Abstract:

Thyropteridae is a family of bats endemic to the Neotropical region, and Thyroptera devivoi is the only species in the family that occurs exclusively in forest patches within savannas of northern South America and north of the Brazilian Cerrado. Primary data on the species are still scarce. Therefore, in this study our objective was to fill knowledge gaps on geographical distribution, roost-use, and echolocation for the species. We observed a T. devivoi colony of 15 individuals living under a dead palm leaf. The bats used the leaf as a roost for at least four days. After capturing one individual, we confirmed the species identification via skull size and the oblong shape of the adhesive disk. The new record reinforces the association of this species with non-forested formations, and its occurrence mainly in savannas. Echolocation calls of T. devivoi are consistent with those known for the genus, with multiharmonic, low intensity and high frequency pulses. Despite these new data, more studies are certainly needed to enhance distribution data for the species, as well as to clarify the biological and ecological requirements of the species.

Keywords:
echolocation; Brazil; Cerrado; Chiroptera; roost; Thyropteridae

Resumo:

Thyropteridae é uma família de morcegos endêmica da região Neotropical e Thyroptera devivoi é a única espécie da família que ocorre exclusivamente em manchas florestais das savanas do norte de América do Sul e do Cerrado Brasileiro. Dados primários da espécie são ainda escassos e o objetivo deste estudo foi preencher lacunas de conhecimento sobre distribuição geográfica, uso de abrigos e padrões de ecolocalização da espécie. Nós observamos uma colônia de T. devivoi com 15 indivíduos vivendo sob uma folha morta de palmeira. Os morcegos usaram a folha como abrigo ao menos por quatro dias. Depois de capturar um indivíduo, nós confirmamos a identificação da espécie por meio da morfologia do crânio e do disco adesivo. O novo registro reforça a associação da espécie com formações não florestais e a ocorrência principalmente em savanas. Os chamados de ecolocalização de T. devivoi são consistentes com o conhecido para o gênero, com pulsos multi-harmônicos de baixa intensidade e alta frequência. A despeito destes novos dados, mais estudos são certamente necessários para aprimorar os dados de distribuição assim como os requerimentos biológicos da espécie.

Palavras-chave:
abrigo; Brasil; Cerrado; Chiroptera; ecolocalização; Thyropteridae

Introduction

The Neotropical region has a rich and unique bat fauna, with six endemic families (Gardner 2008GARDNER, A.L. 2008. Mammals of South America, Volume 1. Marsupials, xenarthrans, shrwes, and bats. The University of Chicago Press, Chicago and London.). Among those families exclusive of the Neotropics, the Thyropteridae, known as Disk-winged bats, are peculiar bats distinguished by the presence of adhesive suction pads near the thumbs and ankles, which allows bats to attach to smooth surfaces of leaves that are used as roosts (Riskin & Fenton 2001RISKIN, D.K. & FENTON, M.B. 2001. Sticking ability in Spix’s disk-winged bat, Thyroptera tricolor (Microchiroptera: Thyropteridae). Canadian Journal of Zoology 79(12):2261-2267., Wilson 2007WILSON, D. E. 2007. Family Thyropteridae Miller 1907. Pp. 392-396 in Mammals of South America, Volume 1. Marsupials, Xenarthrans, Shrews, and Bats (A.L. Gardner, ed.). The University of Chicago Press.). These insectivorous leaf-roosting bats may spend at least half of their lives in the roost, but most Thyroptera roost data involves the young, still-furled leaves of Heliconia species (Findley & Wilson 1974FINDLEY, J.S. & D.E. WILSON . 1974. Observations on the Neotropical disk-winged bat, Thyroptera tricolor Spix. Journal of Mammalogy 55(3):562-571., Riskin & Fenton 2001RISKIN, D.K. & FENTON, M.B. 2001. Sticking ability in Spix’s disk-winged bat, Thyroptera tricolor (Microchiroptera: Thyropteridae). Canadian Journal of Zoology 79(12):2261-2267., Vonhof & Fenton 2004VONHOF, M. J. & FENTON, M.B. 2004. Roost availability and population size of Thyroptera tricolor, a leaf-roosting. Journal of Tropical Ecology 20(3):291-305., Montero & Gillian 2015MONTERO, B.K. & GILLAM, E.H. 2015. Behavioural strategies associated with using an ephemeral roosting resource in Spix’s disc-winged bat. Animal Behaviour 108:81-89.). Such roosts are well described and are the best-known roost type for this group of bats. However, such leaves usually form temporary roosts because developing leaves may remain furled for up to 60 h and occupation lasts for only a day (Vonhof & Fenton, 2004VONHOF, M. J. & FENTON, M.B. 2004. Roost availability and population size of Thyroptera tricolor, a leaf-roosting. Journal of Tropical Ecology 20(3):291-305.).

