Chiroptera Neotropical 20(1): 1237-1242, July 2014 1237 First ...

Chiroptera Neotropical 20(1): 1237-1242, July 2014 First occurrence of Molossus coibensis Allen, 1904 (Chiroptera, Molossidae) in Atlantic Forest Vinícius Pimenta*, Bruna S. Fonseca, João Paulo M. Hoppe, Albert D. Ditchfield Laboratório de Estudos em Quirópteros (LABEQ), Departamento de Ciências Biológicas, Universidade Federal do Espírito Santo (UFES), Avenida Marechal Campos, Bonfim, Vitória, Espírito Santo, CEP 29040-090, Brasil. * Corresponding author. [email protected] ARTICLE Manuscript history: Submmited in 31/Oct/2013 Accepted in 24/Mar/2014 Available on line in 30/Aug/2014 Editor: Maria João R. Pereira

Abstract. We report the first occurrence of the Coiban mastiff bat Molossus coibensis Allen, 1904 in the Atlantic Forest, and the third record of this species for Brazil. Our study is based on 39 adult specimens captured in Reserva Biológica de Sooretama, an Atlantic Forest preservation unit in Espírito Santo state, southeastern Brazil, apparently sharing the same shelter with M. molossus (Pallas 1776) and M. rufus E. Geoffroy, 1805. Morphological and morphometric data allows the confident separation of the two species of small Molossus. Keywords: Espírito Santo, New occurrence, Southeastern Brazil, Coiban mastiff bat

Introduction The genus Molossus Geoffroy, 1805 is characterized by smooth lips, minute tragus, a rounded antitragus constricted at its base, and short, rounded ears that arise from the same point on the forehead. The snout lacks a prominent longitudinal, medial ridge behind the nostrils. The sagittal crest is well developed in adults, the palate is arched, and the basisphenoid pits are distinct. Upper incisors are short, relatively broad, noncaniniform, and upper molars show little or no trace of a hypocone (Freeman 1981, Dolan 1989, Eger 2008). Molossids have a mostly Neotropical distribution, with eight or nine species recognized (Simmons 2005, González-Ruiz et al. 2011). In Brazil, the genus has a wide distribution, being easily found inhabiting human constructions such as bridges, rooftops, attics and buildings in general (Fabián & Gregorin 2007). There are six recognized species of Molossus in Brazil: M. aztecus Saussure, 1860 (Gregorin et al. 2011), M. currentium Thomas, 1901, M. molossus (Pallas 1766), M. pretiosus Miller, 1902, M. rufus E. Geoffroyi, 1805, and M. coibensis Allen, 1904 (Paglia et al. 2012). The Coiban mastiff, M. coibensis, was confirmed to occur in Brazil after Dolan (1989) synonymized it with M. cherriei Allen, 1916, known only from the holotype (AMNH 36669; skin only, the skull is lost), collected at Mato Grosso state, Tapirapuã (Gregorin et al. 2011), and formally included in

Brazil only in Simmons (2005). Recently, the species was reported in the Brazilian Amazon (Costa et al. 2013) based in eight females captured at Pará state, Bragança, making it the second confirmed occurrence for the species in Brazil. Furthermore, the species is known to occur in Colombia, Ecuador, French Guiana, Guyana, Panama, Peru, Venezuela and Mexico (Dolan 1989, Eger 2008). Molossus coibensis is the smallest species of the genus (forearm length = 33.5– 34.7 mm (Brazil, Costa et al. 2013), 32.6– 37.7 mm (Panama, Guyana, Peru; Dolan 1989, Lim & Engstrom 2001, Díaz 2011)). The dorsal pelage is short (2–3 mm), primarily deep black in color but varying to a chocolate brown tonality, with a small, weakly contrasting grayish band at the base (Dolan 1989, Díaz 2011). Here, we report a new occurrence of Molossus coibensis, the first for the Espírito Santo state, southeastern Brazil and the Atlantic Forest biome, and the third record for Brazil. Materials and Methods Study Area The Reserva Biológica de Sooretama has 24 250 hectares (coordinates: 18º33'–19º05' S, 39º55'–40º15' W), located mainly in the municipality of Sooretama, but also spanning two others in northern Espírito Santo (Jaguaré and Linhares), with a perimeter of 120 km, representing 0.5% of the state area (MMA 2007).

