List of amphibian species (Vertebrata, Tetrapoda) of Burkina Faso

ABSTRACT We related the first commented list of the amphibian species of Burkina Faso. To obtain contemporary data, we investigated six sites from July 2017 to September 2018. The survey is unique for West Africa in combining a variety of different habitat types, e.g. Sahelian areas, grassland and woodland savannahs, floodplains, gallery forests and agricultural sites. Animals were found at varying spatial scales by opportunistic visual encounter surveys after sunset supplemented with acoustic searching. Further data were based on museum vouchers collected between the years 1959 and 2011 and deposited in European and American museums, and the literature review focusing on the country species. We listed 36 anuran species from 11 families. Surprisingly seven taxa, namely Arthroleptis poecilonotus Peters, 1863, Afrixalus vittiger (Peters, 1876), Afrixalus weidholzi (Mertens, 1938), Kassina cassinoides (Boulenger, 1903), Ptychadena schillukorum (Werner, 1908), Hyperolius lamottei Laurent, 1958 and Amnirana albolabris (west) (Jongsma et al. 2018), were new country records. A few rare, hard to record or little known species, including Arthroleptis poecilonotus, Hyperolius lamottei, Xenopus tropicalis (Gray, 1864) and Amnirana albolabris (west) can be confirmed. The origin of a specimen of Sclerophrys mauritanica (Schlegel, 1841) mentioned as coming from Burkina Faso deposited in the collections of MNHN must be considered as an error. We briefly discussed the taxonomy and indicated the habitats of all species mentioned in this country so far. The discovery of several new country records highlights that the amphibian fauna of Burkina Faso is still incompletely known and that many poorly explored sites may still harbour a high diversity.


INTRODUCTION
Assessment of biodiversity requires the collaboration with several other disciplines that are involved not only in species protection, but also for sustainable conservation (Thiombiano et al. 2006). In Burkina Faso, since independence in 1960, many areas have been designated as national parks or nature reserves to preserve biodiversity. These areas are the country's ultimate biodiversity protection sites (SP/CONEDD 2010;Kangoyé 2013). In order to preserve and ensure the sustainable management of this bio-diversity, it is important to know more about it, in particular, as natural habitats are increasingly threatened by the expansion of human populations and their activities (Maydell 1983). In addition, this strong environmental disruption is amplified by frequent soil erosion (Cesar et al. 2011) and changing climate (Kambiré et al. 2015). Because frogs and toads have diphasic life-cycle and semi-permeable skin, they are likely to be more sensitive to habitat disturbances and indicative of local sources of wetland contamination than are most other vertebrates (Wells 2007;Baillie et al. 2010). Amphibians could be the most affected vertebrates in the context of savannah habitat disturbance because of their limited mobility and high skin permeability. In comparison to other West African countries (Benin, Ivory Coast, Ghana, Guinea, Nigeria, Senegal and Togo), Burkinabe amphibian fauna is poorly studied. However, some authors had reported the presence of amphibian species (Lamotte 1967a;Schiøtz 1967;Lamotte & Xavier 1981;Böhme et al. 1996;Rödel 2000;Böhme & Heath 2018). Mohneke et al. (2010a) recently reported 17 species in Burkina Faso. Further data provided by  and  increased the country checklist up to 25 amphibian species, thus being very low to expected species richness.
The objective of this study was to provide an updated list of all amphibian species reported and collected in Burkina Faso. We further present specimens examined from some museum collections and literature information.

Study area
Burkina Faso covers an area of 274.200 km 2 and is a landlocked Sahelian country situated almost within the heart of West Africa.
It is located between 9.33333° S and 15.05000°N; -5.03000°W and 2.33333°E. Along its northern border, the country is limited by Niger and Mali, while Ivory Coast, Ghana, Togo and Benin limit the southern parts (Dembélé 2010; Fig. 1). The country is characterized by a Sudano-Sahelian climate with two annual seasons: a dry season extending from October to April, followed by a rainy season between May and September. Furthermore, three climatic zones extend from the south to the north: the Sudanese zone (between 10.00000°N and 11.50000°N), the Sub-Sahelian zone (between 11.50000°N and 14.00000°N) and the Sahelian zone (north of 14.00000°N). The Sudanese zone has an annual rainfall ranging from 900-1200 mm while respective annual rainfalls for the Sub-Sahelian zone and the Sahelian zone are comprised between 600-900 mm and less than 600 mm (Dembélé 2010;Akoudjin et al. 2016).