The family Thyropteridae has five recognized species, all belonging to the genus Thyroptera and occurring throughout the Neotropical region (Wilson 2007WILSON, D. E. 2007. Family Thyropteridae Miller 1907. Pp. 392-396 in Mammals of South America, Volume 1. Marsupials, Xenarthrans, Shrews, and Bats (A.L. Gardner, ed.). The University of Chicago Press., Velazco et al. 2014VELAZCO, P. M., GREGORIN, R., VOSS, R.S. & SIMMONS, N.B. 2014. Extraordinary local diversity of disk-winged bats (Thyropteridae: Thyroptera) in northeastern Peru, with the description of a new species and comments on roosting behavior. American Museum Novitates 3795:1-28.). The most common and well known are Thyroptera discifera (Lichtenstein & Peters 1854) and T. tricolor Spix 1823. Both species are distributed from Central America to south-eastern South America (Findley & Wilson 1974FINDLEY, J.S. & D.E. WILSON . 1974. Observations on the Neotropical disk-winged bat, Thyroptera tricolor Spix. Journal of Mammalogy 55(3):562-571., Tschapka et al. 2000TSCHAPKA, M., BROOKE, A.P. & WASSERTHAL, L.T. 2000. Thyroptera discifera (Chiroptera : Thyropteridae): A new record for Costa Rica and observations on echolocation. Zeitschrift für Saugetierkunde 65(4):193-198., Vonhof & Fenton 2004VONHOF, M. J. & FENTON, M.B. 2004. Roost availability and population size of Thyroptera tricolor, a leaf-roosting. Journal of Tropical Ecology 20(3):291-305., Dechmann et al. 2006DECHMANN, D. K. N., SAFI, K. & VONHOF, M.J. 2006. Matching morphology and diet in the disc-winged bat Thyroptera tricolor (Chiroptera). Journal of Mammalogy 87(5):1013-1019., Gillam & Chaverri 2012GILLAM, E. H. & CHAVERRI, G. 2012. Strong individual signatures and weaker group signatures in contact calls of Spix’s disc-winged bat, Thyroptera tricolor. Animal Behaviour 83(1):269-276., Buchalski et al. 2014BUCHALSKI, M.R., CHAVERRI, G. & VONHOF, M.J. 2014. When genes move farther than offspring: Gene flow by male gamete dispersal in the highly philopatric bat species Thyroptera tricolor. Molecular Ecology 23(2):464-480., Montero & Gillam 2015MONTERO, B.K. & GILLAM, E.H. 2015. Behavioural strategies associated with using an ephemeral roosting resource in Spix’s disc-winged bat. Animal Behaviour 108:81-89.). The other species are Thyroptera lavaliPine et al. 1993PINE, R.H. 1993. A new species of Thyroptera-Spix (Mammalia, Chiroptera, Thyropteridae) from the Amazon Basin of northeastern Peru. Mammalia 57(2):213-225., an Amazonian species occurring in northern South America (Solari et al. 2004SOLARI, S., VAN DEN BUSSCHE, R.A., HOOFER, S.R. & PATTERSON, B.D. 2004. Geographic distribution, ecology, and phylogenetic affinities of Thyroptera lavali Pine 1993. Acta Chiropterologica 6(2):293-302.), and the recently described Thyroptera wynneae Velazco et al. (2014)VELAZCO, P. M., GREGORIN, R., VOSS, R.S. & SIMMONS, N.B. 2014. Extraordinary local diversity of disk-winged bats (Thyropteridae: Thyroptera) in northeastern Peru, with the description of a new species and comments on roosting behavior. American Museum Novitates 3795:1-28., known only by four specimens collected in the forests of Peru and southeastern Brazil (Hoppe et al. 2014HOPPE, J.P.M., PIMENTA, V.T. & DITCHFIELD, A.D. 2014. First occurrence of the recently described Patricia’s Disk-winged bat Thyroptera wynneae (Chiroptera: Thyropteridae) in Espírito Santo, southeastern Brazil. Check List 10(3):645-647., Velazco et al. 2014VELAZCO, P. M., GREGORIN, R., VOSS, R.S. & SIMMONS, N.B. 2014. Extraordinary local diversity of disk-winged bats (Thyropteridae: Thyroptera) in northeastern Peru, with the description of a new species and comments on roosting behavior. American Museum Novitates 3795:1-28.). The fifth species, Thyroptera devivoiGregorin et al. (2006)GREGORIN, R., GONÇALVES, E., LIM, B. K. & ENGSTROM, M.D. 2006. New Species of disk-winged bat Thyroptera and range extension for T . discifera. Journal of Mammalogy 87(2):238-246., is the only one known to occur in non-forested habitats, as it lives in savanna ecosystems found in the municipality of Bom Jesus, state of Piauí, (08º52′S, 44º57′W); Jalapão, in the state of Tocantins (10º33′S, 46º45′W); Barreirinhas, in the state of Maranhão (3º0´S, 43º6´W) (Santos et al. 2013SANTOS, C.L.C., PEREIRA, A.C.N., BASTOS, V.D.J.C., GRACIOLLI, G. & REBÊLO, J.M.M. 2013. Parasitism of ectoparasitic flies on bats in the northern Brazilian cerrado. Acta Parasitologica / Witold Stefański Institute of Parasitology, Warszawa, Poland 58(2):207-14.); Tamton, Upper Takutu-Upper Essequibo Region, Guyana (2º21′N, 59º42′W) (Gregorin et al. 2006GREGORIN, R., GONÇALVES, E., LIM, B. K. & ENGSTROM, M.D. 2006. New Species of disk-winged bat Thyroptera and range extension for T . discifera. Journal of Mammalogy 87(2):238-246.) and in the Department of Casanare, Colombia (06º02′15″N, 070º12′43″ W) (Rodriguez-Posada et al. 2017RODRIGUEZ-POSADA, M., FERNÁNDEZ-RODRÍGUEZ, C., MORALES-MARTÍNEZ, D. & CALDERÓN-CAPOTE, M. 2017. First record of the De Vivo’s disk-winged bat, Thyroptera devivoi Gregorin, Gonçalves, Lim & Engstrom, 2006 (Chiroptera,Thyropteridae), from Colombia, with comments about the record of Thyroptera lavali Pine, 1993 from the country. Check List 13(4):355-361.).

Although widely distributed, species of Thyropteridae are very elusive and not usually captured in mist nets, a fact that means they are generally poorly sampled in inventories, and few studies exist on the biology and ecology of most species (Solari et al. 2004SOLARI, S., VAN DEN BUSSCHE, R.A., HOOFER, S.R. & PATTERSON, B.D. 2004. Geographic distribution, ecology, and phylogenetic affinities of Thyroptera lavali Pine 1993. Acta Chiropterologica 6(2):293-302., Velazco et al. 2014VELAZCO, P. M., GREGORIN, R., VOSS, R.S. & SIMMONS, N.B. 2014. Extraordinary local diversity of disk-winged bats (Thyropteridae: Thyroptera) in northeastern Peru, with the description of a new species and comments on roosting behavior. American Museum Novitates 3795:1-28.) reassuring the importance of any data on these rare animals. With the popularization in the recent years of bat recorders and acoustic study methods, bat vocalizations have begun to be used for sampling and species identification (Rydell et al. 2002RYDELL, J., ARITA, H.T., SANTOS, M. & GRANADOS, J. 2002. Acoustic identification of insectivorous bats (order Chiroptera) of Yucatan, Mexico. Journal of Zoology 257(1):27-36., Barataud et al. 2013BARATAUD, M., GIOSA, S., LEBLANC, F., RUFRAY, V., DISCA, T., TILLON, L., DELAVAL, M., HAQUART, A. & DEWYNTER, M. 2013. Identification et écologie acoustique des chiroptères de Guyane française. Le Rhinolophe 19:103-145., Jung et al. 2014JUNG, K., MOLINARI, J. & KALKO, E.K.V. 2014. Driving factors for the evolution of species-specific echolocation call design in New World free-tailed bats (Molossidae). PLoS ONE 9. e85279., Arias-Aguilar et al. 2018ARIAS-AGUILAR, A., HINTZE, F., AGUIAR, L.M.S., RUFRAY, V., BERNARD, E. & PEREIRA, M.J.R. 2018. Who’s calling? Acoustic identification of Brazilian bats. Mammal Research 63(3):231-253.), especially for taxa rarely captured by traditional netting methods (O’Farrell & Gannon 1999O’FARRELL, M.J. & GANNON, W.L. 1999. A comparison of acoustic versus capture techniques for the inventory of bats. Journal of Mammology 80(1):24-30.).