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Chiroptera Neotropical 20(1): 1237-1242, July 2014

This conservation unit is contiguous with the Reserva Florestal Vale do Rio Doce, and together they form the largest and best reserved Atlantic Forest fragment of the Espírito Santo, favoring a great biodiversity (IPEMA 2007). The dominant vegetation type is lowland dense tropical rain forest, commonly known as “Mata de Tabuleiros”. The climate is classified as Tropical Highland (Cwb in Koppën's classification), with a rainy season in the summer and a short dry season in the winter. Mean temperatures is 23 ºC ranging between 19.9 ºC to 25.6ºC, and annual precipitation of 1 250.5 mm (range: 810.6 – 1 638.8 mm) (MMA 2007). Sampling We opened two mist-nets in front of the lodging for researchers of the Reserva Biológica de Sooretama (19º03'20.60"’ S, 40º08'50.75" W; altitude 94 m), one meter from the ground, in five nights of work between October 2008 and May 2009. Captured animals were fixed in formaldehyde, and then preserved in alcohol 70% with the skull removed and cleaned using skin beetles (Coleoptera: Dermestidae). We also extracted a sample of liver tissue, preserved in alcohol 70% and maintained at –10 ºC. All material is housed at the Laboratório de Estudos em Quirópteros (LABEQ), Universidade Federal do Espírito Santo (UFES), under the acronym VP (personal catalogue of Vinícius T. Pimenta) (see Appendix). All animals captured were kept in cotton bags for a half hour to collect the feces samples. The feces are preserved in alcohol 70%. Identification All captured specimens had their external characters analyzed during fieldwork, being: forearm length, body mass, sex, pelage color. For the collected individuals, we also took measurements of the skull following the methodology of Vizzoto & Taddei (1973): total length (Ct), condyle-basal length (Cb), condylecanine length (Cc), basal length (B), palatal length

(Cpt), upper toothrow length (CM-S), mandibular length (Cm), lower toothrow length (CM-I), width across upper canines (Lc), external width between upper molars (Lm), post-orbital length (Lpo), braincase breadth (Lcx), mastoid breadth (Lmt), and zygomatic breadth (Lz). We also measured the upper canine length (CC-S) and the distance between the coronoid and angular process (Ca). We ran a Principal Component Analysis (PCA) using all skull measurements of the collected M. coibensis and M. molossus, analyzing males and females separately due to the sexual dimorphism common in the family Molossidae (Freeman 1981). We also did a Mann-Whitney test comparing the forearm length of M. coibensis and M. molossus, and comparing the same variable between males and females of each species, in order to verify sexual dimorphism in size. Results We recorded 148 captures of three species of the genus Molossus, apparently sharing the same shelter, a space between the roof and wood lining of the lodging for researchers of the Reserva Biológica de Sooretama. Almost 60% of our captures were of M. molossus (n=88), followed by M. coibensis (n=39) and M. rufus (n=21). The animals were observed in daytime, however we only managed to capture them with mist-nets at nightfall, when they exited the roof. For M. coibensis, we caught 24 females and 15 males. Pregnant females were captured in October (n=4), November (n=3) and January (n=4). Lactating females were not observed. No clear reproductive pattern was detected in the males. Fragments of weevils (Coleoptera: Curculionidae) were present in their feces samples. The activity period of M. coibensis seemed to begin 30 minutes before the sunset, similar to the pattern presented by M. molossus. Molossus coibensis and M. molossus are both small species of Molossus, but there are various characters that permitted the confident

Table 1: External characters utilized for the identification of Molossus coibensis and Molossus molossus collected at the Reserva Biológica de Sooretama. Forearm length and weight are provided separated for males and females. Means are followed by range (in parentheses), and one standard deviation of the mean.

