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Wilson Gómez-Corea*, Jonathan Hernández, Cristopher Antúnez-Fonseca,David Mejía-Quintanilla and Hermes Vega
Leucism and updated geographic distribution ofMolossus nigricans Miller, 1902 (Chiroptera:Molossidae) in Hondurashttps://doi.org/10.1515/mammalia-2019-0153Received December 18, 2019; accepted June 23, 2020;published online September 7, 2020
Abstract: We present the first record of leucism of Molos-sus nigricans a chromatic disorder rarely documented inmammals of Honduras, as well as species’ biological andecological information. In addition, we present thecurrently known distribution and altitudinal range ofM. nigricans in Honduras, based on acoustic records,opportunistic findings and previous records. We confirmthe presence of M. nigricans in sixteen departments ofwhich four are new departmental records.
Keywords: acoustic recordings; atypical colorations;chromatic disorders; echolocation; pigment.
1 Introduction
Like other mammals, bats are susceptible to chromatic
disorders – genetic disorders that affect pigmentation –including albinism, leucism, flavism, and melanism
(Lucati and López-Baucells 2016; Zalapa et al. 2016;
Zamolo et al. 2013). Such disorders have been reported for
the order Chiroptera in the families Molossidae, Ves-
pertilionidae, Phyllostomidae, and Mormoopidae in
different countries of America (Lucati and López-Baucells
2016; Rengifo et al. 2014; Zalapa et al. 2016; Zortea and
Silva 2017) including Mexico (Zalapa et al. 2016),
Guatemala (Trujillo and Barahona 2014), Honduras
(Espinal et al. 2016), and Costa Rica (Zalapa et al. 2016).Molosid bats are swift aerial insectivores, distrib-
uted throughout the world. They comprise two sub-families, the South American endemic Tomopeatinaeand the cosmopolitan Molossinae (Eger 2008), consist-ing of 21 genera and 125 species (Wilson and Mittermeier2019). Recently Loureiro et al. (2020) for the genusMolossus, increases the number of species 11 (Loureiroet al. 2019) to 14. Loureiro et al. (2020) divide Molossusrufus into three clades, validating old names previouslyconsidered synonymous of M. rufus: Molossus rufus E.Geoffroy, 1805, Molossus nigricans Miller, 1902 andMolossus fluminensis Lataste, 1891. M. rufus previouslyknown for its wide distribution in America, from Mexicoto Peru, northern Argentina, Bolivia, Paraguay,Uruguay, Brazil, Venezuela, Suriname, the Guianas andTrinidad (Dolan 1989; Eger 2008; Simmons 2005),currently remains as a species geographically distrib-uted only for Ecuador, Peru, Bolivia, Venezuela, Guy-ana, Suriname, French Guiana, Central and NorthernBrazil, and Trinidad and Tobago (Loureiro et al. 2020).M. nigricans, has its type locality in Acaponeta, Nayarit,Mexico and is distributed in the countries of Mexico,Guatemala, El Salvador, Honduras, Nicaragua, CostaRica, and Panama (Loureiro et al. 2020). In Honduras,M. nigricans has been registered in 14 departments:Atlántida, Choluteca, Colón, Comayagua, Copán,Cortes, El Paraíso, Francisco Morazán, Islas de la Bahía,
*Corresponding author: Wilson Gómez-Corea, Universidad NacionalAutónomadeHonduras en el Valle deSula (UNAH-VS), SanPedroSula,Cortes, Honduras; Universidade Estadual de Santa Cruz (UESC),Programa de Pós-Graduação em Zoologia, Ilheus, Brasil; andPrograma de Conservación de Murcielagos en Honduras (PCMH),Tegucigalpa, Honduras, E-mail: [email protected] Hernández, Programa de Conservación de Murcielagos enHonduras (PCMH), Tegucigalpa, Honduras; and Jardín Botánico yCentro de Investigación Lancetilla, Universidad Nacional de CienciasForestales (UNACIFOR), Tela, Atlántida, Honduras,E-mail: [email protected] Antúnez-Fonseca, Universidad Nacional Autónoma deHonduras en el Valle de Sula (UNAH-VS), San Pedro Sula, Cortes,Honduras; and Departamento de Ambiente y Desarrollo, CentroZamorano de Biodiversidad, Escuela Agrícola Panamericana (EAP)Zamorano, Valle de Yeguare, Francisco Morazán, Zamorano,Honduras, E-mail: [email protected] Mejía-Quintanilla, Programa de Conservación de Murcielagosen Honduras (PCMH), Tegucigalpa, Honduras; and Fundación enCiencias para el Estudio y Conservaciónde la Biodiversidad (INCEBIO),Tegucigalpa, Honduras, E-mail: [email protected] Vega,Mancomunidad del Parque Nacional Celaque, Gracias,Honduras; and Programa de Conservación de los Murcielagos enHonduras (PCMH), Tegucigalpa, Honduras,E-mail: [email protected]
Mammalia 2020; aop
Table : Records of Molossus nigricans: previous and new corresponding to departments of Honduras.
