Review of the distribution of Lophostoma carrikeri (Chiroptera: Phyllostomidae), with range extension to transitional vegetation zones in the southwestern Amazon

Revisão da distribuição geográfica de Lophostoma carrikeri (Chiroptera: Phyllostomidae), com ampliação de distribuição em áreas de transição no sudoeste da Amazônia

ABSTRACT

Lophostoma carrikeri has been mostly recorded within the Amazon biome. There are scarce records in the northern Brazilian Amazon, but also records outside this biome, which were neglected in literature. The aim of this study was to update and extend the distribution of L. carrikeri. Seven new localities in Brazil were provided, including the first records for the states of Rondônia and Mato Grosso, filling a large gap in the species distribution, and three additional records for the state of Pará. Our results reinforce the notion that L. carrikeri is widely distributed in the Amazon, but is also present in other biomes in Brazil, such as Caatinga, Cerrado, and transitional areas.

KEYWORDS:
Carriker’s round-eared bat; Phyllostomini; savanna; rainforest; ecotone

RESUMO

Lophostoma carrikeri tem sido registrado principalmente no bioma Amazônia. Há escassos registros no norte da Amazônia brasileira, mas também há registros fora deste bioma que foram negligenciados na literatura. Nosso objetivo foi atualizar e ampliar a distribuição de L. carrikeri. Reportamos sete novas localidades no Brasil, incluindo os primeiros registros para Rondônia e Mato Grosso, preenchendo uma grande lacuna na distribuição desta espécie, e três registros adicionais para o Pará. Nossos resultados reforçam a noção de que L. carrikeri é amplamente distribuída na Amazônia, mas também está presente em outros biomas, como Caatinga e Cerrado, além de áreas de transição.

PALAVRAS-CHAVE:
morcego; Phyllostomini; savana, floresta tropical; ecotono

Lophostoma carrikeri (J.A. Allen 1910), the Carriker’s round-eared bat, is one of the species of round-eared bats endemic to South America (Williams and Genoways 2008; Camacho et al. 2014). Despite its wide distribution, only a few records of L. carrikeri are known from central Colombia (McCarthy et al. 1983), Guyana (Lim et al. 1999), Venezuela (Allen 1910; Gardner 1988), French Guiana (Williams and Genoways 2008), Suriname (Genoways and Williams 1984; Lim et al. 2005), south and northeastern Ecuador (Camacho et al. 2014), east and northeastern Peru (Gardner 1976; Solari et al. 2006), northern Bolivia (Koopman 1976), and northern and central Brazil (Gribel and Taddei 1989; Gregorin et al. 2008, 2011; Sampaio et al. 2003; Dias et al. 2009; Santos et al. 2009; Zortéa et al. 2009).

Generally associated with forested habitats, most records of L. carrikeri are from the Amazon (Williams and Genoways 2008; Velazco and Gardner 2012). The most recent taxonomic revision and geographic distribution for the species (Camacho et al. 2014; Camacho et al. 2016) lists a single record in Brazil outside of the Amazon (from Teresina, Piauí state) (Vizotto et al. 1980). However, other records are known for the Cerrado savanna (Zortéa et al. 2009; Gregorin et al. 2011) and the xerophytic Caatinga region (Gregorin et al. 2008), in central and northeastern Brazil, respectively. Thus, most recent publications describe the distribution of L. carrikeri in Brazil as scattered and mostly restricted to the northern portion of the country. Here, we review the known records of L. carrikeri in Brazil and report a range extension to the western portion of the country, including the first record in transitional areas between the Amazon and Cerrado biomes.

Specimens analyzed here (Table 1) are deposited in Zoology Museum of Universidade de São Paulo (MZUSP), São Paulo, Brazil. We measured specimens according to Camacho et al. (2016). Most individuals refer to recent captures with the use of mist-nets at ground level and were handled according to Sikes et al. (2011), fixed in 10% formaldehyde and preserved in 70% ethanol. Some records are from faunal monitoring for a hydroelectric dam on the upper Madeira River (Rondônia state) and mining areas in the Comodoro municipality (Mato Grosso state). Other records refer to museum specimens. Voucher MZUSP 22707 (skin and skull, Figure 1) refers to the uncatalogued specimen reported by McCarthy and Handley (1987).

