Non-volant mammals from Baturité Ridge, Ceará state, Northeast Brazil

Check List the journal of biodiversity data Check List 11(3): 1630, April 2015 doi: http://dx.doi.org/10.15560/11.3.1630 ISSN 1809-127X © 2015 Check List and Authors LISTS OF SPECIES Non-volant mammals from Baturité Ridge, Ceará state, Northeast Brazil Hugo Fernandes-Ferreira1*, Newton Mota Gurgel-Filho1, Anderson Feijó1, Sanjay Veiga Mendonça2, Rômulo Romeu da Nóbrega Alves3 and Alfredo Langguth1 1 Universidade Federal da Paraíba, Departamento de Sistemática e Ecologia, Laboratório de Mastozoologia, João Pessoa, Paraíba State, Brazil, CEP 58051-900 2 Universidade Estadual do Ceará, Departamento de Avicultura, Laboratório de Estudos Ornitológicos, Fortaleza, Ceará State, Brazil, CEP 60714-903 3 Universidade Estadual da Paraíba, Departamento de Biologia, Campina Grande, Paraíba State, Brazil, CEP 58429-500 * Corresponding author. E-mail: fernandes-ferreira@ufpb.br Abstract: Baturité Ridge is an important Atlantic Forest remnant inserted in the Caatinga Morphoclimatic Domain located in the Ceará state, Northeast Brazil. Although this area presents high rates of endemism and has been investigated by many researchers in the past, there was never an investigation regarding local mammals. In this context, this study aims to survey the non-volant mammals of this region to serve as a basis for future ecological and conservation studies. he work was conducted between 2009 and 2014, based on analyses of voucher specimens from zoological collections, capture of specimens in ieldwork, visual and photographic records, and interviews with selected local residents. Altogether, 32 species were documented and seven are present on lists of endangered animals. In addition, interviews indicated that three non-recorded species probably occur in the area and another two were pointed out by local people as locally extinct. Discussions about identiication and conservation aspects were presented. semi-arid biome endemic to Brazil, but have lora and fauna typically related to both the Amazonian and Atlantic Forests, as well as ancient areas that connected these two biomes, as presented by several studies (Vanzolini et al. 1980; Andrade‑Lima 1982; Mares et al. 1985; Figueiredo and Barboza 1990; Borges‑Nojosa and Caramaschi 2003; Sousa 2004; Borges‑Nojosa 2007). he Brazilian state of Ceará is covered by cloud forests in areas of high altitude, such as in the Ibiapaba, Araripe, Maranguape, Aratanha and Baturité ridges, the last one being where this research was developed. Baturité is the region richest in species and has a great importance in maintaining biodiversity and water resources for the state (Mantovani 2007). For example, this area is where Hoogmoed et al. (1994) described the frog Adelophryne baturitensis; Rodrigues and Borges (1997) revealed the lizard Leposoma baturitensis; Tribe (2005) proposed a new subspecies of rodent (Rhipidomys cariri baturiteensis); Passos et al. (2007) described the snake Atractus ronnie; Feijó and Langguth (2013) discovered Coendou baturitensis, a new species of porcupine, and Roberto et al. (2014) revealed a new species of Bufonidae (Rhinella casconi). Additionally, this is one of the most important bird conservation sites in Northeast Brazil, due to the presence of 12 endangered species, including Pyrrhura grisepectus (Gray-breasted Parakeet), the most endangered parakeet of the Americas (Olmos et al. 2005; Girão 2007). Due to these factors, Oliveira et al. (2003) considered this region to have high conservation priority. he study of mammals in Ceará, despite being approached by several authors, still faces major gaps in knowledge. Fernandes-Ferreira et al. (2014), in reviewing the history of vertebrate zoology research of this state, showed that there are few studies involving Key words: Atlantic Forest, brejos de altitude, Caatinga, mammalian, survey INTRODUCTION According to Prance (1982), Northeast Brazil