The genus Osteolaemus (Crocodylidae) in Angola and a new southernmost record for the genus
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1 Herpetology Notes, volume 11: (2018) (published online on 22 April 2018) The genus Osteolaemus (Crocodylidae) in Angola and a new southernmost record for the genus Luis M. P. Ceríaco 1,2, *, Sango dos Anjos Carlos de Sá 3, Aaron M. Bauer 1 Abstract. African Dwarf Crocodiles (genus Osteolaemus) are West and Central Africa endemics with a distribution extending from Senegal to Angola. In Angola the genus is only known to occur north of the lower Congo River in the Cabinda enclave, based on 19 th century records. No modern specimens have been documented, despite its anecdotal occurrence in other parts of the country. We provide the first confirmed record of Osteolaemus (probably O. osborni) in mainland Angola based on a vagrant individual believed to have come from the Kwanza River system. This constitutes the southernmost record for Osteolaemus in Africa, by approximately 400 km. More information is needed to assess the systematic and conservation status of Dwarf Crocodiles in Angola, but the bushmeat and leather trades are likely sources of threat to Osteolaemus throughout their range Keywords: Osteolaemussp., Angola, Kwanza River, Distribution, Conservation Introduction The African Dwarf Crocodiles, genus Osteolaemus Cope, 1861, are endemic to West and Central Africa, occurring from Senegal to the northwestern borders of Angola, east to the Central Africa Republic and the north and central parts of the Democratic Republic of the Congo (Eaton et al., 2009). The genus was long considered monotypic, with Osteolaemus tetraspis Cope, 1861 described on the basis of a single specimen from the Ogobai (currently Ogooué) River Basin in Gabon. Schmidt (1919), based on specimens from the Congo Basin, described a new genus and species closely related to Ostelolaemus which he named Osteoblepharon osborni. Werner (1933), Mertens (1943) and Inger (1948), 1 Department of Biology, Villanova University, 800 Lancaster Avenue, Villanova, Pennsylvania , USA. 2 Departamento de Zoologia e Antropologia (Museu Bocage), Museu Nacional de História Natural e da Ciência, Universidade de Lisboa, Rua da Escola Politécnica 58, Lisboa, Portugal. 3 Departamento de Gestão da Biodiversidade, Instituto Nacional da Biodiversidade e Áreas de Conservação, Ministério do Ambiente de Angola, Centralidade do Kilamba, Rua 26 de Fevereiro, quarteirão Nimi ya Lukemi, edifício Q11, 3º andar, Angola. * Corresponding author. luisceriaco@gmail.com Figure 1. Map of the localities with confirmed records of Osteolaemus sp. in Angola (purple dots), the new record presented here (Yellow star-centred dot), release area of the specimen, and other relevant localities cited in the text (black dots). Green area and rivers represent the Congo River Basin, Red the Kwanza River Basin, and Blue smaller coastal rivers.
2 338 Luis M. P. Ceríaco et al. Figure 2. View of a diorama representing the Kwanza River area in the Natural History Museum of Luanda, with stuffed specimens of two Osteolaemus sp. (far left and right) and a juvenile Crocodylus niloticus in the middle. The installation and arrangement of these dioramas date back to the pre-independence era (before 1975). Photo by L.M.P. Ceríaco. however, all considered Osteoblepharon as a junior synonym of Osteolaemus, although they maintained osborni as a full species. Wermuth (1953) treated osborni as a subspecies of O. tetraspis, an opinion that has been accepted until very recently. Ray et al. (2001) provided the first molecular evidence of high levels of genetic variability within Osteolaemus, suggesting that more detailed studies would clarify the taxonomy of the group. Based on skull morphology, Brochu et al. (2007) elevated O. osborni to species level again. Eaton et al. (2009a) provided a baseline molecular phylogeny of the genus based on extensive sampling across West and Central Africa using three mitochondrial and two nuclear genes. Their findings pointed to the existence of three distinct lineages within the genus. These findings have since been corroborated by Eaton et al. (2009b), Shirley and Eaton (2010), Franke et al. (2012) and Shirley et al. (2014a,b). Supported by molecular analyses of newly collected samples. Smolensky et al. (2015) presented more detailed data on the distribution of the three Osteolaemus lineages. According to their results the undescribed Osteolaemeus lineage occurs in West Africa, west of the Ogooué Basin (Senegal, Guinea-Bissau, Guinea, Sierra Leone, Liberia, Ivory Coast and Ghana), O. tetraspis occurs in the Ogooué Basin, including parts of Nigeria, Cameroon, Equatorial Guinea, Gabon, Republic of the Congo and Angola s Cabinda enclave, and O. osborni is restricted to the Congo Basin, especially in the southeastern areas of Cameroon, northwestern tip of Gabon, eastern half of the Republic of the Congo, all northern and central regions of the Democratic Republic of the Congo, and extending to the northwestern Angolan province of Zaire. However, the distribution of the first two species from eastern Ghana to eastern Nigeria were considered unknown and there were no molecular samples from south of