Department Location Bibliographic source
Previous records
FranciscoMorazán
Tegucigalpa Goodwin
Cortés La Lima, San Pedro Sula, San Francisco de Yojoa and ParqueNacional Cusuco
Goodwin , Dolan , , Thompson andVulinec
La Paz San Jose and Santa Elena Goodwin , Dolan
Ocotepeque Sinuapa and Nueva Ocotepeque Goodwin , Dolan
Yoro Yoro and Santa Rita Dolan
Santa Bárbara Santa Bárbara Dolan
Copán Copán Dolan
Atlántida La Ceiba and Tela Dolan
Choluteca San Marcos de Colón Mora and Espinal Colón Parque Nacional Capiro y Calentura Supplementary Appendix Comayagua Comayagua Supplementary Appendix Islas de la Bahía Roatán Supplementary Appendix Olancho Catacamas Supplementary Appendix El Paraíso El Chichicaste Supplementary Appendix
New records Latitude Longitude Habitat Year
Atlántida Cuenca del Rio Cangrejal °′″N °′″W BF
Jardín Botánico Lancetilla °′″N °′″W BF
Choluteca Choluteca °′″N °′″W DF
San Marcos de Colón °′″N °′″W DF
Colón Parque Nacional Montaña de Botaderos °′″N °′″W BF
Comayagua Comayagua °′″N °′″W UC
Siguatepeque °′″N °′″W UC
Taulabé °′″N °′″W A
Copán Copán Ruinas °′″N °′″W SV
Macaw Mountain °′″N °′″W SV
Cortés Cuyamel, Omoa °′″N °′″W A
Lago de Yojoa °′″N °′″W SV
Rawakala, Omoa °′″N °′″W BF
San Pedro Sula °′″N °′″W SB a
Santa Cruz de Yojoa °′″N °′″W SV
El Paraíso Danlí °′″N °′″W UC
San Lucas °′″N °′″W A
Francisco Morazán Parque Nacional La Tigra °′″N °′″W PF
Tatumbla °′.″N °′.″W PF
Valle de Ángeles °′″N °′″W PF
Gracias a Dios Juan Francisco Bulnes °′″N °′″W BF
Mavita, Puerto Lempira °′″N °′″W PF
Intibucá Montaña Verde °′″N °′″W BF
La Paz Marcala °′″N °′″W SH a
Lempira Gracias °′″N °′″W UC
Lepaera °′″N °′″W DF
Olancho Catacamas °′″N °′″W A
Cuevas de Talgua, Catacamas °′″N °′″W BF
Ocotepeque El volcan, Ocotepeque °′″N °′″W A
Nueva Ocotepeque °′″N °′″W UC
Cayahuanca °′″N °′″W SV
Santa Bárbara Las Vegas °′″N °′″W VS
Valle Amapala °′″N °′″W BF
Zacate Grande °′″N °′″W MS
House andMejía (), was used to classify habitat type in some localities. (BF) Broadleaf Forest, (A) Agroecosystems, (PF) Pine forest, (DF) DryForest, (SV) Secondary Vegetation, (MS) Mangrove Swamp, (UC) Urbanized City, (SH) Shelter at Home, (SB) Shelter in Building.a Opportunistic findings, the specimen of San Pedro was collected (UVS-V ).
2 W. Gómez-Corea et al.: Molossus nigricans of Honduras
La Paz, Ocotepeque, Olancho, Santa Bárbara and Yoro(Table 1 and Supplementary Appendix 1). In this studywe present the first record of Leucism for M. nigricansand update its geographic distribution in Honduras,using primarily acoustic records.
2 Materials and methods
2.1 Identification, measurements and age
We made an opportunistic collection of an individual ofM. nigricans,and we determined its leucistic condition, based on the color of theskin and the eyes of black color, according to Lamoreux et al. (2010)and Lucati and López-Baucells (2016). We made external morpho-metric measurements, following Borisenko and Kruskop (2003) andusing a digital caliper with 0.01 mm accuracy. We abbreviate thefollowing terms: head and body length (HBL), tail length (TL), tibialength (TiL), hindfoot length (HF), ear length (EL), tragus length (TrL),forearm length (FA) and wingspan (WS). We compared the externalmeasurements to those of Dolan (1989) and Medina-Fitoria (2014),described and previously included in M. rufus. The age was deter-mined by the method of Brunet-Rossini and Wilkinson (2009). Thespecimen was preserved in formalin 10% and then in ethanol 75%before depositing it in the mastozoology collection of the NaturalHistory Museum of the Universidad Nacional Autónoma de Hondurasin Valle de Sula UNAH-VS.
