Revalidation of Pyxicephalus angusticeps Parry, 1982 (Anura: Natatanura: Pyxicephalidae), a bullfrog endemic to the lowlands of eastern Africa Author Scott, Elizabeth Author Visser, John D. Author Yetman, Caroline A. Author Oliver, Lauren Author Broadley, Donald G. text Zootaxa 2013 3599 3 201 228 journal article 10.11646/zootaxa.3599.3.1 67a77c56-6304-42ec-b6bf-a5c0d17a734e 1175-5326 217094 C5975855-F625-42B8-9FC3-EE91D0428DE7 Pyxicephalus angusticeps Parry, 1982 New Status Figs 1–4 , 6 , 10 G–H, 11A–C, 12B, 13E. Pyxicephalus adspersus angusticeps Parry 1982 : 281 –292, figs 1, 4, 5, 7, table 1. Poynton & Broadley 1985 : 123 –124. Pyxicephalus edulis : Channing, Du Preez & Passmore 1994 : 141 –148, fig. 1b, plate 1b, synonymized P. adspersus angusticeps . Channing 2001 : 349 –351, figs 22.5, 281. Channing & Howell 2006 : 322 –323, fig. 22.6. Pyxicephalus edulis : Pickersgill 2007 : 105 –108 (part), figs 45, 46. Type material. Holotype : Adult 3, NMSA 1992 (UNP 3099, NMSA Type number 2581), from Beira, Mozambique ( Fig. 2 ). Paratypes : One adult 3, NMSA 1991 (UNP 3098), and two subadults, NMSA 1990 (UNP 3063), NMSA 1993 (UNP 3100) with same data as the holotype ; twelve subadult paratypes NMZB-UM 6451 (two specimens), NMZB-UM 7516 (five specimens), NMZB-UM 19774 (four specimens; no. A shown in Figs 11 A–C) and NMZB-UM 23374, from Beira, Mozambique . Diagnosis. This species is assigned to the genus Pyxicephalus by the combination of presence of mandibular odontoids (outgrowths of the dentary), femoral glands, cranial exostosis on the frontoparietals and nasals, hypertrophied inner metatarsal tubercle, and supraorbital flanges on the frontoparietals (see Scott 2005 for comparisons of these characters in other genera of ranoid frogs). Pyxicephalus angusticeps can be distinguished from P. obbianus ( Figs 8 , 10 C–D, 11D–F) by the: (1) rudimentary webbing between the toes (more extensive in P. obbianus ; Fig. 8 F); (2) tympanum width less than eye diameter (more than one and one half times eye diameter in adult male P. obbianus ; Figs 8 A, 8C), positioned approximately one tympanum width or slightly less from eye (less than half the tympanum width in P. obbianus ; Fig. 8 C); and (3) vertebral stripe running most of the length of body (restricted to the snout in adult P. obbianus ; Figs 8 A, 8D). Pyxicephalus angusticeps can be distinguished from P. edulis ( Figs 5 , 7 , 10 E–F, 12C–D) and P. adspersus ( Figs 9 , 10 A–B, 12A) by: (1) nuptial pads present only on innermost finger (Digit II) of breeding males (as in P. obbianus , but present on Digits II–IV in P. adspersus and P. e d u l i s ); (2) head of breeding males less proportionately enlarged (see Fig. 10 ), particularly in width, than in P. adspersus and P. e d u l i s ; (3) distinct subadult gular colouration ( Fig. 11 C), which is darkly marbled and more persistent in the adult female ( Fig. 3 F) than in P. adspersus and P. e d u l i s ; (4) small, triangular, pointed odontoids, not longer than wide ( Fig. 12 B in P. angusticeps vs. Figs 12 C–D in P. e d u l i s ; Fig. 8 D in P. obbianus ), whereas odontoids are large and well-developed in all other species of Pyxicephalus ; (5) presence of at most poorly-developed dorsal ridges, usually the most distinct running from behind eyes (dorsum of type material covered only by weakly or strongly developed oval or round warts), whereas these are thick and highly developed in P. adspersus ( Fig. 10 A); and narrower, finer and often continuous in P. e d u l i s ( Figs 5 A, 10E); (6) vertebral stripe wide, pale (coppery-orange in preservation) and diffuse, formed by pale background colour visible between densely-packed, dark dorsal blotches, which are absent medially, with fine, dark stippling present elsewhere between dark dorsal blotches ( Figs 3 , 4 ), whereas the vertebral stripe is absent in adults of P. adspersus , and variably (but usually) present, thin and pale green-yellow in P. e d u l i s ( Figs 7 A, 10); (7) femoral glands well-developed and relatively larger and more conspicuous than in all other species of Pyxicephalus . FIGURE 1. Distribution of P. angusticeps Parry, 1982 New Status (black triangles) and P. edulis Peters, 1854 (grey squares) in east Africa. Localities of juvenile specimens are not included. Redescription of the holotype . Adult male, NMSA 