Natalina cafra cafra (Férussac, 1821)

Herbert, D. G. & Moussalli, A., 2010, Revision of the larger cannibal snails (Natalina s. l.) of southern Africa - Natalina s. s., Afrorhytida and Capitina (Mollusca: Gastropoda: Rhytididae), African Invertebrates 51 (1), pp. 1-1 : 31-35

Natalina cafra cafra (Férussac, 1821)

Figs 4A , 5 , 7A , 11G , 13B , 15B , 16–20

Helix (Helicophanta) cafra: Férussac 1821 in 1821–22: 25 [or 29 depending on issue]; 1821 in 1819–32, pl. 9A, fig. 8; Beck 1837 in 1837–38: 46; Deshayes & Milne-Edwards 1838: 107; Deshayes 1851 in Férussac & Deshayes 1820 –51: 198, pl. 9A, fig. 8 (as Helix caffra [sic]). Type loc.: ‘La Cafrerie’ [Delalande] = E. Cape. (Connolly cited the locality ‘Uitenhage (fide Férussac)’ but we have been unable to find reference to Uitenhage in any of Férussac’s works. Deshayes (1851 in Férussac & Deshayes 1820 –51) later gave the locality as ‘la Cafrerie aux environs du cap de Bonne Espérance, et particulièrement vers la baie d’Algoa’.)

Helix caffra [sic]: Wood 1828: 40, pl. 7, fig. 36; Catlow & Reeve 1845: 120; Krauss 1848: 75 (in part); Pfeiffer 1848: 40; 1851 in 1850–53: 52, pl. 74, figs 1–3 (plate dated 1849); Reeve 1851 in 1851– 54: sp. 179; Hanley 1856: 228, supplement, pl. 7, fig. 36; Morelet 1889: 19.

Paryphanta caffra [sic]: Adams & Adams 1855 in 1854–58: 226.

Aerope caffra [sic]: Mörch 1865: 395; Pfeiffer 1878 in 1878–81: 26; Tryon 1885: 131, pl. 25, fig. 13; Pilsbry 1890: 41, pl. 1, figs A–F.

Rhytida caffra [sic]: Gibbons 1880: 95–96.

Natalina caffra [sic]: Pilsbry 1893 in 1892–93: 135; Woodward 1895: 270–277; Melvill & Ponsonby 1898: 170; Sturany 1898: 30 (in part); Murdoch 1901: 171, pl. 17, fig. 11; Möllendorff 1903: 20, pl. 3, figs 4–7; Connolly 1912: 90; Hodgson 1989: 30.

Natalina cafra: Watson 1934: 157 ; Connolly 1939 (in part): 104; Hoffmann 1940: 87–96; Barnard 1951: 142, pl.xxi, fig.6; Kilburn 1973: 10–11 (in part); Herbert 1991: 6–11 (in part); Bieler & Slapcinsky 2000: 38, fig. 26, map 25; Schileyko 2000: fig. 969.

Natalina compacta Connolly, 1939: 108 , pl. 3, figs 1–3 [in part]; Hodgson 1989: figs 2, 3a (radula). Type loc.: Mountain Drive , Grahamstown, E. Cape [Farquhar]. Syn. n.

not Natalina caffra [sic]: Bruggen 1969: 57, nor Natalina cafra: Herbert & Kilburn 2004: 220 [= Natalina cafra natalensis subsp.n.], nor Natalina cafra: Bruggen 2004:46 [= Natalina quekettiana complex].

Etymology: From Latin cafer, orig. Arabic kafir (a non-believer).

Identification: Shell large to very large; proportions very variable, some specimens globose, others more depressed with a low spire and somewhat more rapidly expanding whorls; umbilicus open, width narrow to moderate, partially obscured by reflected columella lip. Cannot be reliably distinguished from other subspecies of N. cafra using shell characters alone. N. beyrichi differs in having a much wider, unobstructed umbilicus and is typically more depressed. Southern E. Cape.

