1
Federal University of Rio Grande do Norte
Postgraduate Program in Ecology (PPGE)
“Diversity and structure of bat (Chiroptera) assemblages
in Caatinga dry forests in northeastern Brazil”
MSc. Juan Carlos Vargas Mena
Advisor: Dr. Eduardo Martins Venticinque Federal University of Rio Grande do Norte Co-advisor: Dr. Bernal Rodríguez Herrera University of Costa Rica
2020
2
Universidade Federal do Rio Grande do Norte - UFRN Sistema de Bibliotecas - SISBI Catalogação de Publicação na Fonte. UFRN - Biblioteca Setorial Prof. Leopoldo Nelson - •Centro de Biociências - CB
Vargas-Mena, Juan Carlos. A diversidade e estrutura de assembleias de morcegos (Chiroptera) na Caatinga do Rio Grande do Norte, Brasil / Juan Carlos Vargas Mena. - Natal, 2020. 196 f.: il.
Tese (Doutorado) - Universidade Federal do Rio Grande do Norte. Centro de Biociências. Programa de Pós-graduação em Ecologia. Orientador: Prof. Dr. Eduardo Martins Venticinque. Co-orientador: Prof. Dr. Bernal Rodríguez Herrera
1. Quirópteros - Tese. 2. Cavernícolas - Tese. 3. Diversidade beta - Tese. I. Venticinque, Eduardo Martins. II. Universidade Federal do Rio Grande do Norte. III. Título.
RN/UF/BSCB CDU 599.4
3
Juan Carlos Vargas Mena
“A diversidade e estrutura de assembleias de morcegos (Chiroptera) na Caatinga
do Rio Grande do Norte, Brasil”
Dissertação apresentada ao programa de Pós- Graduação em Ecologia da Universidade Federal do Rio Grande do Norte, como parte do requerimento para obtenção do título de
doutor em Ecologia.
Aprovada em 5 de março de 2020
______Dr. Enrico Bernard (UFPE) Examinador Externo à Instituição
______Dra. Valeria da Cunha Tavares (UFPB/UFMG) Examinador Externo à Instituição
______Dr. Marlon Zortéa (UFJ/UFG) Examinador Externo à Instituição
______Dr. Mauro Pichorim (UFRN) Examinador Interno ______Dr. Eduardo Martins Venticinque (UFRN) Presidente
4
TABLE OF CONTENTS
RESUMO ...... 7 ABSTRACT: ...... 8 INTRODUCTION ...... 13 THESIS FRAMEWORK ...... 27 REFERENCES ...... 28 Chapter 1...... 42 Alpha and Beta diversity of bat assemblages in the heterogeneous Caatinga dry forests in northeastern Brazil ...... 42 ABSTRACT ...... 43 INTRODUCTION ...... 44 METHODOLOGY ...... 47 RESULTS...... 54 DISCUSSION ...... 65 CONCLUSIONS ...... 74 REFERENCES ...... 74 SUPPLEMENTARY MATERIALS ...... 82 Chapter 2...... 94 Seasonal structure and reproductive patterns of cave-dwelling bat assemblages in Caatinga dry forests in northeastern Brazil ...... 94 ABSTRACT ...... 95 INTRODUCTION ...... 96 METHODOLOGY ...... 99 RESULTS...... 105 DISCUSSION ...... 114 CONCLUSION ...... 126 REFERENCES ...... 126 SUPPLEMENTARY MATERIALS ...... 134 Chapter 3...... 142 The bats of Rio Grande do Norte, northeastern Brazil...... 142 RESUMO: ...... 143 INTRODUCTION ...... 144 MATERIAL AND METHODS ...... 145 RESULTS...... 147 DISCUSSION ...... 153 5
REFERENCES ...... 165 GENERAL CONCLUSIONS ...... 171 APPENDIX 1 ...... 174 APPENDIX 2 ...... 175
6
RESUMO Na Caatinga a heterogeneidade espacial das diferentes ecorregiões e fitofisionomias, bem como a sazonalidade das chuvas e os pulsos dos recursos alimentares, foram atribuídos como fatores chaves no controle da estrutura e a dinâmica das assembleias de morcegos nesta floresta seca. Quase 95% do estado do Rio Grande do Norte (RN) corresponde à Caatinga, que abriga abundantes cavidades subterrâneas (~ 1000 cavernas). Como os padrões de diversidade espacial e temporal da fauna de morcegos são praticamente desconhecidos na Caatinga, o objetivo principal desta tese foi explorar os padrões espaciais e temporais de riqueza, abundância e composição de espécies de assembleias de morcegos em diferentes paisagens, fitofisionomias e em seus abrigos em cavernas. No Capítulo 1, explorei a riqueza e diversidade espacial e temporal na composição espécies e trófica de morcegos através de capturas com redes de neblina em 5 habitats diferentes de Caatinga em seis regiões do RN. Em 99 noites de amostragem, capturei 1575 indivíduos de 31 espécies, com um esforço de captura de 242 425 hm2. Foram encontradas diferenças na composição de especeis e guildas tróficas entre as assembleias tanto nas diferentes áreas de estudo como nos diferentes habitats amostrados, provavelmente relacionadas às preferências ecológicas especificas das espécies e pelas características da paisagem de cada área. A riqueza e a composição das espécies não apresentaram variação sazonal, e abundância variou pouco entre as estações. Os recursos alimentares encontrados ao longo do ano podem ser o principal fator que sustenta uma estrutura semelhante da assembleia durante a estação seca e chuvosa. No capítulo 2, monitorei nove cavernas em quatro regiões da Caatinga do RN para examinar os efeitos das estações e do tamanho das cavernas sobre a riqueza, abundância e composição das espécies de morcegos cavernícolas. Utilizando dois métodos, registramos 17 espécies de morcegos em 2020 indivíduos capturados e 3200 indivíduos observados durante 61 dias de amostragem. A riqueza e a composição das espécies não mudaram sazonalmente e não foi encontrado um recambio temporal das espécies entre as estações. Um aumento na abundância geral de morcegos foi encontrado na estação chuvosa, principalmente pelos insetívoros, e alguns nectarívoros, especificamente no final da estação chuvosa. Foi encontrada uma interação entre as estações e o tamanho da caverna. Na estação chuvosa, as cavernas maiores tenderam a variar mais em abundância do que as cavernas menores provavelmente pela maior capacidade de carga das cavernas maiores (maior espaço e diversidade de microclimas). No entanto, a composição das espécies entre cavernas grandes e pequenas foi diferente. Em geral, o aumento sazonal da abundância nas cavernas é provavelmente atribuído à disponibilidade temporária de recursos alimentícios e a fins reprodutivos. Os morcegos frugívoros, insetívoros e animalívoros foram reprodutivamente ativos durante a estação chuvosa, onde seu alimento preferido é mais abundante. Enquanto aos sanguinívoros, onívoros e nectarívoros estiveram reprodutivamente ativos durante as duas estações já que seus recursos alimentícios estiveram disponíveis durante o ano todo. Já no capítulo 3, fiz uma revisão taxonômica em coleções e uma revisão bibliográfica para determinar a diversidade 7 gamma de morcegos no RN resultando na primeira lista oficial de morcegos do estado, incluindo novos registros e discussões sobre áreas de conservação e áreas de pesquisa prioritária. Como resultado geral desta tese, consegui registar 32 espécies de 3595 indivíduos capturados e mais de 3200 morcegos observados durante 161 dias de amostragem. O analises dos dados indicam que, em geral, as assembleias de morcegos são adaptadas para permanecerem o ano todo nas mesmas áreas, mas são fortemente afetadas pela estrutura espacial da vegetação de suas áreas preferidas de forrageio, a disponibilidade sazonal de alimento e as características dos seus abrigos subterrâneos. Além disso, reforça a importância de cavernas durante a época chuvosa para a reprodução de várias espécies de morcegos na Caatinga potiguar, incluindo para espécies endêmicas e ameaçadas de extinção. Os resultados desta tese, junto com a colaboração fundamental de muitas pessoas valiosas, é um esforço para descrever e ter uma visão mais profunda da história natural e a ecologia da diversa fauna de morcegos da Caatinga brasileira.
Palavras Chave: cavernas, cavernícolas, diversidade beta, floresta sazonalmente secas, guildas tróficas, quirópteros, registros novos, sazonalidade, reprodução
ABSTRACT: In the Caatinga dry forest, the spatial heterogeneity of the different ecoregions and phytophysiognomies, as well as the seasonality of rainfall and the pulses of food resources, were attributed as key factors in controlling the structure and dynamics of bat assemblages. Almost 95% of the state of Rio Grande do Norte (RN) corresponds to the Caatinga, which harbors abundant underground cavities (~ 1000 caves). As the patterns of spatial and temporal diversity of bat fauna are practically unknown in the Caatinga, the main objective of this thesis was to explore the spatial and temporal patterns of richness, abundance and species composition of bat assemblages in different landscapes, phytophysiognomies and cave roosts. In Chapter 1, I explored the spatial and temporal richness, abundance and trophic and species composition of bats through captures using mist nets in five different Caatinga habitats in six areas in RN. In 99 sampling nights, I captured 1575 individuals of 31 species, with a capture effort of 242 425 hm2. Differences in the structure was found at the species- and ensemble-level (trophic guilds) between the assemblages both in the different studied areas and in the different habitats. This is likely related to species specific preferences to favor specific landscape characteristics and foraging habitats. Richness and species composition presented no evident seasonal variation between season. Food resource found along the year may be the key factor that sustain a similar structure of the bat assemblage year-round. In Chapter 2, I monitored nine caves in four regions of the Caatinga of RN to examine the effects of the seasons and the size of the caves on the richness, abundance and composition of the species of cave bats. Using two methods, we recorded 17 species of bats of 2020 captured individuals and 3700 individuals observed during 61 sampling days. Species richness and composition did not change seasonally and no
8 temporal species turnover was found. An increase in the general abundance during in the rainy season was found, especially in insectivores and some nectarivores, specifically at the end of the rainy season. An interaction was found between the seasons and the size of the caves. In the rainy season, the larger caves tended to vary more in abundance than the smaller caves, probably due to the greater carrying capacity of larger caves (greater space and diversity of microclimates). However, the species composition between large and small caves was different. In general, the seasonal increase in abundance in caves is attributed to the temporary availability of food resources and reproductive purposes. Frugivores, insectivores and animalivores were reproductively active during the rainy season, where their preferred food is abundant. Sanguinivores, omnivores and nectarivores were reproductively active during both seasons as their food resources were available throughout the year. In chapter 3, I did a taxonomic review in museum collections and a bibliographic review to determine the gamma diversity of bats in RN resulting in the first official list of bats in the state, including new records and discussions on conservation areas and areas of research priority. In this thesis, I managed to register 32 species of 3595 captured individuals and more than 3700 observed bats during 161 days of sampling. In general, the data indicates that the bat species are adapted to remain in the same areas all year round, but the structure of bat assemblages are different depending on the foraging habitats and landscape contexts. However, changes in abundance can be found in their cave roosts depending on the trophic guild, and likely attributed to the seasonal availability of food and to the different use that the species are giving to the cave (e.g. reproduction). In addition, our data reinforces the importance of caves during the rainy season for the reproduction of several bat species in the Caatinga of RN, including for endemic and endangered species. The results of this thesis, together with the fundamental collaboration of many valuable people, is an effort to describe and to have a deeper insight of the natural history and ecology of the diverse bat fauna of the Brazilian Caatinga.
Key Words: caves, cave-roosting, Chiroptera, conservation, beta diversity, new records, Seasonal dry tropical forests, trophic guilds, reproduction
9
ACKNOWLEDGMENTS
[Portuguese]
Fazer uma tese de doutorado por si só é praticamente impossível. É por isso que durante esses quatro anos tive a ajuda essencial e inestimável de muitas pessoas incríveis que conheci e tive o prazer de trabalhar em conjunto. São muitas pessoas, mas espero não deixar ninguém de fora.
Primeiro aos meus pais, Nuria e Robert, que me trouxeram a este mundo, e que por sempre terem me ensinado desde criança a trabalhar duro, a ir sempre além, nunca abaixar a cabeça e me adaptar às mudanças e adversidades que a vida nos coloca, incluindo em nossos momentos de fraqueza emocional. A eles, juntamente com meus irmãos Jessica e Robert, e sobrinhos Jose, Gabriel, Saúl e
Liat, agradeço infinitamente o apoio incondicional desde longe lá na Costa Rica que me deu tanta força para enfrentar esta aventura aqui no Brasil. Não sei como explicar para vocês o muito que os amo. Igual, obrigado a meus primos, tios, e avós que igual, sempre estiveram pendentes e me torcendo por mim aqui no Brasil. Também a minha avó Sara e tia Xinia que estão em algum melhor lugar e que sempre me apoiaram e aconselharam a estudar. A saudade de vocês é gigante.
No mato por onde andei tanto, tive vários pais temporários que me guiaram, me protegeram e me alimentaram com comida incrivelmente deliciosa, reparadora e cheia de amor. Me receberam de maneira indescritível. Graças a eles, conheci a realidade e as dificuldades do povo nordestino e, por isso, cheguei a amar tanto a Caatinga. O que eu ensinei a eles sobre morcegos não se compara a tudo o que eles me ensinaram sobre a vida no Sertão. Talvez com a pessoa que compartilhamos mais tempo em campo foi com Seu João. Obrigado pela paciência, sabedoria, histórias, músicas, ensinamentos e proteção, por me mostrar a caatinga pela primeira vez na Serra do Feiticeiro. Talvez uns dos melhore mateiros com os quais já andei Também a Darquinha com sua comida incrível, e a Pedrinho pela ajuda no mato procurando cavernas e Jusara pelos momentos legais e brincadeiras, aos pais de Seu João, Seu
Lourival e Dona das Dores, pelo acolhimento e inumeráveis cafezinhos que a gente bebeu. Em
Mossoró e Barauna, quero agradecer a Iatagan que tanto me ajudou e me ensinou do mato e
10 espeleologia, desde saber onde botar os pés para descer numa fenda de 7m até sua ajuda em tirar dezenas de morcegos nas redes da boca das cavernas. Sua dedicação e amor pela Caatinga e pelo parque (PARNA Furna Feia) é uma das coisas que poucas vezes vi, é admirável. A Rielson pela ajuda no mato e seus pais por me receberam lá no seu sitio e a comida também incrível, e pelo acolhimento na sua casa para eu ir no parque. Aos mateiros em Felipe Guerra, Valtenci, com sua energia e histórias inacreditáveis, a Edinho com sua perspicácia e alegria, e ao Juninho que tanto salvou a gente tirando morcegos, e carregando quilos de equipamento pelo Lajedos a mais de 40 graus de quentura, com uma força admirável. A companhia de vocês na noite na Caatinga foi incomparável. A Seu Cicero, esposa e filhas pelo acolhimento, alegria imensa e comida maravilhosa. Realmente posso falar que comi comida nordestina autentica e sensacional. A Leonardo Brasil, chefe do PARNA, por permitir a gente entrar no parque e descobrir seus morcegos. A ajuda técnica e logística do Diego do CECAV foi chave nesta tese e Lucia que me ensinou a importância de educação ambiental nas comunidades. Aos dois, obrigados pela amizade e colaboração. Enfim, sem todos vocês os dados não teriam sido coletados e essa tese não existiria.
Aos meus amigos, Julia, Ricardo, Marina, Pocas, Camura, Eli, Helô, Juanpy, Rafa, Dardo,
Carols, Hada, Angélica, Patri, Rodrigão, Felipe, Phillip, Lica, Guga, Isa, Duka, Marília, Bruno, Caro e
Helder, a amizade de vocês sem dúvida alguma foi essencial para poder afrontar o doutorado com tantos churrascos, praias, surf, ressacas, risos, historias e doideras. A mis amigos ticos que coincidentemente estuvimos aquí en Brasil estudiando, Adri y Pichi, por compartir juntos el mal de patria y afrontar la distancia de la familia y de Tiquicia. Também quero agradecer a meus amigos e companheiros de laboratório, Paulo, Virginia, Fer, e Ellen, pela ajuda em campo, papos, risos e geladas para sobreviver a pós-graduação. Vai dar certo!
Aos meus orientadores, realmente sua dedicação e esforço pela ciência de vocês é inspiradora.
Dadão, muito obrigado pelos ensinos, conversas, risos e surf sessions que fizemos, e por ter me aceitado há 6 anos atrás como seu estudante, sua paciência e conhecimento é admirável. A Bernal, que
11 conheci há 8 anos atrás em Tirimbina, você tem sido como um irmão mais velho para mim, suas palavras de incentivo, dicas, conselhos e conhecimento de mamíferos e morcegos não tem preço. Sem vocês eu não poderia ter esses títulos acadêmicos que tenho hoje, obrigado por tudo e pela sua amizade. Também agradecer a todos aos professores do DECOL que tanto aprendi de vocês, em especial ao Carlinhos, Gis, Serginho, Marcio, Liana, Gabriel.
E por último, a Eu! Eu, não sei por onde empezar, poderia escrever tantas coisas que seria quase uma tese (haha). Mas em resumo, te agradeço não só pela ajuda física em campo, que não tivesse dado certo sem você, mas também pela ajuda psicológica e moral que foi incondicional durante todos esses anos. Em todo esse processo, desfrutamos, rimos e comemoramos, também choramos, sofremos e suamos, mas sem dúvida tudo ficou muito mais fácil com você ao meu lado. Aqueles momentos em que eu tirava das redes centos de morcegos enquanto você processando todos eles, é algo nunca vou esquecer. Obrigado por acreditar em mim.
O presente trabalho foi realizado com apoio com fundamental do CNPq (Pesquisador Visitante
Especial-PVE - Projeto de Ecologia e Conservação de Morcegos na Caatinga Potiguar: 401467 / 2014-
7), The Rufford Small Grants Foundation, The National Geographic Society e Wildlife Conservation
Society Brasil pelo apoio na logística de campo. E por último, agradecer a Coordenação de
Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Código de Financiamento 001, pela bolsa de doutorado que recebi durante esses 4 anos, auxilio clave para o desenvolvimento deste trabalho. And, finally,
Finalmente, quero agradecer à nossa mãe terra que nos brinda abrigo e comida todos os dias.