Table 1
Data on specimens of Lophostoma carrikeri reported in the present study. The locality number refers to Figure 3.

Voucher	Locality	Biome	Habitat	Date of capture	Sex	Reproductive stage
MZUSP 35889	1	Amazon/Cerrado	Ecotone	06 Nov 2008	♂	Scrotal testes
Released animal	2	Amazon/Cerrado	Ecotone	04 Sep 2012	♀	Pregnant (Figure 2)
MZUSP 35887, 35888	3, 4	Amazon	Primary rainforest	29 Aug 2010 16 Jul 2015	♂	All with scrotal testes (Figure 2)
MZUSP 35890	5	Amazon	Primary rainforest	30 Mar 2008	♂	-
MZUSP 35886	6	Amazon	Primary rainforest	07 Dec 2008	♀	Pregnant
MZUSP 22707	7	Amazon	Riparian rainforest	18 Oct 1986	♀	Lactating

Figure 1
Dorsal, ventral and lateral views of the skull and lateral view of the mandible of Lophostoma carrikeri (MZUSP 22707).

Lophostoma carrikeri can be distinguished from congeners by a suite of morphological characters: medium size (forearm length > 42 mm) (Table 2); lack of small wart-like granulations on head, wings, and legs; flanks, shoulders and anal region have a pale grayish-brown pelage; white hairs on the throat and chest, which may extend to the abdomen (Figure 2); basisphenoid pits well developed and divided by a median septum; sagittal crest usually high and well developed (Figure 1) (Velazco and Gardner 2012; Camacho et al. 2016; Díaz et al. 2016).

Table 2
External and craniodental measurements of Lophostoma carrikeri from this study (MZUSP 22707) and the literature (values are the mean ± SD and the range).

Measurement (in mm)	MZUSP 22707	Camacho et al . (2016) 2 (n = 16)
Forearm length	47	45.6 ± 1.5 (42.2 - 47.7)
Greatest length of skull	23.9	24.3 ± 0.9 (23.0 - 26.6)
Metacarpal III length	36	37.7 ± 1.4 (34.1 - 40.0)
Condyloincisive length	20	21.0 ± 0.8 (19.8 - 23.0)
Condylocanine length	19.1	20.3 ± 0.7 (19.0 - 21.3)
Braincase breadth	9.5	9.6 ± 0.3 (9.0 - 10.3)
Zygomatic breadth	10.7	11.2 ± 0.6 (10.3 - 12.7)
Postorbital breadth	3.2	3.8 ± 0.2 (3.3 - 4.1)
Mastoid width	11.2	9.6 ± 0.3 (9.0 - 10.2)
Palatal length	8.9	10.5 ± 0.5 (9.2 - 11.1)
Maxillary toothrow length	7.7	8.3 ± 0.4 (7.7 - 9.4)
Molariform toothrow length	5	6.8 ± 0.3 (6.0 - 7.3)
Width at M2	5.6	7.6 ± 0.4 (7.1 - 8.8)
Dentary length	20	15.0 ± 0.7 (13.8 - 16.9)
Mandibular toothrow length	9	9.3 ± 0.6 (8.6 - 11.0)
Coronoid height	5.6	5.6 ± 0.5 (5.0 - 7.0)

Figure 2
Lophostoma carrikeri captured in locality 3 (A) and 2 (B) from Figure 3. This figure is in color in the electronic version.

We obtained seven new records of Lophostoma carrikeri in Brazil (Table 1), three from the central and eastern Amazon (Pará state), two from the southwestern Amazon (Rondônia state), and two from transitional areas between the Amazon and Cerrado in Mato Grosso state (Figure 3). The specimens include three reproductive males, collected in July, August and November (Rondônia and Mato Grosso), two pregnant females in September and December (Mato Grosso and Pará) (Table 1). Non-reproductive females have been reported in April and November (Colombia), July (Peru) and August (Suriname); lactating females in June and September (Ecuador), May (Suriname) and October (Pará, Brazil) (Williams and Genoways 2008; Camacho et al. 2014). Although limited, our data fit the bimodal reproduction pattern for L. carrikeri suggested by McCarthy et al. (1992).