However, to unequivocally identify vocalizations recorded in nature, especially in places with a large number of species with undescribed calls, it is necessary to have a call database that permits between-species comparisons (Arias-Aguilar et al. 2018ARIAS-AGUILAR, A., HINTZE, F., AGUIAR, L.M.S., RUFRAY, V., BERNARD, E. & PEREIRA, M.J.R. 2018. Who’s calling? Acoustic identification of Brazilian bats. Mammal Research 63(3):231-253.). Moreover, some bats emit very low-intensity calls that are difficult to capture with most bat recorders, so that only fragmentary information is available for such Neotropical bat families, as the Thyropteridae, Furipteridae, Phyllostomidae, and Natalidae (Fenton 2013FENTON, M.B. 2013. Questions, ideas and tools: Lessons from bat echolocation. Animal Behaviour 85(5):869-879., Falcão et al. 2015FALCÃO, F., UGARTE-NÚÑEZ, J. A., FARIA, D. & CASELLI, C.B. 2015. Unravelling the calls of discrete hunters: Acoustic structure of echolocation calls of furipterid bats (Chiroptera, Furipteridae). Bioacoustics 24(2):175-183.). Within the Thyropteridae only two species have echolocation calls described in detail are T. discifera (Tschapka et al. 2000TSCHAPKA, M., BROOKE, A.P. & WASSERTHAL, L.T. 2000. Thyroptera discifera (Chiroptera : Thyropteridae): A new record for Costa Rica and observations on echolocation. Zeitschrift für Saugetierkunde 65(4):193-198.) and T. tricolor (Fenton et al. 1999FENTON, M.B., RYDELL, J., VONHOF, M.J., EKLÖF, J. & LANCASTER, W.C. 1999. Constant-frequency and frequency-modulated components in the echolocation calls of three species of small bats (Emballonuridae, Thyropteridae, and Vespertilionidae). Canadian Journal of Zoology 77(12):1891-1900., Barataud et al. 2013BARATAUD, M., GIOSA, S., LEBLANC, F., RUFRAY, V., DISCA, T., TILLON, L., DELAVAL, M., HAQUART, A. & DEWYNTER, M. 2013. Identification et écologie acoustique des chiroptères de Guyane française. Le Rhinolophe 19:103-145.). Both species are characterized by low intensity broadband calls, with multiple harmonics.

Therefore, in this study, we aimed to fill knowledge gaps on the ecology, distribution, and echolocation of Thyroptera devivoi, one of the least-known but most ecologically distinct species in the family Thyropteridae. Accordingly, we present new information on roost use and provide the first detailed description of vocalizations for the species.

Materials and Methods

1. Study Area

Fieldwork was carried out in Chapada das Mesas National Park (CMNP), a Brazilian federal protected area located in Carolina municipality, Maranhão state (Figure 1). The National System of Nature Conservation Units - SNUC in its Article 8 defines that National Parks are Units of Integral Protection. According to Köppen-Geiger classification, Carolina has a Aw tropical climate (humid tropical savanna) (Peel et al. 2007PEEL, M. C., FINLAYSON, B.L. & MCMAHON, T.A. 2007. Update world map of the Köppen-Geiger climate classification. Hydrology and Earth System Science 11:1633-1644.), with high temperatures ranging between 26-29ºC and low temperatures between 20-23ºC, with two well-defined seasons: dry winters (May to September) and rainy summers (October to April). Average annual rainfall is 1614 mm. August is the driest month and March that of greatest precipitation. The region is in a vegetational transition zone, with high biodiversity including species of three important Brazilian morphoclimatic domains: the Amazon, the Caatinga and the Cerrado (Ab’Sáber 2000AB’SÁBER, A. N. 2000. The natural organization of Brazilian inter- and subtropical landscapes. Revista do Instituto Geológico 21(1):57-70. ). CMNP area is largely occupied by Cerrado and has a typical mosaic landscape, with enclaves of forest formations in a matrix predominantly composed of savannas and pastures (Olson et al. 2001OLSON, D.M., DINERSTEIN, E., WIKRAMANAYAKE, E.D., BURGESS, N.D., POWELL, G.V.N., UNDERWOOD, E.C., D'AMICO, J.A., ITOUA, I., STRAND, H. E., MORRISON, J.C., LOUCKS, C.J., ALLNUTT, T.F., RICKETTS, T. H., KURA, Y., LAMOREUX, J.F., WETTENGEL, W.W. HEDAO, P. & KASSEM, K. R. . 2001. Terrestrial Ecoregions of the World : A New Map of Life on Earth. BioScience 51(11): 933-938., Moraes & Lima 2007MORAES, R.C. & LIMA, L.P. 2007. Utilização de SIG como ferramenta na gestão do Parque Nacional Chapada das Mesas (Carolina/MA). Pp. 4057-4064 in Anais XIII Simpósio Brasileiro de Sensoriamento Remoto (INPE, ed.). Florianópolis.). Bat captures of took place in a large forest enclave in the Cerrado located in the north of the park at coordinates 6º56'52.5"S, 47º21'37.7"W.

