Hyperolius viridiflavus (Duméril & Bibron, 1841)

Channing, Alan, 2022, Colour patterns to sequences: a perspective on the systematics of the Hyperolius viridiflavus group (Anura: Hyperoliidae) using mitochondrial DNA, Zootaxa 5134 (3), pp. 301-354 : 320-325

Hyperolius viridiflavus (Duméril & Bibron, 1841)

Eucnemis viridi-flavus Duméril & Bibron, 1841 . Syntypes MNHNP 412 , 4599 , NHMW 22896 , “Abyssinie”. Adwa , Ethiopia. Back green with yellow spots, limbs dark pink, ventral surfaces yellow with small red spots.

Rappia bayoni Boulenger, 1911 . Syntypes MSNG and BMNH 1947.2.9.32–36, Entebbe , Busso , Bululu , Jinja and Kabulmuliro , Uganda. Synonymy by Laurent (1950). Pale brown back, with a dark lateral band edged with white, sometimes with a similar colour vertebral band, and a similar band along the outer limb surfaces, which are usually brown or dotted with brown.

Hyperolius kwidjwiensis Ahl, 1931 . ZMB 52449, “ Insel Kwidjwi im Kivu-See” Idjwi Island, Lake Kivu, DRC. Synonymy by Laurent (1952). Colour in alcohol: Back pale yellow with a thin brown band running from the nostrils to the groin. This band becomes the colour of the back along the body, leaving two thin dark margins running backwards from the level of the eye. Tibia the same colour as the body, with a darker brown stripe.

Hyperolius variabilis Ahl, 1931 . ZMB 36122, “Deutsch-Ost-Afrika”. Bukoba, Tanzania. Synonymy by Schiøtz (1975). Colour in alcohol: Back silvery grey to white, with highly variable red-brown or black-brown markings. These are reproduced here as part of Fig. 3 , after Ahl (1931, fig. 173), drawn from Tornier (1896, pl. 4) ( Tillack et al. 2021). Ventral surface pale with reddish spots.

Hyperolius punctatissimus Ahl, 1931 . ZMB 39013, “Bukoba”, Tanzania. Synonymy by Laurent (1952). Colour in alcohol: Back pale grey with many small dark spots or flecks, that may cover the back to produce a uniform dark grey colour. A pale line runs from the upper lip along the side of the body to the upper leg, demarcating the dark back. Limbs similarly patterned.

Hyperolius kandti Ahl, 1931 . ZMB 46526, “Kivu-See”. Lake Kivu, DRC. Synonymy by Laurent (1947). Colour in alcohol: Uniform beige back and sides. a thin dark line from nostril to eye that broadens into a lateral brown band to the flank. Tibia with dark flecks.

Hyperolius schubotzi Ahl, 1931 . Type unknown. “Kissenji”, Rwanda. Synonymy by Laurent (1947). Colour in alcohol: Back grey-blue, covered densely with small dark spots or vermiculations. Upper surfaces of limbs as for the back. Throat pale with small round spots, belly yellow, hidden surfaces of legs red.

Hyperolius wettsteini Ahl, 1931 . ZMB 36103, “Bukoba”, Tanzania. Synonymy by Laurent (1952). Colour in alcohol: Back and sides violet-grey, with large dark violet flecks arranged in longitudinal rows. Ventral surfaces pale yellow, with brown stipples on the throat.

Hyperolius phrynoderma Ahl, 1931 . Syntypes ZMB 39000 and ZMB 77734–36, “Zentrales Deutsch-Ostafrika ”, corrected to north-eastern Tanzania ( Tillack et al. 2021). Provisionally placed as a synonym of H. viridiflavus ( Tillack et al. 2021) . Colour in alcohol: Pale yellow all over.

Hyperolius karissimbiensis Ahl, 1931 . ZMB 46525, “Bambusurwald und Waldwiesen ca. 2400 m hoch, beim Dorf des Mhcabu Gahama am Karissimbi”, Mhcabu Gahama village on Mt Karissimbi, Rwanda. Synonymy by Laurent (1952). Colour in alcohol: Back pale grey with fine blue stipple. A thin dark line runs from snout tip, below the canthus rostralis to under the eye. It starts again on the flank and runs to the vent. The dark line is bordered by white. A dark vertebral stripe. Dark longitudinal line run from between the eyes, interrupted near the armpit, continuing to the vent. These lines have pale borders. Upper surfaces of limbs yellowish with a dark longitudinal line.

Hyperolius mohasicus Ahl, 1931 . ZMB 36094, “Mohasi-See, Ruanda ” Muhasi Lake, Rwanda. Synonymy by Schiøtz (1975). Colour in alcohol: Back, sides and upper surfaces of limbs white with many moderately large, rounded or long reddish marks, arranged in longitudinal rows. Small bright red-brown warts present.