Figure 3
Geographic distribution of Lophostoma carrikeri in South America and Brazil (detailed map). Present records: BRAZIL: Mato Grosso state: (1) Juína (-11.553055,-58.3425), (2) Comodoro (-13.79772,-60.457181); Rondônia state: (3, 4) Madeira River, Mutum Paraná (-9.43694,-64.830432; -9,591301,-65,048552); Pará state: (5) FLONA Tapirapé-Aquiri, Marabá (-5.7666,-50.5000), (6) Porto de Moz (-1.735591,-52.235599), (7) Iriri River, Altamira (-3.8333,-52.6666). Coordinates datum SAD 69. Literature records: BRAZIL: Roraima state: (8) Ilha de Maracá, Amaraji; Amazonas state: (9) Biological Dynamics of Forest Fragments Project site, 80 km N of Manaus; Pará state: (10) Floresta Nacional do Tapajós, (11) Belterra, 30 km SW of Santarém, (12) Parque Nacional da Amazônia, Santarém; (13) Utinga, Belém; Piauí state: (14) Teresina, (17) Parque Nacional da Serra das Confusões, Guaribas; Maranhão state: (15) Povoado Quebra-Pote, São Luís; Amapá state: (16) Highway BR-156, Reserva Extrativista do Rio Cajari; Tocantins state: (18) Estação Ecológica Serra Geral do Tocantins, Jalapão; Goiás state: (19) São Domingo. Vegetation distribution according to Olson et al. (2001). This figure is in color in the electronic version.

The new records presented herein help to fill a large gap between the southern records known for the species in northern Bolivia to those in northern Pará and Amazonas states (Velazco and Gardner 2012; Camacho et al. 2014), extending 750 km eastwards from the nearest record in northern Bolivia and to the southeastern range of the species in the Amazon (Figure 3). Most of the new records are in the Amazon, but two are from transitional areas between the Amazon and Cerrado in Mato Grosso state. Such areas are characterized by a mosaic of phytophysiognomies, where savannas and forests mingle and the climate is markedly seasonal (Veloso et al. 1991). In dry forests of Cerrado and Caatinga (Zortéa et al. 2009; Gregorin et al. 2008; 2011) most L. carrikeri specimens were captured in Cerrado riparian forests, or near wet areas in Caatinga. Thus, the recent records indicate that L. carrikeri can dwell in dry forests near mesic areas.

The new records from Mato Grosso and Rondônia lie in an area where several new records of bat species have been recently reported (e.g. Rocha et al. 2015; Brandão et al. 2016; Dalponte et al. 2016;Pedroso et al. 2018). Western Brazil is a highly diverse area, not only for bats but for other mammals as well (Brandão et al. 2019), where field-survey efforts should be increased and fauna conservation deserves higher attention.

ACKNOWLEDGMENTS

We thank Instituto Chico Mendes de Conservação da Biodiversidade and Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis for the licenses provided (CGFAP 215/2010, 260/2010, 190/2012; 52/2012), Arcadis Logos S/A, and L.F. Silveira and J.G. Barros (MZUSP). PAR thanks Coordenação de Aperfeiçoamento de Pessoal de Nível Superior − CAPES (Process: 88882.317933/2019-01).