The Sahelian vegetation ranges from grassy to wooded savannahs (Ganaba 2008). In the Sudanese zone, forest islets, especially sacred groves can be found within different savannah habitats. The main rivers (Mouhoun, Nakambé, Nazinon, Comoé and Pendjari) are bordered by gallery forests widening towards the South. The country average altitude is 400 m a.s.l., reaching 125 m a.s.l. in the South-East (Pama region) and 749 m a.s.l. in the South-West (Takakourou peak) (MEE 1999). data collection Data for this study stem from three sources: literature review, museum collection and field sampling.
The species taxonomy was critically revised to be in accordance with the current state of science. We refer to the version 6.1 on 31 October 2020 of the online reference of Frost (2019) for current taxonomy. examination of muSeum collectionS Specimens from the herpetological collections of MNHN (France), ZFMK (Germany), MHNG (Switzerland) and MVZ (USA) were analysed. About 400 museum specimens were studied: 325 from MNHN, 25 from ZFMK, 40 from MHNG and 10 from MVZ.
field Sampling Field work was conducted to complete our data. Six sites across Burkina Faso were prospected from July 2017 to September 2018, in both rainy and dry seasons. Prospected areas were the National Parks of Arly and W, the Comoé-Léraba Forest, the Kou Forest, the Deux Balés National Park (protected areas), the rural areas of Pabré, Loumbila and Koubri (unprotected areas) and the peri-urban area of Dori-Yakouta (unprotected area) (Table 1). These areas were selected on the basis of vegetation cover and rainfall, the need to present faunal lists for protected areas, or particular gaps in the amphibian data for these parts of the country.
Because of the intense heat during the day, particularly in Sahelian regions, frogs and toads were mostly active after sunset. These animals were hence searched at night between 18.00-21.30 GMT. We investigated six general areas, each during seven and ten days, and applied opportunistic visual searches in various habitats such as temporary and permanent ponds, gallery forests, agricultural sites, grasslands and open savannah woodlands (Fig. 2). Systematic visual searches consisted in scraping through leaf litter, lifting rocks and logs, looking around or within burrows and termite mounds. Additional supports of acoustic signals and dip netting for tadpoles were applied (Rödel & Ernst 2004). Specimens were collected by hand and photographed. We used a hand-held GPS receiver (GPS Garmin etrex-10) to record the geographical positions of all study sites. After capture, scientific name to species or subspecies level, sex, SVL, reproductive condition, date, time and habitat characteristics (presence of water bodies, vegetation type, etc.) were recorded for each specimen. Frogs and toads were measured with dial-calipers (accuracy ± 0.1 mm) and their SVL were given in mm. Each animal not kept as voucher was released at its site of capture. Voucher specimens were euthanized humanly in a 1,1,1-Trichloro-2-methyl-2-propanol hemihydrate (MS222) solution or in a chlorobutanol and thereafter preserved in 70% ethanol. Tissue samples (muscle or liver) were conserved in 70% alcohol for future genetic studies.
The specimens were inventoried at the Laboratoire de Biologie et Ecologie Animales of the University of Joseph Ki-Zerbo. Some voucher specimens (158 specimens) and approximately 200 tissue samples were deposited at the MNHN in Paris. Released specimens are listed in the paragraph Field material.

local termS
Bouli, an artificial water body constructed to collect runoff water during the rainy season for animals is generally composed of a supply channel and a protective dike (MERH 2012). In dry season, these boulis obtain water from boreholes. A bouli is also generally deeper than a pond.  habitat. -The historical specimens and the recent samples of A. poecilonotus were from Kou Forest (Fig. 2E). At this site, males were seen at night on leaves of shrub and grass at heights varying from 0.2-1 m. Females and subadults were seen hiding in leaflitter.