1992 (field number UNP 3099, NMSA Type Number 2581, Fig. 2 ), collected at Beira, the swamp beyond Estoril [ 19°50'37"S , 34°50'20"E ]: Jan. 26, 1959 , Nyasaland- Mozambique Expedition [of the University of Natal , Pietermaritzburg]. Head. Tympanum visible, subcircular (oval) in shape, slanted slightly anteriorly. Tympanum width smaller than that of eye. Tympanum positioned approximately its own width in distance from eye (i.e. less than one times width of eye away from eye). White spot or marking absent from right tympanum, but minute white spot present on left tympanum ( Fig. 2 C). Upper lip with thin rim of light colouration. Upper jaw with four pale coppery-orange brown bars on each side; posterior two broader than anterior two. Two anterior-most bars on upper jaw on each side of face meet anterior to eyes. Gular region pale with diffuse brown colouration laterally. Light irregular spots (not a complete crossbar) across head above eyes. Head narrow, not as wide as body at level of sacrum, not disproportionately wide. Odontoids in lower jaw weakly-developed, triangular. Tongue notched, typically ranid, no mid-lingual papilla. Nostrils large, situated slightly closer to eyes than tip of snout. FIGURE 2. Holotype of Pyxicephalus angusticeps Parry, 1982 New Status : NMSA 1992, adult 3 from Beira, Mozambique. 2A. Dorsal view. 2B. Ventral view. 2C. Lateral view, left. 2D. Frontal view. 2E. Hand. 2F. Foot. Scale bar = 1 cm. Secondary sexual characteristics. Nuptial pads visible only on Digit II (inner finger) of hand, covering most of dorsal and lateral surfaces of these digits, including side of thenar tubercle. Forearms only slightly thickened, indicating youth. Testes large, elongated, dark yellow in preservation with blackened mesenteric tissue above. Limbs. A gracile, slender-bodied animal. Toes slightly webbed, web extending to half length of longest toe (approximately to level of proximal subarticular tubercle), such that three phalanges of longest toe free of webbing; remaining length of toes with slight paler lateral flanges. Inner metatarsal tubercle hypertrophied, spade-like; outer metatarsal tubercle absent. Digits of hand elongated, tapering, with slight paler lateral flanges. Ventral surface of hands lighter, dorsal side brown. Digit II (inner finger) longer than Digit III (second finger) and Digit V (fourth finger), Digit IV (third finger) longest. Subdigital tubercles present, large and rounded. Subarticular tubercles present on Digit IV, inconspicuous on other fingers. Thenar tubercle large and bilobed (not divided completely), palmar tubercle present. Palms of hands otherwise smooth. Digit tips unexpanded, rather narrowing distally, with a paler hardened tip. Dorsal and dorso-lateral surfaces of thighs, calves and along margin of tarsus with small white asperites, arranged loosely into lines on weak skin ridges on dorsal surfaces of calves. White asperites present on posterior third of dorsum, set on small raised tubercles, most densely arranged around cloaca. White asperites absent from ventral surfaces of limbs. Femoral granules present around cloaca, and on posterior-dorsal surface to half length of thighs. Ventral colouration. Colouration of dorsal surface of calves extending onto ventral surface of calves. Flanks and underside of limbs lightly stippled with diffuse brown pigment. Abdomen off-white, granular. Pectoral region with two medially directed triangular ‘waistcoat’ scars1 on each side, interior of which is coloured with diffuse light brown stippling. Glands. Pectoral glands present, small, elongate, triangular and inconspicuous. Femoral glands large, elongate, oval, brown, inconspicuous, set within pigment horizon of ventral thighs, which is indistinct, grading into ventral colouration. Femoral glands positioned closer to knee than cloaca, confined to distal two-fifths of length of thighs. FIGURE 3. Pyxicephalus angusticeps Parry, 1982 New Status . 3A, 3B: AC 1104, adult 3 from Beira, Mozambique, dorsal and ventral views. 3C, 3D: AC 1112, adult 3 from Beira, Mozambique, dorsal and ventral views. 3E, 3F: MP 3143, adult ♀ from Dondo, Mozambique, dorsal and ventral views. Scale bar = 1 cm. 1. These triangular ‘waistcoat’ patterns are commonly observed in Pyxicephalus , and may be relictual scars from the emergence of forelimbs. FIGURE 4. Pyxicephalus angusticeps Parry, 1982 New Status . 