Systematics of big-eyed bats, genus Chiroderma Peters, 1860 (Chiroptera: Phyllostomidae) Author Garbino, Guilherme S. T. Pós-graduação, Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Avenida Antônio Carlos 6627, Pampulha, 31270 - 901, Belo Horizonte, Minas Gerais, Brazil Author Lim, Burton K. Department of Natural History, Royal Ontario Museum, 100 Queen’s Park, Toronto, Ontario M 5 S 2 C 6, Canada Author Tavares, Valéria Da C. Laboratório de Mamíferos, Departamento de Sistemática e Ecologia, CCEN / DSE, Universidade Federal da Paraíba, Campus I, 58059 - 900 João Pessoa, Paraíba, Brazil text Zootaxa 2020 2020-09-07 4846 1 1 93 journal article 20998 10.11646/zootaxa.4846.1.1 2c8355fa-af80-4a52-be9a-a3c36a99bb19 1175-5326 4017497 6F6EBF63-5598-416C-8694-14C4A8687693 C. v. jesupi Allen, 1900 Synonyms: Chiroderma jesupi Allen, 1900: 88 ; type locality “ Cacagualito , Colombia .” Chiroderma isthmicum Miller, 1912: 25 ; type locality “ Cabima , Panama .” Chiroderma isthmica Hall and Jackson, 1953: 645 ; incorrect gender concordance. Chiroderma villosum jesupi : Handley, 1960:466 ; first use of current name combination. Distribution and Habitat. The subspecies C. v. jesupi occurs in the tropical region of trans-Andean South America and also in Central America and México . The taxon has been recorded in México ( Oaxaca , Hidalgo , Veracruz , and states to the south), Guatemala , Belize , El Salvador , Honduras , Nicaragua , Costa Rica , Panamá (including Islas Perlas), western Colombia , western Ecuador , and extreme northwestern Perú ( Tumbes ; Fig. 28 ). Collecting sites of C. v. jesupi are in dry and humid tropical forests. The taxon has been recorded from sea level up to approximately 970 m . In northwestern Perú ( Tumbes ), specimens were captured at 350 m ( Novoa et al. 2011 ). In Colombia ( Tolima ), the taxon was captured at 900 m ( Galindo-Espinosa et al . 2010 ). In southern México ( Chiapas ), the maximum capture elevation was 915 m ( Davis et al. 1964 ). Remarks. The original description of Chiroderma villosum was based on specimen ZMB 408 and on a skeleton from the anatomical collection of the Berlin museum that is probably lost ( Turni & Kock 2008 ; Garbino & Nogueira 2017 ). From the two syntypes , Turni & Kock (2008: 44) selected specimen ZMB 408 as the lectotype , but Thomas (1891: 882) had already designated the same specimen, i.e. the one represented in Peters’ plate, as the lectotype . In the species description, Peters (1860: 748) mentioned only “Brasilia” as the locality and suggested that the lectotype was collected by Friedrich Sellow. In the collection catalogue of the Museum für Naturkunde, the locality of the specimen, handwritten by Peters reads just “ Brasilien ”, and there is no note indicating who collected it ( Garbino & Nogueira 2017 ). Due to the impossibility to further restrict the type locality and the lack of evidence that it was indeed collected by Sellow, we follow most authors in