taxonomic remark. -As stated in Rödel & Bangoura (2004) and Blackburn (2010), it is currently not possible to assign these West African Arthroleptis taxa with certainty to one of the various available names, as intra-specific variability equals or surpasses interspecific differences. As actually understood, A. poecilonotus has an extended distribution range, including West, Central and parts of East Africa (Frost 2019) and probably recovers a group of species. Type locality is in West Africa, in south-eastern Ghana. Further studies, in particular including topotypical material, are needed for taxonomic decisions. deScription. -20 specimens examined. Leptopelis bufonides with small to moderate size and warty skin, stocky body shape, and short legs. In contrast to most other members of that genus, the fingers with small discs on their tips. In life colouration greyish brown with dark spots, including a dark interorbital spot and elongated spots or bands on the back (Fig. 3C). These markings making almost a "m" pattern. The venter light to dark grey, with a dark throat in both sexes. For detailed descriptions, see Schiøtz (1967), Rödel (2000 and Amiet (2012).
habitat. -The species was fossorial during the day and arboreal at night. Leptopelis viridis was found in herbaceous and wooded savannahs (Fig. 2C, E). Males were caught on trees and shrubs around ponds and rivers at heights varying between 0.5-3 m. In contrast to males, females were collected on the ground of the same habitats.  -1944.143, 1951.255, 1989.3863, 1989.3864, 1989.3865, 1989.3866 deScription. -42 specimens examined. Toad with a broad and round head, a very short snout, and very well delimited, broad parotid glands, especially in females. Limbs relatively shorter than in S. maculata and S. regularis. Presence of projecting round granules in the dorsal part in all specimens. Dominant colour brownish to dark beige. Dorsal glands or granules reddish (Fig. 3F). The back of the twenty females from MHNG very dark brown or black in alcohol. The venter whitish with a light brown throat. habitat.
habitat. -This is a common species and it is found in numerous habitats, ranging from protected areas, to agricultural and irrigated land and even urban areas in Burkina Faso. deScription. -49 specimens examined. Toad, similar to S. maculata and S. regularis, but skin with very prominent warts bearing spinules, more pointed than those of the two other species. Red pattern on the rear parts of thighs (absent in three other Sclerophrys species) and smooth, kidney shaped parotid glands allowing easy identification in the field. For more information on S. xeros, see Tandy et al. (1976), Lamotte & Xavier (1981), Salvador (1996) and Rödel (2000).
habitat. -Hoplobatrachus occipitalis is usually collected near or in water (Rödel 2000). In the dry season it lives in rivers, pond banks and in irrigated wells. It is found in practically all freshwater habitats in wet season. Migrations were related in the dry season to the edge of rivers and the in wet season to surroundings of ponds (Spieler 1997). The species was observed on clayey and sandy soils. This frog is an important source of animal protein in the nutrition of local population from the south-eastern part of Burkina Faso (Mohneke et al. 2010b deScription. -15 specimens examined. Small frogs with a triangular head and a very pointed and short snout. Morphologically sturdy with strong limbs, adapted for burrowing (Fig. 4A). Skin soft and smooth (Laurent 1972;Rödel 2000). Dorsal colouration of living frogs yellowish with some dark brown spots on the back. In alcohol, yellow colour whitish dorsally and ventrally. habitat.
-Hemisus marmoratus was difficult to see during our survey periods and is probably much more abundant in convenient habitat and at the right saison. We found this fossorial species in the vicinity of a paddy field on the "Ancien barrage" edge in Koubri, on a trail leading to a small water body in W National Park. We heard the male calling under flooded grasses around a pond (1 km southwest of the Kabougou forest post office) in W National Park. The species was also found in Baboro swampy valley in Comoé-Léraba where males could be heard calling among grasses nearby a small water body in Folonzo village swampy valley on 6 August 2018. This was unusual as Hemisus usually breeds in the early rainy season or even before the rains set in (see e.g. Rödel et al. 1995;Kaminsky et al. 1999). In a floodplain near Bouliabou pond, we heard males calling and recorded three males in Arly National Park. In the Sahelian part, we captured this species during rainy weather on sandy soils close to a millet field in N'Djomga and on the roadside in Yakouta. Hemisus marmoratus is mostly fossorial, in relatively moist, loose soils and is often captured during earthworks such as plowing fields (Lamotte & Xavier 1981;Rödel 2000 habitat. -This species was usually collected on grass at a height not exceeding 0.5-1.5 m (Fig. 2D). During the day, resting animals can be found above water on plants (Lamotte & Xavier 1981;Schiøtz 1967Schiøtz , 1999. Males call at night, usually on high grasses, a few meters from the pond edges (Rödel et al. 2006 (2001). In life, specimens with a yellowish back framed by dark lateral bands with narrow yellow edges, extending from the eyes back to above the legs (Fig. 4E). Sometimes, back showing a brown and greyish pattern with very small dark spots. Dorsal coloration lighter and with less contrasting pattern at night. habitat.