3A, 3B: CAS 164712, adult 3 from Malindi-Mombasa road, Kenya, dorsal and ventral views. 3C, 3D: CAS 164708, adult 3 from Malindi-Mombasa road, Kenya, dorsal and ventral views. 3E, 3F: CAS 202691, adult Ƥ from Zaraninge [Kiono] Forest Reserve, Tanzania, dorsal and ventral views. Scale bar = 1 cm. Dorsal colouration. Dorsum dark brownish-grey in preservation. Small rounded darker dorsal blotches visible anteriorly, indistinct posteriorly. No symmetrically arranged (opposite or alternate) blotches visible over urostyle region. Vertebral stripe broad, coppery-orange brown, the edges formed by irregularly-positioned, dark rounded dorsal blotches; vertebral stripe extending to tip of snout, but narrowing anteriorly from approximate level of eyes, and indistinct from approximate level of sacrum posteriorly. Small patches of mottling and stippling apparent anteriorly against pale base colour of dorsum, becoming less conspicuous posteriorly. Dorsal ridges and warts. Primary Dorsal Ridge Series 2 broken and only partially visible on right side, not extending full length of dorsum. Primary Dorsal Ridge Series 1 and 3 are greatly reduced to few weakly-developed warts. Lateral ridge absent on left, weakly present on right. Numerous conspicuous but narrow, raised oval warts present on flanks. Dorsum otherwise relatively smooth, with few slightly raised warts. Weak supratympanic ridge of warts apparent. FIGURE 5. Lectotype of Pyxicephalus edulis Peters, 1854 : ZMB 50301 (formerly one of two specimens accessioned under ZMB 10056), adult 3 from Tete, Mozambique. 5A. Dorsal view. 5B. Ven t ral vi ew. 5C. Lateral view, right. 5D. Lateral view, left. 5E. Frontal view. 5F. Hand. 5G. Foot. Scale bar = 1 cm. FIGURE 6. Paralectotype of Pyxicephalus edulis Peters, 1854 : ZMB 10056, determined here to be P. angusticeps Parry, 1982 New Status , adult 3 from Tete, Mozambique. 6A. Dorsal view. 6B. Ven tr al vi ew. 6C. Lateral view, right. 6D. Lateral view, left. 6E. Frontal view. 6F. Hand. 6G. Foot. Scale bar = 1 cm. FIGURE 7. Pyxicephalus edulis Peters, 1854 : MNHNP 2010.0153, adult 3 from Nhica do Rovuma, Mozambique. 7A. Dorsal view. 7B. Ventral view. 7C. Lateral view, left. 7D. Frontal view. 7E. Hand. 7F. Foot. Scale bar = 1 cm. FIGURE 8. Pyxicephalus obbianus Calabrezi, 1927 : MZUF 10337, adult 3 from Òbbia, ca . 100 km NW of, along track Òbbia to Galcàio, Somalia. 8A. Dorsal view. 8B. Ventral view. 8C. Lateral view, left. 8D. Frontal view. 8E. Hand. 8F. Foot. Scale bar = 1 cm. FIGURE 9. Pyxicephalus adspersus Tschudi, 1838 : CAS 160245, adult 3 from Katima Mulilo, Namibia. 9A. Dorsal view. 9B. Ventral view. 9C. Lateral view, left. 9D. Frontal view. 9E. Hand. 9F. Foot. Scale bar = 1 cm. FIGURE 10. Comparison of adult males of Pyxicephalus Tschudi, 1838 . 10A, 10B. Pyxicephalus adspersus Tschudi, 1838 : CAS 160245, Katima Mulilo, Namibia. 10C, 10D. Pyxicephalus obbianus Calabrezi, 1927 : MZUF 10337, Òbbia, ca . 100 km NW of, along track Òbbia to Galcàio, Somalia. 10E, 10F. Pyxicephalus edulis Peters, 1854 : MNHNP 2010.0153, Nhica do Rovuma, Mozambique. 10G, 10H. Pyxicephalus angusticeps Parry, 1982 New Status : CAS 164712, Malindi-Mombasa road, Kenya. Scale bar = 1 mm. FIGURE 11. Subadult and metamorphs of Pyxicephalus Tschudi, 1838 . 11A, 11B, 11C. Paratype of Pyxicephalus angusticeps Parry, 1982 New Status : NMZB-UM 19774A, subadult, dorsal, lateral and ventral views. 11D, 11E, 11F. Pyxicephalus obbianus Calabrezi, 1927 : MZUF 10446, metamorph, dorsal, lateral and ventral views. 11G, 11H, 11I. Pyxicephalus adspersus Tschudi, 1838 : MP 4600, metamorph, dorsal view. Scale bar = 1 cm. FIGURE 12. Odontoids of Pyxicephalus Tschudi, 1838 . 12A. Unvouchered live adult 3 specimen of P. adspersus Tschudi, 1838 . 12B. Pyxicephalus angusticeps Parry, 1982 New Status : CAS 164711, adult 3, Malindi-Mombassa road, Kenya. 12C. Pyxicephalus edulis Peters, 1854 : CAS-SUA 18321, adult 3, Livalr District, Tanzania. 