Forearm (mm) Weight (g) Dorsal hair (mm) Dorsal pelage Ventral pelage Upper incisors Basal band of the dorsal hair

Molossus coibensis Males Females 37.37(36.5 37.17(35.5 38.1)0.46 38.1)0.65 15.06(13.0 15.98(12.0 18.0)1.70 20.5)2.45 Shorter (2.6 - 3.1) Deep black Lighter brown Spatulated

Molossus molossus Males Females 40.23(38.2 39.24(35.3 42.3)1.22 42.2)1.68 17.08(12.0 15.97(11.5 23.5)2.34 21.0)2.35 Longer (3.6 - 4.8) Brown Lighter brown Pointed

Grayish

1/2 to 1/3 White

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Table 2: Skull measurements (in mm) of males and females of Molossus coibensis and Molossus molossus collected at the Reserva Biológica de Sooretama. Means are followed by range (in parentheses), and one standard deviation of the mean. Acronyms for the characters in the Materials and Methods. *Only one individual available. M. coibensis

M. molossus

Males

m

Females

m

Males

m

Females

m

TL CC CB

16.77-17.34 14.83-15.26 15.5-15.71

17.07 15.63 15.10

16.05-16.75 14.45-15.04 14.6-15.25

16.51 14.69 14.97

17.4-17.83 15.75-15.96 15.71-16.58

17.64 15.88 16.25

16.56-16.73 15.04-15.08 15.49-15.64

16.65 15.07 15.57

B PL Cm2/3U CM Cm2/3L WC WM PoL ZB

12.03-12.48 5.04-5.35 5.84-6.18 11.54-11.79 6.64-6.88 4.62-4.85 7.98-8.11 3.83-4.05 11.21-11.55

12.33 5.22 6.03 11.71 6.75 4.72 8.06 3.94 11.34

11.73-12.68 4.9-5.12 5.81-6.01 11.04-11.66 6.4-6.56 4.4-4.52 7.48-7.8 3.71-3.83 10.57-11.01

12.18 5 5.91 11.3 6.51 4.43 7.69 3.78 10.77

13.07-13.38 5.58-5.78 6.18-6.33 11.86-12.37 6.83-7.19 4.41-4.61 7.77-7.8 3.66-3.92 10.95-11.47

13.22 5.69 6.26 12.19 7.06 4.54 7.79 3.77 11.18

12.67-12.78 5.07-5.55 6.03-6.04 11.41-11.44 6.67-6.83 4.15-4.33 7.61-7.69 3.57-3.68 10.63-10.74

12.74 5.31 6.05 11.43 6.74 4.22 7.65 3.62 10.70

BB MB PW

9.41-9.77 11.02-11.21 3.53-3.66

9.59 11.05 3.6

9.06-9.4 9.96-10.75 3.22-3.67

9.20 10.45 3.41

8.87-9.46 10.77-11.08 3.37-3.67

9.18 10.96 3.48

8.85-9.25 10.12-10.34 3.4-3.42

9.07 10.25 3.41

CA CL

5.07-5.24 2.71-2.86

5.18 2.80

4.84-5.21 2.21-2.37

5.01 2.31

5.48-5.7 2.78-3.1

5.57 2.98

4.46-4.85 2.48-2.54

4.71 2.51

Total

4

4

3

identification of the specimens. Externally, M. coibensis has shorter dorsal pelage, deep black in color with a weakly contrasting grayish at the base of the hair, and a dark brown belly. In contrast, M. molossus has a longer dorsal pelage, lighter brown with a distinct white color at the base, ranging from a third to a half of the length of the hair. The belly also is a lighter brown. They also differ in forearm length, with M. coibensis shorter than M. molossus (Table 1). The skull of M. coibensis is shorter, with a braincase more globular than M. molossus (Figure 1). M. coibensis also has a shorter rostrum, thereafter have shorter upper and lower toothrow, showing little overlap between these characters (Table 2). The upper incisors are more spatulated, while in M. molossus they are more conical and pointed. We observed greater mean values for all the skull measurements between the males and females of M. coibensis and M. molossus, with

