Natalina cafra natalensis, Herbert & Moussalli, 2010

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 : 42-47

Natalina cafra natalensis subsp. n.

Figs 3A–C , 6C , 9A , 10D , 12A, B , 13A, D , 14B , 15D, E , 16 , 27–29

Helix caffra [sic]: Krauss 1848: 75 (in part).

Natalina caffra [sic]: Sturany 1898: 30 (in part); Connolly 1912: 90 (in part); Bruggen 1969: 57.

Natalina cafra: Connolly 1939: 104 , pl. 3, fig. 7, text-fig. 8 (in part); Kilburn 1973: 10–11 (in part); Herbert 1991: 6–11 (in part); Herbert & Kilburn 2004: 220.

not Natalina cafra: Bruggen 2004: 46 [= N. quekettiana complex].

Etymology: Name derived from its geographical occurrence, the province of KwaZulu-Natal.

Identification ( Fig. 27 ): For general description see Natalina c. cafra . Closely resembles the nominotypical subspecies, from which it cannot be reliably distinguished using shell characters alone. Shell proportions and level of periphery variable, but H:D ratios fall entirely with the range of those of N. c. cafra . Generally less globose than N. c. eumacta and particularly N. c. amathole .

Dimensions: Holotype diameter 59.4 mm, height 49.2 mm; largest specimen (NMSA A7041, ‘Natal’), diameter 75.0 mm, but few specimens exceeding 65 mm in diameter; H:D of adults 0.67–0.85 (N=27).

Living animal ( Figs 15D, E ): Head-foot pale fawn-brown to yellowish brown or orange-brown, occasionally grey; dorsal part of neck usually darker; neck region often with a paler longitudinal stripe running backward from base of each optic tentacle; pedal margin and mantle skirt usually yellowish, less often orange.

Radula ( Fig. 28 ): See Natalina c. cafra , no morphological differences evident; formula 1+5+(20–30) (N=8, two in BMNH); length in adult up to 58 mm (fide Connolly 1939), perhaps more in very large individuals), with 50–60 transverse rows of teeth. Connolly (1939) reported a newly hatched juvenile from Pietermaritzburg as having a formula 1+5+12 (slide in BMNH).

Distal genitalia ( Figs 12 , 13A, D ): As in N. c. cafra . In most specimens the epiphallus lacks a distinct bulla, but there is evidence of a slight swelling in some specimens. The longitudinal ridges lining the epiphallus lumen extend for almost its entire length.

Spermatophore ( Fig. 14B ): A fresh spermatophore was spontaneously produced by and isolated captive animal in September (NMSA W7136). In general form this closely resembled the spermatophores of N. c. amathole and N. c. eumacta ; anterior 2/3 with 6–8 primary longitudinal ridges; posterior third smooth but retaining three indistinct keels, two lateral and one dorsal; straightened length 18.3 mm. A small finger-like process was present at the base of the recurved tail region. This was stouter than that sometimes present on the N. c. eumacta spermatophore, but less well developed than that of N. beyrichi .

An allospermatophore ( Fig. 10D ) was found in a further specimen, collected in January (paratype, NMSA E7682/T2375). This was less strongly curved and had more well-developed longitudinal ridges, the strongest of which extended posteriorly, as three angular keels, almost to the tail tip; straightened length 16.3 mm. However, in this example a finger-like process was not evident on the tail region, suggesting that, as in N. c. eumacta , the presence of this structure is a variable feature.

Holotype ( Figs 27A–C ): SOUTH AFRICA: KZN: Ashburton , nr Pietermaritzburg (29.670°S: 30.453°E), 670 m, in thornveld garden, R. Miller, ii/1996 ( NMSA V3293 /T2365).