Graças às plantas, entre outros seres vivos, que me ajudaram muito, e aos morcegos por existir e reforçar minha paixão pela fauna com a qual habitamos esta terra.
OBRIGADO!!
O presente trabalho foi realizado com apoio da Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Código de Financiamento 001.
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001 12
INTRODUCTION Early community ecology was preoccupied with the identification and listing the species found in particular localities (Elton 1966). However, the understanding the species diversity patterns and the structural properties in the communities that the species form has been an important focus in modern ecology (Peet 1974, Koleff and Gaston 2002, Magurran 2004, Begon et al. 2006, Morin
2009). In general, an ecological community consists of a set of species that occur together in space and time (Begon et al. 2006). However, the definition of community may be more complex and the concept could include a combination of boundaries used to delimit a community per se, such as a space, time, the species interactions and its phylogenetic relationships (see Fauth et al. 1996).
MacArthur (1965) was one of the first to describe the diversity and composition of different communities using islands as a model. He identified two main components in a community: 1) the diversity within habitats, and 2) the diversity among habitats. Based on this, MacArthur concluded that the total diversity of an archipelago was the diversity within the islands, as well, the degree of species differentiation among islands. Years later, Whittaker (1972) named these community components – alpha, beta and gamma diversities (Fig. 1). The Alpha diversity (α) is the species richness of a particular community regarded as homogeneous (within the habitat diversity). Beta diversity(β) is a
Figure A. (a) The spatial components of landscape diversity proposed by Whittaker, where α is within-habitat species richness, β is between-habitats turnover, and γ is the cumulative species richness of the habitat. (b) The temporal components of habitat diversity along different times, α is the habitat species richness in each sample, β is between-samples species turnover, and γ is the cumulative species richness of the habitat during a sampling period. Figure taken from Moreno & Halffter (2001).
13 measure of the difference in species composition, or species turnover, and comprehends changes or the replacement of the species identity between different communities of different habitats (spatial β- diversity). Similarly, the β-diversity measures devised to express species turnover or changes in species composition across time can be equally applied across time in a habitat or region. Thus, a temporal species turnover is an explicit measure of change over time (temporal β-diversity) and addresses the number of species added or eliminated per unit time (Magurran 2004). Finally,
Whittaker (1972) proposed that the total number of species in a region, the gamma (γ) diversity, is the result of the combination of alpha and beta diversity. These two diversities can be combined in many ways to result in gamma diversity (Shmida and Wilson 1985).
According to Whittaker (1975), the study of the differences in the identity of the species between two or several sites or regions is therefore important to understand how a community is organized, how is its structure , or its non-randomness, this as a living system of populations of interplaying species. Though, most communities are very complex and consequently community ecologists often focus on conspicuous sets of species, or subsets, that are ecologically or taxonomically similar. One important subset of a community is an assemblage (Fig. B). According to
Fauth et al. (1996), an assemblage is taxonomically or phylogenetically related group of species populations that occur together in space and time (e.g. bat assemblages) and is not determined by the use of a particular resource, hence it can include, for example, trophic groups (e.g. frugivorous, nectarivorous, insectivorous bats). Conversely, a subset of the community that exploits the same kind of resources in a similar functionally way is called a guild (Fig. B), thus a guild for instance, of frugivores, may include bats, primates and birds. In the other hand, when a group of species under consideration is defined by both phylogenetically and functionally, this subset is referred to as an ensemble (Fauth et al. 1996, Stroud et al. 2015).
14
In general, an species assemblage are recognized to be shaped by 1) historical factors,
including small- and large-scale isolation events that influence speciation, migration and extinction;
and by 2) ecological conditions like interactions between species ( e.g. mutualism, competition and
predation), distribution and availability of resources, and abiotic factors (e.g. climate, topography);
which all play key roles in the structuring processes of an assemblage (Ricklefs and Schluter 1993).
Because of the complexity of the interaction of such factors, in community studies, results largely
depend upon the choice of study organisms and upon the spatio-temporal scale at which those studies
are conducted (Ricklefs and Schluter 1993). Therefore, throughout this thesis, I will use the
abovementioned theoretical framework to characterize and analyze in spatio-temporal scale the
different assemblages and ensembles of Neotropical bats (Chiroptera) in the Caatinga, a seasonal dry
forest endemic from Brazil.
Figure B. Venn’s diagram representing that populations under study may be divided into three different sets defined by phylogeny (Set A), geography (Set B), and resources (Set C). The intersections of these sets provide definitions for the terms of “assemblage”, “guild” and “ensemble”. The intersection of guild and taxa denotes an entity for which no term exists. Taken and modified from Fauth et al. 1996.
Diversity in Neotropical bat assemblages
Assemblages of the Chiroptera order (bats) are among the richest in species and only second
to rodents (Fenton and Simmons 2015). Just in the Neotropics, around 380 bat species distributed in
98 genera has been described – the largest gamma diversity of any other biogeographical region
(Solari and Martínez-Arias 2014). The alpha and gamma diversities in some Neotropical regions can
15 reach to more than 60 and 100 species, respectively, and surpassing that of most other mammal assemblages (Brosset et al. 1996, Kalko et al. 1996, Simmons and Voss 1998). The patterns of diversity within bats assemblages, however, are not evenly distributed in the Neotropics and as we get closer to the equator, the phylogenetic (Stevens et al. 2006), taxonomic (Stevens and Willig 2002) and functional (Stevens et al. 2003) diversity of chiropterans increases.
Considering the high ecological diversity of bats within a single assemblage, the classification bats into guilds or ensembles, either by their preferred diet (e.g. fruits, insects, nectar and pollen, fish, vertebrates, blood) (Mcnab 1971, Fleming 1986, Kalko 1998, Kunz and Fenton 2003, Giannini and
Kalko 2004), their foraging habitats (Norberg and Rayner 1987, Kalko 1998, Patterson et al. 2003), echolocation strategies (Kalko 1998, Schnitzler and Kalko 2001, Jung et al. 2007) or roosting ecology
(Kunz 1982, Simmons and Voss 1998, Bernard and Fenton 2003, Kunz and Lumsden 2003, Vargas-
Mena et al. 2018b) is a very straightforward method to understand the structure of these assemblages.
In Neotropical bat assemblages, few species dominate, followed by a large number of uncommon and rare species. In general, frugivores bats dominate in the assemblages, while a low number of species is found per guild (Kalko 1998). The Leaf-nosed bats (Phyllostomidae) are the most functionally and taxonomically diverse family in the Neotropics (Stevens et al. 2003, Solari and
Martínez-Arias 2014) and comprehends most of the proportion of the species composition.
Nevertheless, these patterns might not reflect the reality of the species composition of the assemblages and might be subject to methodological or sampling bias. For instance, phyllostomid bats are easily detected, or captured, using mist nets, the conventional capture method in most of the bat studies
(Kunz and Kurta 1988). However, mist nets fails to detect other guilds with fine echolocation capabilities that easily avoids mist nest, like those who feed on insects (MacSwiney et al. 2008). Thus,
Neotropical insectivorous bats are commonly undetected and undersampled. The use of other methods other than mist nets like echolocation recorders, the use of canopy mist nests and search of roost sites, will help to correct the bias and provide a detection of a largest amount of species of a determined assemblage (Kalko 1998, Moreno and Halffter 2000, Flaquer et al. 2007, Silva and Bernard 2017).
16
Nevertheless, bat assemblages in the Neotropics are very rich in number of guilds, which is much higher than in temperate zones (10 guilds vs. 4), as well the number of species within each guild
(Kalko 1998). Frugivores dominate the assemblage and the structure of the guild seems to be similarly organized as the assemblage as whole, with few species being very abundant and followed by a series of uncommon ones. Other guilds, like gleaning animalivores, are less common and the species seems to be more evenly distributed within the guild (Mares et al. 1981, Kalko et al. 1996, Simmons and
Voss 1998). It is likely the different feeding ecology of bats and the distribution and abundance of food resources contributes to these patterns in the assemblages (Kalko 1998).
As explained before, the spatial β-diversity describe changes in the species composition. This spatial β-diversity is known to be influenced by the species biogeographic history, the spatial scale
(the extent of the study), niche limitations and the organism’s dispersal capabilities (Barton et al. 2013,
Calderón-Patrón et al. 2013). When dispersal ability is low the spatial beta diversity is high (Baselga et al. 2012). For instance, among terrestrial vertebrates the lowest beta diversity occurs in birds, which have the highest vagility. Reptiles and mammals have intermediate values, while amphibians have the highest values due to their limited ability to disperse (Koleff et al. 2008, Dobrovolski et al. 2012).
However, considering the flight ability of bats, it is expected the high gamma diversity in region could be explained by the high species richness (alpha diversity) in most of its localities that most contribute to the overall gamma diversity, and not by a high turnover of species associated to a spatial variation in species composition (beta diversity). This is expected because a geographic barrier or habitat variation that could limit, for instance, a small non-flying mammal, would be more likely to be overcome by bats due to their flying capability (Norberg and Rayner 1987). Such mobility capacity provides dispersal potential and reduces their dependence on an environmental characteristic or on particular habitat (Willig and Moulton 1989). This was found to explain the diversity bats in Mexico
(Arita 1997, Moreno and Halffter 2001, Arita and Rodríguez 2002, Rodríguez and Arita 2004) and in central Brazil (Santos et al. 2016).
17
However, López-González et al. (2014) presented contrary evidence to this hypothesis as well in Mexico. Authors found that bats responded directly to habitat composition and structure where the beta diversity and vegetational heterogeneity were significantly correlated. The authors conclude that the significant relationships between beta diversity and environmental variation revealed differences in habitat specialization by bats, hence explaining the high bat diversity in all Mexico. Therefore, the high gamma diversity of bats in region could be explained by a high turnover of species or beta diversity associated to a spatial variation in species composition, contrary to the initial hypothesis of a high species richness (alpha diversity) in most of its localities. This means that areas with spatial differences or characteristic can harbor assemblages with high differences in its species composition, despite the flight and high dispersal capacity of bats.
This high spatial beta diversity hypothesis is plausible since Neotropical bats are characterized by having ecological specializations and life history traits to specific habitats and resources (Kunz and
Pierson 1994). For instance, studies have found that the diversity and species composition in a particular assemblage can change significantly in response to a particular habitat or to a particular landscape composition or configuration (Medellín et al. 2000, Gorrensen and Willig 2004). As well, studies on both Neotropical natural and human-modified landscapes have found that the structural patterns of the studied bat assemblages had species-, guild- and ensemble-specific responses to the composition and configuration of the landscape (Medellín et al. 2000, Gorrensen and Willig 2004,
Gorrensen et al. 2005, Faria 2006, Pinto and Keitt 2008, Klingbeil and Willig 2009, Avila-Cabadilla et al. 2012, Dias-Silva et al. 2018, Willig et al. 2019). This studies evidence that the structure of bat assemblages can be affected by spatial differences as a result of the habitat specialization by the different species of bats.
Nevertheless, in the Neotropics as a whole, Stevens and Willig (2002), found a dramatic increase in the species richness at broad scales of resolution toward the tropics (gamma diversity) where it was attributed to both the increased richness at the local level (alpha diversity) and to the latitudinal increase in the species turnover among the communities (beta diversity). Moreover,
18
Varzinczak et al. (2017) found that for phyllostomid assemblages, spatial processes explained better the species composition and phylogenetic lineages than environmental and historical processes, likely as a result of topographic complexities limiting the species dispersal, regardless of the bat’s dispersal capabilities. Overall, the structure of bat assemblages seems to be related to complementary ecological and evolutionary processes at different levels of diversity and geographical scales throughout the
Neotropics.
Bat ecology in Seasonally Dry Tropical Forests In general, Seasonally Dry Tropical Forests (SDTF) present the most extreme climate conditions among tropical ecosystems and mammals inhabiting these forests are adapted to cope with high temperatures, pronounced seasonality on the precipitation distribution with long dry seasons (4-6 months) (Dirzo et al. 2011). Plant communities present a distinct phenology characterized by being deciduous during the dry season and evergreen during the rainy season (Mooney et al. 1995). As a result of this, the availability of food and water resources fluctuates throughout the year (Dirzo et al.
2011).
Such resource fluctuation consequently exerts strong pressures on most mammalian species that inhabits SDTF (Stoner and Timm 2011). For instance, small mammals like bats, are known to present behavioral adaptations that include changes and flexibility in diet, local movements, short- and long-distance migrations, timing of activity and/or foraging, and seasonality of reproduction, in function of the seasonal availability of resources found in the landscape (Stoner and Timm 2004). Of these behavioral adaptations, the seasonality of reproduction is a common adaptation found in bats that inhabits in SDTF (Stoner and Timm 2011). In general, bats are especially sensitive to timing birth with food availability, since lactation is the most energetically costly activity of the reproductive cycle
(Racey 1982, Racey and Entwistle 2000). Thus, bats in SDTF show a clear pattern of birth related to seasonality and hence to resource abundance (Stoner and Timm 2004, 2011).
However, patterns of seasonal reproduction of Neotropical bats in SDTF are scarce and mostly concentrated to the northern hemisphere. For instance, two peaks of pregnancy and two of lactation – a
19 bimodal reproduction – has been found in leaf-nosed bats (Phyllostomidae) throughout the year, especially in nectarivores and frugivores in SDTF, and with parturition occurring at the beginning and middle of the rainy season, a time with highest resource abundance (fruits, flowers, nectar). This has been found mainly in Central America (Mares and Wilson 1971, Fleming et al. 1972, Stoner 2001,
Stoner and Timm 2004) and Mexico (Stoner et al. 2003, Sperr et al. 2011, Ferreyra-García et al.
2018), but as well in Brazil (Willig 1985a, 1985b, Cordero-Schmidt et al. 2017). Nevertheless, most of the reproductive patterns of SDTF’s bats comes from studies on the Phyllostomidae, a family easily captured than high-flying aerial insectivore bats for instance. Despite this, in insectivorous
(Vespertilionidae and Mormoopidae) and piscivorous bats (Noctilionidae) a seasonal unimodal reproduction have been reported with one peak of pregnancy and lactation during the beginning of the rainy season in Mexico and northeastern Brazil (Garrido-Rodríguez et al. 1984, Mares et al. 1985,
Willig 1985b, 1985a). As in most of the Neotropical SDTF, the northeastern region of Brazil harbors one of the world’s largest SDTF but data on the bat community ecology are scarce and patterns for instance on their reproductive ecology and biology is poorly known.
Bats in the Caatinga Dry Forests Brazil contains the New World’s largest and most diverse SDFT – the Caatinga (Silva et al.
2017). Located in the semiarid region of northeastern Brazil and occupying an area of 912 529 km2, the Caatinga dry forest encompasses parts of nine states of Brazil (Alagoas, Bahia, Ceará, Paraíba,
Pernambuco, Piaui, Sergipe, Minas Gerais and most of Rio Grande do Norte (Leal et al. 2003).
Mistakenly considered to be poor in species, the Caatinga is actually a rich and complex ecological system harboring a unique natural and cultural heritage of global importance (Leal et al. 2003).
However, is the most populated dry forest of the world with about 28.6 million people that depends largely on the exploitation of the natural ecosystem for several purposes such as fuelwood and raising livestock (Melo 2017). This has cause large deforestation rates that has converted at least 63.3% of the
Caatinga into anthropogenic ecosystems (Silva and Barbosa 2017).
20
Unlike other Brazilian tropical forests, the Caatinga presents extreme environmental and meteorological parameters: high solar radiation, low cloudiness, the highest average annual temperature, the lower rates of relative humidity, higher potential evapotranspiration (Prado 2003). It has a low and irregular rainfall (300-1000 mm/year) concentrated and unevenly distributed in 3-6 months (Silva et al. 2017) and long droughts of 8-11 months may occur between years (Marengo et al.
2018). Such extreme climatic conditions characteristic of semiarid regions influences directly the plant phenology (Prado 2003, Silva et al. 2017). Like in most SDTFs, plants in the Caatinga are evergreen and produce flowers and fruits during the short rainy season, while in the long dry season most of plants are deciduous but some species retain their leaves and can produce flowers and fruits (Leal et al.
2003).
The Caatinga is a very heterogeneous region with highly diverse biota and endemism, hence considered as the most diverse SDTF (Silva et al. 2017). Eight different ecoregions have been described within the Caatinga (Velloso et al. 2001) where 13 different phytofisiognomies occurs
(Andrade-Lima 1981) distributed into six main vegetational units (Prado et al. 2003). Such vegetational heterogeneity yields a plant richness of 3150 species where 23% are endemic to Caatinga
(Queiroz et al. 2017). The fauna is also rich and 187 species of bees (32% endemic) (Zanella and
Martins 2003), 98 amphibians (21% endemic) (Garda et al. 2017), 116 reptiles (Rodrigues 2003), 548 birds (Araujo and Silva 2017), 386 Fishes (52% endemic) (Lima et al. 2017) and 183 species of mammals (6% endemic) mostly represented by rodents and chiropterans (bats) (Carmignotto and
Astúa 2017).
In Brazil the bat diversity is one of largest of the world, harboring 14% of all the chiropterans of the world (Paglia et al. 2012). Recent revisions and studies a megadiverse country, have recorded
182 species of bats have been officially listed (Nogueira et al. 2018). That is about one-quarter of the overall diversity of the Brazilian mammal species (Paglia et al. 2012). However, of the six terrestrial ecoregions found in Brazil, only the Atlantic Forest is well sampled, leaving the Caatinga with only
10% of its area sampled, hence its chiropterofauna is poorly known in relation to other ecoregions in
21
Brazil (Bernard et al. 2011). However, in the recent years there has been a significant increase in studied on its chiropterofauna. In the last 30 years, the gamma diversity of Caatingas’ bats have gone from 46 species (Willig and Mares 1989) to 96 species (Silva et al. 2018). The taxonomical composition of Caatingas’ bats are dominated by the Phyllostomidae family (52 species.), followed by
Molossidae (17), Vespertilionidae (12), Emballonuridae (8), Mormoopidae (3), Noctilionidae (2) and
Natalidae and Furipteridae with one species (Silva et al. 2018). Two species are endemic of Caatinga,
Lonchophylla inexpectata (Moratelli and Dias 2015) and Chiroderma vizottoi (Taddei and Lim 2010).