Description ( Figs 17 , 18 ): Shell large to very large, thin and fragile; shell proportions very variable, some specimens globose ( Fig. 18A, i.e . those named N. compacta by Connolly) others considerably more depressed ( Fig. 18F ); last whorl descending gently toward aperture in adult, but suture at outer lip generally remaining slightly above mid-whorl. Protoconch diameter typically 7–8 mm ( Fig. 4A ).Apical surface dull, sculptured by close-set axial riblets; riblets become weaker below periphery and evanesce toward umbilicus; umbilical margin sculptured by growth-lines rather than riblets; base generally more glossy, particularly around umbilical margin, but there is no clear line of disjunction between dull apical surface and base; growth flaws and repairs frequent and often distinct, particularly on last adult whorl; umbilical width moderate to rather narrow; umbilicus usually partially obscured by reflected columella lip; aperture drooping outward basally, its long axis somewhat oblique; outer lip very thin with a projecting periostracal fringe. Periostracum greenish to olive-brown in fresh specimens, with frequent, unevenly spaced, radial bands in darker shades, particularly on last whorl; old specimens frequently faded and more yellowish. Underlying shell translucent white or almost transparent when fresh, with exterior colour and banding showing through.

Dimensions: Largest specimen, diameter 75.5 mm (fide Connolly 1939), but few specimens exceeding 65 mm in diameter; H:D of adults 0.60–0.94 (N=27).

Living animal ( Figs 5 , 15B ): Head-foot grey or greyish brown to dark orange-brown; darker dorsally and usually but not always with a paler longitudinal stripe running backward from base of each optic tentacle; tentacles and labial palps darker grey-brown; skin texture finely granular; posterior portion of foot flat and trigonal, tip of tail rather acutely pointed; mantle edge frequently orange or orange-brown, even when the body is grey-brown; labial palps well developed.

Radula ( Fig. 19 ). Formula 1+5+(20–30) (N=4); length up to 53 mm, with up to 57 transverse rows of teeth (but no radulae from very large specimens available). Pilsbry (1890) illustrated only 11 marginal teeth per half row of an adult specimen, but it seems probable that he failed to observe some of the minute outer teeth. The radula of a small juvenile (NMSA W3272, diameter 12.5 mm) was approximately 12 mm in length with 47 transverse rows and formula 1+5+10, suggesting that the number of marginals increases with growth, but the number of laterals does not (see also Connolly (1939: 106) for similar observations concerning a juvenile of N. c. natalensis ).

Distal genitalia: Few mature specimens available. Epiphallus with a well-developed bulla on outer wall near its junction with vas deferens ( Fig. 13B ); lumen of epiphallus lined by 4 or 5 well-developed longitudinal ridges with weaker second and third order intermediaries; ridges microscopically transversely fimbriate, those on the inner wall (adjacent to penis) extending for entire length of epiphallus, those on outer wall ending at base of bulla, which itself has a hollow core.

Spermatophore: Unknown.

Type material: Two syntypes of Helix cafra Férussac, 1821 in MNHN (21050), one is the figured specimen, diameter 58.6 mm, height 43.0 mm ( Figs 17A–C ). Holotype and paratype of Natalina compacta Connolly, 1939 in BMNH (1937.12.30.1305–6), holotype ( Figs 17D–F ) diameter 50.4 mm, height 46 mm (51 mm and 43 mm fide Connolly, 1939); one possible paratype in Manchester Museum (EE.5691, Grahamstown, fide McGhie 2008).