Figure 1
Map of the known localities of Thyroptera devivoi records, showing an occurrence restricted to neotropical savannas. Numbers refer to previous records: 1) Gregorin et al. (2006)GREGORIN, R., GONÇALVES, E., LIM, B. K. & ENGSTROM, M.D. 2006. New Species of disk-winged bat Thyroptera and range extension for T . discifera. Journal of Mammalogy 87(2):238-246.; 2) Santos et al. (2013)SANTOS, C.L.C., PEREIRA, A.C.N., BASTOS, V.D.J.C., GRACIOLLI, G. & REBÊLO, J.M.M. 2013. Parasitism of ectoparasitic flies on bats in the northern Brazilian cerrado. Acta Parasitologica / Witold Stefański Institute of Parasitology, Warszawa, Poland 58(2):207-14.; 3) Rodriguez-Posada et al. (2017)RODRIGUEZ-POSADA, M., FERNÁNDEZ-RODRÍGUEZ, C., MORALES-MARTÍNEZ, D. & CALDERÓN-CAPOTE, M. 2017. First record of the De Vivo’s disk-winged bat, Thyroptera devivoi Gregorin, Gonçalves, Lim & Engstrom, 2006 (Chiroptera,Thyropteridae), from Colombia, with comments about the record of Thyroptera lavali Pine, 1993 from the country. Check List 13(4):355-361.. The limits for the South American biomes were obtained from Olson et al. (2001)OLSON, D.M., DINERSTEIN, E., WIKRAMANAYAKE, E.D., BURGESS, N.D., POWELL, G.V.N., UNDERWOOD, E.C., D'AMICO, J.A., ITOUA, I., STRAND, H. E., MORRISON, J.C., LOUCKS, C.J., ALLNUTT, T.F., RICKETTS, T. H., KURA, Y., LAMOREUX, J.F., WETTENGEL, W.W. HEDAO, P. & KASSEM, K. R. . 2001. Terrestrial Ecoregions of the World : A New Map of Life on Earth. BioScience 51(11): 933-938.. Locality 2 is in a transition zone, but the capture of T. devivoi in this study occurred in a Cerrado area (see Santos et al. 2013SANTOS, C.L.C., PEREIRA, A.C.N., BASTOS, V.D.J.C., GRACIOLLI, G. & REBÊLO, J.M.M. 2013. Parasitism of ectoparasitic flies on bats in the northern Brazilian cerrado. Acta Parasitologica / Witold Stefański Institute of Parasitology, Warszawa, Poland 58(2):207-14.). The star refers to the location of the present study.

2. Bat roost, collection, and identification

We found a colony of Thyroptera devivoi in a roost and filmed it before the sunset on 11/October/2015 (Figure 2). Two days later (13/10/2015) we returned to the roost site to make a visual estimation of the number of individuals present in the colony. Later on that same day, we installed and opened three mist nets forming a triangle around the exit of the roost. On 14/10/2015 we returned to the bat roost to record the bat calls in the colony and to manually capture a specimen for correct species identification. Capture was achieved with the aid of a cloth bag installed at the roost exit. We collected a specimen and took tissue samples from the bat's patagium. The specimen was euthanized via anesthetic inhalation (Isoflurane) and later fixed and deposited in the Chiroptera Collection of the University of Brasília - CCUnB under accession number CCUnB1189.

Figure 2
The dead palm leaf used as roost by a colony of Thyroptera devivoi found in 2015 at Chapada das Mesas, Maranhão state, Brazil.

For species identification, we used identification keys and articles related to the genus Thyroptera (Pine 1993PINE, R.H. 1993. A new species of Thyroptera-Spix (Mammalia, Chiroptera, Thyropteridae) from the Amazon Basin of northeastern Peru. Mammalia 57(2):213-225.; Solari et al. 2004SOLARI, S., VAN DEN BUSSCHE, R.A., HOOFER, S.R. & PATTERSON, B.D. 2004. Geographic distribution, ecology, and phylogenetic affinities of Thyroptera lavali Pine 1993. Acta Chiropterologica 6(2):293-302.; Gregorin et al. 2006GREGORIN, R., GONÇALVES, E., LIM, B. K. & ENGSTROM, M.D. 2006. New Species of disk-winged bat Thyroptera and range extension for T . discifera. Journal of Mammalogy 87(2):238-246.; Velazco et al. 2014VELAZCO, P. M., GREGORIN, R., VOSS, R.S. & SIMMONS, N.B. 2014. Extraordinary local diversity of disk-winged bats (Thyropteridae: Thyroptera) in northeastern Peru, with the description of a new species and comments on roosting behavior. American Museum Novitates 3795:1-28.; Díaz et al. 2016DÍAZ, M. M., SOLARI, S., AGUIRRE, L.F., AGUIAR, L.M.S. & BARQUEZ, R.M. 2016. Clave de identificación de los murciélagos de Sudamérica. Publicacion Especial no. 2. Programa de Conservación de los Murciélagos de Argentina.160pp. ). We made the following external and cranial measurements based on Velazco et al. (2014)VELAZCO, P. M., GREGORIN, R., VOSS, R.S. & SIMMONS, N.B. 2014. Extraordinary local diversity of disk-winged bats (Thyropteridae: Thyroptera) in northeastern Peru, with the description of a new species and comments on roosting behavior. American Museum Novitates 3795:1-28.: Total Length (TL), Length of Tail (LT), Hind Foot Length (HF), Ear Length (Ear), Free Tail Length (FTL), Forearm Length (FA), Greatest Length of Skull (GLS), Condyloincisive Length (CIL), Braincase Breadth (BB), Rostral Length (ROL), Zygomatic Breadth (ZB), Postorbital Breadth (PB), Maxillary Toothrow Length (MTRL), Width at M3 (M3-M3), Length of Mandible (LMA) and Mandibular Toothrow Length (MANDL).