As well, the species Xeronycteris vieirai (Gregorin and Ditchfield 2005) (see Fig. C) is found to be endemic to Caatinga and Cerrado ecosystems (Dias and Oliveira 2019). It should be noted that these endemic species were recently described which reflects the job of the increasing number of studies on the Caatinga’s bats in last years. Nonetheless, given the inconspicuousness of this mammalian group, the total number of bat species in Caatinga may be higher (Silva et al. 2018).
As in other Neotropical ecosystems, the structure of Caatinga bat assemblages contains members of all of these trophic ensembles (Paglia et al. 2012). In general, frugivorous bats are very diverse within the Caatinga’s assemblages occurring from forested to disturbed habitats (Mares et al.
1981, Willig 1983, Willig and Mares 1989, Silva 2007, Gregorin et al. 2008, Sá-Neto and Marinho-
Filho 2013, Novaes and Laurindo 2014, Rocha et al. 2018, Soares et al. 2018), while nectarivores are found to be also abundant, in spite of the low richness in certain localities (Willig 1983, Sá-Neto and
Marinho-Filho 2013, Novaes and Laurindo 2014, Cordero-Schmidt et al. 2017, Rocha et al. 2018,
Soares et al. 2018). Gleaning animalivorous bats are found to be rich in species but found in low abundances and more associated to more forested Caatingas (Mares et al. 1981, Silva 2007, Guimaraes
Beltrâo and Aguiar Fracasso 2011, Sá-Neto and Marinho-Filho 2013, Nogueira et al. 2015, Silva et al.
2015). Omnivore bats are poor in species but seems to be locally common in some areas (Sá-Neto and
Marinho-Filho 2013, Nogueira et al. 2015, Soares et al. 2018) while sanguinivores seems to be common in disturbed areas (Gregorin et al. 2008, Nogueira et al. 2015, Rocha et al. 2018, Soares et al.
2018) and rather less common in preserved forested Caatingas (Vargas-Mena et al. 2018b). As for
22 insectivorous bats, a considerable richness in the Caatinga have been reported but with few individual per species (Gregorin et al. 2008, Novaes and Laurindo 2014, Beltrão et al. 2015, Soares et al. 2018) but some localities can be abundant (Silva 2007, Beltrão et al. 2015, Novaes et al. 2015). However, the diversity of insectivorous bats in the Caatinga might be underestimated due to sampling bias since common sampling techniques used in most of the available studies relies on the solely use of mist nets, a method easily avoided by insectivore bats which possesses a fine and strong echolocation
(MacSwiney et al. 2008).
Cave-dwelling bat assemblages
Bats spend more than half their lives in their roost environment, consequently their roosting habits are influenced by roost abundance and availability, risk predation, distribution and abundance of food resources, social organization and energy economy imposed by body size and environmental abiotic factors (Kunz 1982). But the evolution of flight and echolocation has allowed bats to exploit roost resources virtually unavailable to other vertebrates, specially a wide variety of internal shelters, such as caves, rock crevices, tree cavities, and man-made structures (Kunz 1982). Particularly, caves and underground cavities are very common roosting sites for bats and most families and genera include species that dwells in caves.
Caves are normally stable and last for long periods of time, hence provide to bats protection against predators, adverse environmental conditions, areas for breeding and offspring care, and for hibernation in temperate zones (Kunz 1982, Trajano 1995, Tuttle and Moreno 2005). Many caves have become to harbor traditional locations for resident populations, therefore play a key role in the protection of bat populations, especially those species that form large colonies (Trajano 1985, 1995,
Arita 1993, Arita and Vargas 1995, Avila-Flores and Medellín 2004, Medellín et al. 2017). A single cave for instance, can alone provide a wide variety of structural substrates, including crevices, cavities, textured walls and ceilings, massive rooms, rock outcrops, and rock rubble on floors to be occupied by several bat species (Kunz et al., 2012). This is possible because bats have specific microclimate requirements when choosing a roost, like temperature and humidity (Avila-Flores and Medellín 2004).
23
The morphological complexity found inside a cave is expected to create a spatial variation in temperature and humidity conditions that can create a greater diversity of roosting sites in larger caves than in smaller caves, for instance (Brunet and Medellín, 2001). Thus, a wide array of different species with different ecological adaptations can colonize a single large cave (Altrigham 1996). However, parameter of these microclimates can vary depending on latitude and altitude, depth and volume of cave (Kunz 1982, Kunz et al. 2012, Oliveira et al. 2018).
The diversity and structure of cave bat assemblages are known to be strongly influenced by factors related to cave structure and size, where larger and more geomorphologically complex caves tend to harbor richer bat assemblages (Arita 1996, Brunet et al. 2001, Cardiff 2006, Niu et al. 2007,
Luo et al. 2013, Phelps et al. 2016, Torquetti et al. 2017, Vargas-Mena et al. 2020). However, other studies have also found that the diversity and structure patterns of cave bat assemblages are affected by other factors such as intra- and interspecific interactions (Arita and Vargas 1995, Rodríguez-Durán and Soto-Centeno 2003), species-specific microclimate preferences (Rodríguez-Durán and Soto-
Centeno 2003, Avila-Flores and Medellín 2004), relative humidity (Brunet and Medellín 2001, Rocha and Bichuette 2016), roost disturbances by humans (Luo et al. 2013, Voigt and Kingston 2016), and the external environment or “landscape context” where a cave is located (Furey and Racey 2016,
Phelps et al. 2016, Vargas-Mena et al. 2020).
In some cases, a single cave may contain thousands, even millions of individuals of one or more species (Kunz, 1982), where, particularly in the Neotropics, caves have been frequently reported hosting more than 10 species (Arita 1993, Guimarães and Ferreira 2014, Pérez-Torres et al. 2015,
Felix et al. 2016, Vargas-Mena et al. 2018b). Some caves can gather features required by large colonies; therefore, these caves have been used for thousands of years (Tuttle & Moreno, 2005).
Caves, mines, and other artificial underground habitats are critical sites for bats and some species rely almost exclusively on such sites for roosting and breeding and (Hutson, 2001). Unfortunately, underground habitats are particularly vulnerable to the effects of a range of human activities including tourism, caving, guano collection, and quarrying (Furey and Racey 2016).
24
In Brazil, more than 17 000 cavities have been officially registered (CECAV 2018). Such cavities provide an important roost resource for Brazilian bats and from the 183 species of recorded in the country (Nogueira et al. 2014, Feijó et al. 2015, Fischer et al. 2015, Moratelli and Dias 2015,
Gregorin et al. 2016, Rocha et al. 2016), up to 72 (39%) species have been found roosting in caves
(Oliveira et al. 2018). The Brazilian cave-dwelling bat assemblages are particularly rich in bats from the Phyllostomidae family, especially those belonging to the subfamily Phyllostominae (Trajano
1995). Aerial insectivorous are a common as well, and species from the Mormoopidae family are known to form exceptionally large colonies (Pteronotus sp.) (Núñez-Novas et al. 2016, Otálora-Ardila et al. 2019), and members of the Emballonuridae family are also very common (Guimarães and
Ferreira 2014). Species from the Furipteridae (Furipterus horrens) and Natalidae (Natalus macrourus) families are known be roost only in caves in Brazil but are rare species (Reis et al. 2007, Leal et al.
2012) and considered vulnerable to extinction (MMA/ICMBio 2014).
In Caatinga, cave-roosting bat assemblages are poorly explored. For instance, less than 3% of all of the Brazilian caves have been studied regarding bats (Guimarães and Ferreira 2014, Oliveira et al. 2018), therefore this percentage is even much lower in the Caatinga where caves in these dry forest are numerous (Jansen et al. 2012, Jansen and Pereira 2014). This large number of caves within the
Caatinga landscape are indeed major roosting sites for local bat species, some of them essential for the conservation of endangered and cave-dependent species such as Natalus macrourus, Furipterus horrens and Lonchorhina aurita (Delgado-Jaramillo et al. 2018, Vargas-Mena et al. 2018b).
Nonetheless, studies have found a bat fauna with assemblages ranging from 3 to 15 species. (Trajano and Gimenez 1998, Gregorin and Mendes 1999, Silva and Guedes 2001, Gregorin et al. 2008, Sbragia and Cardoso 2008, Guimarães and Ferreira 2014, Oliveira et al. 2018, Vargas-Mena et al. 2018b).
Ecological importance of bats
Because of this high functional group diversity, bats provide value to ecosystems as primary, secondary, and tertiary consumers that support simple to complex natural and human dominated ecosystems (Kunz et al., 2011). Many bats are directly involved in several ecological processes. They
25 are pollinators and seed dispersers of a high number of plants (Allen-Wardell et al., 1998; Medellín &
Gaona, 1999; Aguiar et al., 2008; Lobova et al., 2009; Quesada et al., 2009) including several plant species of economic and ecological importance in semiarid environments (e.g. Agavaceae, Cactaceae)
(Kunz et al. 2011). They are predators of vertebrates and invertebrates (Belwood & Morris 1987;
Fenton 1995; Kalka et al., 2008) and control populations of insects including some agricultural pests
(Cleveland et al., 2006; Aguiar & Antonini, 2008; Reiskind & Wund, 2009; Boyles et al., 2011; Kunz et al., 2011). Thus, for directly participating in ecological processes associated with ecosystems and representing a significant portion of the Neotropical mammals, impacts from the strong alteration of the natural landscape affects the population and the ecological services that bats provide.
Moreover, bats that roost in caves play a crucial role in the maintenance of ecological processes in the internal ecosystems on caves (Trajano 1995, Ferreira and Martins 1999). They are responsible for the increase of organic matter in cave ecosystems through guano deposition under roosting sites. This guano is an important food source for the cave fauna due to the general lack of food in caves (Gnaspini and Trajano 2000). Some species of invertebrates are totally dependent on guano for their existence and cave communities can perish if the input of guano falls below certain limits (Trajano, 1995).
Bats in the state of Rio Grande do Norte
The state of Rio Grande do Norte (RN) contains one of the most conspicuous gaps of information (RN) (see Bernard et al. 2011). The earliest records of bats in RN date back to the past century, when Sanborn (1937), Goodwin (1959), Webster (1993), and Jones & Hood (1993) reported few bat records from the coastal region of the state (municipality of Natal) and deposited the specimens in biological collections in United States. Studies on bats in RN slowly began to increase in this century, with new records and distributional expansions (Feijó and Nunes 2010, Barros et al.
2017, Basílio et al. 2017), natural history (Cordero-Schmidt et al. 2016, 2017), community diversity
(Barros et al. 2017, Vargas-Mena et al. 2018b, 2020), and subterranean fauna inventories (Ferreira et
26 al. 2010); including a bibliographic review on the bat fauna in northeastern Brazil by Garcia et al.
(2014). These studies together have recorded a gamma diversity of 38 species of bats in the state.
Considering the small size of Rio Grande do Norte, the state is home of a rich and abundant diversity of cave bats. Seventeen species from five families, mainly phyllostomids, have been recorded in RN. (Basílio et al. 2017, Cordero-Schmidt et al. 2017, Vargas-Mena et al. 2018b). These includes, one Caatinga endemic (Lonchophylla inexpectata) and three vulnerable species in Brazil (Furipterus horrens, Natalus macrourus and Lonchorhina aurita) (Moratelli and Dias 2015, Vargas-Mena et al.
2018b). Therefore, three of the seven species of bats classified as species with high risk of extinction in Brazil (MMA/ICMBio, 2016) have been found roosting in RN (Vargas-Mena et al. 2018b).
Moreover, caves are harbor high richness (e.g. 10 species) and large colonies of insectivore and omnivore bats with more than 5000 individuals (Vargas-Mena et al. 2018b). This ensemble richness account for one-third of the total bat species recorded in the state (Vargas-Mena et al. 2018a).
In spite of this recent effort to unravel the cave bat fauna in RN, data of the temporal diversity, structure and reproduction phenology patterns is Caatinga’s caves are lacking. Therefore, monitoring cave roosts is an ideal method to detect changes in the diversity patterns, species composition, seasonal changes in populations within the cave-roosting bat ensembles. Such data can provide an indirect insight of behavioral adaptations in relation to the strong seasonality that the Caatinga imposes.
THESIS FRAMEWORK
Considering the poor knowledge of the distribution and basic ecology of bats both in the heterogenous landscape and in the numerous cave roosts in the seasonal Caatinga dry forest of Rio
Grande do Norte (RN), I wanted to respond four central questions (How? When? What? Who?) distributed in three chapters within this thesis:
27
1) How is the structure regarding richness (alpha) and species composition (spatial beta
diversity) of bat assemblages in different Caatinga habitats in six different sites in Rio Grande
do Norte State? (Chapter 1)
2) When in time does it occur differences in the diversity and species composition (temporal
beta diversity) of bat assemblages (Chapter 1) and in their roosts (cave-roosting bats)?
(Chapter 2)
3) What is the effect of the seasons the structure and reproduction patterns in cave-dwelling bat
assemblages and their reproduction activity? (Chapter 2)
4) Who composes the gamma diversity of bats in RN? (Chapter 3)
I wanted to generate novel ecological and natural history information about the chiropterofauna in the Caatinga of RN in order to have a first insight about the spatial and temporal patterns of the different assemblages in different habitats, regions and cave roosts and describe their reproductive patterns. The data generated in this thesis will aid to fill the gap information about the diversity of bats and their ecology in one of the least studied regions of the endemic Caatinga dry forest. I hope that the information herein will be considered as reference for futures researches, as well by any non-and governmental organizations or institutions in the creation and execution of conservation policies and protection actions of the local bat populations, roosting sites and Caatinga habitats.