is a center of plant endemism, consisting of deciduous forests, semi-deciduous dry forests, montane and submontane ombrophilous forests, and open and arboreal dry vegetation, with several areas of refuge for fauna and lora. he most important of these refuge areas are the brejos de altitude (altitudinal cloud forests) made up of residual ridges with vegetation that resisted drastic climatic changes during the Pleistocene (Ab’Saber 1992). hese forest areas are surrounded by the Caatinga, a Check List | www.biotaxa.org/cl 1 Volume 11 | Number 3 | Article 1630 Fernandes-Ferreira et al. | Mammals from Baturité Ridge, Ceará, Brazil mammals, and none whatsoever in the central region of the state. Following the studies of Rocha (1908, 1945, 1948) and Paiva (1973), surveys of mammals involving the whole of Ceará’s territory have only been published recently. Gurgel-Filho and Langguth (in press) describe and discuss the morphology of species of Didelphimorphia (Didelphidae), Rodentia (Sigmodontinae) and Chiroptera collected in Ceará and housed in the main Brazilian zoological collections. Feijó and Langguth (2013) conducted a taxonomic revision of medium and large sized species based on morphological characters, also including in their research the neighboring states of Paraíba and Pernambuco. Despite the importance of Baturité for biogeography, ecology and conservation, information about its mammalian fauna has never been appraised and is available only through the Serviço Nacional da Peste (National Service of the Bubonic Plague) ieldwork between 1930 and 1950. he purpose of this government program was to catch small mammals in order to investigate and eradicate tropical diseases (Freitas 1957; Oliveira and Franco 2005). hus, the aim of this paper is to present an updated and comprehensive survey on non-volant mammals of Baturité and discuss aspects of their conservation. MATERIALS AND METHODS Study site Baturité (04°07′48″ S, 038°03′19″ W) is the largest ridge of the Ceará state, encompassing the municipalities of Aratuba, Baturité, Capistrano, Caridade, Guaramiranga, Mulungu, Pacoti and Redenção. his region presents an average altitude of 600 m and a maximum of 1,114 m. he combination of altitude with the course of the relief in relation to the sea results in average temperatures between 23°C at higher altitudes areas to 27°C in the lower sites. Its geographical position promotes orographic rainfall on the windward side, due to coastal winds with high humidity, generating high rainfall rates (900–1,400 mm/year) and corresponding humidity (700 mm/year). hese characteristics established tropical submontane and montane rainforests. On the leeward side, lower relative humidity rates promote a large inluence of deciduous dry vegetation typical of the Caatinga biome. his area is also included in the Baturité Environmental Protection Area (Mantovani 2007). Data collection his survey was conducted between 2009 and 2014 using four sources of information: 1) the analysis of voucher specimens from zoological collections and Figure 1. Location of Baturité Ridge, Ceará state, Northeast Brazil. Check List | www.biotaxa.org/cl 2 Volume 11 | Number 3 | Article 1630 Fernandes-Ferreira et al. | Mammals from Baturité Ridge, Ceará, Brazil museums; 2) the capture of specimens in the ield; 3) visual and photographic records, and 4) interviews with selected local residents. Mammal collections of the following Brazilian institutions were visited: Universidade Federal do Ceará, Fortaleza, Ceará (UFC); Universidade Federal da Paraíba, João Pessoa, Paraíba (UFPB); Museu de Zoologia da Universidade de São Paulo, São Paulo (MZUSP); Museu Nacional de História Natural do Rio de Janeiro, Rio de Janeiro (MNRJ); Universidade Federal de Pernambuco, Recife, Pernambuco (UFPE) and Museu Paraense Emílio Goeldi, Belém, Pará (MPEG). All specimens were examined and their identiications checked and updated according to current taxonomic