3. Sound recordings and analyzed acoustic parameters

We recorded bat echolocation calls using a Song Meter SM2BAT (Wildlife Acoustics, Maynard, Massachusetts, USA) ultrasonic bat detector in mono, with a single SMX-US (Wildlife Acoustics) omnidirectional microphone and a sampling frequency of 384 kHz. Files were saved as WAV files. To capture the echolocation calls ot the colony’s individuals the recorder was placed about 1.5 meters below the entrance to the bat roost. The recorder was programmed to record one file of 30 seconds duration every two minutes during the entire night from 16:50 until 06:00. We selected for analyses those call sequences with at least three pulses and the best aspect-noise-ratio. We measured the following six acoustic parameters of each recorded pulse: pulse duration (ms) - measured from the start to the end of the pulse; pulse interval (ms) - measured from the start of one pulse to the start of the next pulse; maximum frequency (kHz) - measured at the start of the pulse; minimum frequency (kHz) - measured at the end of the pulse; peak frequency, which corresponded to the maximum intensity frequency; and bandwidth, which correspond to the difference between the maximum frequency and the minimum frequency.

We analyzed data using Avisoft-SAS Lab Pro version 5.1.05.30 (Avisoft Bioacoustics, Berlin, Germany), and processed calls with automatic element separation using -20 dB of maximum amplitude, using a 3-threshold algorithm. Pulses were plotted simultaneously on the spectrogram, showing the relationship between frequency, time, and intensity. On the oscillogram, temporal digitization of recordings represented pulse intensity and time. Spectrograms were constructed from 512 fast Fourier transforms using a Hamming window function with 93.75% overlap between consecutive fast Fourier transforms and a frame length of 100%.

The recordings and collections in this work were made as part of the Rede de Pesquisa project Biota do Cerrado under the license number 46596-1 ICMBio/MMA.

Results

No individuals were captured with mist nets. Though, manually we captured one adult male (Figure 3). We visually estimated that the colony consisted of 10 to 15 individuals that were dwelling inside of the sheath of a dead palm leaf that was hanging in the forest canopy (it was the only palm surrounded by neighboring trees) (Figure 2). There was an approximate 2.5m height roost entrance facing downwards (Figure 2). The colony used the same roost for at least four days. The collected T. devivoi specimen was easily distinguished from the other species of the genus by the presence of oval-shaped adhesive suction pads, forearm greater than 35mm, GLS greater than 14mm and less than 15mm, bicolored ventral hairs with darker bases and light brown tips, and calcaneus without obvious dermal projections (Pine 1993PINE, R.H. 1993. A new species of Thyroptera-Spix (Mammalia, Chiroptera, Thyropteridae) from the Amazon Basin of northeastern Peru. Mammalia 57(2):213-225., Gregorin et al. 2006GREGORIN, R., GONÇALVES, E., LIM, B. K. & ENGSTROM, M.D. 2006. New Species of disk-winged bat Thyroptera and range extension for T . discifera. Journal of Mammalogy 87(2):238-246., Velazco et al. 2014VELAZCO, P. M., GREGORIN, R., VOSS, R.S. & SIMMONS, N.B. 2014. Extraordinary local diversity of disk-winged bats (Thyropteridae: Thyroptera) in northeastern Peru, with the description of a new species and comments on roosting behavior. American Museum Novitates 3795:1-28., Díaz et al. 2016DÍAZ, M. M., SOLARI, S., AGUIRRE, L.F., AGUIAR, L.M.S. & BARQUEZ, R.M. 2016. Clave de identificación de los murciélagos de Sudamérica. Publicacion Especial no. 2. Programa de Conservación de los Murciélagos de Argentina.160pp. ) (Table 1, Figure 3).

Figure 3
Specimen of Thyroptera devivoi collected in 2015 at Chapada das Mesas, Maranhão state, Brazil, showing the oval-shaped adhesive suction pads and skull morphology.

Analysis showed Thyroptera devivoi echolocation pulses are frequency modulated (FM), broadband, with low intensity and high frequency. The calls are multiharmonic, with three harmonics, but we were not always able to capture all of them. Most of the time the second harmonic was the one with most energy. We recorded 305 pulses of 65 calls, during one entire night. The pulses had broad bandwidth, ranging from 50 kHz to more than 150 kHz, with regular intervals of about 0.01ms and a short duration (0.002ms) (Table 2; Figure 4). One type of social call was also recorded. These were multiharmonic with fundamental frequencies at 10 kHz, 20 kHz and 30 kHz. Calls had long duration and were emitted at extended intervals. Social calls were emitted throughout the night with the first registration at 18:24 and the last at 05.22.

Figure 4
Sequence of search phase echolocation calls (A) and social calls (B) of Thyroptera devivoi recorded in 2015 at Chapada das Mesas, Maranhão state, Brazil. Power spectrum (left), oscillogram (top) and spectrogram (center), dB = loudness volume.