southern Gabon. Data on the distribution of the genus in Angolan territory is extremely limited and derive from 19th century of records of Osteolaemus sp. from the Cabinda enclave (Bocage, 1866; Peters, 1877), and no confirmed records exists for either O. tetraspis or O. osborni in Angola south of the Congo River (Figure 1; see also Pooley, 1982; Thorbjarnarson 1992). In the dioramas of the Natural History Museum of Luanda there are several mounted specimens of Osteolaemus sp., which are labelled as being from the Kwanza River Basin (Figure 2). However, the catalogues of the museum were lost in the 1990s during an inundation of the museum stores, and, therefore, no more precise data exist for these specimens. Data on the distribution of other crocodilians in mainland Angola is also limited, especially when one takes into consideration the area of the country and the vast river basins that drain it. Two species are currently confirmed to occur in mainland Angola Crocodylus niloticus Laurenti, 1768 (see Bocage, 1866, 1867, 1895; Peters, 1877; Ferreira, 1903; Monard, 1937; Hellmich, 1957; Branch and McCartney, 1992; Ceríaco et al., 2014; Marques, 2015; Branch and Conradie, 2015; Conradie et al., 2016) and Mecistops cf. catraphactus (Cuvier 1825) (see Peters, 1877; Bocage, 1895; Laurent, 1964; Marques, 2015). Whereas the first species has an extensive distribution throughout the country, being
3 The genus Osteolaemus in Angola and a new southernmost record for the genus 339 receives debris carried by the outflow of the Kwanza River, and it is likely that this crocodile followed the same path. It is highly improbable that the specimen came from the inland side of the bay, as the area is extremely urbanized and unsuitable for crocodilian populations. We also believe that it is unlikely that the Mussulo animal represents an escaped animal imported from north of the Congo for the bushmeat or handicraft trade. While some crocodile leather products, including those derived from Osteolaemus, are sold in the informal markets of Angola by Congolese nationals (see below), we presume that those reaching Luanda typically do so as raw or processed skins. Figure 3. Live specimen of Osteolaemus cf. osborni collected in Mussulo, Angola. Photo by Sango dos Anjos Carlos de Sá. known from nine provinces (Cabinda, Lunda Norte, Luanda, Malanje, Kwanza Sul, Benguela, Cunene, Cuando Cubango; Pooley et al., 1982; Marques, 2015), the latter is only known to occur in Cabinda and Lunda Norte provinces (Pooley et al., 1982) and Angolan populations have been considered by Shirley et al. (2014a,b) and Grigg and Kirshner (2015) to represent an undescribed species. In this paper we provide the first confirmed record of an African Dwarf Crocodile in Angola south of the Congo, and briefly discuss its conservation implications. Materials and methods On 30 December 2015, one of us (SACS) was called by the local authorities to rescue a live adult specimen of an Africa Dwarf Crocodile at a beach in the Mussulo region ( ºN, ºE; Figure 1), Angola. The specimen was in good physical condition and did not exhibit any evidence of epizoic marine organisms. Mussulo is a peninsula south of Luanda, about 30 km long and approximately 70 m wide at is base and 1.5 km wide at its widest. It lies about 30 km north of the Kwanza River mouth and was formed from sediments from the river swept north by the Benguela Current. The peninsula forms a shallow, narrow bay fronting the southern outskirts of Luanda. The animal was safely captured and transported approximately 50 km south to the Kwanza River in Kissama National Park ( ºN, ºE; Figure 3), where it was photographed and released. No blood or tissue samples were taken. Given its proximity to the Kwanza River mouth and the south to north coastal currents in the area, Mussulo Results and Discussion Morphological identification of O. tetraspis and O. osborni is difficult as no diagnostic external characters have yet been found to clearly separate the two taxa (de Boer, 2010). However, we tentatively identify the Mussulo animal as O. osborni, as this species is expected to occur in the Zaire region (Smolensky et al., 2015). However, a more definitive identification can only be made with the collection of fresh samples for genetic analysis. Regardless of the specific identity of the Mussulo crocodile, this record represents not only the first mainland Angolan record for the genus, but also the southernmost record of the genus in Africa, extending the range approximately 400 km southward from the limit of O. tetraspis in Cabinda and nearly as far from the predicted (Smolensky et al., 2015), but unvouchered, range limit of O. osborni in Zaire Province. Although the Kwanza River is the largest river in Angola and was an important navigation route during Portuguese colonial times, its biodiversity remains very poorly explored. This is also true for the northwestern parts of the country, where the number of records for both amphibians and reptiles is minimal. However, given this region s climatic and vegetative similarities to southwestern Congo, it is expected that many of the species occurring there also extend into Angola. Recent fieldwork carried out during environmental impact studies at two hydroelectric dam sites on the Kwanza River in Malanje Province Capanda ( ºN, ºE; see Ceríaco et al., 2014) and Lauca ( ºN, ºE) yielded only Crocodylus niloticus, although Osteolaemus was actively sought at the latter site. However, according to several local informants from the Lauca, Dondo ( ºN, ºE) and Kissama areas ( ºN, ºE; see Figure 1) two types of crocodilians
