Colour patterns to sequences: a perspective on the systematics of the Hyperolius viridiflavus group (Anura: Hyperoliidae) using mitochondrial DNA Author Channing, Alan text Zootaxa 2022 2022-05-11 5134 3 301 354 journal article 55577 10.11646/zootaxa.5134.3.1 ce262ea0-57d5-4978-9c39-6ec9169b3135 1175-5326 6538259 E8B09B63-2FDF-4257-861C-E23D38A1CDE8 Hyperolius parallelus Günther, 1858 . Hyperolius parallelus Günther, 1858 . Syntypes BMNH 1947.2.9.41–43 “Süd Afrika”. Boulenger (1882) corrected the locality for the northern specimens to Ambriz , Angola . Above dark brown with three white parallel bands. Upper lip yellowish. Hyperolius marmoratus var. angolensis Steindachner, 1867 type in NHMW, “ Angola ”. Synonymy by Broadley 1971 . Back and upper surfaces of limbs brown. Back with irregular yellow flecks or reticulation, or with a pair of yellow lateral bands and irregular yellow flecks in the middle of the back. Limbs with yellow spots and lines. Hyperolius insignis Bocage, 1868 . Syntypes MBL (now MUHNAC) T. 21–164, “Benguella”, type localities corrected to São Salvador and Novo Redondo, and ZMB 6462 to Benguela , Angola by Perret 1976 . Synonymy by Boettger (1888) . Colour in alcohol: Overall yellow tinted with red. Two wide blue-black bands with bright red edges run from the head to the vent. A similar colour band runs from behind the eye to the shoulder, continuing interrupted to the vent. The upper lip has small blue spots with red borders, with similar markings on the upper limbs. Hyperolius toulsonii Bocage, 1868 . MBL (now MUHNAC) T.27–275, “Loanda” ( Luanda , Angola ). Type destroyed in 1978 fire. Synonymy by Perret, 1976 . Colour in alcohol: back overall grey, with three wide longitudinal white bands. Thighs uniform grey, with forearms and thighs with large rounded white markings. Hyperolius huillensis Bocage, 1873 . MBL (now MUHNAC) 2-166 destroyed in 1978 fire, “Huilla”, Angola . Placed in the synonomy of H. parallelus as sequences from Huila are embedded in the H. parallelus clade. Back and upper surfaces of limbs, excluding the thighs are red with yellow spots, most with black borders. Ventral surfaces and thighs a uniform pale yellow. Hyperolius vermiculatus Peters, 1882 . Syntypes ZMB 10050, “ Malanje ”, Angola . It was initially placed as a synonym of H. marmoratus by Laurent (1952) , but H. marmoratus only occurs on the east coast of southern Africa. Back and upper surfaces of limbs signal red with yellow vermiculation, with black pigment sometimes visible. Rappia plicifera Bocage, 1893 . Syntypes MBL (now MUHNAC) T.22-209 destroyed in 1978 fire. Syntypes NHMW 22895 , Caconda, Duque de Bragança , Angola . Synonymy by Perret (1976) . Colour in alcohol: Above marbled and spotted in brown-violet or red on a grey base. Lower surfaces and thighs a uniform bright yellow. Rappia marmorata var. taeniolata Bocage, 1895 . Types in MBL (now MUHNAC) considered destroyed. “ Duque de Bragança ”, “Huilla”, “Caconda” and “Cahata”, Angola . Synonymy by Laurent (1952) . Back and flanks burgundy with various irregular yellow lines and spots, with black borders. Rappia marmorata var insignis Bocage, 1869 . Syntypes MBL (now MUHNAC) T 21–164 destroyed by fire, surviving syntype ZMB 6462 ( Tillack et al . 2021 ). St. Salvador du Congo, Angola north of Quanza, Novo Redondo, Dombe, Angola . Synonymy by Perret (1976) . Back black with three longitudinal white or yellow bands with red edges. Rappia burgeoni De Witte, 1921 . MRAC 585, “Madyu (Uelé)” DRC . See the section on obscure localities, above. Watsa, Upper Uelé, DRC . This taxon from the northern DRC was regarded as a synonym of H. viridiflavus pachydermus by Laurent (1951a) . Dehling (2015) demonstrated that Rappia pachyderma Werner, 1908 was a junior synonym of Hyperolius papyri (Werner, 1908) , a species of the H. nasutus group ( Channing et al . 2013 ) and that the synonymization of several species of the H. viridiflavus group with this species by Laurent (1951) were thus unwarranted. However, the clade identified as a subspecies of H. viridiflavus by Laurent (1951) does not occur in the northern DRC , while the clade identified as H. parallelus is well represented in the northern DRC . Pale yellow above, with a dark brown lateral band from the snout tip through the eye to the vent. A band of similar colour on the tibia. A darker vertebral band present. Rappia rossii Calabresi, 1925 . Syntypes MSNM 584 “Regione dell’Alto Uellè ( Congo Belga )” Watsa, DRC . The H. viridiflavus clade is not known as far west as Watsa. See also Dehling (2015) and image of syntype in Blackburn & Scali (2014) . Above blue-grey with white tubercles with red centres. Thighs and fingers with pink speckle. Hyperolius bitaeniatus Ahl, 1931 . ZMB 39004, “Konde-Nyika, Deutsch-Ost-Afrika” (northern