Paratypes: SOUTH AFRICA: KZN: Same data as holotype ( NMSA W6615 /T2366, 1 specimen) ; Karkloof , Shafton Estate, De Magtenberg Forest (29.31795°S: 30.19115°E), 1272 m, S. Miya, 13/xii/2006 ( NMSA W5144 /T2373, 1 specimen) ; Karkloof (approx. 29.30°S: 30.23°E), A.J. Taynton, ex Burnup coll’n, pre 1930 (2204/T2368, 1 specimen) ; Pietermaritzburg , 30 Payn St (29.610°S: 30.389°E), suburban garden, found dead in pond, D. Herbert, xii/2001 ( ELM D16035 (ex NMSA V9637 ), 1 specimen) ; Pietermaritzburg , Scottsville (29.6230°S: 30.3967°E), in garden, D. Herbert, ii/1989 ( BMNH 20100124 [ex NMSA E7579 /T2369], 1 specimen) ; Pietermaritzburg , Prestbury (29.615°S: 30.337°E), in garden, P. Croeser, 1995 ( NMSA V2515 / T2374, 1 specimen) ; south of Tugela R. mouth (approx. 29.233°S: 31.492°E), dune forest, A.C. & W.H. van Bruggen, 03/i/1964 ( NMSA B0035 /T2367, 1 specimen) ; Durban , Stella Bush (approx. 29.880°S: 30.988°E), H. Bell-Marley, 11/xi/1930 ( NMSA E7896 /T2376, 1 specimen) ; Ngele Forest (30.533°S: 29.633°E), 1300 m, mist-belt Podocarpus forest, S. Bourquin, 1995 ( NMSA V2514 /T2371, 1 specimen) ; Port Edward (approx. 31.055°S: 30.225°E), J. Stannard, i/1987 ( NMSA E7682 /T2375, 1 specimen) ; Mtamvuna Gorge Nat. Res. , Loerie Trail (31.0600°S: 30.1717°E), riverine/scarp forest, in leaf-litter, D. Herbert, 27/xii/2002 ( NMSA W0308 /T2370, 1 specimen) .