REFERENCES
Arita, H. T. 1993. Conservation Biology of the Cave Bats of Mexico. Journal of Mammalogy 74:693– 702. Arita, H. T. 1996. The conservation of cave-roosting bats in Yucatan, Mexico. Biological Conservation 76:177–185. Arita, H. T. 1997. The non-volant mammal fauna of Mexico : Species richness in a megadiverse country. Biodiversity and Conservation 6:787–795. Arita, H. T., and P. Rodríguez. 2002. Geographic range , turnover rate and the scaling of species. Ecography 25:541–550. Arita, H. T., and J. A. Vargas. 1995. Natural History , Interspecific Association , and Incidence of the 28
Cave Bats of Yucatán , México 40:29–37. Avila-Cabadilla, L. D., G. A. Sanchez-Azofeifa, K. E. Stoner, M. Y. Alvarez-Añorve, M. Quesada, and C. A. Portillo-Quintero. 2012. Local and landscape factors determining occurrence of phyllostomid bats in tropical secondary forests. PLoS ONE 7. Avila-Flores, R., and R. A. Medellín. 2004. Ecological, Taxonomic, and Physiological Correlates of Cave Use By Mexican Bats. Journal of Mammalogy 85:675–687. Barros, M. A. S., C. M. G. Morais, B. M. B. Figueiredo, G. B. de Moura Júnior, F. F. dos S. Ribeiro, D. M. A. Pessoa, F. Ito, and E. Bernard. 2017. Bats (Mammalia, Chiroptera) from the Nísia Floresta National Forest, with new records for the state of Rio Grande do Norte, northeastern Brazil. Biota Neotropica 17. Barton, P. S., S. A. Cunningham, A. D. Manning, H. Gibb, D. B. Lindenmayer, and R. K. Didham. 2013. The spatial scaling of beta diversity. Global Ecology and Biogeography 22:639–647. Baselga, A., J. M. Lobo, J. Svenning, P. Aragón, and M. B. Araújo. 2012. Dispersal ability modulates the strength of the latitudinal richness gradient in. Global Ecology and Biogeography 21:1106– 1113. Basílio, G. H. N., J. P. M. de Araujo, J. C. Vargas-Mena, P. A. Rocha, and M. A. F. Kramer. 2017. Chrotopterus auritus (Peters, 1856) (Chiroptera, Phyllostomidae): first record for the state of Rio Grande do Norte, northeastern Brazil. Check List 13:1–8. Begon, M., C. R. Townsend, and J. L. Harper. 2006. Ecology: From Individuals to Ecosystems. 4th edition. Blackwell Publishing company, Oxford. Beltrão, M. G., C. G. Zeppelini, M. P. A. Fracasso, and L. C. S. Lopez. 2015. Inventário de morcegos em uma área de Caatinga no Nordeste brasileiro, com uma nova ocorrência para o estado da Paraíba. Neotropical Biology and Conservation 10:15–20. Bernard, E., L. M. S. Aguiar, and R. B. Machado. 2011. Discovering the Brazilian bat fauna: A task for two centuries? Mammal Review 41:23–39. Bernard, E., and M. B. Fenton. 2003. Bat Mobility and Roosts in a Fragmented Landscape in Central Amazonia, Brazil1. Biotropica 35:262. Brosset, A., P. Charles-Dominique, A. Cockle, J.-F. Cosson, and D. Masson. 1996. Bat communities and deforestation in French Guiana. Canadian Journal of Zoology 74:1974–1982. Brunet, A. K., and R. A. Medellín. 2001. the Species–Area Relationship in Bat Assemblages of Tropical Caves. Journal of Mammalogy 82:1114–1122. Brunet, A. K., R. a. Medellín, and A. K. Brunet. 2001. the Species–Area Relationship in Bat Assemblages of Tropical Caves. Journal of Mammalogy 82:1114–1122. Calderón-Patrón, J. M., C. E. Moreno, R. Pineda-lópez, and G. Sánchez-rojas. 2013. Vertebrate Dissimilarity Due to Turnover and Richness Differences in a Highly Beta-Diverse Region : The 29
Role of Spatial Grain Size , Dispersal Ability and Distance. PLoS ONE 8:1–10. Cardiff, S. G. 2006. Bat Cave Selection and Conservation in Ankarana, Northern Madagascar. Columbia University, New York. Carmignotto, A. P., and D. Astúa. 2017. Mammals of the Caatinga : Diversity , Ecology , Biogeography , and Conservation. Pages 211–254 in J. M. C. da Silva, I. R. Leal, and M. Tabarelli, editors. Caatinga: The Largest Tropical Dry Forest Region in South America. Springer International Publisher, Cham, Switzerland. Cordero-Schmidt, E., E. Barbier, J. C. Vargas-Mena, P. P. Oliveira, F. D. A. R. Santos, R. A. Medellín, B. R. Herrera, and E. M. Venticinque. 2017. Natural History of the Caatinga Endemic Vieira’s Flower Bat, Xeronycteris vieirai. Acta Chiropterologica 19:399–408. Cordero-Schmidt, E., M. Medeiros-Guimarães, J. C. Vargas-Mena, B. Carvalho, R. L. Ferreira, B. Rodriguez-Herrera, and E. M. Venticinque. 2016. Are Leaves a Good Option in Caatinga’s Menu? First Record of Folivory in Artibeus planirostris (Phyllostomidae) in the Semiarid Forest, Brazil. Acta Chiropterologica 18:489–497. Delgado-Jaramillo, M., E. Barbier, and E. Bernard. 2018. New records, potential distribution, and conservation of the Near Threatened cave bat Natalus macrourus in Brazil. Oryx 52:579–586. Dias-Silva, L., G. T. Duarte, R. Alves, M. J. R. Pereira, and A. Paglia. 2018. Feeding and social activity of insectivorous bats in a complex landscape: The importance of gallery forests and karst areas. Mammalian Biology 88:52–63. Dias, D., and M. B. De Oliveira. 2019. Firts record of Xeronycteris vieirai Gregorín & Ditchfield, 2005 (Chirptera, Phyllostomidae) from the Cerrado Biome. Oecologia Australis:1–14. Dirzo, R., H. S. Young, H. A. Mooney, and G. Ceballos. 2011. Seasonally Dry Tropical Forests: Ecology and Conservation. Island Press, Washington. Dobrovolski, R., A. S. Melo, F. A. S. Cassemiro, and J. A. F. Diniz-filho. 2012. Climatic history and dispersal ability explain the relative importance of turnover and nestedness components of. Global Ecology and Biogeography 21:191–197. Elton, C. S. 1966. The Pattern of Animal Communities. Page (2012 Springer Science & Business Media, Ed.). Michigan U. Springe International Publisher. Faria, D. 2006. Phyllostomid bats of a fragmented landscape in the north-eastern Atlantic forest, Brazil. Journal of Tropical Ecology 22:531–542. Fauth, J., J. Bernardo, and M. Camara. 1996. Simplifying the Jargon of Community Ecology : A Conceptual Approach Source : The American Naturalist , Vol . 147 , No . 2 ( Feb ., 1996 ), pp . 282-286 Published by : The University of Chicago Press for The American Society of Naturalists Stable URL : htt. The American … 147:282–286. Feijó, A., P. Adriano, D. A. Rocha, and S. L. Althoff. 2015. New species of Histiotus (Chiroptera: 30
Vespertilionidae) from northeastern Brazil. Zootaxa 4048:412–427. Feijó, J. A., and H. L. de F. L. Nunes. 2010. Primeiro registro de Myotis nigricans (Schinz, 1821) para o estado do Rio Grande do Norte, nordeste do Brasil. Chiroptera Neotropical 16:531–534. Felix, S., R. L. M. Novaes, R. F. Souza, and L. S. Avilla. 2016. Bat assemblage in a karstic area from northern Brazil: Seven new occurrences for Tocantins state, including the first record of Glyphonycteris sylvestris Thomas, 1896 for the Cerrado. Check List 12. Fenton, M. B., & Simmons, N. B. 2015. Bats: A World of Science and Mystery. University of Chicago Press. Ferreira, R. L., and R. P. Martins. 1999. Trophic structure and natural history of bat guano invertebrate communities, with special reference to Brazilian caves. Tropical Zoology 12:231–252. Ferreira, R. L., X. Prous, L. F. de O. Bernardi, and M. Souza-Silva. 2010. Fauna Subterrânea Do Estado Do Rio Grande Do Norte: Caracterização E Impactos. Revista Brasileira de Espeleologia 1:1–27. Ferreyra-García, D., R. A. Saldaña-Vázquez, and J. E. Schondube. 2018. La estacionalidad climática no afecta la fenología de murciélagos cavernícolas con dieta omnívora. Revista Mexicana de Biodiversidad 89:488–496. Fischer, E., C. F. Santos, L. F. A. da C. Carvalho, G. Camargo, N. L. da Cunha, M. Silveira, M. O. Bordignon, and C. de L. Silva. 2015. Bat fauna of Mato Grosso do Sul, southwestern Brazil 15:1–17. Flaquer, C., I. I. Torre, and A. Arrizabalaga. 2007. Comparison of Sampling Methods for Inventory of Bat Communities. Journal of Mammalogy 88:526–533. Fleming, T. H. 1986. The structure of Neotropical bat communities: a preliminary analysis. Revista Chilena de Historia Natural 59:135–150. Fleming, T. H., E. T. Hooper, and D. E. Wilson. 1972. Three Central American Bat Communities : Structure , Reproductive Cycles , and Movement Patterns. Ecology 53:556–569. Furey, N. M., and P. A. Racey. 2016. Conservation Ecology of Cave Bats. Pages 463–500 in C. C. Voigt and T. Kingston, editors. Bats in the Anthropocene: Conservation of Bats in a Changing World. Springe International Publisher, London. Garcia, A. C. L., E. S. B. Leal, C. Rohde, F. G. Carvalho-Neto, and M. A. Montes. 2014. The bats of northeastern Brazil: A panorama. Animal Biology 64:141–150. Garda, A. A., M. G. Stein, R. B. Machado, M. B. Lion, F. A. Juncá, and M. F. Napoli. 2017. Ecology , Biogeography , and Conservation of Amphibians of the Caatinga. Pages 133–149 in J. M. C. da Silva, I. R. Leal, and M. Tabarelli, editors. Caatinga: The Largest Tropical Dry Forest Region in South America. Springer International Publisher, Cham, Switzerland. Garrido-Rodríguez, D., P. F. Servin, M. G. Boyer, and S. J. Vergara. 1984. Patrón de reproducción del 31
murciélago insectívoro Pteronotus parnellii mexicanus Miller, 1902 (Chiroptera: Mormoopidae). Revista de Biología Tropical 902:253–262. Giannini, N. P., and E. K. V. Kalko. 2004. Trophic structure in a large assemblage of phyllostomid bats in Panama. Oikos 105:209–220. Gnaspini, P., and E. Trajano. 2000. Guano communities in tropical caves. Pages 251–268 Ecosystems of the World. Gorrensen, P. M., and M. R. Willig. 2004. Lanscape responses of bats to habitat fragmentation in Atlantic Forest of Paraguay. Journal of Mammalogy 85. Gorrensen, P. M., M. R. Willig, and R. E. Strauss. 2005. Multivariate Analysis of Scale-Dependent Associations Between Bats and Landscape Structure. Ecological Applications 15:2126–2136. Gregorin, R., A. P. Carmignotto, and Alexandre R. Percequillo. 2008. Quirópteros do Parque Nacional da Serra das Confusões, Piauí, nordeste do Brasil. Chiroptera Neotropical 14:366–383. Gregorin, R., and A. D. Ditchfield. 2005. New Genus and Species of Nectar-Feeding Bat in the Tribe Lonchophyllini (Phyllostomidae: Glossophaginae) From Northeastern Brazil. Journal of Mammalogy 86:403–414. Gregorin, R., and L. de F. Mendes. 1999. On Chiroptera (Emballonuridae, Phyllostomidae, Natalidae) of two caves at Chapada Diamantina, Bahia, Brazil. Iheringia Serie Zoologia 86:121–124. Gregorin, R., L. H. Mora Martins, LigianeAcosta, K. L. Vasconcellos, F. R. dos Santos, and R. Ca. Paca. 2016. A new species of Eumops ( Chiroptera : Molossidae ) from southeastern Brazil and Bolivia. Mammalian Biology 81:235–246. Guimaraes Beltrâo, M., and M. P. Aguiar Fracasso. 2011. Morcegos da RPPN Fazenda Almas, Sâo José do Cordeiros, Paraíba. Centro de Ciências Biològicas e da saúde:43. Guimarães, M. M., and R. L. Ferreira. 2014. Morcegos Cavernícolas Do Brasil: Novos Registros E Desafios Para Conservação. Revista Brasileira de Espeleologia 2:1–33. Jansen, D. C., L. F. Cavalcanti, and H. S. Lamblém. 2012. Mapa de potencialidade de ocorrência de cavernas no Brasil, na escala 1:2.500.000. Revista Brasileira de Espeleologia 2:42–57. Jansen, D. C., and K. Pereira. 2014. Distribuição e caracterização das cavernas brasileiras segundo a base de dados do CECAV. Revista Brasileira de Espeleologia 2:47–70. Jung, K., E. K. V Kalko, and O. Von Helversen. 2007. Echolocation calls in Central American emballonurid bats: Signal design and call frequency alternation. Journal of Zoology 272:125– 137. Kalko, E. K. V. 1998. Organization and diversity of Tropical bat communities through space and time. Zoology 101:281–297. Kalko, E. K. V., Charles O. Handley Jr., and D. Handley. 1996. Organization, diversity, and Long- Term Dynamics of a Neotropical Bat Community. Pages 503–553 in M. L. Cody and Jeffrey A. 32
Smallwood, editors. Long-Term Studies of Vertebrate Communities. Academic Press, San Diego. Klingbeil, B. T., and M. R. Willig. 2009. Guild-specific responses of bats to landscape composition and configuration in fragmented Amazonian rainforest. Journal of Animal Ecology 43:203–213. Koleff, P., and K. J. Gaston. 2002. The relationships between local and regional species richness and spatial turnover. Global Ecology and Biogeography 11:363–375. Koleff, P., J. Soberón, H. T. Arita, P. Dávila, Ó. Flores-Villela, J. Golubov, G. Halffter, A. Lira- Noriega, C. E. Moreno, E. Moreno, M. Munguía, M. Munguía, A. G. Navarro-Siguenza, O. Téllez, L. Ochoa-Ochoa, A. T. Peterson, and P. Rodríguez. 2008. Patrones de diversidad espacial en grupos selectos de especies. Pages 323–364 Capital natural de México, vol 1: Conocimiento actual de la biodiversidad. CONABIO, México. Kunz, T. H. 1982. Roosting Ecology of Bats. Pages 1–58 in T. H. Kunz, editor. Ecology of Bats. Plenum Publishing Corporation, New York. Kunz, T. H., and M. B. Fenton. 2003. Ecology of Bats. Page (T. H. Kunz and M. B. Fenton, Eds.). University of Chicago Press, Chicago. Kunz, T. H., and A. Kurta. 1988. Capture Methods and Holding Devices. Pages 1–30 in T. H. Kunz, editor. Ecological and behavioral methods for the study of bats. Smithsonian Institution Press, Washington D.C. Kunz, T. H., and L. F. Lumsden. 2003. Ecology of Cavity and Foliage Roosting Bats. Pages 3–89 in T. H. Kunz and M. B. Fenton, editors. Bat Ecology. University of Chicago Press, Chicago. Kunz, T. H., S. W. Murray, and N. W. Fuller. 2012. Bats. Pages 45–54 in W. B. White and D. C. Culver, editors. Enciclopedia of caves. Elsevier Academic Press. Kunz, T. H., and E. D. Pierson. 1994. Bats of the World: An Introduction. Pages 1–46 in R. M. Nowak, editor. Walker’s Bats of the World. John Hopkins University Press. Leal, E. S. B., D. D. F. Ramalho, B. G. Miller, P. D. B. P. Filho, J. G. D. P. Neto, F. V. P. V. Nova, R. M. De Lyra-Neves, G. J. B. De Moura, and W. R. Telino-Junior. 2012. Primeiro registro da família Natalidae (Mammalia : Chiroptera) para a Caatinga do Estado da Paraíba , Nordeste do Brasil. Revista Brasileira de Zoociencias 14:243–253. Leal, I. R., M. Tabarelli, and J. M. C. da Silva. 2003. Ecologia e Conservação da Caatinga. Page Ecologia e Conservação da Caatinga. Universida. Universidade Federal de Pernambuco, Recife. Lima, S. M. Q., T. P. A. Ramos, M. J. da Silva, and R. S. Rosa. 2017. Diversity , Distribution , and Conservation of the Caatinga Fishes : Advances and Challenges. Pages 97–131 in J. M. C. da Silva, I. R. Leal, and M. Tabarelli, editors. Caatinga: The Largest Tropical Dry Forest Region in South America. Springer International Publisher, Cham, Switzerland. López-González, C., S. J. Presley, A. Lozano, R. D. Stevens, and C. L. Higgins. 2014. Ecological 33
biogeography of Mexican bats: The relative contributions of habitat heterogeneity, beta diversity, and environmental gradients to species richness and composition patterns. Ecography 37:1–12. Luo, J., T. Jiang, G. Lu, L. Wang, J. Wang, and J. Feng. 2013. Bat conservation in China: Should protection of subterranean habitats be a priority? Oryx 47:526–531. MacArthur, R. H. 1965. Patterns of species diversity. Biological Reviews 40:510–533. MacSwiney G, M. C., F. M. Clarke, P. A. Racey, M. C. MacSwiney, F. M. Clarke, and P. A. Racey. 2008. What you see is not what you get: The role of ultrasonic detectors in increasing inventory completeness in Neotropical bat assemblages. Journal of Applied Ecology 45:1364–1371. MacSwiney, M. C., F. M. Clarke, and P. A. Racey. 2008. What you see is not what you get: The role of ultrasonic detectors in increasing inventory completeness in Neotropical bat assemblages. Journal of Applied Ecology 45:1364–1371. Magurran, A. E. 2004. Measuring Biological Diversity. Blackwell Publishing company, Victoria. Marengo, J. A., L. M. Alves, R. C. S. Alvala, A. P. Cunha, S. Brito, and O. L. L. Moraes. 2018. Climatic characteristics of the 2010-2016 drought in the semiarid Northeast Brazil region. Anais da Academia Brasileira de Ciências 90:1973–1985. Mares, M. A., M. R. Willig, and T. E. Lacher. 1985. The Brazilian Caatinga in South American Zoogeography: Tropical Mammals in a Dry Region. Journal of Biogeography 12:57–69. Mares, M. A., M. R. Willig, K. E. Streilein, and T. E. Lacher. 1981. The mammals of northeastern Brazil: a preliminary assessment. Annals of the Carnegie Museum of Natural History 50:81–137. Mares, M. A., and D. E. Wilson. 1971. Bat Reproduction during the Costa Rican Dry Season. BioScience 21:471–477. Mcnab, B. K. 1971. The Structure of Tropical Bat Faunas. Ecology 52:352–358. Medellín, R. A., M. Equihua, and M. A. Amin. 2000. Bat Diversity and Abundance as Indicators of Disturbance in Neotropical Rainforests\rDiversidad y Abundancia de Murciélagos como Indicadores de Perturbaciones en Selvas Húmedas Neotropicales. Conservation Biology 14:1666–1675. Medellin, R. A., R. Wiederholt, and L. Lopez-Hoffman. 2017. Conservation relevance of bat caves for biodiversity and ecosystem services. Biological Conservation 211:45–50. Melo, F. P. L. 2017. The Socio-Ecology of the Caatinga: Understanding How Natural Resource Use Shapes an Ecosystem. Pages 369–382 in J. M. C. da Silva, I. R. Leal, and M. Tabarelli, editors. Caatinga: The Largest Tropical Dry Forest Region in South America. Springer International Publisher, Cham, Switzerland. Mooney, H. A., S. H. Bullock, and E. Medina. 1995. Introduction. Pages 67–88 Seasonally Dry Tropical Forests. Cambridge University Press, Cambridge. Moratelli, R., and D. Dias. 2015. A new species of nectar-feeding bat, genus Lonchophylla, from the 34