Hyperolius multicolor Ahl, 1931 . ZMB 39002, 39005, 74953–74956. “Bambusurwald und Waldwiesen ca. 2400 m hoch, beim Dorf des Mhcabu Gahama am Karissimbi” Mhcabu Gahama village on Mt Karisimbi, Rwanda. Synonymy with Hyperolius karissimbiensis by Laurent (1950). Colour in alcohol: Head and shoulder yellowish to reddish, back red-brown to brown. A dark brown quadratic mark between the eyes, a thin blue vertebral stripe from the shoulder blades to the sacrum. A large dark brown lateral marking between the limbs reaches up to the level of the sacral vertebrae, with a wide black border. A white to yellow regular stripe runs from the level of the sacrum to the vent.

Hyperolius macrodactylus Ahl, 1931 . ZMB 39100, “Kivu-See” Lake Kivu, DRC. Synonymy by Laurent (1947). Colour in alcohol: Back and sides bright yellow, with many irregular longitudinal dark brown markings forming a marbling. The upper surfaces of the limbs similarly coloured.

Hyperolius flavoguttatus Ahl, 1931 . ZMB 39011, “Bukoba”, Tanzania. Synonymy by Laurent (1952). Colour in alcohol: Dark brown back with large numbers of round spots more or less in lines. These were bright yellow in life. Upper surfaces of limbs similarly coloured.

Hyperolius monticola Ahl, 1931 . ZMB 39010, “Niansa, Ruanda, 1500 m hoch” Nyabisundu , Nyanza District , Rwanda. Synonymy with Hyperolius variabilis by Laurent (1943). Colour in alcohol: White above, with four longitudinal lines of small brown markings. Upper surfaces of limbs similar.

Hyperolius oculatus Ahl, 1931 . ZMB 58570, Balaibo, DRC. Synonymy with H. viridiflavus pachydermus by Laurent (1952). Colour in alcohol: Grey-brown above, with many irregularly spaced pale brown spots with red-brown centres. Hidden surfaces of limbs bright red. In life the back is green with red spots with yellow borders.

Hyperolius stuhlmanni Ahl, 1931 . ZMB 13008, “Vitschumbi, Südende des Albert-Eduard-See’s” Witschumbi, Lake Edward, DRC. Synonymy by Schiøtz (1975). Colour in alcohol: Pale above, on the sides and upper surfaces of limbs, with many irregular short dark wormlike lines that divide and intertwine. There are also some paler lines in between the darker markings.

Hyperolius irregularis Ahl, 1931 . ZMB 36105, ZMB 75606, “Mohasi-See, Ruanda ” Muhasi Lake, Rwanda. Synonymy by Schiøtz (1975). Colour in alcohol: Silver-grey above, on the sides and on upper surfaces of limbs, with more or less large, rounded, or elongated dark to red brown markings.

Hyperolius koehli Ahl, 1931 . ZMB 26089, “Kissenji, Deutsch-Ost-Afrika”, Kissenji, Rwanda. Synonymy by Laurent (1950). Colour in alcohol: Uniform dark brown above.

Hyperolius taeniolatus Laurent, 1940 . MRAC 39471, “Lacs Mokoto” Mokoto Lake, DRC. Preoccupied by Hyperolius taeniolatus Bocage, 1895 . Synonymy with H. viridiflavus bayoni by Laurent (1950). Colour in alcohol: Upper surfaces dark, with hidden surfaces pink. Head and tibia with pink vermiculation, oriented longitudinally. Tarsus and toes pink with black flecks. Ventral surfaces pale with black stipple.

Hyperolius ornatus Laurent, 1940 . MRAC 3836, Rutshuru, DRC. Synonymy by Laurent (1972). Colour in alcohol: Back dark with pale reticulation and red dots along the flanks. Upper limbs with large dark spots.

Hyperolius schubotzi ruandensis Laurent, 1943 . MRAC 38371, “Nyakatare, Ruanda ” ( Rwanda). Synonymy by Laurent (1983). Colour patterns very diverse, with dark irregular marbling arranged longitudinally.

Hyperolius destefanii Scortecci, 1943 . Type lost ( Blackburn & Scali 2014). “Nargi”, Ethiopia. Synonymy by Schiøtz (1999). Colour description from Schiøtz (1999): “Dorsum green to bluish green, unmarked or with small dark blue or black dots and freckles; posterior face of thigh iridescent pale blue to purple with blackish speckling”.