REFERENCES

• Allen, J.A. 1910. Mammals from the Caura District of Venezuela, with description of a new species of Chrotopterus Bulletin of the American Museum of Natural History, 28: 145-149.
• Brandão, M.V.; Rocha, P.A.; Mendes, P.; Bernardo, P.V.; Cunha, I.N.; Colas-Rosas, P.F.; Pedroso, M.A.; Aquino, C.C.; Aires, C.C. 2016. Lampronycteris brachyotis (Dobson, 1879): filling gaps and the first record from Rondônia and Goiás states, Brazil. Mastozoología Neotropical, 23: 147-155.
• Brandão, M.V.; Garbino, G.S.T.; Semedo, T.B.F.; Feijó, A.; Nascimento, F.O.; Fernandes-Ferreira, H.; Vieira Rossi, R.V.; Dalponte, J.; Carmignotto, A.P. 2019. Mammals of Mato Grosso, Brazil: Annotated species list and historical review. Mastozoología Neotropical, 6: 263-307.
• Camacho, M.A.; Tirira, D.G.; Dick, C.W.; Burneo, S.F. 2014. Lophostoma carrikeri (Allen, 1910) (Chiroptera: Phyllostomidae): First confirmed records in Ecuador. Check List, 10: 217-220.
• Camacho, M.A.; Chávez, D.; Burneo, S.F. 2016. A taxonomic revision of the Yasuni Round-eared bat, Lophostoma yasuni (Chiroptera: Phyllostomidae). Zootaxa, 4114: 246-260.
• Dalponte, J.C.; Gregorin, R.; Esteves-Costa, V.A.; Rocha, E.C.; Marcelino, R. 2016. Bat survey of the lower Juruena River and five new records for the state of Mato Grosso, Brazil. Acta Amazonica, 46: 227-232.
• Dias, P.A.D.; Santos, C.L.C.; Rodrigues, F.S.; Rosa, L.C.; Lobato, K.S.; Rebelo, J.M.M. 2009. Espécies de moscas ectoparasitas (Diptera, Hippoboscoidea) de morcegos (Mammalia, Chiroptera) no estado do Maranhão. Revista Brasileira de Entomologia, 53: 128-133.
• Díaz, M.M.; Solari, S.; Aguirre, L.F.; Aguiar, L.; Barquez, R.M. 2016. Clave de identificación de los murciélagos de Sudamérica Publicación Especial 2, Programa de Conservación de los Murciélagos de Argentina, Tucumán, Argentina, 160p.
• Gardner, A.L. 1976. The distributional status of some Peruvian mammals. Occasional Papers of the Museum of Zoology, Louisiana State University, 48: 1-18.
• Gardner, A.L. 1988. The mammals of Parque Nacional Serranía de la Neblina, Territorio Federal Amazonas, Venezuela. In: Brewer-Carías, C. (Ed.). Cerro La Neblina: Resultados de la Expedición 1983-1987 Editorial Sucre, Caracas, p.695-765.
• Genoways, H.H.; Williams, S.L. 1984. Results of the Alcoa Foundation-Suriname Expeditions. IX. Bats of the genus Tonatia (Mammalia: Chiroptera) in Suriname. Annals of the Carnegie Museum, 53: 327- 346.
• Gregorin, R.; Carmignotto, A.P.; Percequillo, A.R. 2008. Quirópteros do Parque Nacional da Serra das Confusões, Piauí. Chiroptera Neotropical, 14: 366-383.
• Gregorin, R.; Gonçalves, E.; Aires, C.C.; Carmignotto, A.P. 2011. Bats (Mammalia: Chiroptera) from Estação Ecológica Serra Geral do Tocantins.Biota Neotropica, 11: 299-311.
• Gribel, R.; Taddei, V.A. 1989. Notes on the distribution of Tonatia schulzi and Tonatia carrikeri in the Brazilian Amazon. Journal of Mammalogy, 70: 871-873.
• Koopman, K.F. 1976. Zoogeography. In: Baker, R.J.; Jones Jr., J.K.; Carter, D.C. (Eds.). Biology of bats of the New World family Phyllostomidae Part I. Special Publications 10, Museum of Texas Tech University, Lubbock, p.39-47.
• Lim, B.K.; Engstrom, M.D; Timm, R.M.; Anderson, R.P.; Watson, L.C. 1999. First records of 10 bat species in Guyana and comments on diversity of bats in Iwokrama Forest. Acta Chiropterologica, 1: 179-190.
• Lim, B.K.; Engstrom, M.D.; Genoways, H.H.; Catzeflis, F.M.; Fitzgerald, K.A.; Peters, S.L.; Djosetro, M.; Brandon, S.; Mitro, S. 2005. Results of the Alcoa Foundation-Suriname Expeditions. XIV. Mammals of Brownsberg Nature Park, Suriname. Annals of the Carnegie Museum, 74: 225-274.