-Hyperolius nitidulus was found on grasses and bushes in floodplains, in swampy valleys and farmland such as maize and paddy fields, plantain plantations and vegetable gardens. It was also found on plants above water at nearby ponds and rivers. This species inhabits shrublands, grasslands and wetlands in the Guinean and Sudanian savannahs, from central Guinea to Cameroon (Lamotte 1967b;Rödel 2000;Rödel et al. 2010a (Fig. 4F).
habitat. -Kassina cassinoides and K. fusca Schiøtz, 1967 were calling at night from holes at the base of shrubs, at the beginning of rainy season. Three of our vouchers were collected on the ground near water (in about 10-50 m distance) in June and July. One was found on a tree where it was calling (in about 100 m from the water) in August. Rödel (2000)   deScription. -29 specimens examined. According to Schiøtz (1999) and Rödel (2000), SVL of this species ranging from 29-40.5 mm in both sexes. In the observed specimens, males measure 29.8-35.5 mm and females 31.4-42.7 mm SVL. The back of living specimens of a light green-olive colouration with scattered larger and smaller darker spots (Fig. 5A).
habitat. -This species calls at night from holes at the base of shrubs. After rain these frogs may be found moving on the open ground, between grasses and bushes during the night. This species was not found in Dori and Yakouta in the Sahel region of Burkina Faso. It is a common West African savannah species, with a distribution ranging from southern Senegal to western Nigeria (Böhme et al. 1996;Schiøtz 1999;Rödel 2000;Nago et al. 2006;Segniagbeto et al. 2007 deScription. -9 specimens examined. Size within the range given by Rödel (2000). Characterized by a unique body shape and a red back (Fig. 5D). Presence of a fine dark brown vertebral line on the back. In alcohol, the red colouration getting a greyish.
habitat. -The species calls often below shrubs and from holes. In Comoé-Léraba Forest, males were collected in shrubs on the edge of a large dark scorpion hole where they were calling. It was also found on the edge of water under a tree. A female was found on an anthill ready to withdraw into a hole. The species has been reported to often occur within ant nests and scorpion burrows (Rödel & Braun 1999;Rödel et al. 2013).
habitat. -Phrynobatrachus francisci is restricted to humid habitats and is abundant in all seasons close to water. During the dry season, we collected these frogs on the edge of ponds and rivers, under pebbles and rocks ( Fig. 2A, B). It is also found near wells, fountains and cattle troughs. This species has a wide distribution in drier savannahs of West Africa (Rödel 2000; Onadeko 2016). deScription. -39 specimens examined. Voucher specimens morphologically similar to frogs described by Rödel (2000). Similar to P. francisci but the warts on the neck often less distinct in P. latifrons. Breeding males with a completely smooth skin (Fig. 5F), (Rödel 2000). A yellow vocal sac in males (black in P. francisci) and a more pronounced black lateral bands distinguishing P. latifrons from P. francisci.
-Hildebrandtia ornata was collected on garbage dumps filled after rainfalls on Kabougou River banks (W National Park). We found it as well under deadwood on the edge of a groundnut field in Koti. At Pabré, it was seen in a swimming pool in the hostel court. We saw a calling male between grasses in Arly National Park.