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small overlap between any given parameter (Table 2). The PCA revealed two groups based on the size, PC1, separating the males and females of M. coibensis and M. molossus (Figure 2, Table 3), but no clear separation between the species. However, the PC2, describing mostly the breadth of the rostrum, distinguishes both species clearly. For M. coibensis, a 95% confidence interval shows differentiation of males and females, although there is an overlap of both sexes in our data (Figure 2). The Mann-Whitney tests revealed a significant difference between the forearm length of both species (W = 3040, p-value < 0.001), but not between males and females of each species (M. coibensis: W = 191.5, p-value = 0.2425; M. molossus: W = 741, p-value = 0.3981). Our sample of external and skull characters is too small to concretely establish a reliable effect, but the distribution of the specimens on PC space

Figure 1: Skulls of adult males of Molossus coibensis (VP 84) (A) and Molossus molossus (VP 25) (B) in superior view.

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suitable to species delimitation (Gregorin et al. 2011). Dolan (1989) still is the major revision for the genus, however it is focused on a Central America sampling, leading to problems when applied to South America populations. For example, Freeman (1981) believed that Molossus coibensis did not constitute a full species, more likely a subspecies of M. bondae or M. molossus, and Eger (2008) synonymized M. coibensis with M. barnesi, a question still unsolved (Gregorin et al. 2011). Although there is a number of revisions for the group in South America (e.g. Simmons & Voss 1998), they are locally restricted, and the taxonomy of the Molossus is considered provisional, pending morphometric and genetic studies focusing in the entire continent (Lim & Engstrom 2001). Figure 2: Scatterplot of individual loadings of the first two The external and skull characters used principal components (PC1 and PC2) based on 14 cranial variables. Molossus coibensis – circles, Molossus molossus – in this study clearly separate the small triangles; males – black symbols, females – white symbols. Dashed Molossus that occurs in Espírito Santo lines – separation in PC space of M. coibensis and M. molossus, state. We observed somewhat larger solid lines – separation in PC space of males and females of M. individuals in the Atlantic Forest than those coibensis. given in the literature. The forearm length (FA) has a mean of 36.72 ± 0.76 mm, (range = 35.95–37.87 mm) for this biome. In the Table 3: Eigenvectors of the first and second principal components (PC1 and Brazilian Amazon, Costa et al. (2013) reported FA PC2) of Molossus based on 14 skull ranging between 33.5 to 34.7 mm, based on 6 characters. Acronyms for the characters adult females. For the Cerrado of Mato Grosso, in the Materials and Methods. the holotype of M. cherriei, now recognized as a M. coibensis, has a FA of 33.8 mm (Simmons & Variables PC1 PC2 Voss 1998). For Panama, Dolan (1989), based on Ct -0.3220 0.0241 two populations and 74 specimens, reported FA Cb -0.3311 -0.0897 between 32.6 to 36.8 mm, males larger than Cc -0.3319 -0.1388 females. Lim & Engstrom (2001) founded FA B -0.2762 -0.2615 varying between 35–36 mm, based on three males Cpt -0.2808 -0.1722 and three females. In the Peruvian Amazon, a CM.S -0.2653 -0.1931 study with 15 specimens reported FA from 34.54 Cm -0.3103 -0.1415 to 37.70 mm (Díaz 2011). CM.I -0.3429 -0.0280 This can be explained due to two factors: (1) Lc -0.1637 0.4144 the first occurrence of the species in the Atlantic Lm -0.1466 0.4351 Forest, and (2) the overall low sampling of the Lpo -0.0510 0.4508 species. As we said before, there is great Lcx -0.1148 0.4131 uncertainty in the taxonomy of South American Lmt -0.2547 0.2778 Molossus, and given the anterior classification of CC.S -0.3291 0.0623 “large” and “small” Molossus in M. rufus and M. suggests differentiation of the skull not only due molossus only, we can expect that many to taxonomy but sexual dimorphism too, although specimens of M. coibensis (and other small this view is not supported by the Mann-Whitney Molossus) have been misidentified as M. molossus statistics in inventory works and museum collections (Gregorin et al. 2011). Even with our small Discussion and Conclusions sample, we could separate both species based on The genus Molossus has a very difficult external and skull data. However, despite the taxonomic history, especially regarding the small differences between the measurements of males sized species. Mostly, the taxonomic problem is and females in Molossus coibensis and M. due to poor diagnoses provided for each taxon, molossus (Table 1, Table 2), they are not using characters that have too much variation, significant in the statistical analysis. overlapping between species, therefore not