Discussion

Our new geographical record reinforces the presence of T. devivoi in the northern portion of the Cerrado, being the sixth known location for this species (Gregorin et al. 2006GREGORIN, R., GONÇALVES, E., LIM, B. K. & ENGSTROM, M.D. 2006. New Species of disk-winged bat Thyroptera and range extension for T . discifera. Journal of Mammalogy 87(2):238-246., Rodriguez-Posada et al. 2017RODRIGUEZ-POSADA, M., FERNÁNDEZ-RODRÍGUEZ, C., MORALES-MARTÍNEZ, D. & CALDERÓN-CAPOTE, M. 2017. First record of the De Vivo’s disk-winged bat, Thyroptera devivoi Gregorin, Gonçalves, Lim & Engstrom, 2006 (Chiroptera,Thyropteridae), from Colombia, with comments about the record of Thyroptera lavali Pine, 1993 from the country. Check List 13(4):355-361.). Thyroptera devivoi is one of the lesser known species of this family (Gregorin et al. 2006GREGORIN, R., GONÇALVES, E., LIM, B. K. & ENGSTROM, M.D. 2006. New Species of disk-winged bat Thyroptera and range extension for T . discifera. Journal of Mammalogy 87(2):238-246., Velazco et al. 2014VELAZCO, P. M., GREGORIN, R., VOSS, R.S. & SIMMONS, N.B. 2014. Extraordinary local diversity of disk-winged bats (Thyropteridae: Thyroptera) in northeastern Peru, with the description of a new species and comments on roosting behavior. American Museum Novitates 3795:1-28.), and has a disjunct distribution, with populations in the northern Brazilian Cerrado and other populations inhabiting the savannas of Colombia and Guiana, in northern South America (Gregorin et al. 2006GREGORIN, R., GONÇALVES, E., LIM, B. K. & ENGSTROM, M.D. 2006. New Species of disk-winged bat Thyroptera and range extension for T . discifera. Journal of Mammalogy 87(2):238-246., Rodriguez-Posada et al. 2017RODRIGUEZ-POSADA, M., FERNÁNDEZ-RODRÍGUEZ, C., MORALES-MARTÍNEZ, D. & CALDERÓN-CAPOTE, M. 2017. First record of the De Vivo’s disk-winged bat, Thyroptera devivoi Gregorin, Gonçalves, Lim & Engstrom, 2006 (Chiroptera,Thyropteridae), from Colombia, with comments about the record of Thyroptera lavali Pine, 1993 from the country. Check List 13(4):355-361.) (Figure 1). In a personal communication to the IUCN, B. Lim (Royal Ontario Museum, Toronto) suggests that populations occurring in the Cerrado can be separated from those occurring in the other savannas of northern South America (Llanos and Rupununi savannas), so that they may be two different species (Solari 2015SOLARI, S. 2015. Thyroptera devivoi. The IUCN Red List of Threatened Species 2015.). As with previous records, the studied T. devivoi colony was found in a forest enclave naturally embedded in a savanna matrix, confirming that T. devivoi a thyropterid endemic to savanna areas (Gregorin et al. 2006GREGORIN, R., GONÇALVES, E., LIM, B. K. & ENGSTROM, M.D. 2006. New Species of disk-winged bat Thyroptera and range extension for T . discifera. Journal of Mammalogy 87(2):238-246., Santos et al. 2013SANTOS, C.L.C., PEREIRA, A.C.N., BASTOS, V.D.J.C., GRACIOLLI, G. & REBÊLO, J.M.M. 2013. Parasitism of ectoparasitic flies on bats in the northern Brazilian cerrado. Acta Parasitologica / Witold Stefański Institute of Parasitology, Warszawa, Poland 58(2):207-14., Velazco et al. 2014VELAZCO, P. M., GREGORIN, R., VOSS, R.S. & SIMMONS, N.B. 2014. Extraordinary local diversity of disk-winged bats (Thyropteridae: Thyroptera) in northeastern Peru, with the description of a new species and comments on roosting behavior. American Museum Novitates 3795:1-28., Rodriguez-Posada et al. 2017RODRIGUEZ-POSADA, M., FERNÁNDEZ-RODRÍGUEZ, C., MORALES-MARTÍNEZ, D. & CALDERÓN-CAPOTE, M. 2017. First record of the De Vivo’s disk-winged bat, Thyroptera devivoi Gregorin, Gonçalves, Lim & Engstrom, 2006 (Chiroptera,Thyropteridae), from Colombia, with comments about the record of Thyroptera lavali Pine, 1993 from the country. Check List 13(4):355-361.), and the only one known with such preferences.

When disturbed, the bats of the colony flew into the woods within a radius of approximately 5-10 meters near the roost, even during the day, which allowed us to estimate the number of individuals using the roost. The studied colony represents a relatively large group when compared to another species of the genus (T. tricolor), where groups may contain up to 11, with a mode of 4 to 7, individuals (Findley & Wilson 1974FINDLEY, J.S. & D.E. WILSON . 1974. Observations on the Neotropical disk-winged bat, Thyroptera tricolor Spix. Journal of Mammalogy 55(3):562-571., Vonhof & Fenton 2004VONHOF, M. J. & FENTON, M.B. 2004. Roost availability and population size of Thyroptera tricolor, a leaf-roosting. Journal of Tropical Ecology 20(3):291-305.). The roost was large (Figure 2) and despite its ephemeral nature (i.e. it would soon transform into a structure not suitable for roosting), it was a multi-day roost, compared to the more commonly used furled Heliconia spp. leaf roots that are occupied for only one night (Vonhof & Fenton 2004VONHOF, M. J. & FENTON, M.B. 2004. Roost availability and population size of Thyroptera tricolor, a leaf-roosting. Journal of Tropical Ecology 20(3):291-305.). The use of a larger roost allows a colony to contain more individuals, and the roost durability allows the colony to stay for several days.

Because they depend on ephemeral and specific roosts (i.e. smooth unfurled leaves, dead leaves), roosts may often be a limiting resource and the local abundance of Thyroptera species is associated with the availability of such roosts (Findley & Wilson 1974FINDLEY, J.S. & D.E. WILSON . 1974. Observations on the Neotropical disk-winged bat, Thyroptera tricolor Spix. Journal of Mammalogy 55(3):562-571., Vonhof & Fenton 2004VONHOF, M. J. & FENTON, M.B. 2004. Roost availability and population size of Thyroptera tricolor, a leaf-roosting. Journal of Tropical Ecology 20(3):291-305.). Current knowledge on thyropterid roost use is largely based on studies of a single species (T. tricolor). However, Velazco et al. (2014)VELAZCO, P. M., GREGORIN, R., VOSS, R.S. & SIMMONS, N.B. 2014. Extraordinary local diversity of disk-winged bats (Thyropteridae: Thyroptera) in northeastern Peru, with the description of a new species and comments on roosting behavior. American Museum Novitates 3795:1-28. suggest that there is a strong selection in Thyroptera to diversify the type of roosts used, with species using smoother (e.g., Heliconia spp. and Musa spp.) or rougher roosts (e.g., dry leaves of Cecropia spp. or palm trees). These differences on roost preference may allow the sympatric occurrence of congeneric (2 up to 4) in some localities (Velazco et al. 2014VELAZCO, P. M., GREGORIN, R., VOSS, R.S. & SIMMONS, N.B. 2014. Extraordinary local diversity of disk-winged bats (Thyropteridae: Thyroptera) in northeastern Peru, with the description of a new species and comments on roosting behavior. American Museum Novitates 3795:1-28.) and could also explain the generalist approach of T. devivoi by its capacity to use roosts with more rugged surfaces, like dead dried leaves recorded here and previously (Gregorin et al. 2006GREGORIN, R., GONÇALVES, E., LIM, B. K. & ENGSTROM, M.D. 2006. New Species of disk-winged bat Thyroptera and range extension for T . discifera. Journal of Mammalogy 87(2):238-246., Velazco et al. 2014VELAZCO, P. M., GREGORIN, R., VOSS, R.S. & SIMMONS, N.B. 2014. Extraordinary local diversity of disk-winged bats (Thyropteridae: Thyroptera) in northeastern Peru, with the description of a new species and comments on roosting behavior. American Museum Novitates 3795:1-28.). Another hypothesis raised by Velazco et al. (2014)VELAZCO, P. M., GREGORIN, R., VOSS, R.S. & SIMMONS, N.B. 2014. Extraordinary local diversity of disk-winged bats (Thyropteridae: Thyroptera) in northeastern Peru, with the description of a new species and comments on roosting behavior. American Museum Novitates 3795:1-28. is that Thyroptera species with a light or whitish venter would roost on leaves that permits light entrance through the leaves, while darker venter species would roost in dead leaves. Though, it is interesting to call the attention that T. devivoi from Jalapão was collected in a "vereda" rich in Heliconia (Gregorin et al. 2006GREGORIN, R., GONÇALVES, E., LIM, B. K. & ENGSTROM, M.D. 2006. New Species of disk-winged bat Thyroptera and range extension for T . discifera. Journal of Mammalogy 87(2):238-246.) while we found the species in dead leaves.