Hyperolius karissimbiensis xanthogrammus Laurent, 1950 . MRAC types unknown. Paratypes in LACM. “Cyumbe, Marais de la Mulindi (alt. 1.950 m.), Territoir de Biumba, Ruanda.” Mulindi Swamp, Rwanda. Synonymy by Laurent (1952). Back pale beige to red-brown, with fine yellow to orange dots and vermiculation arranged in three longitudinal lines.

Hyperolius karissimbiensis françoisi Laurent, 1950 . Type in MRAC, paratypes in LACM, “ Bururi alt 1900–1950m, arrondissement de Bururi ”, Bururi, Burundi. Synonymy by Laurent (1952). Back with a pale vertebral stripe, two lateral-dorsal parallel lines and another between the eyes. An oblique line on the tibia.

Hyperolius karissimbiensis intermedius Laurent, 1950 . MRAC B 80021.3242 “Marais Rugushu, Kayanza, alt 1900m, terr. de Ngozi ”, Rugushu Swamp, Burundi. Synonymy by Laurent (1952). The pattern is intermediate between H. karissimbiensis xanthogrammus and H. k. françoisi. A pale-yellow interorbital bar and a transverse yellow bar over the scapula, in addition to the patterns described above.

Hyperolius viridiflavus hybridus Laurent, 1951 . MRAC B 80021.3865 – 3883 , “Etang de la Mukura, alt. 1700 m. près d’Astrida” Mukura pond (= Huye), Rwanda. Colouration variable, with a red thigh.

Hyperolius viridiflavus mwanzae Schiøtz, 1975 . Swamp north of Mwanza, Tanzania. Phase F translucent green with or without bluish spots. No red pigmentation.

Hyperolius burgeoni De Witte, 1921 and Rappia rossii Calabresi, 1925 were provisionally removed from the synonymy of H. viridiflavus as both occur in northern DRC where the H. viridiflavus clade has not been recorded, and placed in the synonymy of H. parallelus . Hyperolius viridiflavus angeli Laurent, 1951 from the Central African Republic was removed from the synonymy of H. viridiflavus which does not occur north of the Congo Basin and placed in the synonymy of Hyperolius nitidulus .

Altogether 28 sequences were available from Uganda, northern Tanzania, the Kenyan highlands, Burundi, Rwanda, and Ethiopia. The minimum uncorrected p- distances from other clades were 4.2–7.6% ( Table 2 ). The sequences were reported in GenBank as Hyperolius viridiflavus , H. v. viridiflavus , H. v. variabilis , H. v. destefanii , and H. v. bayoni .

The earliest species description in this complex is Hyperolius viridiflavus Duméril & Bibron, 1841 , from Adwa in Ethiopia. Only one clade has records from Ethiopia, and this clade is assigned to H. viridiflavus ( Fig. 4 ). See Table 3 for localities of synonyms. The map reflects the distribution in Ethiopia reported in Largen & Spawls (2010).

The most common pattern elements in the descriptions of the types included in H. viridiflavus are small blue, black or red dark spots (26%), with the next most common elements being marbling on the back (22%), a dark lateral band (19%), and various markings arranged in longitudinal rows (19%). The percentages are not additive, as some individuals share pattern elements. Many of the descriptions were based on preserved material, and a large number of colour patterns is expected when fresh material is examined. Figure 3 illustrates some of the patterns recognised by Laurent (1983) and Ahl (1931) for material they described, here recognised as H. viridiflavus . This sample indicates the problems of identification based on colour patterns.

Lötters et al. (2004) illustrate a call (as H. viridiflavus ) from Kakamega Forest, Kenya with a distinct pulsed structure and an emphasised frequency of 2971 Hz. A specimen from the same locality was sequenced ( AY323920 ) ( Lötters et al. 2004) and found within the H. viridiflavus clade. An advertisement call from Kitale, Kenya consists of a brief whistle with an emphasised frequency of 2600–3000 Hz ( Schiøtz 1975 as H. v. viridiflavus ). The advertisement call of a specimen from Sango Bay, Uganda, consists of a very brief note with an emphasised frequency of 2400 Hz ( Schiøtz 1999).

Figures

FIGURE 3. Colour patterns of some of the variation recognised in taxa now included in H. viridiflavus. After Laurent (1983): 1–9, 11–13 Hyperolius karissimbiensis françoisi; 10, 14, 16–18 Hyperolius viridiflavus xanthogrammus; 15, 19–26 Hyperolius viridiflavus hybridus. After Ahl (1931): 27–31 Hyperolius variabilis. Ahl’s illustrations were taken from Tornier (1897).

FIGURE 4. Localities of sequences (black circles), type locality (star) and location of junior synonyms of Hyperolius viridiflavus. Locality codes are explained in Table 3.