Additional material (all NMSA unless otherwise indicated): SOUTH AFRICA: KZN: Thukela valley and southern Zululand: Qudeni Forest (28.64882°S: 30.90391°E), mist-belt forest, A. Moussalli & D. Stuart-Fox, 21/v/2003 (W4833); Mfongosi (28.713°S: 30.805°E), W.E. Jones (3365); Nkandla Forest Res., Chibini area (28.7227°S: 31.1282°E), 1200 m, mist-belt forest, under logs and in leaf-litter, D. Herbert, M. Bursey & T. Nangammbi, 20/x/2003 (W1167); Eshowe (28.885°S: 31.468°E), 500 m, amongst garden debris, R. Miller, 01/ iv/1996 (V2903); ditto, Dlinza Forest (28.89300°S: 31.44833°E), scarp forest, in leaf-litter, D. Herbert, 24/x/ 1998 (V6663); ditto (28.8945°S: 31.4555°E), scarp forest, D. Eckard, 03/ii/2000 (V8087); ditto (28.90°S: 31.45°E), 520 m, scarp forest, under log, D. Eckard, 29/ix/1997 (V5298); Mtunzini, Umlalazi Nat. Res. (28.95170°S: 31.75083°E), dune forest, found dead in recent excavation, I.M. Porter, 16/v/1987, don. R.H. Taylor (E476); south of Tugela R. mouth (29.23000°S: 31.48804°E), 11 m, coastal forest, in leaf-litter, A. Moussalli & D. Stuart-Fox, 11/xi/2006 (W4699). KZN Midlands: Karkloof Nat. Res. (29.301°S: 30.230°E), 1300 m, mist-belt Podocarpus forest, R. Kilburn, D. Herbert & L. Davis, 27/ii/1995 (V1948, V2021); Karkloof, Mbona Private Nat. Res., Holbeck (29.30087°S: 30.35948°E), found dead in burnt grassland, died eating Cochlitoma granulata, D. Herbert & L. Davis , 01/vii/2006 (W5117); ditto (29.30087°S: 30.35948°E), in burnt grassland, D. Herbert, viii/2004 (W2276); ditto (29.30339°S: 30.36525°E), mist-belt Podocarpus forest, in leaf-litter, D. Herbert, 24/x/2004 (W2405); ditto, lower forest (29.30406°S: 30.36077°E), mist-belt Podocarpus forest, D. Herbert, L. Davis, A. Moussalli & D. Stuart-Fox, 23/v/2005 (W3152); Karkloof, Rockwood farm (29.3083°S: 30.2250°E), O. Bourquin, 02/viii/1981 (B5288); ditto, Leopard’s Bush (29.315°S:30.250°], ca 1350m, mist-belt Podocarpus forest,in leaf-litter, D. Herbert, M.Seddon & P.Tattersfield, 09/xii/1998 (V8415); ditto (29.317°S: 30.258°E), mist-belt Podocarpus forest, in leaf-litter,inside dead Cochlitoma shell, D. Herbert, 09/i/1997 (V5322); ditto, Shafton Estate, De Magtenberg Forest (29.31795°S: 30.19115°E), 1272 m, S. Miya, 13/xii/2006 (W5145); Curry’s Post (29.362°S: 30.142°E) (A7045); Albert Falls (29.430°S:30.428), (2205); Hilton (29.555°S: 30.297°E), (A7048); Pietermaritzburg, Ferncliffe Nat. Res. (29.565°S: 30.345°E), mist-belt Podocarpus forest,A. Moussalli, D. Stuart-Fox, D. Herbert & L. Davis, 1/iv/2005 (W4828); ditto, Town Bush Valley (29.56648°S: 30.33917°E), suburban garden, A. Moussalli & D. Stuart-Fox, 24/ii/2006 (W4832); ditto, below World’s View (29.580°S: 30.333°E), grassy hillside with scattered trees, in litter beneath Erythrina latissima, D. Herbert & L. Davis , 13/xi/2005, (W3658); ditto (29.615°S: 30.337°E), garden (with new laid eggs), 28/ii/1989 (W5049); ditto,Alexandra Road (29.617°S: 30.383°E), W.G. Rump, v/1932 (1392); ditto, 17 Oribi Rd (29.628°S: 30.383°E), suburban garden, D. Herbert, xii/1984 (V6368); ditto, Blackburrow’s Ridge, newly hatched, C.F.W. Hime, 05/ix/1926 (3724); Pietermaritzburg area, Mkondeni (29.6512°S: 30.4810°E), 727m, bushland, M. Hamer, 29/x/2007 (W5853); ditto, Mkondeni (29.65180°S: 30.43847°E), 715 m, bushland, M. Hamer, 29/10/2007 (W5847); ditto, Bisley Valley Nat. Res. (29.65767°S: 30.39159°E), open woodland, under rotting log, G. Redman, 01/iii/2003 (W0549); ditto, Ashburton, Kingthorpe farm (29.67915°S: 30.49849°E), 750–800 m, savannah grassland, M. Hamer et al., 12/xi/2008; Boston area, on Impendle road (29.67150°S: 29.95662°E), 1540 m, natural grassland, C. Grant, 20/xi/2006 (W4877); Thornville (29.733°S: 30.383°E) (A7049); Baynesfield, nr Maybole farm (29.750°: 30.267°E), mist-belt Podocarpus forest, O. Bourquin, xi/1964 (V6544); Bulwer area, 3 km to north (29.78160°S: 29.77577°E), highly disturbed montane Podocarpus forest beside stream, crawling at night, A. Moussalli, 06/xii/2003 (W1417); Bulwer (29.877°S: 29.775°E), Dr. E. Warren (V4253); Nkawini Mt, Riverbank farm (29.88601°S: 30.08859°E), 1030 m, Protea savannah burnt during winter, many forbs, half-buried in soil under Protea, A. Armstrong et al. , 8/x/2008 (W6593). Central KZN coast and hinterland: Hawaan Forest (29.7050°S: 31.0917°E), coastal lowland forest, in leaf-litter, D.Herbert & L. Davis, 04/xii/1995 (V2117); Hawaan Forest(29.71 17°S: 31.0883°E), 60 m, coastal lowland forest, in leaf-litter,D.Herbert, M. Seddon & P.Tattersfield, 12/x/1998 (V8106);Drummond (29.748°S: 30.700°E), W.G. Rump, 19/xii/1932 (B0037); Gillitts (29.783°S: 30.800°E), R.S. Benton, 01/x/1963 (B0036); Durban, Burman Bush (29.817°S: 31.017°E), coastal lowland forest, O. Bourquin, 25/x/1962 (3945, B0034); Pinetown (29.820°S: 30.892°E), L. Trotter (2206); Durban, 49 Waller Crescent, Roseglen (29.82445°S: 31.00190°E), suburban garden, C. Uys, 6/iii/2006 (W5025); Durban, Pigeon Valley Nat. Res. (29.86403°S: 30.98506°E), coastal forest, in leaf-litter, A. Moussalli & D. Stuart-Fox, 18/v/2005 (W4362); Durban, Pigeon Valley Park (29.880°S: 30.967°E), 90 m, coastal lowland forest, in leaf-litter, Herbert, Kilburn & Davis, 31/iii/ 1995 (V2363);Durban, Stella Bush (29.880°S: 30.988°E), H. Bell-Marley, 11/xi/1930 (B0038,W1385);Durban, Stellawood, F.G. Cawston (BMNH 37.12.30.1303); Durban, Bellair (29.892°S: 30.953°E), indigenousbush, N. Gardiner (2141); Durban Bluff (29.895°S: 31.047°E), Falcon coll’n (A9124); Umbogintwini (30.0167°S: 30.9170°E), Marley, 03/v/1919 (E7899); Port Natal [= Durban] (BMNH 57.1.16.7, G.C. Cato; 57.3.6.41, Sir W. Jardine Bt). Drakensberg: Cathedral Peak area, Fern Forest (Oqalweni Forest) (28.94329°S: 29.18580°E), montane Podocarpus forest, in leaf-litter, D. Herbert (Earthwatch), 19/iii/2006 (W5483); Cathedral Peak area (28.945°S: 29.205°E), 1900 m, below fire look-out tower, at edge of in open grassland, O. Bourquin, 14/i/1977 (V7109); Giant’s Castle, Bannerman’s Pass (29.2533°S: 29.4200°E), 2350 m, alpine grassland, D.T. Rowe- Rowe, 26/ii/1976 (A7052); Cobham, Sani Pass (29.60800°S: 29.32417°E), 2040 m, shrubland, D. Alletson, 25/iv/1996 (V3285). Southern KZN: Franklin area, Hebron farm (30.40327°S: 29.56253°E), 1650 m, garden, J. Scott, vii/2008; Oribi Gorge Nat. Res., Hoopoe Falls trail (30.70765°S: 30.26992°E), scarp forest, in leaf-litter, D. Herbert, 06/x/2001 (V9434); Port Shepstone (30.742°S: 30.453°E) (A7043);Mar gate (30.863°S: 30.367°E), W.G. Rump, 1929 (B0090); Mtamvuna Gorge Nat. Res., western heights (31.000°S: 30.167°E), in wetland area, R. Markham , 19/viii/1997 (V5271).