Additional material examined (all NMSA unless otherwise indicated): SOUTH AFRICA: South-western E. Cape: Baviaanskloof wilderness area, Kougaberge (33.67188°S: 24.33008°E), 800–1000 m, grassland/fynbos, D. Clark, 1999 (V8525); Baviaanskloof Wilderness Area , vicinity of Berg Plaas (33.61522°S: 24.48499°E), 886 m, montane sparse fynbos, grassland, A. Moussalli & D. Stuart-Fox, 15/iii/2005 (W3255) ; ~ 15 km S of Andrieskraal (33.83867°S: 24.74515°E), 328 m, riverine thicket, in leaf-litter, A. Moussalli & D. Stuart-Fox, 14/iii/2005 (W4600) ; Elandsberge, opposite Cockscomb (33.68893°S: 24.80056°E), 600 m, grassy fynbos, under rocks, station 08–051, D. Herbert, L. Davis & M. Cole, 21/ix/2008 (W6517) ; Hankey, Sarah Bartmann municipal grounds (33.83834°S: 24.88594°E), 75 m, thicket, in leaf-litter and under fallen aloes, station 08–050, D. Herbert, L. Davis & M. Cole, 21/ix/2008 (W6525) ; Hankey area, Kleinrivier road (33.81429°S: 24.95415°E), 255 m, thicket, in leaf-litter and under fallen aloes, station 08–053, D. Herbert, L. Davis & M. Cole, 21/ix/2008 (W6508) ; Cape St Francis, 7 Edward Rd (34.16777°S: 24.83040°E), coastal garden (C. & B. Logie), D. Herbert, 09/x/2000 (V8581) ; Jeffreys Bay area, Kabeljous R. mouth (34.017°S: 24.933°E), on land side of dune on east side of river mouth, C. Logie, ‘ Snailiens’ project, 03/i/2001 (V8862) ; ditto (34.00253°S: 24.94015°E), coastal succulent scrub, in leaf-litter, A. Moussalli & D. Stuart-Fox, 14/iii/ 2005 (W3272) ; ditto (34.00253°S: 24.94015°E), coastal succulent scrub, in leaf-litter, A. Moussalli & D. Stuart-Fox, 16/xii/2005 (W4225) ; St Francis Bay , Van Staden’s beach (33.96667°S: 25.21670°E), C. Vernon, 18/x/1986 ( ELM D10039 ) ; Port Elizabeth area, Island Forest Res. (33.98668°S: 25.37151°E), low coastal forest, in leaf-litter, station 08–040, D. Herbert, L. Davis & M. Cole, 18/09/2008 (W6406) ; Uitenhage (33.76373°S: 25.39764°E), valley thicket, in leaf-litter and under fallen aloes, A. Moussalli & D. Stuart-Fox, 22/xii/2005 (W4830, W5490) ; ditto, Vanes Estate (33.767°S: 25.400°E), ‘ Snailiens’ Project, pupils of Thomas Muir School , 2001 (V9034); Port Elizabeth , Redhouse (33.833°S: 25.567°E), Mrs T.V. Paterson, 1980 (E7905); Port Elizabeth (33.917°S: 25.600°E), F.Holland (E7895); ditto (33.917°S: 25.600°E), F. Cruden, 1927 (A0446, W5984); ditto, Mrs J. Longstaff ( BMNH Acc. No. 906); ditto, Walmer, leg. Staples, 15/xi/ 2006 ( ELM D15211 ) ; ditto, Marine Drive (33.9973°S: 25.6827°E), dune scrub, D. Herbert, 13/x/2000 (V8612) ; ditto, Cape Recife , nr gate to reserve (34.01325°S: 25.69160°E), dune scrub, D. Herbert & G. Rossouw, 13/x/2000 (V8567) . South-central E. Cape: Zuurberg (33.3167°S: 25.5000°E) (A7050); Grassridge, PPC mining concession (33.66244°S: 25.62116°E), bontveld, under fallen aloes and in grass clumps, station 08–042, D. Herbert, L. Davis & M. Cole, 19/ix/2008 (W6416) ; Coerney (33.44828°S: 25.72420°E), 134, m, valley thicket, in leaf-litter, A. Moussalli & D. Stuart-Fox, 12/xii/2005 (W4220) ; Colchester area, WNW (33.680516°S: 25.770376°E), sand/siltstones of Sundays River formation, M. Mostovski, 13/vii/2009 (W6927) ; Bedford, Maestroom Forest (32.64860°S: 26.06833°E), M. Bursey, 15/i/2002 ( ELM D13770 , juvenile) ; Alicedale, Roodekrans (33.3167°S: 26.0830°E) (E7904); Woody Cape Nat. Res. (33.69938°S: 26.35977°E), 216 m, coastal indigenous forest, in leaf-litter, A. Moussalli & D. Stuart-Fox, 11/xii/2005 (W4631) ; ~ 12 km S of Alexandria (33.75207°S: 26.41048°E), 167 m, coastal thicket, in leaf-litter,A. Moussalli & D. Stuart-Fox, 11/xii/2005 (W4739) ; Grahamstown, Mountain Drive (33.32784°S: 26.49952°E), grassy fynbos on top of hill, under old dry eucalypt log, V. Ndibo , 10/iii/2007 (W5212) ; ditto (33.325°S: 26.517°E) (E7863, E7902); Grahamstown (33.300°S: 26.533°E), R.H. Ivy, 01/x/1910 (V2473); Grahamstown, Resolution , Fort Brown (33.133°S: 26.617°E) (E7894, E7909); Kasouga (33.64759°S: 26.75219°E), coastal dune forest, in leaf-litter, A. Moussalli & D. Stuart-Fox, 10/xii/2005 (W5472) ; ~ 13 km N of Double Drift Game Res. (32.86658°S: 26.81436°E), valley thicket, under dead aloe, A. Moussalli & D. Stuart-Fox, 02/xii/2005 (W5164) ; Port Alfred (33.6°S: 26.9°E) (E7892); Port Alfred ( Kowie ) (33.6°S: 26.9°E) (E7892, V2456, ELM D10956 ); Port Alfred , east of Kowie R. (33.59194°S: 26.90472°E), coastal forest, M. Bursey, 26/xi/2006 ( ELM D15009 ) ; Alice area, Breakfast Vlei (33.0833°S: 26.9500°E) (E7893); Peddie (33.200°S: 27.117°E), Howard, x/1924 (A7053).