The frog is a fossorial species which emerges only temporarily dur- specimens. A lateral ridge usually absent or only present as a short row of discontinuous light warts. For further detailed descriptions see Lamotte & Ohler (1997) and Rödel (2000). Dorsum a grey to pale brown with numerous tiny dark brown to black spots, restricted to the longitudinal ridges. Light reddish or yellow vertebral lines may be present or absent.
habitat. -We encountered this species under grasses at the edges of ponds and on river banks. It was also found in paddy fields. In the dry season, we collected P. bibroni under rocks, deadwood and accumulated dry grass around ponds. The species was found in dry and wet savannah habitats, intermittent freshwater wetlands, rural gardens, heavily degraded forests (agricultural areas), channels and ditches (Rödel 2000). It is a common species, widely distributed in West Africa (Lamotte & Ohler 1997;Nago et al. 2006;Segniagbeto et al. 2007;Onadeko 2016;Sánchez-Vialas et al. 2017). deScription. -12 specimens examined. SVL of 34.4 mm for the single male and 38.6-39.1 mm for females and thus smaller than size given by Rödel (2000). Specimens with a pointed snout, long legs and webbing formula: I 1 -2 II 1 -2 III 1 -2 IV 2 -1 V. Supernumerary tubercles absent. On the back four pairs of continuous longitudinal folds. The median pair from between eyes to the sacrum. The second pair starting posterior to eye and ranging to lower part of the back. The third pair, shorter and between the second pair and continuous white lateral folds posterior to the eyelid to the groin. A light medio-dorsal line, from the snout to the venter and also a fine white line on the dorsal part of the leg present (Fig. 7C).  -1996.3869, 1996.3870, 1996.3871.  - .7572, 1999- .7573, 1999- .7574, 1996- .3900, 1996- .3901, 1996- .3902, 1996 deScription. -76 specimens studied. Specimens studied 27.2-34.4 mm SVL in males and 29.0-37.1 mm SVL in females; thus within the size range given by Rödel (2000) and Lamotte (1967a). Species with a moderately pointed snout and a slender body. Limbs thin and long; webbing formula: I 1 -2 II 1 -2 III 1 ½ -2 IV 2 -1 V. Supernumerary tubercles absent on toes. Three pairs of symmetrical and continuous ridges present on the back. A white, continuous lateral ridge extending from above the tympanum to the posterior part of the back. Dorsal colour pattern from brown, greenish to greyish with dark brown spots (Fig. 6B, C). Breeding males with greenish colour (Rödel 2000). Presence of a wide white, green or red vertebral band in many specimens.
-Ptychadena pumilio is ubiquitous in Guinean and Sudanese savannah and Sahelian habitats. It may even enter degraded rainforest (Rödel 2000). We found it near water bodies among grasses and sometimes in the humid areas near water bodies in depressions, as well as in flooded zones in the rainy season. In Dori, we found calling males between flooded short grasses. In the dry season, P. pumilio was observed concealing under rocks, heaps of dry grass and cracks of dry mud around ponds and river banks, in Arly and W National deScription. -2 specimens studied. Ptychadena with a compact and less slender body than P. pumilio. Limbs comparatively short; webbing formula: I 1 -1½ II 0 -2 III 1 -2 ½ IV 2 ½ -0 V. Absence of supernumerary tubercles. The back with discontinuous, partly indistinct rows of elongate warts ( Fig. 6D; Fig. 8A). A discontinuous white lateral line, extending from above the tympanum to the rear back. Dorsal colour greyish with some darker spots.
commentS. -Specimens identification based on the discontinuous dorsal ridges and their size (see Nago et al. 2006). However, in other parts of Africa, this name is applied to frogs which look completely different (larger and showing continuous dorsal ridges): see e.g. Channing (2001). Werner (1908) indicated in the original description a size ranging from 35-43 mm for the four females from Sudan.
habitat. -The two males were captured on the edge of a small water body in the floodplain from Arly National Park.
-We have not yet found this species, neither during field work nor in the collections. So the following notes are based on literature only   (2000) and Lamotte & Ohler (2000).
