Chironectes Minimus (Zimmermann

n Glironia venusta Thomas, 1912 and Chironectes minimus (Zimmermann,

istributio Mammalia, Didelphimorphia, Didelphidae, D

Natália Ardente 1* 2 3 1 and Fernanda raphic g 1780): Distribution extension for eastern Amazonia eo 4 , Donald Gettinger , Raul Fonseca , Helena de Godoy Bergallo G

n Martins-Hatano o

1 Universidade do Estado do Rio de Janeiro, Instituto de Biologia Roberto Alcântara Gomes, Departamento de Ecologia, Laboratório de Ecologia de

otes Mamíferos. Rua São Francisco Xavier 524. CEP 20559-900. Rio de Janeiro, RJ, Brazil. N 2 University of Nebraska-Lincoln, Harold W. Manter Laboratory of Parasitology. W529 Nebraska Hall. 68588-0514. Lincoln, Nebraska, U.S.A. 3 Universidade do Estado do Rio de Janeiro, Instituto de Biologia Roberto Alcântara Gomes, Departamento de Zoologia, Laboratório de Mastozoologia. Rua São Francisco Xavier 524. CEP 20559-900. Rio de Janeiro, RJ, Brazil. 4 Universidade Federal Rural da [email protected]ônia, Instituto de Saúde e Produção Animal, , Departamento de Biologia Animal. Avenida Presidente Tancredo Neves, 2501. CEP 66.077-901. Belém, PA, Brazil. * Corresponding author. E-mail: Abstract: We report a new record for the bushy-tailed opossum Glironia venusta Thomas, 1912 and the water opossum Chironectes minimus (Zimmermann, 1780) in the Floresta Nacional de Carajás, municipality of Parauapebas, state of Pará, Brazil (06°03’00” S, 50°15’00” W). This study represents the second record of Glironia venusta for eastern Brazilian Amazon. For Chironectes minimus, this record extends the range of the species 558 km southeastwards from the closest known locality in Pará. , but the first voucher specimen

MN 75062 (Figures 1 and 2). This is the second record of the Floresta Nacional de Carajás in the Brazilian state of G. venusta from the state of Pará and the eighth for Brazil During an inventory of small mammal species within et al.

GlironiaPará, two venusta species Thomas, of poorly 1912 known and andChironectes rarely surveyed minimus (FigureMarabá, 3).Brazil, Rossi by a photograph. (2010) first reported this species (Zimmermann,marsupials were 1780). collected Both species as voucher present specimens: diagnostic in the Floresta Nacional Tapirapé-Aquiri, municipality of

External measurements: Body length, 178 mm; Tail habitats.characters that are easy to identify (see Gardner 2008; length, 214 mm; Hind foot length (including claw), 35 mm; VossThe and genus Jansa Glironia 2009), being highly adapted to specific Ear length from notch, 27 mm. Cranial measurements, species, Glironia venusta medium-sized and bushy-tailed is monotypic, opossum the single (Marshall living Thomas, 1912, is a distinctive

1978a; Wilson and Reeder 2005). Little is known about knownthe real geographic from only distribution 20 localities of inthis South rare and America, vulnerable and species (Bernarde and Rocha 2003; Díaz and Willig 2004),

Brazil,restricted G. venusta to the Amazonhas been Forestrecorded in Bolivia,from the Ecuador, states of Peru, Acre (BernardeBrazil and and Colombia Machado (Marshal 2008), 1978a;Amazonas Gardner (Nogueira 2008). et al. In et al. et al. 1999; Calzada et 2008), al. Pará (Da Silva and Langguth Filho1989; et Rossi al. 2007). 2010), Rondônia (Bernarde and Rocha 2003; Santos-Filho 2007) and Mato Grosso (Santos- an adult male weighting 119 g, was captured in the FlorestaThe Nacional voucher de specimen Carajás (06°03’00” (field number S, 50°15’00” DG 67),W), municipality of Parauapebas, state of Pará, Brazil. The specimen was captured in August, 2010, during the dry season, in a Sherman trap placed in the lower canopy of the rain forest (8.6 m high). The specimen was prepared as a skin and full skeleton, with associated tissue samples,