Caatinga of Brazil (Chiroptera, Phyllostomidae). ZooKeys 2015:73–91. Moreno, C. E., and G. Halffter. 2000. Assessing the completeness of bat biodiversity inventories using species accumulation curves. Journal of Applied Ecology 37:149–158. Moreno, C. E., and G. Halffter. 2001. Spatial and temporal analysis of alpha, beta and gamma diversities of bats in a fragmented landscape. Biodiversity and Conservation 10:367–382. Morin, P. J. 2009. Community Ecology. Page (J. W. & Sons, Ed.). Blackwell Science, Inc., Massachusetts. Niu, H., N. Wang, L. Zhao, and J. Liu. 2007. Distribution and underground habitats of cave-dwelling bats in China. Animal Conservation 10:470–477. Nogueira, M. R., I. P. de Lima, R. Moratelli, V. da C. Tavares, R. Gregorin, and A. L. Peracchi. 2014. Checklist of Brazilian bats, with comments on original records. Check List 10:808–821. Nogueira, M. R., A. Pol, L. M. Pessôa, J. A. de Oliveira, and A. L. Peracchi. 2015. Small mammals (Chiroptera, Didelphimorphia, and Rodentia) from Jaíba, middle Rio São Francisco, northern Minas Gerais State, Brazil. Biota Neotropica 15:1–18. Norberg, U., and J. M. V. Rayner. 1987. Ecological Morphology and Flight in Bats ( Mammalia ; Chiroptera ): Wing Adaptations , Flight Performance , Foraging Strategy and Echolocation. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 316:335–427. Novaes, R. L. M., and R. D. S. Laurindo. 2014. Morcegos da Chapada do Araripe, Nordeste do Brasil. Papeis Avulsos de Zoologia 54:315–328. Novaes, R. L. M., R. D. S. Laurindo, and R. D. F. Souza. 2015. Structure and natural history of an assemblage of bats from a xerophytic area in the Caatinga of northeastern Brazil. Studies on Neotropical Fauna and Environment 50:40–51. Núñez-Novas, M. S., Y. M. León, J. Mateo, and L. M. Dávalos. 2016. Records of the Cave-Dwelling Bats (Mammalia: Chiroptera) of Hispaniola with an Examination of Seasonal Variation in Diversity. Acta Chiropterologica 18:269–278. Oliveira, H. F. M. de, M. Oprea, and R. I. Dias. 2018. Distributional patterns and ecological determinants of bat occurrence inside caves: A broad scale meta-analysis. Diversity 10. Otálora-Ardila, A., J. M. Torres, E. Barbier, N. T. Pimentel, E. S. B. Leal, and E. Bernard. 2019. Thermally-assisted monitoring of bat abundance in an exceptional cave in Brazil ’ s Caatinga drylands. Acta Chiropterologica 21:411–423. Paglia, A. P., G. A. B. Fonseca, A. B. Rylands, G. Herrmann, L. M. S. Aguiar, A. G. Chiarello, Y. L. R. Leite, L. P. Costa, S. Siciliano, S. L. M. Kierulff, V. C. Tavares, R. A. Mittermeier, and J. L. Patton. 2012. Lista Anotada dos Mamíferos do Brasil / Annotated Checklist of Brazilian Mammals. 2a Edição / 2nd Edition. Occasional Papers in Conservation Biology. 35
Patterson, B., M. R. Willig, and R. D. Stevens. 2003. Trophic Strategies, Niche Partitioning and Patterns of Ecological Organization. Pages 536–579 in T. H. Kunz and M. B. Fenton, editors. Bat Ecology. University of Chicago Press. Peet, R. 1974. The Measurement of Species Diversity. Annual Review of Ecology and Systematics 5:285–307. Pereira de Araujo, H. F., and J. M. C. da Silva. 2017. The Avifauna of the Caatinga : Biogeography , Ecology , and Conservation. Pages 181–210 in J. M. C. da Silva, I. R. Leal, and M. Tabarelli, editors. Caatinga: The Largest Tropical Dry Forest Region in South America. Springer International Publisher, Cham, Switzerland. Pérez-Torres, J., D. Martínez-Medina, M. Peñuela-Salgado, M. C. Ríos-Blanco, S. Estrada-Villegas, and L. Martínez-Luque. 2015. Macaregua: The cave with the highest bat richness in Colombia. Check List 11. Phelps, K., R. Jose, M. Labonite, and T. Kingston. 2016. Correlates of cave-roosting bat diversity as an effective tool to identify priority caves. Biological Conservation 201:201–209. Pinto, N., and T. H. Keitt. 2008. Scale-dependent responses to forest cover displayed by frugivore bats. Oikos 117:1725–1731. Prado, D. E. 2003. As caatingas da América do Sul. Pages 3–74 in I. R. Leal, M. Tabarelli, and J. M. C. da Silva, editors. Ecologia e Conservação da Caatinga. Universida. Universidade Federal de Pernambuco, Recife. Racey, P. A. 1982. Ecology of Bat Reproduction. Pages 52–104 in T. H. Kunz, editor. Ecology of Bats. Plenum Publishing Corporation. Racey, P. A., and A. C. Entwistle. 2000. Life-history and Reproductive strategies of Bats. Page (E. G. Crichton and Phillip H. Krutzsch, Eds.) Reproductive Biology of Bats. Academic Press. Reis, N. R. dos, A. L. Peracchi, W. A. Pedro, and I. P. de Lima. 2007. Morcegos do Brasil. Page Morcegos do Brasil. Universidade Estadual de Londrina, Londrina. Rocha, A. D., and M. E. Bichuette. 2016. Influence of abiotic variables on the bat fauna of a granitic cave and its surroundings in the state of São Paulo, Brazil. Biota Neotropica 16:1–8. Rocha, P. A., M. V. Brandaõ, G. S. T. Garbino, I. N. Cunha, and C. C. Aires. 2016. First record of Salvin’s big-eyed bat Chiroderma salvini Dobson, 1878 for Brazil. Mammalia 80:573–578. Rocha, P. A., J. Ruiz-esparza, and S. F. Ferrari. 2018. Differences in the structure of the bat community between a cloud forest refuge and a surrounding semi-arid Caatinga scrubland in the northeastern Brazil. Journal of Arid Environments 151:41–48. Rodrigues, M. T. 2003. Herpetofauna da caatinga. Pages 181–236 in I. R. Leal, M. Tabarelli, and J. M. C. da Silva, editors. Ecologia e Conservação da Caatinga. Universidade Federal de Pernambuco, Recife. 36
Rodríguez-Durán, A., and J. A. Soto-Centeno. 2003. Temperature selection by tropical bats roosting in caves. Journal of Thermal Biology 28:465–468. Rodríguez, P., and H. T. Arita. 2004. Beta diversity and latitude in North American mammals : testing the hypothesis of covariation. Ecography 27:547–556. Sá-Neto, R. J., and J. Marinho-Filho. 2013. Bats in fragments of xeric woodland caatinga in Brazilian semiarid. Journal of Arid Environments 90:88–94. Santos, A. J., T. B. Vieira, and K. D. C. Faria. 2016. Effects of vegetation structure on the diversity of bats in remnants of Brazilian Cerrado savanna. Basic and Applied Ecology 17:720–730. Sbragia, I. A., and A. Cardoso. 2008. Quirópterofauna (Mammalia: Chiroptera) cavernícola da Chapada Diamantina, Bahia, Brasil. Chiroptera Neotropical 14:360–365. Schnitzler, H.-U., and E. K. V. Kalko. 2001. Echolocation by Insect-Eating Bats. BioScience 51:557– 569. Shmida, A., and M. V. Wilson. 1985. Biological Determinants of Species Diversity. Journal of Biogeography 12:1–20. Silva, C. R., and E. Bernard. 2017. Bioacoustics as an Important Complementary Tool in Bat Inventories in the Caatinga Drylands of Brazil. Acta Chiropterologica 19:409–418. Silva, J. M. C. da, and L. C. F. Barbosa. 2017. Impact of Human Activities on the Caatinga. Pages 359–368 in J. M. C. da Silva, I. R. Leal, and M. Tabarelli, editors. Caatinga: The Largest Tropical Dry Forest Region in South America. Springer International Publisher, Cham, Switzerland. Silva, J. M. C. da, I. R. Leal, and M. Tabarelli. 2017. Caatinga: The Largest Tropical Dry Forest Region in South America. Springer International Publisher, Cham, Switzerland. Silva, L. A. M. da. 2007. Comunidades de morcego na Caatinga e Brejo de Altitude, no agreste de Pernambuco. Universidade de Brasília, Brasilia. Silva, S. S. P. da, D. Dias, M. A. Martins, P. G. Guedes, J. G. de Almeida, A. P. da Cruz, N. M. Serra- Freire, J. dos S. Damascena, and A. L. Peracchi. 2015. Bats (Mammalia: Chiroptera) from the Caatinga scrublands of the Crateus region, northeastern Brazil, with new records for the state of Ceará. Mastozoologia Neotropical 22. Silva, S. S. P. da, and P. G. Guedes. 2001. Levantamento preliminar dos morcegos do Parque Nacional Ubajara (Mammalia, Chiroptera), Ceará, Brasil. Revista Brasileira de Zoologia 18:139–144. Silva, U. B. T. da, M. Delgado-Jaramillo, L. M. de Souza Aguiar, and E. Bernard. 2018. Species richness, geographic distribution, pressures, and threats to bats in the Caatinga drylands of Brazil. Biological Conservation 221:312–322. Simmons, N. B., and R. S. Voss. 1998. The mammals of Paracou, French Guiana: a neotropical lowland rainforest fauna Part 1. Bats. Bulletin of the American Museum of Natural History 37
237:399–404. Soares, F. A. M., P. A. da Rocha, A. Bocchiglieri, and S. F. Ferrari. 2018. Structure of a bat community in the xerophytic Caatinga of the state of Sergipe , Northeastern Brazil. Mammalia 83:125–133. Solari, S., and V. Martínez-Arias. 2014. Cambios recientes en la sistemática y taxonomía de murciélagos Neotropicales (Mammalia: Chiroptera). Therya 5:167–196. Sperr, E. B., L. A. Caballero-Martínez, R. A. Medellín, and M. Tschapka. 2011. Seasonal changes in species composition, resource use and reproductive patterns within a guild of nectar-feeding bats in a west Mexican dry forest. Journal of Tropical Ecology 27:133–145. Stevens, R. D., S. B. Cox, R. E. Strauss, and M. R. Willig. 2003. Patterns of functional diversity across an extensive environmental gradient : vertebrate consumers , hidden treatments and latitudinal trends. Ecology Letters 6:1099–1108. Stevens, R. D., and M. R. Willig. 2002. Geographical ecology at the community level: Perspectives on the diversity of new world bats. Ecology 83:545–560. Stevens, R. D., M. R. Willig, and R. E. Strauss. 2006. Latitudinal Gradients in the Phenetic Diversity of New World Bat Communities in the phenetic of New World bat Latitudinal gradients diversity communities. Oikos 112:41–50. Stoner, K. E. 2001. Differential habitat use and reproductive patterns of frugivorous bats in tropical dry forest of northwestern Costa Rica. Canadian Journal of Zoology 79:1626–1633. Stoner, K. E., K. A. O.-Salazar, R. C. R.-Fernández, and M. Quesada. 2003. Population dynamics, reproduction, and diet of the lesser long-nosed bat (Leptonycteris curasoae) in Jalisco , Mexico : Implications for conservation. Biodiversity and Conservation 12:357–373. Stoner, K. E., and R. M. Timm. 2004. Tropical Dry Forest mammals of Palo Verde. Pages 48–66 in G. W. Frankie, A. Mata, and S. B. Vinson, editors. Biodiversity conservation in Costa Rica: Learning the lessons in the seasonal dry forest2. University of California Press, Berkeley. Stoner, K. E., and R. M. Timm. 2011. Seasonally Dry Tropical Forest Mammals : Adaptations and Seasonal Patterns. Pages 85–106 in R. Dirzo, H. S. Young, H. A. Mooney, and G. Ceballos, editors. Seasonally Dry Tropical Forests: Ecology and Conservation. Island Press, Washington. Stroud, J. T., M. R. Bush, M. C. Ladd, R. J. Nowicki, A. A. Shantz, and J. Sweatman. 2015. Is a community still a community ? Reviewing definitions of key terms in community ecology:4757– 4765. Taddei, V., and B. Lim. 2010. A new species of Chiroderma (Chiroptera, Phyllostomidae) from Northeastern Brazil. Brazilian Journal of Biology 70:381–386. Torquetti, C. G., M. X. Silva, and S. Talamoni. 2017. Differences between caves with and without bats in a Brazilian karst habitat. Zoologia 34:1–7. 38
Trajano, E. 1985. Ecologia de populações de morcegos cavernícolas em uma região cárstica do sudeste do Brasil. Revista Brasileira de Zoologia 2:255–320. Trajano, E. 1995. Protecting Caves for the Bats or Bats for the Caves. Chiroptera Neotropical 1:19–21. Trajano, E., and E. A. Gimenez. 1998. Bat Community in a Cave From Eastern Brazil , Including a New Record of Lionycteris (Phyllostomidae, Glossophaginae). Studies on Neotropical Fauna and Environment 33:69–75. Tuttle, M. D., and A. Moreno. 2005. Cave-dwelling Bats of Northern Mexico: Their value and conser vation needs. Page Reading. Vargas-Mena, J. C., K. Alves-Pereira, M. A. S. Barros, E. Barbier, E. Cordero-Schmidt, S. M. Q. Lima, B. Rodríguez-Herrera, and E. M. Venticinque. 2018a. The bats of Rio Grande do Norte state, northeastern Brazil. Biota Neotropica 18:e20170417. Vargas-Mena, J. C., E. Cordero-schmidt, B. Rodriguez-herrera, R. A. Medellín, D. D. M. Bento, and E. M. Venticinque. 2020. Inside or out ? Cave size and landscape effects on cave-roosting bat assemblages in Brazilian Caatinga caves. Journal of Mammalogy:1–12. Vargas-Mena, J. C., E. C. Schmidt, D. D. M. Bento, B. Rodriguez Herrera, R. A. Medellín, and E. M. Venticinque. 2018b. Diversity of cave bats in the Brazilian tropical dry forest of Rio Grande do Norte state. Mastozoologia Neotropical 18:199–212. Varzinczak, L. H., C. S. Lima, M. O. Moura, and F. C. Passos. 2017. Relative influence of spatial over environmental and historical processes on the taxonomic and phylogenetic beta diversity of Neotropical phyllostomid bat assemblages. Journal of Biogeography 45:617–627. Velloso, A. L., E. V. S. B. Sampaio, and F. G. C. Pareyn. 2001. Ecoregiões propostas para o bioma Caatinga. Associação. Associação Plantaaas do Nordeste; The Nature Conservancy do Brasil, Recife. Voigt, C. C., and T. Kingston. 2016. Bats in the anthropocene: Conservation of bats in a changing world. Springe International Publishing, New York. Whittaker, R. H. 1972. Evolution and Measurement of Species Diversity. Taxon 21:213–251. Whittaker, R. H. 1975. Community Structure and Composition. Page 61 in R. H. Whittaker, editor. Communities and ecosystems. MacMillan Publishing Co. Inc., New York. Willig, M. R. 1983. Composition microgeographic variation and sexual dimorphism in Caatingas and Cerrado bat communities from northeastern Brazil. Bulletin of Carnegie Museum of Natural History 23:1–132. Willig, M. R. 1985a. Reproductive activity of female bats northeast Brazil. Bat Research News 26:17– 20. Willig, M. R. 1985b. Reproductive Patterns of Bats from Caatingas and Cerrado Biomes in Northeast Brazil. Journal of Mammalogy 66:668–681. 39
Willig, M. R., and M. A. Mares. 1989. Mammals from the Caatinga: an updated list and summary of recent research. Willig, M. R., and M. P. Moulton. 1989. The Role of Stochastic and Deterministic Processes in Structuring Neotropical Bat Communities. Journal of Mammalogy 70:323–329. Willig, M. R., S. J. Presley, J. Plante, C. P. Bloch, S. Solari, V. Pacheco, and S. C. Weaver. 2019. Guild-level responses fo bats to habitat conversion in a lowland Amazonian rainforest: species composition and biodiversity. Journal of Mammalogy 100:223–238. Zanella, F. C., and C. F. Martins. 2003. Abelhas da Caatinga: Biogeografia, ecologia e conservação. Pages 75–134 in I. R. Leal, M. Tabarelli, and J. M. C. Da Silva, editors. Ecologia e Conservação da Caatinga. Universidade Federal de Pernambuco.
Figure C. The Vieirai's flower bat (Xeronycteris veirai) stretching its tongue inside a cave roost in Lajes, Rio Grande do Norte, Brazil. The species belong to the Leaf-nosed bats, family Phyllostomidae and subfamily Lonchophyllinae. It is endemic to Brazil and has a nectarivorous diet. Photo taken by Juan Carlos Vargas-Mena in 2019.
40
41
Chapter 1
Alpha and Beta diversity of bat assemblages in the heterogeneous Caatinga dry forests in northeastern Brazil
Juan Carlos Vargas Mena 1, Eugenia Cordero-Schmidt1, Bernal Rodríguez- Herrera2, and Eduardo Martins Venticinque1
1 Departamento de Ecologia, Universidade Federal do Rio Grande do Norte, 59078900 Lagoa Nova Natal, RN, Brasil. 2 Escuela de Biología, Universidad de Costa Rica, 2060 Montes de Oca, San José, Costa Rica.
42
ABSTRACT The Caatinga dry forest is solely located in the semiarid region of northeastern Brazil, present many extreme environmental and meteorological parameters, and a very diverse and heterogeneous deciduous phytofisiognomies. Patterns of spatial and temporal diversity of Caatinga`s bat fauna are poorly unknown, and this is the case of the state of Rio Grande do Norte (RN) where 95% of its territory is covered by this endemic dry forest. Factors that controls the structure and dynamics of
Caatinga`s bat assemblages are attribute to spatial heterogeneity of the different phytofisiognomies and to seasonality of rain and pulses of food resource. Thus, we explored the spatial and temporal patterns of richness and species composition of bat assemblages using mist-net captures in five different habitats in six areas throughout RN. In 100 sampling nights, I captured 1575 individuals of
31 species with a net capture effort of 242425 hm2. A difference in the structure of the assemblages at the species- and ensemble-level (trophic guilds) between the different studied areas was found and likely attributed to differences in topography, vegetation composition and landscape context on which each studied region is located. As well differences in the assemblage’s structure between habitats was found and habitats relatively more different in vegetation and structural composition had bat assemblages more different. The riparian and shrubby Caatingas presented the highest bat richness and abundance, however some species seemed to be more abundant or solely occur in specific habitats.
This is likely related to species-specific ecological traits or adaptations that allow them to better exploit resources (e.g. food, roost) that are more likely found in a particular habitat. Moreover, no evident seasonal variation in the richness and species composition where found between seasons.
Despite the seasonal phenology of food resources for bats in the rainy season, some resources are found intermittently but throughout the year and this may be a key factor that allows the bat assemblage not to change structurally throughout the years. Overall, the results of this study evidence that the structure of the studied bat assemblages are more strongly affected by spatial factors
(landscape, topography, vegetation composition) than to temporal factors (seasonal biotic and abiotic), at least in these areas of the Caatinga. Despite the great advance in the knowledge of the diversity,
43 distribution and ecology of bats in this region of the Brazilian Caatinga, more studies are needed in order to better unravel the diverse bat fauna of this endemic dry forest.
Key words: abundance, alpha diversity, beta diversity, Chiroptera, species composition, richness
INTRODUCTION The Caatinga is largest and most diverse seasonally dry tropical forest (SDTF) of the New
World (Silva et al. 2017). Located in the semiarid region of northeastern Brazil, the Caatinga dry forest present many extreme environmental and meteorological parameters: high annual temperature and solar radiation, low rates of relative humidity and irregular and extended droughts (Prado 2003).
This high variation in the abiotic factors leads to a seasonal fluctuation in the availability of food and water resources throughout the year, hence exerting strong pressures on the bat fauna inhabiting the
Caatinga. Mammals in the Caatinga, including bats, seem to exhibit behavioral responses to compensate for these limiting factors instead of pronounced physiological adaptations like in other mammals in semiarid regions (Streilein 1982).