citing “ Brazil ” as the type locality of Chiroderma villosum ( Handley 1960 ; Husson 1962 ; Carter & Dolan 1978 ; Simmons 2005 ; Gardner 2008a ; Turni & Kock 2008 ; Garbino & Nogueira 2017 ). Cabrera (1958: 85) erroneously designated “ Venezuela ” as the type locality of Chiroderma villosum , followed by Goodwin & Greenhall (1961) , and probably by Vieira (1942 , 1955 ), who did not include the species among the Brazilian mammals. Cabrera may have altered the type locality based on the mention of a specimen from St. Esteban, Venezuela by Thomas (1891: 56) , which was the first subsequent precise locality reported for the species. Natural History. C. villosum is a secondarily granivorous frugivore, specializing in chewing the seeds of fruits of Ficus to extract nutritive content ( Nogueira & Peracchi 2003 ; Wagner et al. 2015 ). The species apparently has preference for Ficus , and fruits of this genus may compose 100% of the diet of C. villosum in Panamá ( Bonaccorso 1979 ). Nine species of Ficus have been recorded in the diet of C. villosum in Panamá : Ficus citrifolia , F. dugandii , F. insipida , F. nymphaefolia , F. obtusifolia , F. paraensis , F. pertusa , F. popenoei , and F. trigonata ( Bonaccorso 1979 ; Handley et al. 1991 ; Wendeln et al. 2000 ; Wagner et al. 2015 ). Consumption of infructescences of Cecropia obtusa was recorded in the diet of C. villosum from French Guiana ( Lobova et al. 2003 ; Suárez-Castro & Montenegro 2015 ). C. villosum have been captured at mineral-rich clay licks (“collpas”) in the Peruvian Amazon ( Bravo et al. 2008 ; Ghanem & Voigt 2014 ). In the Guianas, Amazonia, and in the Atlantic rainforest, the species was captured more frequently in the canopy, suggesting that C. villosum is a canopy frugivore ( Ascorra et al. 1996 ; Simmons & Voss 1998 ; Charles- Dominique & Cockle 2001; Kalko & Handley Jr. 2001; Delaval et al . 2005 ; Gregorin et al. 2017 ). The only natural day roost recorded for the species are tree hollows in Venezuela ( Handley 1976 ). In addition to natural shelters, C. villosum has been found in buildings in Brazil , Panamá , and Venezuela ( Goldman 1920 ; Handley 1976 ; data from the DZSJRP collection catalogue). The following ectoparasites have been documented on C. v. jesupi : Aspidoptera busckii (Streblidae) , Trichobius joblingi (Streblidae) , Paratrichobius sp. A ( Wenzel et al. 1966 ). In Venezuela , two species of streblid bat flies ( Trichobius parasiticus and Metelasmus pseudopterus ), two spinturnicid mites ( Periglischurus acustidens and P. iheringi ), and a species of trombiculid mite ( Whartonia nudosetosa ), are known from C. v. villosum ( Herrin & Tipton 1975 ; Reed & Brennan 1975 ; Wenzel 1976 ). Marinkelle & Grose (1981) recorded Megistopoda proxima and Strebla carolliae , two species of streblid bat flies from Colombian C. villosum . The absence or rarity of spinturnicid mites on C. villosum was noted in some studies: in Panamá no mite was recorded on