tip of Lake Malawi ), Tanzania . Placed as a synonym of H. marmoratus mariae by Laurent (1952) but here placed in H. parallelus as the H . mariae clade does not occur in the northern Lake Malawi area. Colour in alcohol: Above light brown, with two yellow or white longitudinal stripes. A dark lateral band runs between the arms and leg. Hyperolius nyassae Ahl, 1931 . ZMB 39006, “Langenburg” Lumbira, Tanzania . Placed as a synonym of H. marmoratus nyassae ( Laurent 1952 ) , but here placed in H. parallelus as the H . marmoratus clade does not occur in the northern Lake Malawi area. Colour in alcohol: Back and upper surfaces of limbs white to yellow or brown. Some individuals have a large triangular mark between the eyes, pointing backwards. A thin dark line runs from the nostril to the eye, where it widens to become a lateral band that ends in the middle of the body. A pair of large markings between the flank and the sacrum, with another pair over the vent. The slightly darker markings are thinly edged in white or yellow. The tibia has a similar transverse marking. Hyperolius fuelleborni Ahl, 1931 . ZMB 86128–86131, “S’ongwe” Songwe, Tanzania , ZMB 85972–85973, “Miramba bei Langenburg”, Miramba near Lumbira, Tanzania , ZMB 77465–77468, “Langenburg” Lumbira, Tanzania , ZMB 85929–85963, 85974–85988, 86017, 86132–86137, 90929–90948, “Rugwe” (Rungwe village, Mbeya Region , Tanzania ). Placed as a synonym of H. marmoratus nyassae by Laurent (1952) , but here moved to H. parallelus as the H . marmoratus clade does not occur in the northern Lake Malawi area. The specimens ZMB 71184–71186, “Neu-Helgoland” Papya Island, Malawi , are retained in H. marmoratus . Colour in alcohol: Pale above with more or less distinct dark brown to black markings that overlap to form a marbled pattern. Hyperolius marungaensis Ahl, 1931 . ZMB 10736, “Marunga, Angola ”, corrected to northern Marunga, DRC by Tillack et al . (2021) . It was considered a synonym of H. marmoratus by Laurent (1961) . The clade identified as H. marmoratus is restricted to the east coast of southern Africa. The colour pattern ( Ahl 1931 : fig. 226) consists of a dark back with three large round markings on the head, five large circular markings arranged in a vertebral line, and another five longer white markings behind each eye running to the flank. Upper lip with a broad white band. Hyperolius decoratus Ahl, 1931 . Lectotype ZMB 36112, “Longa” (=Cuito Cuanavale), Angola . Regarded as a synonym of H. marmoratus (Perret 1962) , but that clade is restricted to the east coast. Colour in alcohol: above wine-red, with many more or less large round, white markings with black borders. Three broad longitudinal stripes, the first running from snout tip to vent, the other two run from the side of the snout to the flanks. Similar patterns are found on the visible surfaces of the limbs. Hyperolius microstictus Ahl, 1931 . ZMB 36100, ZMB 77762, “Longa, oberhalb Minnesera” (=Cuito Cuanavale), Angola . Synonymised with H. marmoratus decoratus by Perret (1962) but that clade is restricted to the east coast. Colour in alcohol: Above and on the visible parts of the limbs when sitting, bright wine-red with many irregular, pointed white markings. Hyperolius decipiens Ahl, 1931 . ZMB 39003, “Westliches Russisi-Ufer und Nordwestufer des Tanganyika-see’s” (Rusizi River west bank and NW Lake Tanganyika, Tanzania ). Synonymy with H. marmoratus argentovittis by Laurent (1952) but here moved to H. parallelus as the H . marmoratus clade does not occur in the northern Lake Malawi area. Colour in alcohol: Above brown to blue-grey without markings. Upper lip with white border. Hyperolius nossibeensis Ahl, 1930 . ZMB 50098–50100, “Nossi-Bé” Madagascar . Corrected by Tillack et al . (2021) to Lunda, Angola . Originally placed as a synonym of H. marmoratus , which is restricted to the east coast. The Angolan coastal locality places it within the distribution of the H. parallelus clade. Colour in alcohol: Above red-brown with a number of silver-white flecks and lines, that flow together to form three longitudinal bands, that may be interrupted and indistinct. The side of the head and body similarly marbled. Hyperolius callichromus Ahl, 1931 . ZMB 78576, “Westliches Russisi-Ufer und nordwestufer des Tanganyika-see’s” (Rusizi River west bank and NW Lake Tanganyika, Tanzania ). Synonymy with H. marginatus by Wieczorek et al. (2000) but here moved to H. parallelus as the H . marginatus clade does not occur in the northern Lake Malawi area. Colour in alcohol: Above deep red-brown, with a wide white vertebral band with black border, that runs from level of nostrils to vent. A similar band runs laterally from upper eyelid to vent. The longitudinal bands may be broken into irregular shapes. Upper lip white, sides with a wide red-brown stripe. Illustrated by Tillack et al. (2021 , fig. 6). Paratypes from Dar es Salaam ZMB 85869–85872 ( Tillack et al . 