In general, behavioral adaptation of mammals in SDTF includes seasonality in reproduction, dietary flexibility, long- and short-distance migration, local movements, and seasonal changes in forging areas (Stoner and Timm 2011). This behaviors are plausible to expect from the bat fauna of the
Caatinga, but still basic data on the natural history, ecology and distribution of bat are scarce in this
Brazilian dry forest, although increasing in the last decades (Carmignotto and Astúa 2017).
Initial assumptions stated the mammalian assemblage in the Caatinga where a sub-set of neighboring Cerrado savannas, with low degree of endemism and relatively poor in species richness
(Mares et al. 1981; Streilin 1982 Willig 1986; Willig and Mares 1989). However, despite being the least studied mammal fauna of the major Brazilian ecological regions (Oliveira et al. 2003), notable progress has been made in expanding the knowledge of Caatinga’s mammals. Its diversity has increased from 80 (Willig and Mares 1989) to 183 species (Carmignotto and Astúa 2017). In fact, bats
44 comprehend almost the half of all Caatinga mammals where 96 species have been recorded
(Carmignotto and Astúa 2017, Silva et al. 2018), where two species are endemic –Lonchophylla inexpectata and Chiroderma vizottoi (Gutiérrez and Marinho-Filho 2017).
The Caatinga is characterized to be very heterogenous where about thirteen different phytofisiognomies (Andrade-Lima 1981) distributed into six main vegetational units (Prado 2003) across eight different ecoregions have been described within (Velloso et al. 2001). Different studies have attributed such spatial factors to have strong effects on the structure of the bat assemblages in the
Caatinga, leading to differences in the richness, species composition and distribution of bats depending on the type of phytofisiognomies and/or ecoregions throughout this dry forest (Willig 1983,
Gregorin et al. 2008, Sá-Neto and Marinho-Filho 2013, Carvalho-Neto et al. 2016, Silva et al. 2018).
Temporal factors regarding the seasonality of rain and pulses of food resources have been attributed as well to affect the structure of bat assemblages in the Caatinga (Novaes et al. 2015, Silva et al. 2015, Rocha et al. 2018, Soares et al. 2018a). Like in any SDTF, plants in the Caatinga have a seasonal phenology where leaves and most of flowers and fruits are produced during a short rainy season, while in the dry season most of plants are deciduous although some can still produce flowers and fruits (Machado et al. 1997, Griz and Machado 2001, Amorim et al. 2009, Quirino and Machado
2014, Rocha et al. 2020). Such temporal dynamic leads to a seasonal fluctuation of food availability for bat populations in the Caatinga, hence potentially affecting the structure of this bat assemblages through time.
Notwithstanding, the species distribution and ecological characterization and dynamics of bat assemblages in the Caatinga dry forest are poor and only 10% of its territory have been properly sampled (Bernard et al. 2011). Consequently, states like Rio Grande do Norte (RN) has been pointed out as a conspicuous gap of information regarding bats, considering that almost 95% of this state correspond to this dry forest. However, a recent revision of bibliography and museum collections recorded 32 species of bats occurring in the Caatinga of RN, that is the 72 % of all the bats recorded in the state (42 spp.) (Vargas-Mena et al. 2018a). This and other novel studies in the last years have
45 helped to fill the states’ information gap with data on new species records (Feijó and Nunes 2010,
Basílio et al. 2017), natural history (Carvalho et al. 2016, Cordero-Schmidt et al. 2016, 2017), community ecology and species diversity (Barros et al. 2017, Soares et al. 2018b, Vargas-Mena et al.
2018b, 2020). Despite recent efforts, patterns of diversity ad structure of bat assemblages through space and time in different regions and phytofisiognomies are yet lacking in RN.
Thus, we aimed to examine the structural patterns and dynamics across space (areas and potential foraging habitats) and time (dry and rainy seasons) of bat assemblages regarding the richness, abundance, species and ensemble (trophic guilds) composition in seven different phytofisiognomies in six different areas of Caatinga in the state of RN. Since the wide variety of phytophysiognomies and ecoregions in Caatinga that seems to be a key factor controlling the species composition of bat assemblages (Willig 1983, Carvalho-Neto et al. 2016), we expect 1) differences in the structure at a species-, ensemble -, and assemblage-levels between the studied areas. Similarly, 2) we expect differences in the abovementioned levels in the structure between habitats
(phytophysiognomies), this considering as well on the premise that bat species have ecological specializations (e.g. wing morphology, types of echolocation) and life history traits (e.g. roost and diet preferences) to specific habitats despite their high mobility (flight) (Kunz 1982, Kunz and Pierson
1994, Kalko 1998, Denzinger and Schnitzler 2013, Norberg and Rayner 2016). Additionally , considering that the seasonal pattern of resource availability in the Caatinga seems to be another key factor controlling the diversity and species composition of bats (Willig 1983), we expect 3) a higher species richness and abundance during the rainy season and changes in the species composition, particularly on phytophagous bats (frugivorous and nectarivorous) where we expect disappearance of species during the dry season attributed to the lower availability of their preferred food resource in the rainy season, such as nectar, flowers, fruits (Griz and Machado 2001, Chesson et al. 2004, Machado and Lopes 2004).
The understating of the spatial and temporal patterns of these bat assemblages will hopefully provide data to determine more accurate protection actions of local bat populations and their foraging
46 habitats of Caatinga. Such data is needed considering the increase of unplanned commercial agriculture, livestock and native lumber extraction, among others, which have resulted in a fast and large land-use change where at least 63% of the Caatinga has been modified (Silva et al. 2017).
Habitat loss has been pointed out as one of the main threats to bat populations worldwide (Voigt and
Kingston 2016), thus the identification and protection of their foraging areas is critical as well in order to perpetuate the ecological services on which bats are involve such as seed dispersion, plant pollination, and vertebrate and invertebrate population control (Kunz et al. 2011).
METHODOLOGY Study area
This study was conducted in the Caatinga dry forest of Rio Grande do Norte State (RN) in northeastern Brazil (Fig. 1.1). Ninety-five percentage of the state corresponds to Caatinga (IDEMA
2018) which is characterized by a semiarid climate (Diniz and Pereira 2015). According to Köppen classification, the climate is BShw (hot and dry) (Alvares et al. 2013). The rainy season is short but varies regionally and can go from January to June with an average annual precipitation of 400−1100 mm, while the dry season is from June or July to December (can extends up to 8-9 months) and with a mean annual rainfall of less than 800 mm (Diniz and Pereira 2015). Physiognomy and plant composition variations determine eight different ecoregions in the Caatinga; however, only two occur in RN: the Northern Sertanejan Depression (NSD) and the Borborema Highlands (BH) (for ecoregions descriptions see Velloso et al. 2001).
We surveyed six different areas separated from at least 55 km throughout the state (Fig 1.1). In total, we survey 22 points that ranged from two to five survey points in each area (Table 1.1) for 99 nights from February 2017 to June 2019. Each survey point was classified into an habitat type based on the main vegetation units and phytofisiognomies found in the Caatinga described by Mares et al.
(1981) and Prado (2003). The different habitats and surveyed nights are: shrubby Caatinga with 26 nights, riparian Caatinga with 42, Medium Caatinga forest with 10, rocky outcrops with 9, Copernicia groves with 5, humid forest enclave with 3, and gardens/orchards with 2 nights. habitats (see
47
Supplementary material 1.1) for habitat descriptions). Habitats were not evenly distributed among the six studied areas (See Table 1.1).
-
Figure 1.1. Map of the location A) of the six sites surveyed in this study, the location of Rio Grande do Norte in Brazil B) and in the Caatinga dry forest C).
Of the six areas, four are found in the NSD and two in the BH ecoregion. Description of each area follows below with regard their localization (main coordinate, altitude), topography, predominant habitats or phytofisiognomies, conservation status and number of survey points and nights.
Municipality of Assú. Açú National Forest (ANF). Federal protected area of 215.25 ha located in the central region, in the peri-urban area west of Assú city (S 5º34’20”, W 36º54’33”) within the
NSD. Altitude 18-100 m. ANF limits to the north with the Lagoa do Piató, a lake with an extension of
18 km. The topography is plain and smooth. The vegetation has 50 years of preservation and predominantly scrubby and secondary arboreal Caatinga, Copernicia palm groves are found at the margins of the Piató lake and gardens/orchard at the rangers/visitors’ facilities. These three habitats were surveyed in five different points during six nonconsecutive nights.
48
Municipality of Serra Negra do Norte. Seridó Ecological Station (SES). With 1123.61 ha, this federal conservation unit is located in the Sertanejan depression in the southwestern region of the state
(S 06º95’, W 37º39’) within the NSD. The relief is smooth and undulated with isolated "inselbergs" standing out in the middle of the flat areas, and altitude from 200 to 385 at the Serra Verde mountain.
Streams are intermittent and large water bodies relies in two semi-perennial lakes and one artificial dam near the main facilities. Vegetation is predominantly of savannah/scrubby and some riparian
Caatingas, medium Caatinga forest near foothills, and plants associated to granitic rock outcrops. Such habitats were surveyed in five different points during 10 nights
Municipalities of Mossoró and Baraúna. Furna Feia National Park (FFNP). A federal protected area of 8494 ha located in the western of the state (S 5º4’14.88”, W 37º32’1.51”) within the NSD. The park’s area is a watershed region between three different hydrographic basins. Altitude varies from 70 m to 280 m at the Serra Mossoró, the highest point of the park. Water bodies are scarce and streams, lagoons and underground rivers occur intermittently. The region is karstic and large calcareous outcrops are found with 206 underground cavities recorded within the park. The vegetation is shrubby
Caatinga and large fragments of medium Caatinga forests, of the last remnants of primary Caatinga in the state. Six nights were sampled in four surveyed points of medium Caatinga forest and one
Garden/Orchard in the buffer zone.
Municipality of Felipe Guerra. Felipe Guerra (FG). Situated in the western region of the state on the Apodí Plateau within the NSD (S 5º35’29”, W 37º41’8”). The relief is smooth and altitude varies from 30-100 m. From south to north the semi-perennial Apodí river divides the area and intermittent streams among small canyons between the outcrops can be found. Numerous and extensive calcareous rocky outcrops are found where 496 caves have been recorded, the largest in the state (Bento et al. 2015). The vegetation is shrubby/arboreal and riparian Caatingas and plant species associated to rocky outcrops are common. Extensive palm groves, mainly of the endemic Copernicia prunifera, are found at the margins of the Apodí and submitted to seasonal flooding. Due to the biological and speleological heritage of the area, it has been proposed as an environmental protection
49 area (APA da Pedra Abelha) but deforestation, hunting and uncontrolled mining and livestock expansion are its main threats (Bento et al. 2015). Copernicia groves, rocky outcrops and riparian
Caatingas were surveyed in four points during 14 nights.
Municipality of Martins. Martins. Located in a mountainous region of Midwest RN (S
6º05’06”, W 37º54’39”) that are considered part of the BH ecoregion despite being isolated and surrounded by lowlands of the NSD. Its topography is constituted by rocky and mountainous terrains with plateaus and altitude varies from 400-800 m. The vegetation on these plateaus is a montane semideciduous forests stands, known as humid forest enclaves, which are sustained by orographic rainfall greater than 1200 mm / year, thus contrasting with the surrounding Caatinga vegetation at lower altitudes (Porto et al. 2004). Despite being core areas of significant importance for unique biota these areas suffer of habitat loss, unplanned agriculture, hunting, and lumber extraction and no humid forest enclave in RN are in any protected area. Two points were surveyed, one at the border of a fragment of Humid forest and in a foothill with a medium Caatinga forest during five nights.
Municipality of Lajes. Lajes. Located in the northernmost distribution of the BH ecoregion in central RN (S 5º42’00”, W 36º14’41”). Is a mountainous area, with a rugged relief, steep slopes and rocky outcrops of granite. Altitude varies from 300 to 600 m. Small rivers and streams are intermittent which depends on rainfall. Contains one of the states’ largest fragments of Caatinga which include arboreal Caatingas on foothills and herbaceous and shrubby Caatingas characterized by large clusters of different species of columnar and shrubby cacti, terrestrial bromeliads and Leguminosae trees
(Cacti forests). The area is not protected and suffers from logging, hunting and mineral exploitation, in addition of future installation of large wind farms. Three points were surveyed of riparian and shrubby
Caatingas during 58 nights. This larger effort in relation to the other areas was in order to address the seasonal structure of only this assemblage.
50
Table 1.1. Sampling area of bat captures in the six different areas of Caatinga dry forest from 2017-2019 in Rio Grande do Norte, northeastern Brazil. Altitude Locality Sampling Site Latitude Longitude Habitat (m.a.s.l.) Açú National Forest (ANF) 18-100 Sitio cables -5.576278 -36.954722 Shrubby Caatinga Sitio carnaubal -5.537781 -36.962528 Copernicia groves Sitio instalações -5.582440 -36.944691 Orchards and gardens Sitio medio -5.562993 -36.956627 Shrubby Caatinga
Seridó Ecological Station (SES) 200-385 Açude e trilha -6.580697 -37.255378 Riparian Caatinga Camninho Lagoa do Junco -6.599227 -37.249024 Medium Caatinga Forest Lajedo -6.575139 -37.267417 Rocky outcrop Pé da serra -6.565667 -37.264667 Medium Caatinga Forest Savana -6.573081 -37.25647 Shrubby Caatinga
Furna Feia National Park (FFNP) 70-280 Sitio Coqueiros (Buffer area) -5.022500 -37.447583 Orchards and gardens Sitio Atolados -5.045963 -37.510515 Medium Caatinga Forest Sitio 1 -5.038146 -37.559421 Medium Caatinga Forest Caminho Abrigo Letreiro -5.055785 -37.537123 Medium Caatinga Forest
Felipe Guerra 30-100 Sitio Passagem Funda -5.572606 -37.675224 Copernicia groves Lajedo do Rosario -5.561032 -37.663018 Rocky outcrop Lajedo do Urubu -5.572894 -37.652178 Rocky outcrop Sitio Barra -5.577348 -37.574361 Riparian Caatinga
Lajes 300-600 Açude Santa Rosa -5.831779 -36.202887 Riparian Caatinga Fazenda Santo Antonio -5.798484 -36.240754 Shrubby Caatinga Sitio Amarante -5.798667 -36.139528 Riparian Caatinga
Martins 300-700 Casa de pedra -6.07142 -37.885478 Medium Caatinga Forest Brejo -6.063889 -37.936472 Humid forest enclave
Bat Captures
In each surveyed point we deployed from 150-220 m of mist nets (7-14 x 2.5m) to capture bats
from dusk until midnight (17:30/18:00-24:00h) on trails, roads, near water bodies (with or without
water), and/or near potential food resources (e.g. Cacti or trees/bushes with flower or fruits),
depending on the habitat. Captured bats were identified using a combination of the identification key
of South American bats by Díaz et al. (2016). Doubtful identification of or new occurrences in the area
specimens were collected and deposited in the Prof. Adalberto Varela’s Mammal collection of the
51
Universidade do Rio Grande do Norte (UFRN). Collecting permits were issued by the Brazilian environmental agency (SISBIO license number 48325-2 MMA, IBAMA and ICMBIO). Bat capture and handle protocols followed the guidelines of the American Society of Mammalogists for the use of wild mammals in research by Sikes et al. (2016).
Because of bat high functional diversity, they occupy almost every trophic level, hence the classification of bats into different trophic guilds can give a better insight of the structure and species composition within and among the bat assemblages. Therefore, using the available natural history information about the primary diet of the bats in Brazil (Reis et al. 2007), the recorded species were classified into trophic guilds based on Hill & Smith (1984). However, we substituted the foliage- gleaning insectivorous and carnivorous guilds for gleaning animalivorous guild, given that bats belonging to these guilds can have both an insectivore and carnivore diet (e.g., subfamily
Phyllostominae) (Gardner 2007). Guilds were aerial insectivores, gleaning animalivores, piscivores, frugivores, nectarivores, omnivores, and sanguinivores.
Monthly precipitation from 2017-2019 of Lajes were taken from the online data base of the rainfall monitoring of Rio Grande do Norte by the Empresa de Pesquisa Agropecárias do Rio Grande do Norte (EMPARN). http://meteorologia.emparn.rn.gov.br:8181/monitoramento/monitoramento.php
Statistical analysis
The sampling effort of each area, habitat, and season (only Lajes), was calculated following
Straube and Bianconi (2002) which multiplies the total area of the mist-nets deployed with the number of hours that nets were open during each night. Due to differences in the sampling effort in each area and habitat, prior the analysis of the spatial and temporal beta diversity, the bat capture data was corrected by the capture effort as follows: [captures N / (mist netting hours * meters2) * 1000]. See
Supplementary Material 1.2 for capture effort per area and Supplementary Material 1.3 for capture effort per habitat.
To measure the sampling efficiency of each area, habitat and season (only Lajes), we used individual-based species accumulation curves using EstimateS Software 9.1.0. The sample order was
52 randomized 1000 times, to eliminate the influence of the order in which days were added to the total number of individuals. If computed curves approaches to an asymptote means that the effort has been sufficient to collect most of the species present in that area or season (Moreno and Halffter 2001).
Curves were also used to analyze and compare alpha diversity of each season, habitats and areas.
Then, a Bray-Curtis index of similarity was performed to generate a distance matrix in order to calculate and compare the beta spatial diversity, or ecological distance between the areas. Then a similarity percentage analysis (SIMPER) was performed to estimate the weight of each species in the assemblage dissimilarity between the areas. To analyze the beta diversity within each Caatinga habitats, we used data on species abundance (corrected by the effort) in each area to run a
Correspondence Analysis (CA). This analysis simultaneously provides an ordination for the habitats and an ordination for the species, as well provides a graphical presentation of the direction of the changes in the assemblage structure through each habitat where similar habitat are placed together along axes and of the relative importance of each species for the assemblage (Braak 1995). The closer two rows are to each other on the plot, the more similar their residuals, additionally, the closer the labels are to the origin (where the x- and y-axes are both at 0), the less distinct they probably are. The length of the lines connecting row/column label to the origin indicates the association between the habitats and one or more bat species (longer line indicates higher association). The angle formed between the two lines indicate association, where angles of 180 degrees indicate negative associations, angles <90 indicate higher association and a 90 degrees angle indicate no relationship.