Additional literature records (material not seen): SOUTH AFRICA: E. Cape: Somerset East (32.717°S: 25.583°E), Miss Bowker ( Connolly 1912); Bedford (32.683°S: 26.083°E) ( Connolly 1912); Bathurst (33.517°S: 26.833°E) ( Connolly 1912).

Distribution ( Fig. 20 ): Known only from the southern E. Cape, along the coast and in the mid and lower catchments of the Gamtoos, Sundays and Great Fish rivers; from the Baviaanskloof in the west to the Peddie area in the east, inland to the Grahamstown area and Great Fish River Conservancy; altitudinal range extending from the coast to approx. 1000 m. Records from the Somerset East and Bedford area require confirmation as they are either literature records or based on juvenile shells.

Habitat: Evidently tolerant of relatively dry environments and occurs in a wide variety of vegetation types in the south of the broader Albany Thicket biome, including coastal fynbos and strandveld, montane grassy fynbos, bontveld, thornveld, various types of thicket, coastal forest and suburban gardens; in leaf-litter beneath shrubs and bushes, buried under rocks and fallen aloes, or within dense grassy clumps and sheltering in rocky outcrops. Common, though generally at low densities, but locally relatively abundant in calcium-rich areas such as the limestone habitats at Grassridge, north of Port Elizabeth (Alexandria Formation).

Notes: Shell proportions vary considerably, but intergrade completely. Depressed specimens may resemble N. beyrichi , but in N. c. cafra such specimens have a more rapidly expanding last adult whorl and the umbilicus remains consistently narrower. Elevated specimens resemble the other E. Cape subspecies, N. c. amathole and N. c. eumacta , except that the umbilicus of such specimens of N. c. cafra is generally narrower.

When proposing the name Natalina compacta, Connolly (1939) distinguished his new taxon from N. cafra solely on the grounds of its more globose shape. Molecular data has shown that similarly globose shells from the type locality of N. compacta cluster together with less elevated specimens ( Moussalli et al. 2009) typical of N. c. cafra . The relative proportions of the shell therefore do not appear to provide reliable taxonomic information. We thus consider Natalina compacta Connolly, 1939 , to be a synonym of N. c. cafra .

Conservation: Natalina c. cafra is widespread and relatively common. Due to its catholic habitat requirements and tolerance of moderately dry environments, its area of occupancy is unlikely to be conspicuously fragmented. There is thus no evidence to suggest that the subspecies is threatened at present.

Figures

Fig. 4. Protoconchs of Natalina, Afrorhytida, Capitina and Nata (all NMSA): (A) Natalina cafra cafra (W4225), scale bar = 5.0 mm; (B) Afrorhytida trimeni (V7904), scale bar = 2.5 mm; (C) Capitina schaerfiae (W5672), scale bar = 2.5 mm; (D) Nata sp. n. (W6029), scale bar = 0.5 mm; arrows mark protoconch/teleoconch junction.

Fig. 5. Natalina cafra cafra (Férussac, 1821), anterior view of head showing sensory appendages.Abbreviations: asg – aperture of suprapedal gland, dg – dorsal skin grooves, e – eye, it – inferior tentacle, lp – labial palp, m – mouth, ob – optic bulb, ot – optic tentacle.

Fig. 7. Pulmonary anatomy of Natalina, Afrorhytida and Capitina (all NMSA): (A) N. cafra cafra (W4220); (B) A. knysnaensis (W5211); (C) C. schaerfiae (W5672).Abbreviations: au – auricle, kid – kidney, pn – pneumostome, pu – primary ureter, pv – pulmonary vein, rec – rectum, su – secondary ureter, uf – ureteric fold on rectum, up – ureteric pore, uv – ureteric vein, ven – ventricle.

