Taxonomy of the super-cryptic Hyperolius nasutus group of long reed frogs of Africa (Anura: Hyperoliidae), with descriptions of six new species Author Channing, A. Author Hillers, A. Author Lötters, S. Author Rödel, O. Author Schick, S. Author Conradie, W. Author Rödder, D. Author Wagner, P. Author Dehling, J. M. Author Du Preez, L. H. Author Kielgast, J. Author Burger, M. text Zootaxa 2013 3620 3 301 350 journal article 10.11646/zootaxa.3620.3.1 a501bd5f-fdee-474a-95cc-f791b29f5155 1175-5326 215983 03B8D237-7C7D-4E79-A020-4305ACF119B7 Hyperolius friedemanni sp. nov. Mercurio & Rödel Friedemann's Long Reed Frog ( Fig. 4 ) Holotype . SMF 85694 (tissue VM11), an adult male, collected at Karonga, Malawi , 7 February 2007 by V. Mercurio, 9°55'59.6'' S , 33°56'44.6'' N , 472 m a.s.l. Paratypes . ZMB 76095 (tissue VM12), an adult female, with the same details as the holotype ; SAIAB 186000, two juvenile specimens (Monkey Bay, Malawi ) ( Fig. 1 ). FIGURE 9 Hyperolius nasutus , Calandula , Angola, ZMB 77311, photo A. Channing (A); Hyperolius poweri , Mkambati NR , South Africa, photo W. Conradie (B); Hyperolius rwandae sp. nov . , Butare, Rwanda, ZMB 77221, holotype, photo J.M. Dehling (C); Hyperolius viridis , Kaningina , Malawi, photo V. Mercurio (D), Hyperolius rwandae sp. nov , female paratype ZMB 77223, photo J.M Dehling (E), Hyperolius dartevellei , Carumbo , Angola, PEM A 10035 , photo W. Conradie (F). Genetic material. SMF 85694, ZMB 76095 ( holotype and paratype ) SAIAB 186000 (two specimens) Monkey Bay, Malawi . Diagnosis . The advertisement call ( Fig. 8 ) consists of a brief initial note of eight pulses, followed by six pulses at a slower rate. The duration of the call is 0.12 s . It can be distinguished from species that produce only a buzz, such as H. acuticeps , H. jacobseni sp. nov . and H. nasutus . It can also be distinguished from H. adspersus , H. dartevellei and H. lupiroensis sp. nov . , which produce only a brief single note. It differs from those species with calls longer than 0.2 s , such as H. benguellensis , H. inyangae sp. nov . and H. viridis . It can be distinguished from those species where the slower part of the call consists of less than half the pulses of the initial note, such as H. howelli sp. nov . , H. igbettensis and H. rwandae sp. nov . Finally, although the structure of the call of H. poweri is similar, the two differ in pitch, H. poweri having the dominant frequency of 5.9 kHz, while H. friedemanni sp. nov. has a dominant frequency of 4.3 kHz. The snout is sharply rounded in profile, which distinguishes it from species with truncated, bluntly rounded, or shark-like snouts; H. adspersus , H. benguellensis , H. howelli sp. nov . , H. igbettensis , H. inyangae sp. nov . , H. jacobseni sp. nov . , H. poweri , H. dartevellei and H. viridis . It is the only species in the study where the webbing reaches the disc on all toes, at least on one side. This distinguishes it from all other species. Description of Holotype . The width of the gular flap is 5.1, hand 5.5. The top of the snout is flat, with the tip of the snout acutely rounded from above and from the side ( Fig. 6 ) (HW/SUL 0.29). The snout is 1.4x eye. The tympanum is not visible. The nostrils are positioned near the snout tip (EN/SL 0.5), nostril opening rounded, slightly protruding. Fine teeth are present on the upper jaw. The choanae are small, round. The tongue is long, with the posterior as wide as the length, with the terminal 20% bifurcated. Vomerine processes absent. The hand is 25.5% of the SUL. A small inner metacarpal tubercle is present. The relative finger lengths are 1<4<2<3. The foot is 0.4 of SUL, and the tibia is 0.52 of SUL. The webbing is shown in Fig. 7 . The skin is smooth on the dorsum and limbs, coarsely granular under the thighs. In preservative the skin becomes transparent. In life the body is pale green, tinged with blue along the legs, and yellow-tipped fingers and toes. There are pale dorsolateral stripes without dark borders that originate at the nostril and run back over the eye to continue to the groin. The iris is golden. Paratype variation . The female paratype is similar to the holotype . Tympanum not visible. The paratypes from Monkey Bay collected by EN are subadults, with skin that is transparent in preservative, showing large numbers of subdermal parasite eggs. Advertisement call. Recorded at Karonga, on 7 February 2002 at 23:40 h, 27°C air temperature, voucher specimen SMF 85694. The call ( Fig. 8 ) consists of the regular repetition of one single biphasic pulsed note with a duration 110–190 ms. Interval between notes is 180–360 ms. The note repetition rate is 1.4 s -1. The dominant frequency is 3900–4500 Hz. The specimen was calling at night from dense grassy vegetation within a swamp in an exposed position about 400 mm above the water. See Table 3 for a summary of call parameters. Eggs and tadpoles. Unknown. Habitat. Swamp along the lakeshore with abundant grassy vegetation and sandy soil. Other common species were: Afrixalus fornasini , Hyperolius pusillus , H. viridiflavus nyassae , H. tuberilinguis , Phrynobatrachus acridoides , P. mababiensis , Ptychadena cf. mascareniensis, P. anchietae , Kassina senegalensis , Amietophrynus gutturalis , A. maculatus , Xenopus muelleri, Arthroleptis stenodactylus, and Hemisus marmoratus . Etymology . We dedicate this new species to Friedemann Schrenk in recognition of his enthusiastic and tireless work for the research and protection of the natural history heritage of Malawi . Remarks. The species is only known from the shores of Lake Malawi , and we suggest that it be regarded as Data Deficient, in terms of the IUCN criteria.