Differences in the assemblage composition among the rainy and dry season in Lajes were tested using a Bray-Curtis index of dissimilarity to perform a distance matrix in order to calculate and compare the temporal beta diversity beta of each season for each year. A paired sampled t-test was done to determine if there were significant mean differences between the seasons and between each season within each sampled year. Data from the rainy season of 2019 was excluded of this analysis due to a low sampling effort in that season. All analyses where done using SYSTAT software version
12.
53
RESULTS
We captured a total of 1575 individuals of bats of 31 species of five families with a net capture effort of 242 425 hm2. Phyllostomidae was the richest family (20 spp.), followed by Molossidae (5),
Noctilionidae (2), Vespertilionidae (2), Mormoopidae (1), and Emballonuridae (1 species). The curve of the overall richness in this study did not presented an asymptote but with trending to stabilize after the capturing 300 individuals and suggesting that a little more effort is needed to register the most of the richness of the surveyed areas (Fig 1.2a). Of the 31 species, 29 species were identified to species level distributed in seven trophic guilds (ensembles) (Supplementary Material 1.4). The ten most abundant species corresponded to Artibeus planirostris (616 individuals) Glossophaga soricina (176),
Desmodus rotundus (153), Lonchophylla mordax (144), Lonchophylla inexpectata (83), Xeronycteris vieirai (72), Myotis lavali (50), Trachops cirrhosus (37), Tonatia bidens (34), Peropteryx macrotis
(30) which represented the 88.3% (1391) of the overall captures. The remaining 11.7%, (29 individuals), were distributed in 21 species.
Assemblage structure between areas
The species accumulation curves of Lajes, Felipe Guerra, and Martins presented a trend to stabilize suggesting an acceptable sampling effort for those areas, while in FFNP, SES and ANF, curves were steeped suggesting that a greater effort is needed and much more species might be recorded. Lajes presented the highest richness with 18 species followed by Felipe Guerra with 16,
Martins and SES with 11 each, FFNP with 10 and ANF with 9 species (Fig 1.2b). With the effort corrected (Table 1.2), the highest abundance was found in Felipe Guerra with 202.4 individuals, followed by Lajes with107.2, Martins with 103.2, ANF with 48.6, SES with 43.8, and 22.4 individuals per 1000 hm2 in FFNP.
The main differences were observed in the composition of species and trophic guilds between the areas. The abundance proportion of the shared most abundant species (A. planirostris, D. rotundus,
G. soricina and M. lavali) were different between the areas. In the SIMPER analysis these four species contributed the most in the dissimilarity of the assemblages (63% cumulative percentage)
54
(Supplementary Material 1.5). Artibeus planirostris was much more abundant in Martins and in Felipe
Guerra and contributed to the 41.12% percentage of the dissimilarity. Myotis lavali was much more abundant in SES (8.35% of dissimilarity), and Desmodus rotundus and G. soricina in Felipe Guerra
(7.63% and 6.30% respectively). As well some areas presented exclusive species like Lajes
(Micronycteris megalotis, L. inexpectata, X. vieirai, Molossus molossus, and Rhogeessa hussoni),
Martins (Phyllostomus hastatus, Anoura geoffroyi, Artibeus lituratus, Sturnira lilium); SES
(Molossops temminckii); and FFNP (Promops nasutus and Eumops sp.) (Table 1.2).
According to the Bray-Curtis similarity matrix, the areas that were less similar between each other in their assemblage structure corresponded to Lajes -SES (0.14), Lajes -MAR (0.19), FFNP-
MAR (0.20), FG-SES (0.25) while the areas more relatively similar were ANF-FG (0.51), FG-MAR
(0.51), however none of the areas had a very high similarity (> 0.60) between them and tended to have distinct structure in their assemblages (Table 1.3).
Regarding the trophic guilds (ensemble), differences were found between areas as well. In
Lajes the assemblage was dominated by nectarivorous bats (51%). In SES, insectivores (43%) dominated and presented the highest proportion of animalivorous bats (11%). In Martins, ANF, Felipe
Guerra, and FFNP, frugivore bats represented the largest proportion of their assemblages (>50%) but the two latter areas presented the highest proportions of sanguinivorous bats with 18% and 17% respectively. Omnivorous were more common in FFNP (12%) while piscivorous occurred only in two areas, Felipe Guerra and SES, but in low proportions (2%) (Fig. 1.3).
55
Figure 1.2. Individual-based species accumulation curves of a) richness (gamma diversity) of the six studied areas, lower and upper confidence intervals are found as dashed lines; b) alpha diversity in Lajes (LAJ); Felipe Guerra (FG); Martins (MAR); Furna Feia National Park (FFNP); Seridó Ecological Station (SES); and Açú National Forest (ANF; c) alpha diversity of seven Caatinga habitats; d) alpha diversity of each season (Dry and Rain) in Lajes, lower and upper confidence intervals are found as dashed lines, of the Caatinga dry forest, Rio Grande do Norte, Brazil, from 2017 to 2019. Curves randomized 1000 times and.
56
Table 1.2. Mean abundance of bat species captured in six areas during 2017-2019 in the Caatinga of Rio Grande do Norte State. Acronyms of trophic guilds are: (I) insectivorous, (A) animalivorous, (F) frugivorous, (S) Sanguinivorous, (O) omnivorous, (P) piscivorous and (N) nectarivorous; and for localities are: (ANF) Açú National Forest, (FFNP) Furna Feia National Park, (SES), Seridó Ecological Station, (FG) Felipe Guerra, (MAR) Martins, (LAJ) Lajes. Ocurr. (%) corresponds to the percentage of occurrence of each species in each locality.
Trophic Occurr. Family/Subfamily Species ANF SES FFNP FG MAR LAJ Total Guild (%) Emballonuridae Peropteryx macrotis I 13 17 30 2 (33.3) (1) Phyllostomidae
(20) Micronycterinae Micronycteris megalotis A 4 4 1 (16.6) Micronycteris sanborni A 9 2 11 2 (33.3) Micronycteris A 1 1 4 6 3 (50) schmidtorum Desmodontinae Desmodus rotundus S 1 1 7 50 5 89 153 6 (100) Diphylla ecaudata S 1 9 19 29 3 (50) Phyllostominae Phyllostomus discolor O 5 7 8 20 3 (50) Phyllostomus hastatus O 2 2 1 (16.6) Tonatia bidens A 1 3 30 34 3 (50) Trachops cirrhosus A 2 1 7 27 37 4 (66.6) Glossophaginae Anoura geoffroyi N 5 5 1 (16.6) Glossophaga soricina N 12 3 29 10 118 172 5 (83.3) Lonchophylla Lonchophyllinae N 83 83 1 (16.6) inexpectata Lonchophylla mordax N 1 7 18 1 117 144 4 (66.6) Lonchophylla sp N 1 3 4 2 (33.3) Xeronycteris vieirai N 72 72 1 (16.6) Carolliinae Carollia perspicillata F 1 16 17 2 (33.3) Stenodermatinae Artibeus lituratus F 6 6 1 (16.6) Artibeus planirostris F 48 34 21 171 178 164 616 6 (100) Platyrrhinus lineatus F 1 1 15 17 3 (50) Sturnira lillium F 29 29 1 (16.6)
Noctilionidae (2) Noctilio leporinus P 1 5 1 7 3 (50) Noctilio sp. P 1 1 2 2 (33.3)
Mormoopidae (1) Pteronotus gymnonotus I 2 4 1 7 3 (50)
Molossidae (5) Eumops sp. I 1 1 1 (16.6) Molossops temminckii I 1 1 1 (16.6) Molossus molossus I 1 1 1 (16.6) Neoplatymops I 5 1 6 2 (33.3) mattogrossensis Promops nasutus I 1 1 1 (16.6)
57
Vespertilionidae Myotis lavali I 8 35 1 1 5 50 5 (83.3) (2) Rhogeessa hussoni I 8 8 1 (16.6) Sampling effort
(hm2) 14198.8 22612.5 14068.8 27102.5 14267.5 150175.0 242425 Abundance 76 96 42 326 268 767 1575 Effort Corrected 48.6 43.8 22.4 202.4 107.2 100.6 Abundance
Table 1.3. Bray-Curtis similarity matrix comparing spatial beta diversity of each surveyed site. Darkest blue (highest value) indicates the most similar areas in species composition of bats, while the lowest value (darkest red) indicates less similar. Acronyms are: Açú National Forest (ANF), Furna Feia National Park (FFNP), Felipe Guerra (FG), Lajes (LAJ), Martins (MAR), and Seridó Ecological Station (SES). Site ANF FFNP FG LAJ MAR SES FFNP 0.44 1.00 FG 0.51 0.33 1.00 LAJ 0.43 0.48 0.42 1.00 MAR 0.36 0.20 0.51 0.19 1.00 SES 0.46 0.46 0.25 0.33 0.14 1.00
Figure 1.3. Relative abundances presented in percentages of seven different trophic guilds of bats in seven different Caatinga habitats from 2016-2019 in Rio Grande do Norte, Brazil.
58
Assemblage structure in Caatinga habitats
The species accumulation curves of the humid forest enclave and the shrubby Caatinga close to reach an asymptote therefore an acceptable sampling effort was effectuated. Other habitats presented steep curves and greater effort seems to be needed to register the most of the richness of these habitats (Fig. 1.1c). the Riparian Caatinga was the richest in (21 species) followed by the
Shrubby Caatinga (17), the Rocky outcrops (15), Humid Forest enclaves (11), Medium Caatinga forests and Copernicia groves with 10 species, and gardens/orchards with six species. After effort correction the highest abundance was found in the shrubby Caatingas with 224.3 individuals per 1000 hm2 , followed by riparian Caatingas with 196 individuals, the rocky outcrops with 113.7 indiv., humid forest enclaves with 94.3 indiv., orchards/gardens with 35.2 indiv., medium Caatinga forests with 33.5 indiv., and Copernicia groves with 31.1 individuals (Table 1.4).
The habitats presented differences in their assemblage structure at guild and species levels.
The shrubby Caatingas had a largest proportion of nectarivores (50% of captures) and the habitat with the largest proportion of animalivorous bats (9%). In the Riparian Caatingas, frugivores (37%) and nectarivores (34%) composed most of the assemblage followed by insectivores (12%). In Humid forest enclaves, frugivores clearly dominated with 92% of the captures. Similarly, in Copernicia groves 81% of captures corresponded to frugivores and the only habitat with the occurrence of piscivores (7%). In orchards and gardens, frugivores dominated as well, followed by insectivores with the 16% of captures. In medium Caatinga forests, frugivores dominated (65%) but sanguinivores were the second to dominate the captures (17%). Lastly, in rocky outcrops, highest capture proportions were distributed by frugivores (33%), nectarivores (23%) and sanguinivores (23%) represented most of the captured bats (Fig. 1.4).
The correspondence analysis (CA) found differences in the species composition between habitats (Fig 1.5). The axis 1 of the CA accounted for 49.9 % of the variation and the axis 2 accounted
20.5%. The CA separated the species and habitats in two groups in relation to the axis 1. The Humid forest enclave, Copernicia groves and orchards and gardens were grouped in the negative values of the
59 axis 1. While the Medium Caatinga Forest, Rocky outcrops, and Riparian and Shrubby Caatingas were grouped in the positive values of the axis 1 and were relatively more similar among each other, especially the riparian Caatingas with the rocky outcrops. The shrubby Caatinga and the orchards/gardens harbored the most differentiated assemblages (longer lines and larger angle degrees of vectors) in relation to the other habitats. Some habitats presented exclusive species such as the
Humid Forest enclave (P. hastatus, A. geoffroyi, A. lituratus, S. lilium), the Riparian Caatingas (M. temminckii, M. molossus, R. hussoni), orchards and gardens (Promops nasutus), and the rocky outcrops (Eumops sp.).
Figure 1.4. Relative abundances presented in percentages of seven different trophic
guilds of bats in seven different Caatinga habitats from 2016-2019 in Rio Grande do Norte, Brazil.
60
Table 1.4. Species composition and number of captured of individuals (without effort correction) per Caatinga habitat surveyed during 2017-2019 in the Caatinga of Rio Grande do Norte State. Occurr (%) means the percentage of occurrence of each species in the habitats.
Family/ Rocky Copernicia Humid Orch Ocurr. Species Riparian Shrubby Medium Total Subfamily outcrops groves forest /gard (%)
Emballonuridae Peropteryx macrotis 2 16 11 1 30 57.1 Phyllostomidae Micronycteris Micronycterinae 2 2 4 28.6 megalotis Micronycteris sanborni 1 10 11 28.6 Micronycteris 2 1 1 1 1 6 71.4 schmidtorum Desmodontinae Desmodus rotundus 29 68 15 37 2 1 1 153 100 Diphylla ecaudata 3 20 6 29 42.8 Phyllostominae Phyllostomus discolor 8 5 5 2 20 57.1 Phyllostomus hastatus 2 2 14.3 Tonatia bidens 3 27 1 3 34 57.1 Trachops cirrhosus 16 19 2 37 42.8 Glossophaginae Anoura geoffroyi 5 5 14.3 Glossophaga soricina 55 78 5 21 1 10 2 172 100 Lonchophylla Lonchophyllinae 37 46 83 28.6 inexpectata Lonchophylla mordax 43 76 1 23 1 144 71.4 Lonchophylla sp 1 3 4 28.6 Xeronycteris vieirai 5 67 72 28.6 Carolliinae Carollia perspicillata 1 16 17 28.6 Stenodermatinae Artibeus lituratus 6 6 14.3 Artibeus planirostris 154 94 50 61 71 155 31 616 100 Platyrrhinus lineatus 5 1 10 1 17 Sturnira lilium 29 29 14.3
Noctilionidae Noctilio leporinus 1 5 1 7 42.8 Noctilio sp. 1 1 2 28.6
Mormoopidae Pteronotus gymnonotus 1 2 4 7 42.8
Molossidae Eumops sp. 1 1 14.3 Molossops temminckii 1 1 14.3 Molossus molossus 1 1 14.3 Neoplatymops 1 5 6 28.6 mattogrossensis Promops nasutus 1 1 14.3
61
Vespertilionidae Myotis lavali 34 9 2 3 1 1 50 85.7 Rhogeessa hussoni 8 8 14.3 Sampling effort 111406 62834 25869 18205 13322 7605 3185 39132 (hm2) Abundance 407 534 86 188 88 235 37 1575 Effort Corrected 195.9 224.3 33.9 112.9 31.1 93.4 35.2 237.4 Abundance
Seasonal structure of bat assemblages in Lajes
During the dry season the species richness was of 16 species (average of 8.6 ± 2.6) and 15
species (average of 8.9 ± 1.5) in the rainy season, and no significant difference was found (t = 0.22, df
= 12, p = 0.82). Both computed curves did not reach an asymptote but presented signs of stabilization
after the capturing 100 individuals and suggests that both seasons were satisfactory sampled (Fig.
1.2d). A total of 64.7 individuals per 1000 m2h (average of 5.88 ± 4.32) was captured in the dry
season, while in the rainy season 42.6 (average of 4.72 ± 2.63) individuals, and no significant
difference was found in the bat abundance between seasons (t = 0.73, df = 17, p = 0.47). The
abundance of each surveyed month varied along the years and tended to fluctuate between the months
of the years (Fig. 1.6). Peaks of abundance were found in both seasons (rainy: May 2017 and February
2018; dry: July 2017 and December 2018), being the latter with the highest capture rate. However,
months with the lowest precipitation presented the lowest capture rates.
According to the Bray-Curtis similarity index, the species composition was not highly
different when comparing the season per year pair to pair as the index of similarity of all seasons were
above 0.63 (Table 1.7). Thus, the species composition seems to be very similar throughout the
surveyed years. However, at the trophic ensemble levels, frugivores and nectarivores tended to have a
higher capture rate during the dry season than in the rainy season., while the other four ensembles did
not change much between seasons (Fig. 1.7).
This was observed at a species level. In the SIMPER analysis, that species that contributed the
most to the assemblage dissimilarity between the seasons was the frugivore A. planirostris and the
62
nectarivore Glossophaga soricina contributing with 21.59% and 13.52% of dissimilarity between
seasons, respectively (Supplementary material 1.6). Both species contributed almost a third (35.1%) of
the cumulative % of dissimilarity between seasons and other species contributed little (< 3.855
individually). This was reflected in the capture rate of this species between seasons (Fig. 1.8.).
Artibeus planirostris had a capture rate of 14.58 indiv. per 1000 m2h m in the dry season and 7.98 in
the rainy season; while G. soricina with 11.52 in the dry versus 3.88 in the rainy season.
18.00 160
16.00 Precipitation (mm) 140 14.00 120 12.00 100 10.00 80 8.00 60
6.00 Precipitation(mm) 40 4.00
Indiv / 1000 m2 hour / 2.00 20
0.00 0
JUL JUL
SEP SEP
FEB FEB FEB
JAN JAN
JUN JUN
DEC APR DEC
ABR
OCT OCT
AUG AUG
NOV NOV
MAY MAY
MAR MAR * * * Rainy Dry * Rainy * Dry Rainy 2017 2018 2019
Figure 1.6. Effort-corrected abundance of captured bats and precipitation in millimeters (mm) along 20 months from 2017- 2019 in Lajes, Rio Grande do Norte, Brazil. Abundance of axis y is number of captured individuals every 1000 m2h of mist netting. * means months not sampled.
Table 1.7. Bray-Curtis dissimilarity matrix comparing temporal beta diversity of season per year in Lajes. Darkest blue (highest value) indicates the most similar season in species composition of bats, while the lowest value (darkest red) indicates highest dissimilarity.