Fig. 11. Suprapedal glands of Capitina, Afrorhytida and Natalina (all NMSA): (A) C. schaerfiae (W5672), scale bar = 5.0 mm; (B) A. knysnaensis (W3351), scale bar = 5.0 mm; (C, D) N. quekettiana lucaris subsp. n. (W3310): (C) pedal cavity with suprapedal gland in situ, scale bar = 10 mm; (D) dissected gland, scale bar = 5.0 mm; (E, F) N. wesseliana (V7668): (E) entire gland, scale bar = 20 mm; (F) enlargement of distal end showing terminal vesicle, scale bar = 5.0 mm; (G) N. cafra cafra (W4220), scale bar = 10 mm. Abbreviations: asg – aperture of suprapedal gland, pa – pedal artery, v – vesicle at posterior end of suprapedal gland.

Fig. 13. Distal genitalia of Natalina s.s. (all NMSA): (A) N. cafra natalensis subsp. n. (1392), lower male tract with penis and epiphallus cut open to show internal structure; (B) N. cafra cafra (W4220), external view of epiphallus showing bulla at base of epiphallus, close to its junction with vas deferens; (C) N. quekettiana quekettiana (W6646), epiphallus opened longitudinally to show internal ridges and intervening diverticulae; (D) N. c. natalensis subsp. n. (1392), lower female tract showing oviduct caecum (caecum dissected away from free oviduct and spermoviduct base to which it is fused with connective tissue in life) and vagina which has been opened longitudinally to reveal internal folds.Abbreviations: bd – bursa copulatrix duct, ct – connective tissue web, d – slit-like diverticulae in epiphallus wall, eb – epiphallus bulla, ep – epiphallus, er – internal epiphallic ridge, fod – free oviduct, ga – genital atrium, obd – opening of bursa copulatrix duct, oc – oviduct caecum, p – penis, pl – penis lumen with micropapillate lining, pp – penis papilla, pr – penial retractor muscle, sod – spermoviduct, v – vagina, vd – vas deferens.

Fig. 15. Natalina s.s., living animals of larger species (all NMSA): (A) N. beyrichi, Hluleka (W2895), shell diameter 41.5 mm; (B) N. cafra cafra, Mountain Drive, Grahamstown (W5212), shell diameter 30.0 mm; (C) N. cafra amathole subsp. n., Hogsback (paratype, W6371/T2309), shell diameter 39.0 mm; (D) N. cafra natalensis subsp. n., Pietermaritzburg (specimen not collected), shell diameter approx. 58 mm; (E) N. c. natalensis subsp. n., Mtamvuna (paratype, W0308/T2370), shell diameter 40.3 mm; (F) N. cafra eumacta, Mazeppa Bay (W4044), shell diameter 40.4 mm; (G) N. c. eumacta, Dwesa (V7868), shell diameter 48.3 mm; (H) N. c. eumacta, egg, Manubi Forest (W4067), scale in millimetres.

Fig. 16. Distribution of Natalina cafra subspecies: N. c. cafra (triangles), N. c. amathole subsp. n. (stars), N. c. natalensis subsp. n. (circles), N. c. eumacta (squares).

Fig. 17. Natalina cafra cafra (Férussac, 1821), type material: (A–C) figured syntype of Helix cafra Férussac, 1821, diameter 58.6 mm (MNHN 21050, photo courtesy of Barbara Buge); (D–F) holotype of Natalina compacta Connolly, 1939, diameter 50.4 mm (BMNH 1937.12.30.1305–6).

Fig. 18. Natalina cafra cafra (Férussac, 1821) (all NMSA): (A) Grahamstown (E7900), diameter 55.0 mm; (B) Grahamstown (V2473), diameter 53.5 mm; (C) Grahamstown, Mountain Drive (W5212), diameter 40.0 mm (animal grew to this larger size in captivity, cf. Fig. 15B); (D) Woody Cape Nat. Res. (W4631), diameter 54.0 mm (W4631); (E) Port Elizabeth (A446), diameter 60.4 mm; (F, G) Woody Cape Nat. Res. (W4631), depressed specimen, diameter 49.5 mm.

Fig. 19. Natalina cafra cafra (Férussac, 1821), radula, Coerney (NMSA W4220): (A) rachidian and lateral teeth, scale bar = 1.0 mm; (B) vestigial marginal teeth, scale bar = 250 µm.

Fig. 20. Distribution of Natalina cafra cafra (Férussac, 1821). Triangles with a white centre indicate localities for specimens used in DNA analyses (Moussalli et al. 2009); contours at 1000 m and 1500 m.