4 340 Luis M. P. Ceríaco et al. Huchzermeyer (1998) reported the commercialization of Osteolaemus leather goods in Cameroon. Purses made with Osteolaemus leather and body parts are sold in the Mercado do Artesanato, a traditional arts and crafts market on the southern outskirts of Luanda (Figure 4); however it is unclear if these products are local or from the Congo, as a substantial percentage of the sellers are of Congolese origin and usually import material from both the Republic of the Congo and the Democratic Republic of the Congo (LMPC, pers. obs.). Figure 4. A handbag made of skin of Osteolaemus sp. offered for sale at the Mercado do Artesanato, Luanda, in August Photo by Luis M.P. Ceríaco. inhabit the waters of the Kwanza the Crocodilo, a small form (maximum 2 m total length) with a shorter and wider snout, that occurs in shallower and smaller streams, and the Jacaré, which tends to be larger (3 4 m), with a more acute snout, and is considered a maneater, which undoubtedly refers to C. niloticus. These differences have been reported Cabral et al. (1944) who, however, dismissed them, and considered that the claimed differences reflected sexual dimorphism within C. niloticus. The recovery of an Osteolaemus so close to the mouth of the Kwanza River certainly lends credence to this folk taxonomy, although it is certainly possible that the Crocodilo may refer to smaller or juvenile Crocodylus. Nevertheless, there is the need for more focused and dedicated surveys to confirm the presence and population status of crocodilians in the Kwanza Basin. Despite the available evidence, the IUCN Red List still only recognizes O. tetraspis as the single member of the genus, which is listed as Vulnerable (Crocodile Specialist Group, 1996). It is, however, expected that the split of O. tetraspis into three taxa, each with a more limited distribution, will require reassessment of their current conservation status. Elsewhere on the continent, Osteolaemus sp. are especially threatened by the bushmeat trade (Hutton, 1991; Huchzermeyer, 1998; Thorbjarnarson and Eaton, 2004; Eaton et al., 2009b; Shirley et al., 2009; Zoer, 2012) and illegal exportation to Europe and the United States, mostly to satisfy the demands for bushmeat by African expatriates (Milius, 2005). While crocodile meat is consumed in Angola, there are almost no data on the species involved or its prevalence, but it is probable that this also affects the local populations of Osteolaemus. Acknowledgments. We thank Aristófanes Pontes and the staff of Instituto Nacional da Biodiversidade e Áreas de Conservação and the Ministry of Environment of the Republic of Angola for the permits allowing our research in Angola, as well as for logistical and technical help in the field. The authors would also like to thank the Companhia de Bombeiros de Luanda for the initial contact regarding the presence of the animal on the Mussulo Peninsula, and for their support during its collection and release. Sara Fernandes and David Elizalde provided the correct coordinates to the collecting and release areas. Christopher Brochu provided a preliminary review and comments to the original manuscript. LMPC and AMB were supported by funding from the National Science Foundation of the United States (DEB and DEB ) and the Gerald M. Lemole Endowed Chair funds through Villanova University. References Bocage, J.V.B. (1866): Lista dos reptis das possessões portuguezas d Africa occidental que existem no Museu de Lisboa. Jornal de Sciencias Mathematicas Physicas e Naturaes 1: Bocage, J.V.B. (1867): Segunda lista dos reptis das possessões portuguezas d Africa occidental que existem no Museu de Lisboa. Jornal de Sciencias Mathematicas, Physicas e Naturaes 1(3): Bocage, J.V.B. (1895): Herpétologie d Angola et du Congo. Lisboa, Portugal, Ministério da Marinha e das Colónias. Branch, W.R., McCartney, C.J. (1992): A report on a small collection of reptiles from southern Angola. Journal of the Herpetological Association of Africa 41(1): 1 3. Branch, W.R., Conradie, W. (2015): Herpetofauna da região da Lagoa Carumbo. In: Avaliação rápida da biodiversidade da região da Lagoa Carumbo, Lunda Norte Angola, p Huntley, B., Francisco, P., Eds., Luanda, Angola, Ministério do Ambiente de Angola. Brochu, C.A. (2007): Morphology, relationships, and biogeographical significance of an extinct horned crocodile (Crocodylia, Crocodylidae) from the Quaternary of Madagascar. Zoological Journal of the Linnean Society 150(4): Cabral, T., Pratas, A., Galvão, H. (1944): Da vida e da morte dos bichos, volume II: Hipototamo Girafa Crocodilo Javalis. Lisboa, Portugal, Livraria Popular de Francisco Franco. Ceríaco, L.M.P., Bauer, A.M., Blackburn, D.C., Lavres, A.C.F.C. (2014): The herpetofauna of the Capanda Dam region, Malanje, Angola. Herpetological Review 45:
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