Hyperolius howelli	sp. nov.	Du	Preez	&	Channing
Howell's Long Reed	Frog
(Fig. 4)

Holotype . SAIAB 118979, collected at Himo Road, Arusha, Tanzania ( 3°21' 29.6" S ; 36°50'15.3" E ), collected 12 April 2008 by L.H. du Preez. Paratypes . SAIAB 118980–1, female, and SAIAB 118980–2, male, collected at Himo Road, near Arusha, Tanzania ( 3°21' 29.6" S ; 36°50'15.3" E ), collected 12 April 2008 by L.H. du Preez; NMK 39221 from Kakamega Forest. Genetic material . SAIAB 118979–80 (Himo Road, Arusha) and a specimen from Madehani, Tanzania (no voucher), NMK 39221 (16S sequence accessioned as AY323926 , 12S sequence determined as part of this study) Kakamega Forest, Kenya (Lötters et al. 2004) ( Fig. 1 ). Diagnosis : The advertisement call ( Fig. 10 ) consists of an initial brief note, followed by three slower pulses, with a duration of 0.12 s . It can be distinguished from species producing only a single note and those producing only a buzz: H. acuticeps , H. adspersus , H. dartevellei , H. jacobseni sp. nov . , H. lupiroensis sp. nov . , and H. nasutus . It differs from species producing a call over 0.2 s : H. benguellensis , H. inyangae sp. nov . and H. viridis . It differs from those species where the slower, pulsed part of the call has five or more pulses: H. friedemanni , H. igbettensis , and H. poweri . The initial note consists of eight pulses, while the superficially similar call of H. rwandae sp. nov . has an initial note consisting of 13 pulses. FIGURE 10. Advertisement calls of H. howelli Arusha (left), H. igbettensis Comoé National Park, Ivory Coast (center) and H. inyangae Rhodes Dam (right). The shark-like profile of the snout distinguishes it from species with truncated or rounded snouts; H. acuticeps , H. adspersus , H. friedemanni sp. nov . , H. igbettensis , H. jacobseni sp. nov . , H. lupiroensis sp. nov . , H. nasutus , H. poweri , H. rwandae sp. nov . and H. viridis . The foot has at least one phalanx free of webbing on every toe. This distinguishes it from species where at least one toe is webbed to the disc, at least on one side: H. adspersus , H. benguellensis , H. friedemanni , H. jacobseni sp. nov . , H. lupiroensis sp. nov . , H. nasutus and H. rwandae sp. nov .. It also differs from those species that have less than one phalanx free, on at least one toe: H. acuticeps , H. igbettensis , H. inyangae sp. nov . , H. poweri , H. dartevellei and H. viridis . Description of Holotype . Body slender, widest at temporal region, slightly tapering to groin; head comparatively small (HL/SUL 0.32, HW/SUL 0.31), not wider than trunk, slightly longer than wide (HL/HW 1.03); snout top flat, tip of snout rounded (SL/HL 0.48), from above the snout is triangular with a rounded tip ( Fig. 6 ), considerably projecting beyond lower jaw with a shark-like profile, wider than long (SL/EE 0.76); canthus rostralis rounded, almost straight-lined from eye to just beyond nostril, slightly convex near tip of snout; loreal region almost vertical, slightly concave; nostril directed laterally; situated much closer to tip of snout than to eye (EN/NS 2.00), separated from each other by distance nearly equal to distance between eye and nostril (NN/EN 1.06); eyes directed anterolaterally, moderately protruding, relatively small (ED/HL 0.36); eye diameter much shorter than snout (ED/SL 0.74); interorbital distance much wider than upper eyelid (IO/EW 0.96), and greater than internarial distance (IO/NN 1.59); tympanum not visible externally; upper jaw with dentition; teeth on premaxilla larger than those on maxilla; choanae small, oval, located far anterolaterally at margins of roof of the mouth; vomer processes and teeth absent; tongue long 4.6, and narrow (2.3 at widest point), free for about three-fourths of length, bifurcated distally for about one-third of length; median lingual process absent; vocal sac single, median, subgular, yellow in colour; gular flap consisting of two areas of thickened skin, the anterior thicker, cream coloured, and the posterior thinner, smooth and white; vocal sac aperture on each side of the mouth, situated lateral from and close to base of tongue, slit-like, long. Dorsal surfaces of head, trunk