Figure 1. Glironia venusta (male, MN 75062) trapped in eastern Amazonia, Floresta Nacional de Carajás , Pará, Brazil. and is deposited in the Museu Nacional, Universidade Federal do Rio de Janeiro (MN), with the reference number 1104 Ardente et al. | Distribution of Glironia venusta and Chironectes minimus following Voss et al. C. (2001) are: Nasal Breadth (NB), minimussemiaquatic can be opossum found in (Marshall tropical and 1978b; subtropical Nowak habitats 1991). 5.85 mm; Least Interorbital Breadth (LIB), 6.74 mm; ofAccording Central and to South Brown America, (2004) in and Panama, Gardner northward (2008), into Least Postorbital Breadth (LPB), 8.46 mm; Zygomatic Breadth (ZB), 24.02 mm; Palatal Length (PL), 23.84 mm; Condylobasal Length (CBL), 39.18 mm; Palatal Breadth southern Mexico, in Colombia, Ecuador, Peru, Bolivia, (PB),The 11.21 monotypic mm; Maxillary genus Chironectes Toothrow (MTR), is represented 16.65 mm; by Paraguay, northeastern Argentina, in Venezuela, Guyana, MolarChironectes Length minimus (LM), 7.77 (Zimmermann, mm. 1780), a large and French Guiana, southern to Brazil. In the Brazilian Amazon, it is known from only four localities in the state of Pará: Utinga,Barcarena and (Pine was recently1973) and recorded according for tothree Brown localities (2004): in Cametá; “Peixe-boi” and Ilha das Onças, in et Belém al. 2007). and C. minimus is still a poorly understoodthe northwestern species of regarding Maranhão its state biogeographic-ecological (Oliveira featuresDespite along its wide the distribution, geographical distribution. According et al. (2009) this species does not show

otherto Galliez marsupial species. Chironectes minimus has some seasonality in its reproduction, as commonly observed in

morphological adaptations to semi-aquatic life, such as an Filhointerdigital et al. membrane in the hind feet, a developed pouch and a laterally compressed tail (Marshall 1978b; Monteiro- 2006). Individuals of water opossum are rarelyet al. captured (Bressiani and Graipel 2008) and few specimenset al. (2006)can be found considered in scientific it a common collections species. (Monteiro-Filho This information is 2006). However, Emmons (1990) and Monteiro-Filho C. minimus et al.in accordance with the methods frequently used to recordet al. 2001) and, such hand-captures as visual reports (Mares (Bergallo et al 1994; Voss 2001), firearms (Mondolfiet al. and Padilla 1958;et Vossal. 2006). .C. 1989; minimus González is not and Fregueiro 1998; Voss 2001; Graipel This difficulty is related to the fact that et al. Figure 2. Glironia venusta attracted to the bait in live traps (Voss and Emmons 1996; Monteiro-Filho and Graipel 2006; Monteiro-Filho (male, MN 75062), dorsal, ventral, and lateral 2006) and inhabit rivers and brooks, where it is difficult views of skull; Floresta Nacional de Carajás, Pará, Brazil.

Figure 3. Glironia venusta et al. et al. et al. et al. 2010), and Geographic the star represents distribution the newof record in Floresta. Black Nacional circles de represent Carajás, dataState from of Pará, literature Brazil. (Da Silva and Langguth 1989; Nogueira 1999; Bernarde and Rocha 2003; Díaz and Willig 2004; Santos-Filho 2007; Calzada 2008; Bernarde and Machado 2008; Gardner 2008; Rossi

1105 Ardente et al. | Distribution of Glironia venusta and Chironectes minimus

important because the Floresta Nacional de Carajás is the There are few records of this species, especially in largest remaining forest fragment in southeastern Pará in areasto set live outside traps. the shores of Brazil. The specimen of C. minimus collected manually, but was found dead in a road inside the importantgood conservation for future condition work with and this the species. area is set within a Floresta Nacionalsurveyed, de anCarajás, adult municipality male, was notof Parauapebas, trapped or complex of protected areas. Such information can be very

Pará, Brazil. It was prepared as a skeleton and deposited at the Museu Nacional, Universidade Federal do Rio de Janeiro (MN), with the reference number MN 78340. agreesHowever, with no the measurements description ofwere C. minimus undertaken (Zimmermann, due to the poor condition of the specimen (Figure 4). The specimen dark brown to black markings that consist of a narrow mid-dorsal1780), with stripedorsal fromcolor thepattern crown silvery to the gray, base overlaid of the with tail, interconnecting four broad blackish patches located, each one, over shoulders, in the center of back, hips, and lower contrastingrump (Figure with 4). theThe gray shoulder color andof the rump sides. patches The muzzle, extend crownlaterally of over the head,the legs. and The a band venter extending is bright through white, sharplythe eye to below the ear, are blackish-brown. The tail is either all Figure 4. Chironectes minimus from Floresta Nacional de Carajás, State of Pará, Brazil. Dorsal view of skin of (male, MN 78340) speciesblack or hasblack a for streamlined about 4/5 bodyof its shape,length and large yellowish- webbed hindwhite feet terminally (Figure 5), (Marshal dense and 1978b; non Nowak wettable 1991). fur. Water This in their opposable 6th opossums are unique among neotropical marsupials “ﬁnger” in the front feet, derived Nowakfrom a 1991). wrist bone, and also in that both sexes have a well-developedThe present record waterproof extends marsupium the geographic (Marshal distribution 1978b; of C. minimus about 558 km southward from the closest known locality in the state of Pará (Figure 6). This record is more inland the Brazilian Amazon, the remaining records are on the coast or on the edge of fragments in the extreme Figure 5. The large webbed hind feet of Chironectes minimus (male, MN southeast of the Brazilian Amazon Forest. This record is

78340) from Floresta Nacional de Carajás, State of Pará, Brazil.