2021 ), are assigned as synonyms of H. mariae . Hyperolius erythromelanus Monard, 1937 . Syntypes in LCFM. Sangev, Angola . Synonymy with H. marmoratus huillensis by Laurent (1952) . The H. marmoratus clade does not occur in Angola . Upper surfaces dark red, almost black with many small white spots, arranged in lines edged with black. Upper surfaces of limbs the same colour as the back. Hyperolius angolensis quarrei Laurent, 1943 . MRAC 37366, “Lusuku (Lomami)”, DRC . Synonymy with H. marmoratus by Laurent (1952) , but that clade is restricted to the east coast. Colour in alcohol: Dorsal surfaces yellow to grey, with rust or red-brown irregular marbled markings. Upper surfaces of limbs with similar markings. Hyperolius latirostris Laurent, 1943 . MRAC 1394, “Kasai”, DRC . Considered a subspecies of H. marmoratus by Laurent (1952) , but that clade does not extend as far west as the DRC . Back and parts of the limbs visible at rest, red-brown, dappled with pale brown and grey, with a violet tinge to the head. Tibia with a trace of brown. Hyperolius brieni Laurent, 1943 . MRAC 5445, “Nyonga (s/Lac Upemba)” DRC . Schiøtz (1975) placed it as a synonym of H. marginatus , but the type locality is close to sequenced material of the H. parallelus clade, with which it is regarded as a synonym. Hyperolius fuliginosus Laurent, 1943 . MRAC 35166, “Kasenga (Katanga)” DRC . Synonymy with H. marmoratus by Schiøtz (1975) . Hyperolius marmoratus does not occur in the DRC , but the locality is close to sequenced material of H. parallelus . Colour in alcohol: Grey-brown above, on the forearm and tibia, with dark brown marbling with indistinct edges. A pale vertebral band and two indistinct lateral bands are present. Limbs finely dotted or with small black spots. Hyperolius hutsebauti Laurent, 1956 . MRAC 52495, “Ibembo, Uelé” DRC . Sequences of specimens identified as H. hutsebauti are embedded in a clade identified as H. parallelus . Earlier studies that recognised H. hutsebauti (e.g. Bell et al . 2017 ) did not compare material with H. parallelus . Female colouration consists of a beige background with dark marbling edged with red. FIGURE 7 . Localities of sequences (black circles), type locality (star) and location of junior synonyms of Hyperolius parallelus . Locality codes are explained in Table 3. Hyperolius marmoratus epheboides Laurent, 1957 . IRSNB 1.158, “Mukana, marais près de Lusinga 1.810 m ” (Mukana swamp near Lusinga) DRC . The H. marmoratus clade is restricted to the east coast, while the type locality is close to sequenced material in the H. parallelus clade. Colour in alcohol: A beige background, with black markings on the flanks, the side of the head, and on the upper surfaces of the limbs. These are intertwined with longitudinal bright red markings. In life the ventral surface has brilliant red markings. Hyperolius marmoratus alborufus Laurent, 1964 . MD 5769, “Cazombo, Alto Zambeze, Moxico , Angola ”. The holotype is figured in Ceríaco et al . (2020) . The H. marmoratus clade is restricted to the east coast, while the type locality is close to sequenced material in the H. parallelus clade. Back with red marbling, covering also the upper arm and tibia. The sides of the tibia and the toes with small black spots. A total of 57 sequences were available from Angola , Burundi , Rwanda , DRC , northern Zambia , and northern Namibia . The minimum uncorrected p- distances from other clades were 2.2–6.5% ( Table 2 ). The sequences were reported in GenBank as H. angolensis , H. parallelus , H. huillensis , H. viridiflavus and H. v. argentovittis . The sample is distributed from northern Namibia , through Angola , across to southern Lake Tanganyika, Burundi , Rwanda and northern DRC ( Fig. 7 ). The type localities of taxa now regarded as junior synonyms of H. parallelus are listed in Table 3 . Hyperolius parallelus Günther, 1858 was described from “Süd-Afrika”. Boulenger (1882) corrected the locality for the northern specimens to Ambriz, on the northern coast of Angola . Only one clade has a distribution that includes coastal Angola , and it is assigned to Hyperolius parallelus . The most common pattern elements in the descriptions of the types included in H. parallelus are dorsal marbling (39%), or a pale lateral band (30%), or a pale vertebral stripe (30%), followed by small yellow spots sometimes with red centres or black edges (17%). The percentages are not additive, as the pattern elements may be shared. The underside may be red, sometimes with red speckles on the throat. Calls from Humpata , Angola , are brief ( 0.03 s ) at an emphasised frequency of 1189–2153 Hz.