literature (Gardner 2008; Paglia et al. 2012; Feijó and Langguth 2013). Field samples were obtained through two stations of pitfall traps (adapted from Aurichio and Salomão 2002), one built in the windward and another on the leeward side of the mountain. Each trap consisted of four buried 30 L buckets and three plies each measuring 10 m long and 60 cm wide. hirty Sherman traps (25 × 8 × 8 cm) were also installed to capture small mammals in the same areas. hese actions were performed sporadically, during both dry and wet seasonal periods, and were authorized by the Brazilian federal authorities (SISBIO / ICMBio license number 19801-02). he animals were handled according to the protocols described by Sikes et al. (2011). All captured animals were deposited in the mammal collection of the Universidade Federal da Paraíba. his methodology was completed with visual and photographic records performed in the forest trails. Local residents with any manner of interaction with wild mammals were interviewed, and the “snowball” technique (Bailey 1994) was applied to select people based on the irst group. In this way a total of 110 “local specialists” (people who consider themselves, and are likewise recognized within the community itself, to be knowledgeable on the subject) were identiied and interviewed (Hays 1976). Visual and photographic records were made in homes of interviewees (in the case of wild pets), many of which also ofered to donate biological samples (e.g., skin, feet, antlers, skeleton, and claws) of game. his practice was approved by the Ethics Committee of the University Hospital of Federal University of Paraíba (Protocol 418/09). RESULTS Altogether, 32 species of non-volant mammals belonging to 12 families and seven orders with conirmed records were documented in Baturité (Table 1, Figure 2, Appendix 1). In addition, interviews revealed that three nonrecorded species probably occur in the area (Nasua nasua, Sapajus libidinosus and Eira barbara) and another two were pointed out by local people as locally extinct (Panthera onca and Cuniculus paca). he presence of Nasua nasua was mentioned by eleven informants. his species occurs in Ceará but the only location with a voucher specimen is the Ibiapaba Ridge, in the northwestern region of the state (Feijó and Langguth 2013). Twentynine informants cited the presence of Eira barbara in the study area. According to these interviews, this mustelid is probably rare in Baturité and inhabits areas above 700 m high. After several people stated the extinction of Sapajus libidinosus, seven informants reported the discovery of a population in rocky areas of the study site. According to thirty-seven respondents, Panthera onca occurred in wetlands of Baturité until about 25 years ago. Ten others claim that its occurrence is still likely. Twelve local hunters airmed the local extinction of Cuniculus paca for about 40 years, caused primarily by excessive hunting. DISCUSSION Most of the non-volant mammalian species recorded in Ceará can be found in Baturité. Of the 21 species of small terrestrial mammals surveyed in this state (Gurgel-Filho and Langguth, in press), 15 (71.4%) were recorded in Baturité. Among the medium and large sized species (Feijó and Langguth 2013) this proportion reaches 61.5%. A detailed description of the species documented here can be found in the studies of Gurgel-Filho and Figure 2. Mammals photographed in Baturité Ridge, Ceará state, Northeast Brazil. A: Didelphis albiventris. B: Didelphis gr. marsupialis. C: Coendou baturitensis. D: Callithrix jacchus (kept as pet by local community). E: Procyon cancrivorus (kept as pet by local community). F: Cerdocyon thous (road-kill). G: Euphractus sexcinctus. Photos by SVM (A) and HF-F (B, C, D, E and F). Check List | www.biotaxa.org/cl 3 Volume 11 | Number 3 | Article 1630 Fernandes-Ferreira et al. | Mammals from Baturité Ridge, Ceará, Brazil Langguth (in press) and Feijó and Langguth (2013), however, some animals deserve some discussion on their their taxonomy. he record of a black-eared Didelphis (Figure 2b) has a problem with its identiication, as the diferences between the two possible species, Didelphis marsupialis and Didelphis aurita, are just morphometric (Cerqueira and Lemos 2000). Baturité is located in a gap of the known distribution of this group which shares the characteristics of black ears (Cerqueira and Tribe 2008). hus, we prefer to considerate it Didelphis gr. marsupialis and suggest eforts in genetic and morphological studies to resolve this problem. he taxonomy of the genus Oligoryzomys is poorly done, because there are many variations of cranial morphometry (see Weksler and Bonvicino 2005). hus, new evidences are required for a safe identiication of the species found in the study area. Among the species identiied and cited here, seven are present on lists of endangered animals (MMA 2014, IUCN 2015). Six of these species, along with another seven, are also documented on lists of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES 2015) (Table 2). It is also important to note that there are no other known occurrence areas of Coendou baturitensis (Figure 2c) beyond Baturité, although some non-published visual and photographic evidence suggest the presence of this species in other rainforests, such as the Ibiapaba and Maranguape ridges. Furthermore, the presence of Speothos venaticus suggests a critically endangered local population of this canid. Its recent discovery represents the irst record of this species in a location within the Caatinga’s Morphoclimatic Domain, done so by means of a female cub carcass that was donated by local residents (FernandesFerreira et al. 2011). Jorge et al. (2013), in a review of the conservation status of this species in Brazil, pointed out the possibility of a misidentiication by the researchers who reported the bush dog in Ceará and, therefore, they did not consider the discovery as an accurate distribution extension. Such suspicion was justiied by a supposed history of confusion in the identiication of species of wild canids in that region. he authors used as Table 1. Non-volant mammals recorded in Baturité Ridge. Order/Family Species Record* Marmosa murina (Linnaeus, 1758) VS Micoureus demerarae (Thomas, 1905) VS Monodelphis domestica (Wagner, 1842) VS, IN Monodelphis americana (Müller, 1776) VS Didelphis albiventris Lund, 1840 VS, PR, VR, IN Didelphis gr. marsupialis Linnaeus, 1758 VS, PR, IN Dasypus novemcinctus Linnaeus, 1758 VS, IN Euphractus sexcinctus (Linnaeus, 1758) VS, PR, IN Didelphimorphia Didelphidae Cingulata Dasypodidae Pilosa Myrmecophagidae Tamandua tetradactyla (Linnaeus, 1758) VS, IN Primates Cebidae Callithrix jacchus (Linnaeus, 1758) VS, PR, IN Leopardus pardalis (Linnaeus, 1758) VS, IN Leopardus tigrinus (Schreber, 1775) VS, IN Leopardus wiedii (Schinz, 1821) VS, IN Carnivora Felidae Puma concolor (Linnaeus, 1771). VS, IN Puma yagouaroundi (É. Geofroy, 1803) VS, IN Canidae Cerdocyon thous (Linnaeus, 1766) VR, PR, IN Speothos venaticus (Lund, 1842) VS, IN Procyonidae Procyon cancrivorus (G. Cuvier, 1798) VS, PR, IN Galictis cuja (Molina, 1782) VR Conepatus amazonicus (Lichtenstein, 1838) VR, IN Mazama gouazoubira (Fischer, 1814) VS, IN Coendou baturitensis Feijó & Langguth, 2013. VS, PR, IN Dasyprocta sp. VR, IN Mephitidae Artiodactyla Cervidae Rodentia Table 2. Endangered mammals from Baturité Ridge and its respective category of threat according to Brazilian Ministry of Environment (MMA 2014), IUCN (2015) and CITES (2015). Erethizontidae Dasyproctidae Species MMA* IUCN* CITES Speothos venaticus VU NT Appendix I VS, IN Cerdocyon thous - - Appendix II VR, IN Leopardus wiedii VU NT Appendix I Leopardus tigrinus EN VU Appendix I VR, IN Puma concolor VU LC Appendix II VS Panthera onca VU NT Appendix I Oligoryzomys cf. nigripes (Olfers, 1818) VS Puma yagouaroundi VU - Appendix II Necromys lasiurus (Lund, 1841) VS Eira barbara - - Appendix III Cerradomys langguthi Percequillo, Hingst-Zaher & Bonvicino, 2008 VS Galictis cuja - - Appendix III Cuniculus paca - - Appendix III Euryoryzomys af. russatus (Wagner, 1848) VS Kerodon rupestris VU - - Holochilus sciureus (Wagner, 1842) VS Callithrix jacchus - - Appendix II Sapajus libidinosus - - Appendix II Caviidae Galea spixii (Wagler, 1831) Kerodon rupestris (Wied, 1820) Echymidae Thricomys laurentius Thomas, 1904 Cricetidae Rhipidomys cariri Tribe, 2005 * VS (voucher specimens); IN (interview); PR (photographic record); VR (visual record). Check List | www.biotaxa.org/cl * VU (vulnerable); NT (near threatened); LC (least concern). 4 Volume 11 | Number 3 | Article 1630 Fernandes-Ferreira et al. | Mammals from Baturité Ridge, Ceará, Brazil the voucher specimen. he presence of these endangered species deserves the attention of researchers and authorities, especially when considering the various factors of environmental impact on Baturité, such as deforestation, overexploitation of natural resources, habitat fragmentation, the introduction of invasive species, pollution of water resources, road kills (Figure 2f), and real estate speculation, as pointed by Oliveira et al. (2007). It is necessary to emphasize that hunting activities were cited in interviews and are related to 22 (68.7%) species, beyond the six species with no conirmed occurrence in Baturité. If considering only medium and large sized mammals, the proportion of game species in relation to the total richness is 100%. In the municipality of Caridade, for example, local residents (n = 12) reported the killing of three individuals of Puma concolor between 2009 and 2010. his species and other carnivores are hunted locally for the purpose of population control, because of its potential attack on domestic animals like calves, pigs, goats and poultry. However, most mammals are used for food purposes. Some species are also kept by local inhabitants as pets, in the case of Callithrix jacchus (Figure 2d), Procyon cancrivorus (Figure 2e), Mazama gouazoubira, Puma yagouaroundi and Tamandua tetradactyla, or even for medicinal practices. he hunting of birds, reptiles and amphibians in Baturité has already been investigated by other studies which indicate large impacts on the local fauna (Fernandes-Ferreira et al. 2012, 2013). his is a reality observed in several locations in Brazil, where hunting and consumption of wild animals persist in all regions of the country, with complete disregard of legal implications (Cullen-Jr. et al. 2001; Peres and Nascimento 2006; Fernandes-Ferreira and Alves 2014). Moreover, the absence of ecological studies focusing on wild mammals in the study area surely does not reveal local threats or population depletion of all species. Figure 3. Morphological comparison between the specimen of Speothos venaticus recorded by Fernandes-Ferreira et al. (2011) in Baturité Ridge (A1 to D1) and some unique characteristics for this species illustrated in Langguth (1969) (A2 to D2). A: Left foot, showing the digital pads of the third and fourth digits united at their inner proximal angles, giving the appearance of fusion of the two pads. B. Shape of rhinarium (supericial vision). C: Shape of rhinarium (frontal vision). D: Simple intestinal caecum. Photos by HF-F. reference for this statement an article on misidentiications of canid species that transmit zoonosis which was based on documents related to epidemiology and human health (Courtenay et al. 1996). herefore, this purely medical paper has no connection to typical zoological work, which examines external and internal morphology by specialized taxonomists in order to ascertain the identity of a specimen. Because Jorge et al. (2013) did not analyze the voucher specimen and did not discuss the zoological information provided by Fernandes-Ferreira et al. (2011), which was based on a vouchered specimen unambiguously identiied