Rejected records: A record of Natalina cafra from Mbabane, Swaziland (Bruggen 2004) was based on a specimen belonging to the N. quekettiana complex (see below, Fig. 35A ). Similarly, Connolly’s record of the species from ‘between Lydenburg and Delagoa’ (Connolly 1939) probably refers either to the N. quekettiana complex or to N. wesseliana , but no material from this region is present in either NMSA or BMNH.

Distribution ( Fig. 29 ): Endemic to KwaZulu-Natal, but widely distributed in central and southern regions, from the Eshowe–Qudeni area south to the border between KwaZulu-Natal and E. Cape (Mtamvuna R.); altitudinal range extensive, from the coast to 2350 m in the central Drakensberg.

Habitat: Occurs in a wide variety of habitats, ranging from indigenous forest (coastal to montane) to thornveld, valley bushveld and mist-belt and subalpine grassland; has also adapted well to suburban gardens; in leaf-litter and under logs or beneath shrubs and grass clumps, essentially in almost any sheltering microhabitat. Relatively common, particularly in the KZN Midlands, but population densities are generally low.

Notes: We have been unable to identify any morphological characters, either conchological or anatomical, which serve to distinguish this subspecies from the nominotypical one. It is clear, however, that specimens of N. cafra from KwaZulu-Natal constitute a monophyletic lineage which is genetically distinct from those occurring in E. Cape ( Moussalli et al. 2009). In addition, there is a clear geographical gap in the north-eastern E. Cape separating the KwaZulu-Natal N. cafra populations from those in the E. Cape. At the coast this gap is filled by N. beyrichi , but evidently remains vacant at inland localities.

It is difficult to discern any clear geography-related pattern in the variability in shell proportions of N. c. natalensis , but specimens from Durban and the KwaZulu-Natal north coast tend to be less elevated (H:D<0.76). Juveniles may be confused with the smaller Afromontane Natalina species, but the latter have a distinctly smaller protoconch (diameter 4.5–6.0 mm compared to 7.0–8.0 mm).

Conservation: Like the nominotypical subspecies, N. c. natalensis is widespread and common, and of catholic habitat requirements. Its distribution is not conspicuously fragmented (acknowledging sampling gaps) and it is evidently able to adapt to some extent to suburban habitats and thus to survive as a synanthrope. At present there is no evidence to suggest that the subspecies is threatened.

Figures

Fig. 3. Feeding in Natalina: (A–C) N. cafra natalensis, captive animals consuming: (A) Achatina immaculata, (B) Cornu aspersum and (C) Elisolimax flavescens; (D) N.beyrichi as found in leaf-litter,Mntafufu, E. Cape, with tail inserted in shell of Gittenedouardia carinifera, extracting calcium (NMSA W2970).

Fig. 6. Mantle edge anatomy of Afrorhytida, Capitina and Natalina, showing variation in left body lobe structure (all NMSA): (A) Afrorhytida knysnaensis (W5211); (B) Capitina calcicola sp. n. (W3201); (C) Natalina (Natalina) cafra natalensis subsp. n. (V8415); (D) Natalina (Tongalina) wesseliana (V7668).Abbreviations: lbl – left body lobe of mantle, pn – pneumostome, rbl – right body lobe of mantle.