habitat. -Ptychadena tournieri inhabits open savannahs (Schiøtz 1967) and breeds in temporary ponds (Perret 1991;Rödel 2000;Nago et al. 2006). It is common in West African savannahs and has been recorded from southern Senegal to northern Benin (Bourgat 1979;Lamotte 1967a;Rödel 2000;Nago et al. 2006;Segniagbeto et al. 2007). deScription. -54 specimens studied. Stout and robust frogs, with a moderately pointed snout, strong and long limbs. An inner and an external metatarsal tubercle present and very protruding as indicated by Rödel (2000) and Sánchez-Vialas et al. (2017).  -1995.1901, 1995.1902 deScription. -20 specimens studied. A plump, large and compact frog with a short and wide head (Fig. 6E, F) habitat. -We recorded A. galamensis in many habitats, i.e. agricultural zones, in water filled depressions of shrubby, grassy and wooded savannah. During the rainy season, we encountered the species around ponds and small water bodies in areas with sand and clay. subadult specimens were caught between cracks and small hollows at the edge of a permanent pond. The species occurs mostly along more permanent, larger waters in humid and dry savannah, including agricultural areas (Rödel 2000). In the dry season, this species can be found along river banks. The distribution area of the species, as currently understood, extends from extreme western Africa across to the horn of Africa and south into Angola, Mozambique, Zambia and Zimbabwe ( Lamotte & Xavier (1981) from Sub-Saharan areas like Burkina Faso but these authors did not mention any voucher specimens. The specimen of S. mauritanica in the MNHN is labelled as having been collected at Garango, in central-east of Burkina Faso, in VI.1962by Michel Lamontellerie (1928-2013.
The collector was an army doctor and stayed for over 20 years in this place. 109 specimens donated by Lamontellerie are present in the MNHN collections coming from Burkina Faso, Mali and France, but none from northern Africa. Nevertheless the collection locality of S. mauritanica in Burkina Faso should be regarded with some doubt, as it is more than 1000 km outside its southern range limit. Future research should carefully check toads from Burkina Faso, but also northern Mali and Niger for the potential presence of this species, south of the Sahara.

diStribution patternS of amphibianS in burkina faSo
In Tables 2 & 3, we represent all amphibian species recorded from Burkina Faso with their habitat type and the source of the record ( Table 2). The species in the Sudanian and Sub-Sudanian zones were more diverse than those in the Sahelian zone, e.g. only 12 species recorded in Dori and Yakouta compared to many other study sites (Table 3). Some amphibian families such as Arthroleptidae and Michrohylidae were absent from the Sahelian area (Dori and Yakouta). The Hyperoliidae were represented there by a single species, Kassina senegalensis. Most of the 36 species reported here can inhabit both disturbed and undisturbed areas. However three taxa, Arthroleptis poecilonotus, Hyperolius concolor concolor and Xenopus tropicalis, had more specific habitat requirements, i.e. gallery forest. This most likely also applies to Amnirana albolabris (west).

DISCUSSION
This study, which combines collection data, recent field data and literature information attempted to summarize the known amphibian species of Burkina Faso. Most amphibian records were from the western (Cascades, Haut-Bassins and Sud-Ouest Regions), central (Centre, Centre-Est and Centre-Sud Regions) and eastern parts (Est Region) of Burkina Faso (Fig. 1). This is likely due to the fact that these regions comprise the majority of protected areas and are more humid than the dry north, which however, is also less well explored. In the rural area (Pabré, Loumbila, Koubri) 21 species were recorded during field work, but these species are not uniformly distributed on these three small sites. The variation in faunal composition may be related to the soil composition (i.e. concerning water holding capacity and the possibility to dig into the soil) and human activities on each site. Irrigation was practiced on all three sites; the banks of Loumbila dam have a soil dominated by gravel and lateritic stones, Pabré and Koubri sites are dominated by a mixture of clay and gravel. In Arly and W National Park, 22 species were recorded and in Comoé-Léraba Forest 23 species have been identified. In these sites, the species number thus was more or less equal, meaning that a large number of species occur in protected and unprotected areas. This is not unusual as most savannah  Böhme et al. 1996;3, Brito et al. 2008;4, Lamotte & Ohler 1997;5, Lamotte 1967b;6, Loumont 1984;7, Mohneke et al. 2010a;Mohneke et al. 2010b;8, Mohneke et al. 2011;9, Mohneke 2011;10, Penner, unpublish. data;11, Rödel & Moritz, unpublish. data;12, Schiøtz 1967 8,9,12 species recorded from Burkina Faso seems very reasonable. The overall high number of amphibian species is mainly due to the richness of relatively humid habitats along rivers and permanent water bodies (lakes, ponds) in the western, central and eastern parts of Burkina Faso.