.INV- 2290). D, E, Anjani, Nashik Dist., Maharashtra (BMNH 1911.8.23.70–71). F, J–L, Torna Fort, Pune Dist., Maharashtra (USNM 317696). G–I, Khandala, Pune Dist., Maharashtra (G, H two views of same specimen; ZSI/WGRS/IR.INV-2293, 2292). M, Torna Fort, Pune Dist., Maharashtra (USNM 317695).

Figure 4. Microsculpture of Cremnoconchus species (viewed by SEM). A, C. dwarakii, Hulikal Ghat, Udupi Dist., Karnataka. B, C. syhadrensis, Matheran, Raigad Dist., Maharashtra. C, C. syhadrensis, Khandala, Pune Dist., Maharashtra. D, C. conicus, 44 km west of Bhor, Pune Dist., Maharashtra. E, C. conicus, 6 km west of Mahabaleshwar, Satara Dist., Maharashtra. F, C. globulus, Lesser Kadambi Falls, Chikmagalur Dist., Karnataka. G, C. cingulatus, Hulikal Ghat, Udupi Dist., Karnataka. H, C. agumbensis, Agumbe, Udupi Dist., Karnataka. I, C. canaliculatus, 10 km west of Mahabaleshwar, Raigad Dist., Maharashtra. J, C. canaliculatus, Dongarwadi, Tamhini, Pune Dist., Maharashtra. K, C. canaliculatus, 5 km south of Mahabaleshwar, Satara Dist., Maharashtra. L, C. castanea, Belkal Thirtha Falls, Udupi Dist., Karnataka. M, C. castanea, Arasinagundi Falls, Udupi Dist., Karnataka. N, C. hanumani, Greater Kadambi Falls, Chikmagalur Dist., Karnataka. O, C. hanumani, Hanuman Gundi Falls, Chikmagalur Dist., Karnataka.

Figure 6. Anatomy of Cremnoconchus syhadrensis. A, B, D–G, penes (A, E–F, fixed in ethanol; B, D, live). E–G are three views of single penis, external (E), with base sectioned (F), and with coiled penial vas deferens displaced to the right to show retractor muscle and with filament sectioned to show continuation of vas deferens to its tip (G). C, pallial oviduct and egg removed from straight section. A, Matheran, Raigad Dist., Maharashtra (BMNH 20120035; shell H = 7.4 mm). B, C, E–G, Matheran, Raigad Dist., Maharashtra (ZSI/WGRS; shell H: B = 7.2 mm; C = 7.2 mm; D = 5.8 mm; E–G = 7.5 mm). D, Khandala, Pune Dist., Maharashtra (ZSI/WGRS). Abbreviations and shading conventions: b, copulatory bursa (dashed outline, visible by transparency); c, cavity surrounding penial vas deferens and retractor muscle (black); d, distal to this point the penial vas deferens is tightly bound to the sheath of the retractor muscle; e.g. egg groove visible by transparency (thick line); f, penial filament; g, opaque glandular region of penial base (medium stipple); gc, firm gelatinous coating of mature egg; i, invagination of penial base (shaded); o, position of terminal opening of pallial oviduct into mantle cavity; oag, opaque part of albumen gland (dense stipple); ov, ovum; pvd, penial vas deferens; rm, retractor muscle of penial filament; ss, straight section of pallial oviduct; tag, translucent region of albumen gland (sparse stipple).

Figure 7. Radulae of Cremnoconchus species (two views of each radula, flat and at 45°). A, B, C. syhadrensis, Matheran, Raigad Dist., Maharashtra (ZSI/WGRS; shell H = 7.0 mm). C, D, C. conicus, 6 km west of Mahabaleshwar, Satara Dist., Maharashtra (ZSI/WGRS; shell H = 4.9 mm). E, F, C. canaliculatus, 10 km west of Mahabaleshwar, Raigad Dist., Maharashtra (ZSI/WGRS; shell H = 9.3 mm). G, H, C. hanumani, Greater Kadambi Falls, Chikmagalur Dist., Karnataka (ZSI/WGRS; shell H = 5.0 mm). Scale bars = 50 Mm.

Figure 8. Distribution of Cremnoconchus species (solid circles). Two or more species names (e.g. syhadrensis + canaliculatus) indicate sympatric occurrence. See Supporting Table S1 for locality details. The shaded area is the Western Ghats region as defined by Irfan-Ullah & Davande (2008). Cities indicated by asterisks.

Figure 13. Radulae of Cremnoconchus species (two views of each radula, flat and at 45°). A, B, C. globulus, Lesser Kadambi Falls, Chikmagalur Dist., Karnataka (ZSI/WGRS; shell H = 7.4 mm). C, D, C. agumbensis, Agumbe, Udupi Dist., Karnataka (ZSI/WGRS; shell H = 9.5 mm). E, F, C. cingulatus, Hulikal Ghat, Udupi Dist., Karnataka (ZSI/WGRS; shell H = 5.7 mm). G, H, C. castanea, Arasinagundi Falls, Udupi Dist., Karnataka (ZSI/WGRS; shell H = 8.5 mm). Scale bars = 50 Mm.

Figure 16. Radula (A, B) and protoconchs (C–F) of Cremnoconchus species. A, B, C. dwarakii (two views of radula, flat and at 45°), Hulikal Ghat, Udupi Dist., Karnataka (shell H = 6.4 mm). C, C. syhadrensis, Matheran, Raigad Dist., Maharashtra. D, C. canaliculatus, 10 km west of Mahabaleshwar, Raigad Dist., Maharashtra. E, C. agumbensis, Agumbe, Udupi Dist., Karnataka. F, C. dwarakii, Hulikal Ghat, Udupi Dist., Karnataka. Scale bars A, B = 50 Mm; C–F = 0.5 mm. White arrowhead marks junction of protoconch and teleoconch.