as Speothos venaticus, we consider that the disagreement on the distribution extension has no scientiic support. Nevertheless, Figure 3 presents a morphological comparison between the specimen recorded by Fernandes-Ferreira et al. (2011) (UFPB 6272) and unique characteristics for this species illustrated in Langguth (1969) in order to clear up this controversy. Other exclusive biological patterns of S. venaticus such as the protruding forehead and the eight symmetrical palatal rugae can be veriied by analyzing Check List | www.biotaxa.org/cl ACKNOWLEDGEMENTS We thank the Conselho Nacional de Desenvolvimento Cientíico e Tecnológico (CNPq) and the Conselho de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for funding the research of the authors; Dr. Diva Maria Borges-Nojosa for scientiic support; Roberto Otoch, for historical information about the local fauna; Cleiton and Gleidison Lima for assistance in ieldwork and the Kenney Blumer and Veiga families for hosting us in the study area. LITERATURE CITED Ab’Saber, A.N. 1992. A teoria dos refúgios. Estudos Avançados 15(1): 9–11. Andrade-Lima, D. 1982. Present-day forest refuges in Northeastern Brazil; pp. 245–251, in: G.T. Prance (ed.). Biological diversiication in the tropics. 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Marmosa murina - Guaramiranga: UFPE 1078. Micoureus demerarae - Aratuba: UFPB-NG10; Pacoti: MNRJ 28987. Monodelphis domestica - Baturité: MNRJ 16653, 16648, 1669, UFC0007; Pacoti: MNRJ 27936, 16667. Monodelphis americana - Pacoti: CMUFC 0142, MZUSP 29458, 29461, 29464; Aratuba: visual record. Didelphis albiventris - Baturité: UFC004; Aratuba, Pacoti, Mulungu, Caridade, Guaramiranga: visual record; Aratuba: photographic record. Didelphis gr. marsupialis - Aratuba: UFPB6261; Mulungu, Pacoti: visual record; Mulungu: photographic record. Euphractus sexcinctus - Guaramiranga, Aratuba: photographic record. Dasypus novemcinctus - Caridade: UFPB 6595, 6596. Tamandua tetradactyla - Mulungu: UFPB 6591, 6598, visual record. Coendou baturitensis - Aratuba: UFPB 6809; Baturité: UFPE 2387; Pacoti: MN 34504; Mulungu: visual and photographic record. Galea spixii - Aratuba: photographic record. Rhipidomys cariri - Pacoti: UFC 0083, MN17373, 17441, 17444, 30010; Baturité: UFC013, 015, 016. Oligoryzomys cf. nigripes Pacoti: MN-SNP– BT 22. Necromys lasiurus - Baturité: MN47979. Cerradomys langguthi - Baturité: MN20701, 20702, 20704, UFC096; Pacoti UFC002. Euryoryzomys af. russatus - Baturité: MZUSP-MRT 05, 011, 015, 027, 038. Holochilus sciureus - Pacoti: MZUSP8704, 8705, 8706, 8707, 8708. Mazama gouazoubira - Aratuba: UFPB HFF10; UFPB 6590, HFF11, UFPB 6598; Caridade: UFPB 6589. Cerdocyon thous Mulungu: photographic record (road-killed specimen, 04º17’34’’ S, 38º58’39’’ W) and visual record. Speothos venaticus - Aratuba: UFPB 6272. Leopardus pardalis - Mulungu: UFPE 2001. Leopardus wiedii - Mulungu: UFPE 1996, 2003. Leopardus tigrinus - Mulungu: UFPE 1942, 2002, 1997, 1998. Puma yagouaroundi - Aratuba: UFPB 6594, visual record; Mulungu: UFPE1992, 1994; Caridade: UFPE1943. Puma concolor - Caridade: UFPB 6597. Procyon cancrivorus - Aratuba: UFPB6656, photographic record. Conepatus amazonicus - Caridade: visual record. Callithrix jacchus - Pacoti: MN3930, 3950, 3938, 5528, 3939, 3947, 3954, 5521, 5544, 3932, 3933, 3935, 3937, 3940, 3942, 3944, 3948, 3949, 3952, 3953, 3956, 5517, 5535, 5536, 5546, 5575, 5577, 23771, 23772, 3945, 5545, 3951, 5543, 5572, 5576, 3941, 3946, 5573, 3955, 5551, 3957, 3943, 3933, 3934, 3931; Baturité: MZUSP 8694, 8695, 8693, 8695, 8696; Mulungu: photographic record. Author’s contribution statement: HF-F, NMG-F and AF collected the data and wrote the text; SVM collected the data; RRNA and AR wrote the text and coordinated the research. Received: December 2014 Accepted: March 2015 Editorial responsibility: Guilherme Siniciato Terra Garbino Check List | www.biotaxa.org/cl 7 Volume 11 | Number 3 | Article 1630