• McCarthy, T.J.; Cadena, G.A.; Lemke, T.O. 1983. Comments on the first Tonatia carrikeri (Chiroptera: Phyllostomidae) from Colombia. Lozania, 40: 1-6.
• McCarthy, T.J.; Handley, C.O.Jr. 1988. Records of Tonatia carrikeri (Chiroptera: Phyllostomidae) from the Brazilian Amazon and Tonatia schulzi in Guyana. Bat Research News, 28: 20-23.
• McCarthy, T.J.; Gardner, A.L.; Handley-Jr, C.O. 1992. Tonatia carrikeri Mammalian Species, 407: 1-4.
• Olson, D.M.; Dinerstein, E.; Wikramanayake, E.D.; Burgess, N.D.; Powell, G.V.N.; Underwood, E.C et al 2001. Terrestrial ecoregions of the world: a new map of life on Earth.BioScience 51: 933-938.
• Pedroso, M.A.; Rocha, P.A.; Brandão, M.V.; Garbino, G.S.T.; Moraes, C.O.; Aires, C.C. 2018. Filling gaps in the distribution of the white winged vampire bat, Diaemus youngii (Phyllostomidae, Desmodontinae): new records for southern Amazonia. Acta Amazonica, 48: 154-157.
• Rocha, P.A.; Brandão, M.V.; Aires, C.C.; Cezari, A. 2015. Range extension of Centronycetris maximiliani (Mammalia: Chiroptera) for southern Amazonia. Acta Amazonica, 45: 425-430.
• Santos, C.L.C.; Dias, P.A.; Rodrigues, F.S.; Lobato, K.S.; Rosa, L.C.; Oliveira, T.G.; Rebêlo, J.M.M. 2009. Moscas ectoparasitas (Diptera: Streblidae) de morcegos (Mammalia: Chiroptera) do município de São Luís, MA: taxas de infestação e associações parasito-hospedeiro. Neotropical Entomology, 38: 595-601.
• Sampaio, E.M.; Kalko, E.K.; Bernard, E., Rodríguez-Herrera, B.; Handley, C.O. 2003. A biodiversity assessment of bats (Chiroptera) in a tropical lowland rainforest of Central Amazonia, including methodological and conservation considerations. Studies on Neotropical Fauna and Environment, 38: 17-31.
• Silva, C.R.; Martins, A.C.M.; Castro, I.J.; Bernard, E.; Cardoso, E.M.; Lima, D.S.; Castro, K.C. 2013. Mammals of Amapá State, Eastern Brazilian Amazonia: a revised taxonomic list with comments on species distributions. Mammalia, 77: 409-424.
• Solari, S., Pacheco, V.; Luna, L.; Velazco, P.M.; Patterson, B.D. 2006. Mammals of the Manu Biosphere Reserve. Fieldiana: Zoology, 110: 13-22.
• Sikes, R.S.; Gannon, W.L.; ASM Animal Care and Use Committee. 2011. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. Journal of Mammalogy, 92: 235-253.
• Veloso, H.P.; Rangel-Filho, A.L.R; Lima, J.C.A. 1991. Classificação da vegetação brasileira, adaptada a um sistema universal MEFP/IBGE/DRNEA, Rio de Janeiro, 124p.
• Velazco, P.M.; Gardner, A.L. 2012. A new species of Lophostoma d’Orbigny, 1836 (Chiroptera: Phyllostomidae) from Panama. Journal of Mammalogy, 93: 605-614.
• Vizotto, L.D.; Dumbra, A.J.; Rodrigues, V. 1980. Primeira ocorrência no Brasil de Tonatia carrikeri (Allen, 1910) (Chiroptera: Phyllostominae). Proceedings VII Congresso Brasileiro Zoologia, Mossoró, p.98-99.
• Williams, S.L; Genoways, H.H. 2007[2008]. Subfamily Phyllostominae Gray, 1825. In: Gardner, A.L. (Ed.). Mammals of South America, v.1, Marsupials, Xenarthrans, Shrews, and Bats University of Chicago Press, Chicago, p.255-300.
• Zortéa, M.; Rocha, Z.D.; Carvalho, H.G; Oliveira, G.C.; Mata, P.S. 2009. First record of the Carriker’s Round-eared Bat (Lophostoma carrikeri; Phyllostominae) in the Cerrado of central Brazil. Chiroptera Neotropical, 15: 446-449.

• CITE AS:

  Brandão, M.V.; Pedroso, M.A.; Colas-Rosas, P.F.; Aires, C.C.; Rocha, P.A. 2020. Review of the distribution of Lophostoma carrikeri (Chiroptera: Phyllostomidae), with range extension to transitional vegetation zones in the southwestern Amazon. Acta Amazonica (Epub Ahead of Print).

Edited by

Associate Editor:

Paulo D. Bobrowiec

Publication Dates

• Publication in this collection
  18 May 2020
• Date of issue
  Apr-Jun 2020

History

• Received
  05 Aug 2019
• Accepted
  29 Feb 2020