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The occurrence of M. coibensis in the Atlantic Forest is unexpected given the data in the literature. Paglia et al. (2012) provided a geographic range for M. coibensis that included the Brazilian Amazon and Cerrado biomes, despite the fact that the only specimen known at the time, the holotype of M. cherriei, occurs in the Cerrado. Probably they asserted this range due to the proximity of the locality with the Amazon and Pantanal biomes. Posteriorly, an occurrence was reported in the Amazon (Costa et al. 2013), supporting Paglia et al. (2012). Our study amplifies this distribution (Figure 3), further supporting that the species has a wide distribution in Brazil throughout the Amazon, Cerrado, Pantanal and Atlantic Forest biomes, probably unrecorded due to difficulties in identification of the species and poor sampling in Brazil. Acknowledgments Authors would like to thank Renato Gregorin for help in identification of the specimens, Alexandre P. Aguiar for help in identification of insect fragments present in the feces samples, Carlos T. Machel and Tatiana M. Miranda for their assistance in fieldwork, and all the reserve personnel who granted access and lodging during

our research. Thanks to two anonymous reviewers, whose contributions and suggestions greatly improved the manuscript. We also thank the Instituto Brasileiro de Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA) for permission to capture and collect bats at the Reserva Biológica de Sooretama (17416-1, emission September 29, 2008). Vinícius Pimenta received a fellowship granted by Fundação de Amparo à Pesquisa do Espírito Santo (FAPES). References Costa L.J.C.; Andrade F.A.G.; Uieda W.; Gregorin R. & Fernandes M.E.B. 2013. First record of Molossus coibensis (Chiroptera: Molossidae) in the Brazilian amazon. Mastozoología Neotropical 20(1): 143–147. Díaz M.M. 2011. New records of bats from the northern region of the Peruvian Amazon. Zoological Research 32(2): 168–178. Dolan P.G. 1989. Systematics of Middle American mastiff bats of the genus Molossus. Special Publications, The Museum Texas Tech University 29: 1–71. Eger J.L. 2008 [2007]. Family Molossidae P. Gervais, 1856. In: Mammals of South America, Volume 1: Marsupials, Xenarthrans, Shrews,

Figure 3: Occurrences of Molossus coibensis in Brazil. Light green area corresponds to the Atlantic Forest area in Brazilian territory, and the asterisk marks the new record in Espírito Santo. Zoomed area details the northern area of Espírito Santo and the perimeter of the Reserva Biológica de Sooretama with the new occurrence. Specific localities are listed: Mato Grosso, Tapirapoan (14º51' S, 57º45' W), (AMNH 36669, holotype of Molossus cherriei) (Dolan 1989); Pará, Bragança (1º13'13" S, 46º45'56" W) (Costa et al. 2013); Espírito Santo, Reserva Biológica de Sooretama (19º03'20.60" S, 40º08'50.75" W).