2.2 Recording and analysis of echolocation calls
To investigate the geographical distribution of M. nigricans, we moni-tored various locations between 2012 and 2019 using two acoustic re-corders (SM2Bat and SM3Bat, both ofWildlife Acoustics, USA). We alsoinclude twoopportunisticfindings.We installed recorders in open areasat an approximate height of one meter above ground level, at an incli-nation of 45° (Adams et al. 2012), the recordings started at 18:00 h andended at 22:00 h on nights without strong winds or rain. Sounds wererecorded in a waveform audio format (WAV). For the identification ofM.nigricansweprocessed andanalyzed the echolocation calls using thesoftware Kaleidoscope that shows color sonograms, with high qualitysound sequences.Weanalyzed eight sonographic parameters includingmaximum frequency (Fmax), minimum frequency (Fmin) of each pulse,mean frequency (Fmean), characteristic frequency (Fc), characteristicslope (Sc), durationof eachpulse (Dur), start frequency (Fstart), and endfrequency (Fend), (Miller 2003; Thong et al. 2018). These parameterswere measured in kilohertz (kHz) and millisecond (ms). We calculatedaverage, standard deviation (SD) and variance (VAR) for the parametersmentioned above (Table 2). The analyzed echolocation calls, are fromdifferent study periods and locations as to avoid autocorrelation andpseudo-replication (Miller 2003). A sonogram of a typical call duringsearch flight of M. nigricans is shown in Figure 2C. To supplement therecords ofM. nigricans in Honduras, we performed an intensive onlinesearch of several international mammal collections, available at GlobalBiodiversity Information Facility (https://www.gbif.org/) (Supplemen-tary Appendix 1).
3 Results
On July 4, 2018 at 12:05, one of the authors collected adeceased juvenile male of M. nigricans (voucher codeUVS-V 2057) on a cobbled street in a residential area withinthe urban perimeter of the city of San Pedro Sula, depart-ment of Cortes, Honduras (15°31′55.2″N, 88°02′02.6″W at94m.a.s.l). This area has an average annual temperature of20–21 °C, with average annual rainfall between 1300 and1600 mm (SEPLAN 2014). The specimen presented whitecoloration pelage in both the dorsal and ventral part of thebody, including bristles, hair of wingmembranes and legs;the wing membranes and cream white uropatagium,slightly pink phalanges and black eyes (Figure 2A). Theexternal morphometry and weight were as follows: HBL67.52, TL 39.15, TiL 14.89; HF 12.51, EL 12.50, TrL 3.46, FA47.95, WS 183.78, Weight of 14 g.
With a sampling effort 816 H/R (Hours/Recorder) usingthe acoustic recording technique and two opportunisticfindings,we extend the knowngeographical distribution ofM. nigricans in Honduras to 16 departments, with noveldepartmental records in the departments of Gracias a Dios,Intibucá, Lempira and Valle (Figure 1 and Table 1). Theresults of the parameters for the identification of echolo-cation calls were divided into: High frequency portion,number of calls = 48 and Low frequency portion, number ofcalls = 62 (Table 2).
4 Discussion and conclusion
4.1 Leucism
We document the first record of M. nigricans in thephenotypic category of leucism according to the classifi-cation of Lamoreux et al. (2010), and Lucati and López-Baucells (2016). Our finding corresponds to the first recordof chromatic disorders within the natural distributionrange of this species and in Honduras is now the thirdspecies after the two Phyllostomidae registered by Espinalet al. (2016).
Some studies show that the collected animals (leucisticor albino) have a body size similar to those with normalcoloration (Zortea and Silva 2017). Our new specimenUVS-V 2057 is a juvenile individual, of a size correspondingto its age, and with a weight below the range of 28–37 g foradults (Medina-Fitoria 2014). The chromatic disordersaffected both the fur and the skin, including the patagium,the ears and the muzzle. The cause of death is unknown,and it is not possible to determine if it is related to the
W. Gómez-Corea et al.: Molossus nigricans of Honduras 3
individual’s leucistic condition. The chromatic disordersand their biological and ecological implication in bats arepoorly known and invite discussion. Acevedo and Aguayo(2008) consider the disorders a disadvantage that makesbats more conspicuous to predators or less attractive topotentialmates. However, Zortea andSilva (2017)mentions
that the registration of adult individuals may be indicativeof success. Rengifo et al. (2014) mentions that cases ofpigmentation disorders in Molossidae bats may be morecommon, therefore we suggest looking for bats in naturaland urban perches in order to better understand chromaticdisorders.
Figure 1: Geographical distribution of Molossus nigricans in Honduras: the new records, previous records and location of the new leucismrecord. See Table 1 and Supplementary Appendix 1 for details of the records.
Table : Selected parameters of echolocation calls of Molossus nigricans from Honduras.