and limbs generally smooth; ventral surface of limbs and gular smooth, chin and abdomen slightly more areolate. Fore limbs slender; hand moderately large (HND/SUL 0.24); tips of fingers enlarged into broad oval disks, each with circummarginal groove; relative length of fingers: I<II <IV <III; subarticular tubercles rounded, well developed, with one on fingers I and II, two on fingers III and IV, with proximal tubercle on finger IV hardly discernible; webbing formula of the hand I 2 +– 2 II 2–2.75 III 2 –2.5 IV ; thenar tubercle indistinct, low; palmar tubercles absent; metacarpals without supernumerary tubercles; nuptial pads or asperities absent. Hind limbs slender, moderately long (LEG/SUL 1.36); tibio-tarsal articulation passing level of tip of snout when legs are adpressed to body; tibiofibula moderately long (TFL/SUL 0.56), longer than thigh (TFL/THL 1.27); heels overlapping each other considerably when knees are flexed and thighs are held laterally at right angle to body; foot shorter than tibiofibula (FOT/TFL 0.70); relative length of toes: I<II<III<V<IV; discs of toes smaller than those of fingers; subarticular tubercles: one on toes I and II, two on toes III and V, and three on toe IV; pedal webbing formula ( Fig. 7 ) I 1– 2 II 2– 1 III 1–1.5 IV 1.5–1.25 V ; inner metatarsal tubercle small, oval, prominent; outer one indistinct. Colouration in life . Holotype was a brown-green overall, with white lateral stripes running from the snout, through the top of the eye, to the groin. The lateral stripe is lined with irregular large melanophores. The top of each eye has a smudge of golden brown. The back has many small dark melanophores, with a few irregularly spaced larger pigment cells. The limb joints are pale green, with the limbs showing a brown tinge. The fingers and toes are green with yellow tips. The skin is smooth above and on the limbs, while the ventrum is rough with large flat granules. Colouration in preservative . The dorsal pattern shows two pale lateral stripes edged with large dark melanophores, filled with opaque white pigment. The head and dorsum is uniformly speckled with small melanophores, with a few irregularly spaced larger pigment cells. A thin dark line runs from the nostril to the eye Paratype variation . The female has a similar body shape to the holotype , Skin texture the same as the holotype . Colour in preservative: pale yellow background with large irregular melanophores on the dorsum, overlaying a uniform fine speckling. A dark line runs from eye to eye below the snout tip, running through the nostril. In life the body is pale green with yellowish sides, with darker leaf green around the eyes. The top of the eye has a brown smudge. The line running from eye to eye below the snout tip is reddish brown, with a faint brown band around the top of the snout. The irregular large black spots are less dense posteriorly. The tibia has many large melanophores, with very small speckles on the forearm. The snout profile is rounded, with the nostrils behind the tip. Paratype measurements are included in Appendix 2. Advertisement call . The call is a harsh insect-like chirp. Males call from elevated positions on vegetation ( Fig 5 ). See Table 3 for a summary of call parameters. Eggs and tadpoles . Lötters et al . (2004) found egg clutches attached to submerged vegetation. The larvae are omnivorous, found in quiet water. Habitat . The type locality was a pond of roughly 20 m x 40 m with deep clear water. Along the periphery were dense stands of Typha sp. where the frogs were present from water level to about one meter above water level. Other species present included Amietia angolensis . In Kakamega, H. cinnamomeoventris , H. kivuensis , H. lateralis and H. viridiflavus were present (Lötters et al . 2004) Etymology . We have pleasure in honouring Kim M. Howell for his contributions to East African zoology, made during a long career at the University of Dar-es-Salaam. Remarks. The species is known from western Kenya , and southern and northern Tanzania . Due to its wide range and large populations, we suggest that it be regarded as Least Concern in terms of the IUCN criteria.