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and Bats (edited by Gardner A.L.), pp. 399– 440. The University of Chicago Press, Chicago and London. Fabián M.E. & Gregorin R. 2007. Família Molossidae. In: Morcegos do Brasil (edited by Reis N.R.; Peracchi A.L.; Pedro W.A. & Lima I.P.), pp. 149–165. Biblioteca Central da Universidade de Londrina, Londrina. Freeman P.W. 1981. A multivariate study of the family Molossidae (Mammalia, Chiroptera): Morphology, ecology, evolution. Fieldiana Zoology 7: vii+1–173. González-Ruiz N.; Ramírez-Pulido J. & ArroyoCabrales J. 2011. A new species of mastiff bat (Chiroptera: Molossidae: Molossus) from Mexico. Mammalian Biology 76(4): 461–469. Gregorin R.; Tahara A.S. & Buzzato D.F. 2011. Molossus aztecus and other small Molossus (Chiroptera: Molossidae) in Brazil. Acta Chiropterologica 13(2): 311–317. Gregorin R. & Taddei V.A. 2002. Chave artificial para a identificação de molossídeos brasileiros (Mammalia, Chiroptera). Mastozoologia Neotropical 9(1): 13–32. Instituto de Permacultura e Ecovilas da Mata Atlântica – IPEMA. 2007. Conservação da Mata Atlântica no estado do Espírito Santo: cobertura florestal e unidades de conservação. 1 ed. Vitória, p. 1–152. Lim B.K. & Engstrom M.D. 2001. Species diversity of bats (Mammalia: Chiroptera) in Iwokrama Forest, Guyana, and the Guianan subregion: implications for conservation. Biodiversity and Conservation 10(4):613–657. Ministério do Meio Ambiente – MMA. 2007. Plano operativo de prevenção e combate aos incêndios florestais da Reserva Biológica de Sooretama. Sooretama, pp. 1–29. Paglia A.P.; Fonseca G.A.B.; Rylands A.B.; Herrmann G.; Aguiar L.M.S.; Chiarello A.G.; Leite Y.L.R.; Costa L.P.; Siciliano S.; Kierulff M.C.M.; Mendes S.L.; Tavares V.C.; Mittermeier R.A. & Patton J.L. 2012. Annotated checklist of Brazilian Mammals, 2nd edition. Occasional Papers in Conservation Biology 6: 1–76. Simmons N.B. 2005. Order Chiroptera. In: Mammals Species of the World: A taxonomic and geographic reference (edited by Wilson D.E. & Reeder D.M.), pp. 312–529. John Hopkins University Press, Baltimore. Simmons N.B. & Voss R.S. 1998. The mammals of Paracou, French Guiana: A neotropical lowland rainforest fauna Part 1. Bats. Bulletin of the American Museum of Natural History 237: 1–219.

Vizotto L.D. & Taddei V.A. 1973. Chave para determinação de Quirópteros brasileiros. Boletim de Ciências da Faculdade de Filosofia, Ciências e Letras de São José do Rio Preto 1: 172. Appendix: Collected specimens of Molossus at the Reserva Biológica de Sooretama, housed at Laboratório de Estudos em Quirópteros (LABEQ) at the Universidade Federal do Espírito Santo (UFES). * Juvenile.

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Specimen nº VP 26

Species

Sex

Molossus coibensis

Male

VP 40

Molossus coibensis

Male

VP 67* VP 80

Molossus coibensis Molossus coibensis

Male Male

VP 83

Molossus coibensis

Male

VP 66

Molossus coibensis

Female

VP 71 VP 84

Molossus coibensis Molossus coibensis

Female Female

VP 93

Molossus coibensis

Female

VP 25 VP 65

Molossus molossus Molossus molossus

Male Male

VP 81

Molossus molossus

Male

VP 22 VP 41

Molossus molossus Molossus molossus

Female Female

VP 43

Molossus molossus

Female