12D. Paratype of P. edulis Peters, 1854 : ZMB 3349, adult 3, from Mozambique. Variation. Adult material from the coastal lowlands of Kenya and Tanzania ( Fig. 4 , Appendix 1) differs from typical Mozambican material of P. angusticeps ( Figs 2 , 3 ) in the following respects. The vertebral stripe is narrower, better defined and a darker orange-red colour in preservation. The dorsum may present more, but poorlydefined and wider broken ridges, and have more distinct dark dorsal blotches. Barring is occasionally absent between the upper lip and the eye. Adults are larger than those from Beira. The asperites on the dorsal surface of the tibia are more irregularly arranged. Metamorphs and subadults. The metamorphs of P. angusticeps can be distinguished from both P. adspersus and P. edulis on at least three external characters. The adult pattern of fewer ridges and conspicuous oval warts is also evident in metamorphs and subadults of P. angusticeps ( Figs 11 A–C). There are only a few broken ridges in place of Primary Dorsal Ridge Series 2, and the dorsum is covered in conspicuous oval warts, usually more pronounced laterally, in metamorph material (with tail vestiges) from NMZB that we assigned to P. angusticeps based on occurrence at the same locality as the distinctive subadult paratypes . These evenly-spaced warts in metamorphs and sub-adults of P. angusticeps are absent from the dorsum in metamorphs of P. adspersus ( Figs 11 G–I), P. e d u l i s and P. obbianus ( Figs 11 D–F), and conform in appearance to those observed in the warty adult individual illustrated by Channing (2001, fig. 22.5) , Channing et al. (1994 , plate 1b), and Channing & Howell (2006, plate 22.6) . They resemble dorsal warts observed in the pyxicephaline genus Poyntonia Channing & Boycott, 1989 . The metamorphs of P. obbianus also differ markedly in colouration from their congeners, being finely vermiculated over the entire dorsum, with larger blotches present only on the limbs, and in having immaculate abdomens. A primary series of six ridges develop in late-stage P. adspersus and P. edulis larvae, and are pronounced by the time metamorphosis is complete ( Figs 11 G–I); these ridges are lacking in metamorphs of P. obbianus ( Figs 11 D–F). Larvae. Tadpoles listed in the account of Pickersgill (2007 fig. 47, top, viz. MP 2155) from Tica, Mozambique , are typical of P. e d u l i s (according to information presented in Du Preez & Carruthers 2009 : 414–417), in having the labial tooth row formula 5(3-5)/3. The tadpole of P. angusticeps is unknown. Distribution. Parry (1982) suggested that P. angusticeps was probably isolated from the western populations of P. edulis by the old course of the Zambezi River, which reached the sea south of Beira. He predicted that the range of P. angusticeps would include the area north to the Zambezi River and west to the Urema Trough. Although the southern limit of the known distribution of P. angusticeps appears to be the type locality, Beira in Mozambique , the species probably extends northwards through the lowland plains of East Africa, as far as Kakuyuni in Kenya (Appendix 1). A distribution map of P. angusticeps in East Africa is presented in Fig. 1 , and is similar to that presented for P. edulis in fig. 252 of Channing & Howell (2006) . There is, however, a substantial disjunction between known records from Mozambique and those from Tanzania and Kenya , which may be due to poor collecting effort in the intervening lowlands. Few herpetological surveys have been undertaken in Mozambique , and even those conducted in areas where Pyxicephalus should occur (e.g. Jacobsen et al. 2010 ) may not detect these frogs, due to their prolonged periods of inactivity. We have used the distinctive characteristics of the metamorphs (discussed above) to assign some metamorphs without associated adult material from two additional localities to P. angusticeps . Jorge (1933DD) is on the Buzi River, about 120 km upstream from its confluence with the Pungwe River estuary. Alvez de Lima (2034AB) was a safari camp ca . 50 km south-west of Beira, far from any major rivers. According to unpublished ecological modeling results (C.A. Yetman), areas in northern Mozambique with potentially suitable habitat for P. angusticeps include parts of north-central Manica Province, south-west of Quelimane on the coast in Zambezia Province, and along the Limpopo River in central Gaza Province. Conservation status. Additional survey work is required to accurately assess the range and conservation status of P. angusticeps , which may be more widespread in East Africa. Currently, it is best considered as ‘Data Deficient’ (IUCN 2011).