Low frequency portion High frequency portion
Average Range SD VAR Average Range SD VAR
Min Max Min Max
Fmax . . . . . . . . . .Fmin . . . . . . . . . .Fmean . . . . . . . . . .Fc . . . . . . . . . .Sc . − . . . . −. . . .Dur . . . . . . . . . .Fstart . . . . . . . . . .Fend . . . . . . . . . .
Min, minimum; Max, maximum.
4 W. Gómez-Corea et al.: Molossus nigricans of Honduras
4.2 Geographical distribution andecholocation
In this study, we recorded M. nigricans in anthropogenicand natural environments, where this species is movingand dispersing, as suggested by Dolan (1989) and Santosand Castro-Arellano (2005). The two opportunistic findingsin the present study were located in roofs and cladding,(Esberard et al. 1999) mention about, that is common inspecies of the genus Molossus, which present gregariousand synanthropic habits. Through 34 records (between 8and 1896 m.a.s.l), we confirm the presence of M. nigricansin 16 departments from Honduras. We could not confirmtheir presence in the departments of Islas de la Bahía andYoro because it was not possible to carry out the respectivesampling.M. nigricans is widely distributed throughout theHonduran territory, based on our results and added to theprevious records, this species has been registered in all 18departments (Dolan 1982, 1989; GBIF.org 2019; Goodwin1942; Mora and Espinal 2012; Thompson and Vulinec 2017)(documented with the previous name M. rufus and his
junior synonym M. ater). M. nigricans is not currentlyclassified in the IUCN Red List of Threatened Species,taking as reference of M. rufus which is classified as LeastConcern (Barquez et al. 2015).
InMolossid bats calls usually show irregular frequencyalternation, variable amplitude, and great plasticity. In ourstudy, the frequency range for M. nigricans was 22.72–31.62 kHz in the low frequency portion and in the highfrequency portion was 25.31–34.34 kHz. The results of thehigh frequency parameters of the call are similar to those ofMiller (2003), the Sc and Dur parameters show variations,due to the fact that the number of samples for the portion ofhigh and low frequency are not the same. The call ofM. nigricans are frequency modulated (FM) in the little firststep of the call and the rest of the call is constant frequency(FC) (Raghuram et al. 2014). The 20–35 kHz frequencyrange for molossid bats according to Jung et al. (2014) isrelated to foraging strategies, allowing these speciesgreater success. Typically, Molossid bats feed in the highaltitude where there is no aerial barrier, issuing calls thatallow for better detection of a wide range of potential prey
Figure 2: Molossus nigricans. (A) Leucistic individual, dorsal view (UVS-V 2057); photo©WGC. (B) AdultM. nigricanswith normal coloration:dark dorsal pelage varying fromdark brown to black, locality Jardín Botánico Lancetilla; photo©JH. (C) Spectrogramandoscillogramof typicalecholocation call emitted during search flight.
W. Gómez-Corea et al.: Molossus nigricans of Honduras 5
of different sizes, and maximizing the response time tohave a successful capture of prey (Jung et al. 2014; Kalko1998).
In inventories with mist nets, records of M. nigricansare generally null or infrequent. However, in Brazil forspecies of the genus Molossus, colonies have been recor-ded that can reach more than 400 individuals (Esberard2011; Marques 1986). Jung et al. 2014, mentions that thepresence or distribution of some species of bats isunderestimated, and they are underrepresented in mostmuseum inventories and collections. The presence ofM. nigricans in the different departments of Hondurasmay indicate the presence of other insectivorous batsspecies that fly high at the canopy level away. Therefore,we suggest that for bat species, which are difficult tocapture through mist nets, acoustic monitoring methods,are used instead.
Acknowledgments: We thank the following people andinstitutions for the support they provided: Blanca Moradel,Eric Flores, Fausto Elvir, Hector Portillo, Juan Pablo Suazo,Keila Bustillo and Maria Flores, part of the technical teamof the PCMH, who were present in the field work, with thecollaboration of Lesly Torres, Roger Flores, M. Arzúa(partial monitoring); Adrián Perdomo who was part of thespecimen collectors; Ana Chavez and Jonny Miller for En-glish review, and Johan Reyes, Franger García and twoanonymous reviewers who kindly made good suggestionsto improve the manuscript; INCEBIO, Macaw Mountain,Hotel Clarion, UNAG, MAPANCE for the efforts and logis-tical support. This research was done under the permit ofthe Instituto Nacional de Conservación y DesarrolloForestal, Áreas Protegidas y Vida Silvestre (ICF), Reso-lución DE-MP-067-2018.Author contribution: All the authors have acceptedresponsibility for the entire content of this submittedmanuscript and approved submission.Research funding: None declared.Conflict of interest statement: The authors declare noconflicts of interest regarding this article.
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