As with most of the available information about the family, little is known about the acoustic biology of Thyropteridae, and that which exists mainly refers to two species (T. discifera and T. tricolor), with some studies focused on social calls (Chaverri et al. 2010CHAVERRI, G., GILLAM, E.H. & VONHOF, M.J. 2010. Social calls used by a leaf-roosting bat to signal location. Biology letters 6:441-444., 2013CHAVERRI, G., GILLAM, E.H. & KUNZ, T.H. 2013. A call-and-response system facilitates group cohesion among disc-winged bats. Behavioral Ecology 24(2):481-487., Chaverri & Gillam 2013CHAVERRI, G. & GILLAM, E.H. 2013. Sound amplification by means of a horn-like roosting structure in Spix’s disc-winged bat. Proceedings of the Royal Society. Biological Sciences 280:20132362., 2015CHAVERRI, G. & GILLAM, E.H. 2015. Repeatability in the contact calling system of Spix’s disc-winged bat (Thyroptera tricolor). Royal Society Open Science 2:140197., Montero & Gillam 2015MONTERO, B.K. & GILLAM, E.H. 2015. Behavioural strategies associated with using an ephemeral roosting resource in Spix’s disc-winged bat. Animal Behaviour 108:81-89.), while others concentrated on echolocation calls (Fenton et al. 1999FENTON, M.B., RYDELL, J., VONHOF, M.J., EKLÖF, J. & LANCASTER, W.C. 1999. Constant-frequency and frequency-modulated components in the echolocation calls of three species of small bats (Emballonuridae, Thyropteridae, and Vespertilionidae). Canadian Journal of Zoology 77(12):1891-1900., Tschapka et al. 2000TSCHAPKA, M., BROOKE, A.P. & WASSERTHAL, L.T. 2000. Thyroptera discifera (Chiroptera : Thyropteridae): A new record for Costa Rica and observations on echolocation. Zeitschrift für Saugetierkunde 65(4):193-198., Barataud et al. 2013BARATAUD, M., GIOSA, S., LEBLANC, F., RUFRAY, V., DISCA, T., TILLON, L., DELAVAL, M., HAQUART, A. & DEWYNTER, M. 2013. Identification et écologie acoustique des chiroptères de Guyane française. Le Rhinolophe 19:103-145., Rivera-Parra and Burneo 2013RIVERA-PARRA, P. & BURNEO, S.F. 2013. Primera biblioteca de llamadas de ecolocalización de murciélagos del Ecuador. Therya 4(1):79-88.). Echolocation calls of T. devivoi recorded by us are of low intensity, which make them difficult to detect (Fenton et al. 1999FENTON, M.B., RYDELL, J., VONHOF, M.J., EKLÖF, J. & LANCASTER, W.C. 1999. Constant-frequency and frequency-modulated components in the echolocation calls of three species of small bats (Emballonuridae, Thyropteridae, and Vespertilionidae). Canadian Journal of Zoology 77(12):1891-1900., Dechmann et al. 2006DECHMANN, D. K. N., SAFI, K. & VONHOF, M.J. 2006. Matching morphology and diet in the disc-winged bat Thyroptera tricolor (Chiroptera). Journal of Mammalogy 87(5):1013-1019.). This seems to be a characteristic of the bats of the genus Thyroptera, since similar calls were identified by Fenton et al. (1999)FENTON, M.B., RYDELL, J., VONHOF, M.J., EKLÖF, J. & LANCASTER, W.C. 1999. Constant-frequency and frequency-modulated components in the echolocation calls of three species of small bats (Emballonuridae, Thyropteridae, and Vespertilionidae). Canadian Journal of Zoology 77(12):1891-1900., Tschapka et al. (2000)TSCHAPKA, M., BROOKE, A.P. & WASSERTHAL, L.T. 2000. Thyroptera discifera (Chiroptera : Thyropteridae): A new record for Costa Rica and observations on echolocation. Zeitschrift für Saugetierkunde 65(4):193-198., Barataud et al. (2013)BARATAUD, M., GIOSA, S., LEBLANC, F., RUFRAY, V., DISCA, T., TILLON, L., DELAVAL, M., HAQUART, A. & DEWYNTER, M. 2013. Identification et écologie acoustique des chiroptères de Guyane française. Le Rhinolophe 19:103-145. and Rivera-Parra and Burneo (2013)RIVERA-PARRA, P. & BURNEO, S.F. 2013. Primera biblioteca de llamadas de ecolocalización de murciélagos del Ecuador. Therya 4(1):79-88.. Echolocation characteristics of T. devivoi recorded in this study are more similar to those of T. discifera recorded by Tschapka et al. (2000)TSCHAPKA, M., BROOKE, A.P. & WASSERTHAL, L.T. 2000. Thyroptera discifera (Chiroptera : Thyropteridae): A new record for Costa Rica and observations on echolocation. Zeitschrift für Saugetierkunde 65(4):193-198. (Table 2). However, they are different from T. discifera calls registered by Fenton et al. (1999)FENTON, M.B., RYDELL, J., VONHOF, M.J., EKLÖF, J. & LANCASTER, W.C. 1999. Constant-frequency and frequency-modulated components in the echolocation calls of three species of small bats (Emballonuridae, Thyropteridae, and Vespertilionidae). Canadian Journal of Zoology 77(12):1891-1900., which had low bandwidth and long duration (5 to 8 ms). The results of Dechmann et al. (2006)DECHMANN, D. K. N., SAFI, K. & VONHOF, M.J. 2006. Matching morphology and diet in the disc-winged bat Thyroptera tricolor (Chiroptera). Journal of Mammalogy 87(5):1013-1019. on T. discifera echolocation show strong contrasts to those calls of T. discifera recorded by Fenton et al. (1999)FENTON, M.B., RYDELL, J., VONHOF, M.J., EKLÖF, J. & LANCASTER, W.C. 1999. Constant-frequency and frequency-modulated components in the echolocation calls of three species of small bats (Emballonuridae, Thyropteridae, and Vespertilionidae). Canadian Journal of Zoology 77(12):1891-1900. and Tschapka et al. (2000)TSCHAPKA, M., BROOKE, A.P. & WASSERTHAL, L.T. 2000. Thyroptera discifera (Chiroptera : Thyropteridae): A new record for Costa Rica and observations on echolocation. Zeitschrift für Saugetierkunde 65(4):193-198.. The kind of high-frequency and low-intensity calls recorded dissipate rapidly in space and are used for short-range detection in areas with many obstacles. This allows the bats to obtain high-quality detailed information on their surroundings (Schnitzler and Kalko 2001SCHNITZLER, H.U. & KALKO, E. K. V. 2001. Echolocation by insect-eating bats. BioScience 51:557-569.). We recorded a social call similar to that described by Montero and Gillam (2015)MONTERO, B.K. & GILLAM, E.H. 2015. Behavioural strategies associated with using an ephemeral roosting resource in Spix’s disc-winged bat. Animal Behaviour 108:81-89. for T. tricolor, who qualified it as SQCF (short quasi-constant frequency). We do not know the purpose of this call for T. devivoi, but it is present during certain times of the night between periods of echolocation and, therefore, may possibly be emitted in flight.