Fig. 9. Distal genitalia of Natalina, Afrorhytida and Capitina (all NMSA): (A) N. cafra natalensis subsp. n. (E7682), (B) A. knysnaensis (W4643), (C) C. schaerfiae (W5672). Abbreviations: bd – bursa copulatrix duct, ep – epiphallus, ga – genital atrium, oc – oviduct caecum, p – penis, pr – penial retractor muscle, sod – spermoviduct, v – vagina, vd – vas deferens.

Fig. 10. Spermatophores of Capitina, Afrorhytida and Natalina (all NMSA):(A) C. calcicola sp. n. (paratype, W5670/T2265), length 8.2 mm; (B) A. burseyae sp. n. (paratype, W5231/T2260), length 10.5 mm; (C) A. kraussi kraussi (W5803), length 20 mm; (D) N. cafra natalensis subsp. n. (paratype, E7682/T2375), length 16.3 mm; (E) N. quekettiana lucaris subsp. n. (paratype, W3305/T2559), length 26.5 mm; (F) N. wesseliana (V7668), length 32 mm. The head of the spermatophore is uppermost in all cases and the lengths given are for the spermatophore as if straightened out.

Fig. 12. Natalina s.s. genital system: (A, B) N. cafra natalensis subsp. n. (paratype, NMSA E7682/T2375): (A) entire reproductive tract, scale bar = 10 mm; (B) oviduct caecum (with spermatophore), teased away from free oviduct, scale bar = 5.0 mm; (C) N. quekettiana lucaris subsp. n. (paratype, NMSA W3305/T2559), oviduct caecum (with spermatophore) twisted around free oviduct and base of spermoviduct, scale bar = 5.0 mm.Abbreviations: ag – albumen gland, bc – bursa copulatrix, bd – bursa copulatrix duct, ep – epiphallus,fod – free oviduct,ga – genital atrium, hd – hermaphrodite duct, oc – oviduct caecum, ot – ovotestis, p – penis, pr – penial retractor muscle, s – spermatophore, sod – spermoviduct, v – vagina, vd – vas deferens.

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. 14. Natalina s.s. spermatophores (all NMSA): (A) N.cafra amathole subsp. n. (W4193), length 21 mm; (B) N. cafra natalensis subsp. n. (W7136), length 18.3 mm; (C) N. cafra eumacta (W4055, Manubi Forest), distorted spermatophore with finger-like process on tail region, length 12 mm; (D) N. c. eumacta (W4160, Manubi Forest), well preserved spermatophore lacking finger-like process on tail region, length 18.5 mm; (E) N. beyrichi (W4123), length 25.8 mm; (F) N. quekettiana lucaris subsp. n. (paratype, W3305/T2559), length 26.5 mm. The lengths given are for the spermatophore as if straightened out.

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. 27. Natalina cafra natalensis subsp. n.: (A–C) holotype (NMSA V3293/T2365), diameter 59.0 mm; (D–F) Durban Bluff, olive-green specimen (SAMC 36934), diameter 63.0 mm; (G) Karkloof, high spired specimen (faded) with periphery below mid-whorl (paratype, NMSA 2204/T2368), diameter 56.0 mm; (H) Prestbury, Pietermaritzburg, globose specimen (paratype, NMSA V2515/ T2374), diameter 59.0 mm; (I) ‘Natal’, large, depressed specimen (NMSA A7041), diameter 75 mm.

Fig. 28. Natalina cafra natalensis subsp. n., radula, Karkloof Forest (NMSA V8415): (A) rachidian and lateral teeth, scale bar = 1.0 mm; (B) vestigial marginal teeth, scale bar = 250 µm.

Fig. 29. Distribution of Natalina cafra natalensis subsp. n. Triangles with a white centre indicate localities for specimens used in DNA analyses (Moussalli et al. 2009); contours at 1000 m and 1500 m.

Fig. 35. Natalina quekettiana complex, living animals and eggs (all NMSA):(A) N. q. quekettiana, Ferncliffe, Pietermaritzburg (W6646), shell diameter 31.3 mm; (B) N. q. lucaris subsp. n., Ngome Forest (paratype, V2249/T2563), shell diameter 29.4 mm; (C) N. q. dracomontana subsp. n., Injasuthi (holotype, V7992/T2451), shell diameter 27.2 mm; (D) N. q. dracomontana subsp. n., Monk’s Cowl area (paratype, W4101/T2452), shell diameter 26.4 mm; (E) N. q. montistempli subsp. n., Oqalweni, Cathedral Peak (holotype, W4084/T2422), shell diameter 23.9 mm; (F) N. q. quekettiana, eggs (W6646), scale in millimetres.