Figure 6. Chironectes minimus et al. and the star represents the new record from Floresta Nacional de Carajás, in the State of Pará, Brazil. Geographic distribution of . Black circles represent data from literature (Brown 2004; Oliveira 2007; Gardner 2008),

1106 Ardente et al. | Distribution of Glironia venusta and Chironectes minimus

Acknowledgments: Chironectes minimus Zimmermann). Memoria de la We thank the Instituto Chico Mendes da Mondolfi,Fundación E. and La G.M.Salle de Padilla. Ciencias 1958. Naturales Contribución al conocimiento del Conservação da Biodiversidade (ICMBio) (License: IBAMA 009-B/2009 “perrito de agua” ( MAB/FAUNA) for permission to collect mammal specimens in the Floresta Natural da Cuíca-d’água Chironectes minimus 17: 141-155. e da cuíca-marrom Nacional Serra dos Carajás. This study was funded by Vale (previously Monteiro-Filho,Lutreolina crassicaudata E.L.A., M.E. Graipel and N.C.In Cáceres. 2006. História Cia. Vale do Rio Doce), and coordinated by Fernanda Martins-Hatano Monteiro-Filho (ed.). Marsupiais do Brasil: Biologia, Ecologia e from Universidade Federal Rural da Amazônia (UFRA). During the study, Evolução ; p. 287-295 Cáceres, N.C. and E.L.A. Natália Carneiro Ardente and Donald Gettinger received a grant from Vale-UFRA (process 02018.001735/2006-91). Helena G. Bergallo thanks . Campo Grande, MS: Editora da Universidade Federal do FAPERJ (E-26/103.016/2011), CNPq (307715/2009-4) and Prociência/ 17-27Mato Grosso In do Sul. Marsupiais do UERJLiterature for the researcherCited grants. Monteiro-Filho,Brasil: Biologia, E.L.A Ecologia and M.E. e Evolução Graipel. 2006. Captura e Marcação; p. Cáceres, N.C. and E.L.A. Monteiro-Filho (ed.) area in southeastern Brazil. Studies on Neotropical Fauna and . Campo1999. Grande, Morphology MS: Editora of the da Bergallo,Environment H.G. 1994. Ecology of a small mammal community in an Atlantic Universidade Federal do Mato Grosso do Sul. Nogueira, M.R., M.N F. da Silva, G.G.O. Câmara. 29:Glironia 197-217. venusta male genital system of the bushytailed opossum Glironia venusta Bernarde,to the state P.S. andof Acre, R.A. Brazil. Machado. Check 2008. List Mammalia, Didelphimorphia, Thomas, 1912 (Didelphimorphia,Walker’s mammals of the world (5th edition). 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A.L. 669 2008. p. 1-236.French Guiana: a neotropical lowland rainforest fauna: Nonvolant 1998.. Chicago: Primer The registro University de Chironectes of Chicago Mammal Species of the World: 263(2): a minimus Comunicaciones Taxonomic and Geographic Reference. González,Zoológicas E.M. del and Museo G. Fregueiro. de Historia Natural de Montevideo Wilson, D.E. and D.M. Reeder. 2005. para Uruguay (Mammalia, Didelphidae). GeographischeBaltimore: Geschichte Johns der Menschen, Hopkins 12: 1-8. undUniversity der algemein Press. 1945 verbreiteten p. vierfu¨ ssigen Thiere. Zweiter Band. Graipel, M.E., J.J. Cherem, E.L.A. Monteiro-Filho and L. Glock. 2006. Zimmermann, E. A. W. 1780. MastozoologiaDinâmica populacional Neotropical de marsupiais e roedores no Parque Municipal da Lagoa do Peri, Ilha de Santa Satarina, sul do Brasil. Leipzig:Wenganschen Buchhandlung, 2:6. distribution and ecology of 13(1): the mammals 31-49. of the cerrado grasslands Mares,of central M.A, J.K. Brazil. Braun Annals and of D.Carnegie Gettinger. Museum 1989. Observations on the Glironia venusta. Mammalian Species Received: June 2012 Chironectes minimus. Mammalian 58: 1-58. Species Accepted: September 2013 Marshall, L.G. 1978a. 107: 1-3. Published online: October 2013 Marshall, L.G. 1978b. 109: 1-6. Editorial responsibility: Ana Paula Carmignotto

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