There are few data on the echolocation of bats of the Thyroptera family. Acoustic data are from only three of the five species, being T. tricolor (Fenton et al. 1999FENTON, M.B., RYDELL, J., VONHOF, M.J., EKLÖF, J. & LANCASTER, W.C. 1999. Constant-frequency and frequency-modulated components in the echolocation calls of three species of small bats (Emballonuridae, Thyropteridae, and Vespertilionidae). Canadian Journal of Zoology 77(12):1891-1900., Rivera-Parra and Burneo 2013RIVERA-PARRA, P. & BURNEO, S.F. 2013. Primera biblioteca de llamadas de ecolocalización de murciélagos del Ecuador. Therya 4(1):79-88., Barataud et al. 2013BARATAUD, M., GIOSA, S., LEBLANC, F., RUFRAY, V., DISCA, T., TILLON, L., DELAVAL, M., HAQUART, A. & DEWYNTER, M. 2013. Identification et écologie acoustique des chiroptères de Guyane française. Le Rhinolophe 19:103-145.), T. discifera (Tschapka et al. 2000TSCHAPKA, M., BROOKE, A.P. & WASSERTHAL, L.T. 2000. Thyroptera discifera (Chiroptera : Thyropteridae): A new record for Costa Rica and observations on echolocation. Zeitschrift für Saugetierkunde 65(4):193-198. and Barataud et al. 2013BARATAUD, M., GIOSA, S., LEBLANC, F., RUFRAY, V., DISCA, T., TILLON, L., DELAVAL, M., HAQUART, A. & DEWYNTER, M. 2013. Identification et écologie acoustique des chiroptères de Guyane française. Le Rhinolophe 19:103-145. e) and T. devivoi (this study). Despite the scarcity of data, we believe that echolocation calls of the Thyropteridae bats can be identified by the presence of three FM harmonics, the first about 50 kHz, the other about 100 kHz and the last about 150 kHz, with pulses of short duration, small interval between pulses and large bandwidth. Except for Fenton et al. (1999)FENTON, M.B., RYDELL, J., VONHOF, M.J., EKLÖF, J. & LANCASTER, W.C. 1999. Constant-frequency and frequency-modulated components in the echolocation calls of three species of small bats (Emballonuridae, Thyropteridae, and Vespertilionidae). Canadian Journal of Zoology 77(12):1891-1900. that recorded quasi-constant frequency (QCF) calls, long duration, and low bandwidth, all other studies have identified similar multi-harmonic calls (although not all have recorded the three harmonics.), with short duration and interval between the pulses, and large bandwidth (see table 2). The absence of a third harmonic may be due to the difference between the recording equipment as they may restrict the sample rate of the recordings (Biscardi et al. 2004BISCARDI, S., ORPRECIO, J., FENTON, M.B., TSOAR, A. & RATCLIFFE, J.M. 2004. Data, sample sizes and statistics affect the recognition of species of bats by their echolocation calls. Acta Chiropterologica 6: 347-363.). All acoustic parameters analyzed in this study overlap with literature data, except for the bandwidth that is lower in T. devivoi in all harmonics when compared with other species. However, as there are few samples of other species, we suggest caution in the acoustic identification of species of the family Thyroptera. The data that exists so far is not robust enough to identify any of the species with certainty.

Acknowledgments

LMSA (process # 309299/2016-0) thanks to the National Council for Scientific and Technological Development (CNPq) for her productivity research grant. MS thanks the Coordination of Improvement of Higher Level Personnel (CAPES) for his Scholarship of the National Postdoctoral Program (PNPD). The other authors thanks both agencies for their graduate scholarship. Adrian Barnett helped with the English. Ana Paula Carmignotto and Roberta Paresque told us about the colony and gave us the slow-motion footage.

References

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