any specimen, in the Peruvian Amazon no mite was collected from 33 specimens , and only two mites were collected from a sample of 724 Venezuelan C. villosum ( Furman 1966 ; Herrin & Tipton 1975 ; Gettinger 2018 ). Two flesh fly larvae of the genus Sarcophaga (Sarcophagidae) , were found in the abdominal cavity of a freshly-dead female, suggesting that they parasitized the live animal ( Goodwin & Greenhall 1961 ). Blood parasites of the family Trypanosomatidae , subfamily Leishmaninae , are known from C. v. villosum from central Brazil , and Trypanosoma ( Schizotrypanum ) is documented in this species from Colombia ( Marinkelle 1982 ; Lourenço et al. 2018 ). One C. v. villosum from southeastern Brazil had traces of hantavirus infection, making C. villosum one of the few species of frugivorous bat to host this virus ( Sabino-Santos et al. 2015 ). Reproductive data from specimens we examined and from the literature ( Davis et al. 1964 ; Jones et al. 1971 ; Taddei 1976 ; Bonaccorso 1979 ; Anderson 1997 ) suggest seasonal polyestry. In Central America ( Nicaragua and Panamá ), pregnant females were recorded in January, February, and March, just before the beginning of the rainy season, and lactating C. villosum were found in February, March, and April. In South America, pregnancies were also recorded before the rainy season in July and August ( Rondônia , Brazil ) and in August and September (Bolivian, Ecuadorian, and Peruvian Amazon). In southeastern Brazil ( São Paulo ), C. villosum were recorded as pregnant in July and August. In Venezuela , pregnancies were recorded both before the rainy season in January, February, March, and April, and during the rainy season in June, and July; whereas, lactating individuals were documented in February, June, and July. Specimens Examined (N = 509): Belize : Toledo , Bladen Nature Reserve ( USNM 583035 , 583036 ) . Bolivia : Beni , Río Iténez ( AMNH 209529–209533 ) , Vacadiaz ( USNM 390606 ) ; La Paz , Santa Ana de Madidi ( AMNH 261677 ) ; Pando , Independencia ( AMNH 262526–262529 ) , Río Nareuda ( 248884 , 248885 ) ; Santa Cruz , Buenavista ( AMNH 61754 ) , Parque Nacional Noel Kempff Mercado ( AMNH 264078 , 264079 ) . Brazil : without specific locality ( ZMB 408 [lectotype of villosum ]) ; Acre , Seringal Lagoinha ( DZSJRP 13029–13033 ) , Parque Nacional da Serra do Divisor ( ALP 7011 , 7018 , 7022 , 7023 , 7050 , 7059 , 7160 , 7308 ) ; Alagoas , Mata de Coimbra ( UFPB 4349 ) ; Amazonas , Comunidade Cachoeirinha ( LMUSP [ ICA048 ]) , Humaitá ( DZSJRP 14793 ) , Igarapé Taracuá ( LMUSP [ JAP76 ]) , km 27 of BR319 ( DZSJRP 14121 , 14651 ) , km 5 of BR230 ( DZSJRP 13134 ) , opposite to Comunidade São Pedro ( LMUSP [ ICA169 ], LMUSP [ ICA170 ]), Vila de Santa Fé ( LMUSP [ JAP84 ]) ; Bahia , Ilhéus ( CMU- FLA 1076 , 1078 , 1119 ) ; Espírito Santo , Aracruz Celulose ( MZUSP 35032 ) , Fazenda Santa Terezinha ( MZUSP 35030 , 35031 ) , Reserva Natural Vale ( ALP 2806 , 2810 , 3009 , 3249 , 3327 , 3408 , 4560 , 4758 ) ; Mato Grosso , 264 km N Xavantina ( USNM 393712–393714 ) , Aricá ( MZUSP 6494 ) , Cláudia ( MZUSP [ PEV 1225-1226 ]) , Nossa Senhora do Livramento ( UFMT 1146 , 1147 ) , Parque Nacional do Juruena ( CMUFLA 1290 , 1299 ) , Sinop ( ALP 3419 ) , U.H.E. foz do Apiacás ( UFMT 1952 , 1953 ) , Usina Teles Pires ( UFMT 2137 , 2138 ) ; Mato Grosso do Sul , Estação Ecológica Dahma ( ZUFMS 492 ) , Maciço do Urucum ( ZUFMS 208 , 209 ) , Pantanal de Aquidauana ( ZUFMS 1904 ) , Pantanal de Nhecolândia ( ZUFMS 244 , 1896 ) ; Minas Gerais , Dores do Indaiá ( UFMG 3760 ) , Estação Ecológica de Pirapitinga ( ALP 9166 , 9370 ) , Fazenda Cabriúna ( CMUFLA 465 ) , Fazenda Marinheiro ( DZSJRP 14480 ) , Parque Nacional do Peruaçu ( CMUFLA 907 , 1532–1536 , 1676–1678 , 1680 , 1682 , 1684 , 1686 ), Parque Estadual do Rio Doce ( CMUFLA 1158 , 1161 , 1834 , 1839–1841 ) ; Pará , 52 km SSW Altamira ( MZUSP 22677 ) , Centro Kaiapó de Estudos Ecológicos ( MZUSP 29150–29152 ) , Floresta Nacional de Carajás ( UFMG [ VCT6305 ]) , Floresta Nacional de Carajás , Serra Norte ( UFMG [ VCT2303 ]) , Floresta Nacional de Carajás , Serra Sul , Corpo A ( UFMG [ VCT1959 ], UFMG [ VCT5157 ]), Floresta Nacional de Carajás , Serra Sul , Corpo C ( UFMG [ VCT2019 ], UFMG [ VCT5073 ], UFMG [ VCT5079 ]), Lago Jacaré ( MZUSP 13335 ) , Lago Leonardo ( MZUSP 13209 , 13197 ) , Platô Greig ( UFMG 3258 ) , Platô Monte Branco ( UFMG 3244 ) , Porto Trombetas ( UFMG 3212 , 3214 , 3221 , 3246 ) , Projeto Alemão ( UFMG [ VCT4394 ], UFMG [ VCT4444 ]), Rio Xingu , left bank ( MPEG 4112 ) , Sta.A , IAN ( USNM 361724 , 361725 ) , Várzea , Belém ( USNM 460128–460130 ) ; Paraíba , Fazenda Pacatuba ( UFPB 4 ) , João Pessoa ( UFPB 10333 , 10335 , 10336 ) ; Pernambuco , Recife ( UFMG [ M1 ], UFMG [ M2 ], UFMG [ M3 ]) ; Piauí , Boqueirão da Esperança ( ZUEC 2066 ) , Parque Nacional da Serra das Confusões ( MZUSP 33502 ) ; Rio de Janeiro , Jardim Botânico ( ALP 7419– 7424 , 7426–7431 , 8278 ) , Parque Estadual Serra da Tiririca ( ALP 5578 , 5579 ) ; Rondônia , Calama ( AMNH 37041 ) , Costa Marques ( AMNH 209575 ) , Pedra Branca ( MZUSP 22827 ) , Pedras Negras ( AMNH 209576 ) , Cachoeira de Nazaré , Rio Machado ( MZUSP 20200 , 20201 ) , U.H.E. Jirau ( MZUSP 35408 ) ; Roraima , Estação Ecológica da Ilha de Maracá ( DZSJRP 11487 ) ; São Paulo , São José do Rio Preto ( DZSJRP 4586 , 4676 ) , Engenheiro Schmidt ( DZS- JRP 4804 ) , Fazenda São Paulo ( DZSJRP 14302 , 14305 , 14319 ) , Roberto ( DZSJRP 16549 ) , Parque Natural Municipal Grota de Mirassol ( DZSJRP 4000 , 4032 , 4033 ) , Fazenda Paraguassu ( ZUEC 968 ) , Sítio Progresso ( DZSJRP 3783 , 3922 , 4337 , 4386–4390 ) ; Sergipe , Estação Ecológica de Itabaiana ( CMUFS 64 ) , Mata do Junco ( CMUFS 97 ) , Parque Nacional Serra de Itabaiana ( ALP 8971 ) ; Tocantins , U.H.E. São Salvador ( MZUSP [ SSI178 ]) . Colombia : no specific locality ( USNM 598086 ) ; Amazonas , Puerto Nariño ( USNM 483777 ) ; Antioquia , La Tirana ( IAvH-M 930 , USNM 449480–499482 ) , Vereda La Pola , Parque Nacional Natural Los Katíos ( IAvH-M 4923 ); Chocó , Corregimiento Gilgal , P.N.N. Los Katíos ( IAvH-M 4924–4926 ), Reserva Florestal Especial Las Teresitas ( IAvH-M 3257 ), Vereda El Tilupo, P.N.N. Los Katíos ( IAvH-M 4927–4929 ) ; Magdalena , Cagualito ( AMNH 14574 [holotype of jesupi ]), Parque Nacional Natural Tayrona ( IAvH-M 4198 ), Vereda El Congo ( IAvH-M M-9665 ) ; Putumayo , Caño Caucayá ( IAvH-M M-624 ); Sucre , Estación Primates ( IAvH-M 9583 ), Quebrada El Sereno ( IAvH-M 9593 ) ; Valle del Cauca , Río Zabaletas ( USNM 483770–483776 ) ; Vaupés , Caño Arara ( IAvH-M 1550 ). Costa Rica : Puntarenas , Corcovado National Park ( USNM 565813 ) . El Salvador : La Libertad , Deininger Park ( TTU 63906 ) ; La Paz , Hacienda Escuintla ( TTU 63911 ) ; La Unión , El Tamarindo ( TTU 63912 ) . Ecuador : Los Ríos , Beata Elvira ( USNM 498921 , 498922 ) , El Papayo ( USNM 498923 , 522435–522437 ) , Hacienda Santa Teresita ( USNM 522438 ) , Lima Pareja ( USNM 498924 , 498925 , 522434 ) , Río Nuevo ( USNM 534315 , 534316 ) , Vinces ( USNM 534314 ) ; Pastaza , Lorocachi ( USNM 548240 , 548241 ) , Santiago (not located; USNM 548242 ) , Tiguino ( USNM 574537 , 574539 ) , Yosa (not located, USNM 548237–548239 ) ; Pichincha , Río Palenque Science Center ( USNM 528541 ) . Guatemala : Jutiapa , Colonia Montufar ( AMNH 217417 ) , Santa Rosa , La Avellana ( AMNH 235312–235315 ) . Guyana — Barima-Waini , North West , Santa Cruz ( ROM 98850 ) ; Cuyuni-Mazaruni , 24 km along Potaro road from Bartica ( BMNH 1965.645 ) , Namai Creek ( ROM 108219 ) ; Upper Demerara-Berbice , Dubulay Ranch ( USNM 582328 ) ; Upper Takutu-Upper Essequibo , Chodikar River ( ROM 106644 ) . French Guiana : Sinnamary , Paracou ( AMNH 267190 , 267191 , 268534 – 268536 ) . México : Veracruz , Xalapa (= Jalapa ) ( BMNH 81.10.27.1 ) . Nicaragua — Zelaya (currently Región Autónoma de la Costa Caribe Sur) , 4,5 km NW Rama ( TTU 12794 ) . Panamá — Bocas del Toro , Almirante ( USNM 315559–315562 ) , Isla Popa ( USNM 464304 ) , Sibube ( USNM 335298 , 335299 ) ; Colón , Bohio Peninsula ( USNM 503637 ) ; Darién , Cana ( USNM 179619 ) , El Real ( USNM 338045 ) , Jaqué ( USNM 362920 ) , Punta Piña ( USNM 314718 ) , Tacarcuna Village Camp ( USNM 309894 , 309896–309900 ) ; Los Santos , Cerro Hoya ( USNM 323451–323453 ) , Guánico Arriba ( USNM 323448–323450 ) ; Panamá , Barro Colorado Island ( USNM 304904 , 304905 , 304907–304909 , 332053 , 457954 , 544896 ) , Cabima ( USNM 173834 [holotype of isthmicum ], USNM 173836 ), Cerro Azul ( USNM 305386 ) , Culebra ( USNM 223402 ) , Gamboa ( USNM 520557 , 520558 ) , Isla San José ( USNM 448449 ) , Punta de Cocos ( USNM 314719 , 314720 , 314721 ) , Río Mandinga ( USNM 305385 ) ; San Blas (currently Guna Yala ) , Armila ( USNM 335300–335316 ) ; Veraguas , Isla Cébaco ( USNM 360219 ) . Perú : Cusco , Camisea ( USNM 582836 ) , Camisea , Armihuari ( MUSM 13606 , 13631 , 13634 , 13636 , 13637 , 13639– 13641 ) , Camisea , Konkariari ( MUSM 14742 ) , Camisea , Pagoreni ( MUSM 13610 , 13615 , USNM 582839 ) , Camisea , San Martín ( MUSM 13618 , 13644 , USNM 582840 , 582841 ) , Jenaro Herrera ( MUSM 6791 ) , Ridge Camp ( USNM 588033 ) ; Loreto , 13,6 km NW Albarenga ( MUSM 26545 ) , Alto Río Pauya ( MUSM 17734 ) , Centro de Investigaciones Jenaro Herrera ( MUSM 4221 , 4222 ) , Estación Biologica Allpahuayo ( MUSM 16476 ) , Ninarumi ( MUSM 29560 , 29561 ) , Paujil ( MUSM 29562 ) , Puesto de Vigilancia Castaña ( MUSM 21136 ) , Quistococha ( USNM 337940 ) , Río Lagartococha ( MUSM 21137 ) , Río Pisqui , Campamento Llanura ( MUSM 17735 ) , Río Samiria ( MUSM 29562 ) , Río Samiria , Flor de Yarina ( MUSM 1637 ) , Río Samiria , Tacshacocha ( MUSM 1638 , 1639 ) , San Lorenzo ( BMNH 1924.3.1.75 , 1924.3.1.76 ), Zungarococha ( MUSM 29563 ) ; Madre de Dios , CICRA ( MUSM 26106 ) , Cocha Salvador ( MUSM 733 ) , Estación Biológica Cocha Cashu ( MUSM 15856 ) , Explorer’s Inn Lodge ( MUSM 1640 ) , Hacienda Amazonia ( MUSM 9757 ) , Maskoitania ( MUSM 19671 ) , Pakitza ( MUSM 6781 , USNM 566544 ) , Quebrada Aguas Calientes ( MUSM 16653 , 16660 , 16661 , 16665–16667 ) , Reserva Cuzco Amazónico ( MUSM 6168 , 6169 ) , Santuario Nacional Pampas del Heath ( MUSM 12827 ) ; Pasco , Campamento Río Lobo ( MUSM 10232 ) , Cerro Chontiya ( MUSM 10225 , 10230 , 10231 ) , San Juan ( USNM 364418 ) , Villa America ( MUSM 1641 ) ; San Martín , Concesion de Conservación Valle del Biavo ( MUSM 43843 , 43844 , 43485 ) , Juanjuí ( MUSM 1642 ) , Saposoa ( MUSM 1643 ) , Yurac Yacu ( BMNH 27.1.1.63 ) ; Tumbes , Carrizalillo ( MUSM 22123 ) , Parque Nacional Cerros de Amotape ( MUSM 22121 , 22122 ) , Quebrada Las Pavas ( MUSM 24479 ) ; Ucayali , 59 km W Pucallpa ( USNM 461256 ) , Concesión de Conservación Río La Novia ( MUSM 44186 , 44187 , 44472 ) . Suriname : Brokopondo , Brownsberg Nature Park ( ROM 114212 ) ; Sipaliwini , Kushere Landing ( ROM 120226 ) . Trinidad and Tobago : Tobago , Charlotteville ( USNM 540676 ) ; Trinidad , without specific locality ( AMNH 256325 ) , Diego Martin ( AMNH 183167 ) , Grande Riviere ( AMNH 172149 ) , Guaico Tamana ( AMNH 172148 ) , Maracas Valley ( AMNH 175599 ) , Waterloo ( BMNH 1897.6.7.44 ) . Venezuela : Amazonas , 9 km SE Puerto Ayacucho ( MZUSP 27168 ) , Cerro Neblina base camp ( USNM 560606 , 560607 , 560767 , 560768 , 560769 , 560770 , 560771 , 560772 ) , Río Cunucunuma ( USNM 405127 , 405165 , 405167–05171 ) , Río Manapiare ( USNM 408624–408660 , 408662–408678 ) , Río Mavaca ( USNM 405175 ) , San Carlos de Rio Negro ( USNM 560604 , 560605 ) , Tamatama ( USNM 405176 , 405177 , 408611–408617 ) ; Bolívar , El Manaco ( USNM 387205–387209 , 387212 , 387213 , 387126 , 387210 , 387211 , 387214 , 387215 ) , Hato La Florida ( USNM 405164 ) , Hato San José ( USNM 405162 ) , Río Supamo ( USNM 387204 ) ; Sucre , Manacal ( USNM 408620 ) ; Yaracuy , 19 km NW Urama ( USNM 372145 , 372146 , 372149 , 372150 ) .