Season year Rainy 2017 Dry 2017 Rainy 2018 Dry 2017 0.63 Rainy 2018 0.78 0.64 Dry 2018 0.69 0.71 0.76
63
Figure 1.7. Effort corrected abundance of trophic ensembles of bats in Lajes, Rio Grande do Norte, Brazil from 2017-2019. Indiv/1000m2/hour is number of individuals captured every 1000 hm2 of mist nets.
Figure 1.8. Abundance of bats corrected by the capture effort in the rainy and dry seasons in Lajes, Rio Grande do Norte from 2017-2018. Indiv/1000 hm2 is the number of individuals captured every 1000 hm2 of mist nests. Specie acronyms are: Neoplatymops mattogrossensis (Nm), Pteronotus gymnonotus (Pg), Molossus molossus (Mmol), Micronycteris megalotis (Mmeg), Phyllostomus discolor (Pd), Myotis lavali (Ml), Rhogeessa hussoni (Rh), Trachops cirrhosus (Tc), Peropteryx macrotis (Pm), Diphylla ecaudata (De), Tonatia bidens (Tb), Desmodus rotundus (Dr), Xeronycteris vieirai, Lonchophylla inexpectata (Li), Lonchophylla mordax (Lm), Glossophaga soricina (Gs), and Artibeus planirostris (Ap).
64
DISCUSSION
Richness and species composition
Although we recorded a gamma diversity of 32 species, the richness per area (alpha diversity) was relatively low (18-9 spp) compared to other Caatinga bat assemblages where richness exceeded 19 species (Willig 1983, Silva 2007, Gregorin et al. 2008, Sá-Neto and Marinho-Filho 2013, Novaes and
Laurindo 2014, Beltrão et al. 2015, Nogueira et al. 2015, Novaes et al. 2015, Silva et al. 2015, Feijó and Rocha 2017). Despite the low richness per area, four of the six studied areas presented exclusive species (11 spp. in total) (Table 1.2). This species comprehends slightly more than a third of the gamma diversity recorded herein.
Such differences in the species composition between areas resulted in the fact that each area contained a smaller proportion of the species occurring in the region (gamma diversity of RN). Thus, the findings are consistent to our first prediction. It seems that the gamma diversity in RN may be explained not by a high alpha diversity, but by a high turnover of species associated to a spatial variation in species composition (spatial beta diversity), despite the vagile ability by bats. This diversity pattern was found in bats in Mexico and central Brazil (López-González et al. 2014, Santos et al. 2016, Zortéa and D’arc 2019). This contraries the hypothesis that the bat gamma diversity of a region is the result of a high alpha diversity in single localities and low beta diversity due to the high dispersal ability of bats to overcome any barrier or habitat variation (Willig and Moulton 1989,
Moreno and Halffter 2001, Rodríguez and Arita 2004).
However, is important to consider that the spatial beta diversity of a particular organism are also influence by other factors such as the species biogeographic history, the spatial scale (the extent of the study), niche limitations and the organism’s dispersal capabilities (eg. flying or terrestrial organisms) (Barton et al. 2013, Calderón-Patrón et al. 2013). In our studied areas, the species composition and trophic guild structure were different between them (Table 1.3 and Fig. 1.3). Also, the species distribution among areas seems to be not homogeneous. (Table 1.2) For instance, most of
65 the assemblages (except in FG and ANF) and ecoregions (NSD and BH) presented exclusive species.
Similar to the results of Carvalho-Neto et al. (2016), though in a smaller spatial universe (in RN).
The differences in the species composition among the areas might be related to the particular ecoregion characteristics on which each studied area is located such as differences in topography
(lowlands vs mountains /plateaus), vegetation composition (humid forest enclaves vs shrubby
Caatingas), or even related to the landscape context (protected vs disturbed areas). This array of factors found spatially differentiated between the areas are likely molding differently the structure of the assemblages therefore yielding different patterns of richness and species compositions. This spatial effect as result of the natural heterogeneity found in the Caatingas has been partially supported by plants (Ferreira et al. 2009, Santos et al. 2012, Apgaua et al. 2014), invertebrates (Hernández 2007) and vertebrates (Guedes et al. 2014).
The differences in altitude and topography might seem to be an important factor in the differences between assemblages. For instance, Martins presented one of the most different assemblage with the highest richness (e.g. C. perspicillata, A. planirostris, A. lituratus, P. lineatus and
S. lilium) and proportion of frugivorous bats – almost 90% of the assemblage. The area of Martins is a plateau with the highest altitude of all sampled areas (500-700 m), as well with remnants of perennial humid forest vegetation and high orographic rainfall (>1000 mm). In the other surveyed areas located in lowlands of NSD with semiarid climate and with Caatinga vegetation strictu senso, frugivores richness was low and dominated by A. planirostris (P. lineatus and C. perspicillata were rare) (Table
1.3).
The other area with a very distinct assemblage was Lajes where surveys were done at the Serra do Feiticeiro, a quartzitic escarpment of about 400m of altitude with a scarped topography and with one of the largest and well-preserved Caatinga fragments, rare in other lowlands Caatingas of NSD.
Here the assemblage was very different and presenting the highest richness and dominance of nectarivores with 51% of the total captures (e.g. G. soricina, X. vieirai, L. mordax and L. inexpectata)
(Fig. 1.3 and Table 1.2). This area characterized to harbor a high diversity of columnar cacti
66
(Supplementary material 1.1) and patches of granitic outcrops might explain the occurrence of this high richness and abundance of nectarivorous bats by offering abundant nectar and roost resources.
However, areas found at lowlands within the NSD presented assemblages with differences among them, but not as markedly as those of Martins and Lajes. In this lowland areas, the landscape composition and preservation context on which each area is located might be a factor that explain such differences in their assemblage structure, For instance, despite Felipe Guerra and FFNP are similar in harboring vast lowlands, karstic areas with rocky calcareous outcrops with numerous cave clusters and the largest proportion of sanguinivorous bats, they are located in two contrasting landscape contexts
(see Vargas-Mena et al. 2018b). Felipe Guerra contains high levels of anthropic activities (high livestock densities and home of ~6000 people) and the double of mean abundance of vampires D. rotundus and D. ecaudata (see Fig. 1.3 and Supplementary materials 1.5) in relation to FFNP, that protects about 8000 ha of shrubby/Medium Caatinga forests (Bento et al. 2011). This high abundance of vampire bats can be considered an indicator of landscape disturbance (Medellín et al. 2000) and the anthropic activities in Felipe Guerra’s landscape are likely favoring the formation and maintenance of large populations of vampire bats. Vargas-Mena et al. (2020) found that in caves where the livestock density around them was high, colonies of vampires were two-fold larger than those in the FFNP. This was attributed to a stable and abundant year-round food resource for D. rotundus which prefers to feed from livestock rather than from native mammals in disturbed landscapes (Voigt and Kelm 2006,
Bobrowiec et al. 2015).
Species and trophic composition in habitats The assemblages within the Caatinga habitats were relatively different and assemblages presented particular characteristics at the species and ensemble (trophic guilds) levels, consistent to our second prediction. Some species were common and widespread, while others only occurred in specific habitats, therefore the species composition varied among habitats. This pattern is likely due to differences in plant species composition and vegetation structures between habitats, that are offering different foraging areas to be exploited by species with different natural history traits (e.g. specific or
67 generalist diet and/or roost) and ecological adaptations (e.g. wing morphology, type of echolocation, sensorial capacities) (Kunz 1982, Kunz and Pierson 1994, Kalko 1998, Denzinger and Schnitzler
2013, Norberg and Rayner 2016). These wide variety of phytophysiognomies and floristic composition found in the Caatinga seems to be a factor controlling the species composition of bats in this dry forest, as proposed by Willig (1983).
The separation of the habitats showed along the CA’s axis 1 (highest variation percentage
49.9 %) (Fig 1.5) coincides with differences in the vegetational structure and plant species composition of each habitat. Heterogeneous semi-open habitats that shared many common and widespread plant species (see Table 1.2), for instance, the rocky outcrops, shrubby and riparian
Caatingas, tended to be relatively more similar in the structure of their assemblages (Fig 1.4).
However, the scrubby Caatinga presented the highest association of nectarivorous bats in RN, where
50% of the captured bats corresponded to this ensemble (Fig 1.4.) Nectar-feeding bats are found to be common in shrubby Caatingas but at low richness (Willig 1983, Silva 2007, Sa-Neto and Marinho-
Filho 2013, Rocha et al. 2018, Soares et al. 2019), however in the shrubby Caatinga of Lajes, the richness of this bats can be relatively high, likely due to the abundant floral resources (nectar) provided by cacti, their main food item (e.g P. pachycladus, P. gounellei, C. jamacaru, Melocatus spp.) (Cordero-Schmidt et al. 2017, Cordero-Schmidt, 2020). In general, a high diversity of cacti is found shrubby Caatingas, but in Lajes, large clusters of several species of the columnar Cacti species are found in vast extension. Therefore, we encourage surveys and roost search in other shrubby caatingas of the Borborema Highlands to verify if nectarivorous ensembles are similar to that in Lajes.
Especially in areas with this Cacti “forests” (Figure D), where X. vieirai apparently only occurs and roost year-round under big granitic boulders (see chapter 3).
Unexpectedly, the proportion of gleaning animalivorous bats was largest as well in the shrubby Caatingas and T. bidens, T. cirrhosus and M. megalotis were found to be more associated to this habitat. Small granitic rocky outcrops are commonly found sparsely within the shrubby Caatingas, providing potential roosting areas of underground cavities and rock boulders for the animalivores – the
68 only natural roost used by this ensemble in the Caatinga of RN (Vargas-Mena et al. 2018b). This bat might be emerging from their roost to forage in here or adjacent areas, therefore increasing their probability to be capture. This might be the same case of the rocky outcrops. Their bat assemblages were similar to the shrubby Caatinga but with less proportion of nectarivores and more hematophagous (Fig. 1.4) and with high association of species of different ensembles (M. sanborni, P. gymnonotus, Eumops sp., D. rotundus). These vast calcareous outcrops bring a great spatial heterogeneity of semi-open foraging areas with patches of shrubs, cacti and Leguminosae trees, and small water ponds in the rainy season, in addition to the large number of potential caves roosts (>100 caves in a sing) for a wide array of species. Caves found in these rocky outcrops are known to roost about one third of all bats known to occur in RN, therefore highlights the importance of this habitats for a large portion of bats in the state, including large colonies (~10 000 indiv.) of P. gymnonotus, for instance (Vargas-Mena et al. 2018a, 2018b).
Riparian Caatingas presented the highest bat richness of all habitats (21 spp) and more species could be recorded considering that its species accumulation curve needed was not yet asymptotic, despite its large sampling effort (Fig 1.1c). These areas are associated to natural or artificial water bodies and present a mixed composition of plants of adjacent Caatingas with riparian-associated species (see table 1.2). Consequently, riparian Caatingas may harbor a high heterogeneity of foraging habitats. The hypothesis of habitat heterogeneity states that an increase in the number of habitats and/or an increase in their structural complexity, at a different scale, leads to an increased species diversity (MacArthur and MacArthur, 1961; MacArthur and Wilson, 1967; Connor and McCoy,
1979). This might explain the high richness found in this habitat. A larger number of habitats implicates a larger number of foraging areas, hence more exploitable niches for a wider array of bat species than in less heterogeneous habitats.
Moreover, Riparian Caatingas harbored the highest proportion of aerial insectivore bats, including Rhogeessa sp., captured only in these habitats (Fig.1.5). In SES, several natural ponds and a small artificial dam that might explain the high abundance of M. lavali. Water bodies are important for
69 insectivorous bats either for drinking and as important areas to forage for aquatic emergent insects
(Grindal et al. 1999, Korine and Pinshow 2004, Razgour et al. 2010, Costa et al. 2012). These water bodies are likely providing insect prey and drinkable water for M. lavali, especially during the dry season. Similarly, Novaes et al (2015) found a high richness and abundance of M. lavali and other aerial insectivores near water bodies in a Caatinga of Piaui. Considering the limitation of water in the
Caatinga during the dry season, the protection of riparian Caatingas and their associated water bodies are critical for local bat conservation, especially in dry forests and semiarid environments (Bader et al.
2015, Korine et al. 2016). However, more studies using acoustic monitoring will provide a better insight of aerial insectivore richness, activity and seasonal habitat use within these habitats.
Copernicia groves presents a structure conspicuously different from other habitats, despite being a riparian habitat. Its structure is conspicuously different with Carnauba palms of 10-20m high at water bodies margins, absent understory or less developed, and a dynamic seasonal flooding during the rainy season. Piscivore bats (N. leporinus) were more associated to this habitat (Fig 1.5) likely due to adjacent water bodies (Lake Piató in ANF and the Apodi river in FG) that provide the optimal foraging habitat for fish and aquatic insects, its main diet (Hood and Jones Jr. 1984). Nevertheless, the assemblage was found to be dominated by frugivores, consistent with Willig 1981, but poor in frugivore species. Artibeus planirostris was abundant in this habitat possibly foraging for fruiting
Copernicia prunifera. We have seen plenty of seeds of C. prunifera under A. planirostris roosts in several caves in FG. Because our effort was low and species accumulation curve did not stabilize, we encourage more focus on these habitats considering its seasonal flooding dynamic and the role of seed dispersal by A. planirostris of C. prunifera, an endemic palm with a socioeconomical importance in this region of the Caatinga (Johnson 1972).
Humid forest enclaves in contrast to Caatinga habitats, differed widely in abundance and species composition and clearly dominated by frugivores (Fig. 1.4), consistent with the few studies in this enclaves across the Caatinga (Sousa et al. 2004, Silva 2007, Novaes et al. 2013, Rocha et al.
2018). Humid forest enclaves present a completely different vegetation of evergreen and
70 semideciduous plants of 10-20m, and a well-developed understory. This enclaves are found scattered only on plateaus and mountains north the San Francisco river in the Caatinga (Porto et al. 2004).
Moreover, in other humid forest enclaves, 88% of the recorded plant species were zoochoric species while in the Caatinga only 44%, and most were anemochoric (Griz and Machado 2001),Vicente et al.
2003, Machado et al. 2012). That said, the potential abundant fruit resource found in humid forests enclaves unlike adjacent Caatingas, might explain the high abundance (Table 1.4) and association
(Fig. 1.5) of frugivore bats to this habitat. As well, exclusive occurrences of Anoura geofroyii and
Phyllosotomus hastatus in the enclave might be related to a food or roost resources uniquely found in these habitats. Regarding, A. geofroyii seems to be rare in the Caatinga and captured in low number in more mesic habitats (Silva 2007, Gregorin et al. 2008, Rocha et al. 2018). We poorly explored this region and roost search (nearly 50 caves are found in Martins), captures and acoustic surveys in other areas of the plateau are needed in order to understand more deeply this unique bat fauna in RN. This mesic areas are considered refugia for mammal fauna in the Caatinga semiarid landscape (Mares et al.
1981, Sousa et al. 2004, Rocha et al. 2018).
Seasonal structure of the bat assemblage in Lajes
Our third prediction was not consistent. In Lajes, the richness between seasons did not varied significantly and the difference in the species composition between the seasons were subtle (>0.60 dissimilarity index) (Table 1.7). Therefore, it seems that the bat assemblage in Lajes has no major seasonal changes neither on the richness nor on the species identity between the seasons throughout the two sampled years. While in other bat assemblages in Caatinga differences between season were found (Silva et al. 2015, Novaes et al. 2015, Rocha et al. 2018, Soares et al. 2019), the stability of richness and species composition seem to be uncommon and only consistent with Silva (2007) in
Pernambuco.
Contrary to our third prediction, phytophagous bats did not disappear during the dry season.
The presence of frugivorous and nectarivorous bat all year might be explained by the year-round food resource (flower and fruits) offered by different plant species. In Caatinga, plant species produce 71 flower and fruits year-round where production peaks are generally found during the rainy season for most plant species, but some other species can have during the dry season a low but stable production of flowers and fruits (Machado et al. 1997, Griz and Machado 2001, Amorim et al. 2009, Quirino and
Machado 2014, Rocha et al. 2020). Consistent with this, phenological data of nine species of bat- visited plants in the same capture area in Lajes presented a peak of flowering in the rainy season but some presented flowers in low numbers during the dry season, mainly Columnar cacti species (see
Cordero-Schmidt 2020). Such phenological pattern in plants provides a key nectar source for local nectarivorous bats during the harsh dry season (Cordero-Schmidt 2020). Such year-round availability of floral resources may function as a strategy of plants to maintain pollinator populations and ensuring the reproductive success of plants, especially in semiarid and seasonal dry forest like the Caatinga
(Quirino and Machado 2014). The occurrence of nectarivorous year-round is consistent with Soares et al. (2018) and Rocha et al. (2018) in other Caatingas.
Regarding the only frugivore recorded in Lajes, A. planirostris was found year-round as well.
Paixão (2020) obtained data on fruit phenology in Lajes of cacti species which presented peaks of fructification during the rainy season but and some production during the dry season – potential food resource for A. planirostris. However, in the six-month-long study monitoring cacti fruit dispersers, bats unexpectedly were not recorded (Paixão 2020). This suggest that cacti fruits are not an important resource for A. planirostris in Lajes, consistent with the bat diet analysis by Silva (2007) in a Caatinga of Pernambuco. However, it is known that in Lajes, A. planirostris eats on leaves during the dry season, (see Cordero-Schmidt et al. 2016), and fruits of the introduced Prosopis juliflora (Algaroba) and native Anacardium occidentale (Cajú), both species that fructify in the dry season (Carvalho et al.
2016, personal observations). Overall, the low abundant but available resource during the harsh moments of the dry season are likely maintaining populations of phytophagous bats in Lajes to occur year-round. In fact, colonies of A. planirostris, X. vieirai and G. soricina were found to be year-round in their roost throughout the two years of monitoring in nearby caves (see Chapter 3).
72
Several studies have recorded an increase in the bat abundance during the rainy season, but overall bat abundance in Lajes presented no significant differences between seasons. found (Silva et al. 2015, Novaes et al. 2015, Rocha et al. 2018, Soares et al. 2019) However, when analyzing by guilds and species, A. planirostris and G. soricina were more captured and contributed more to the dissimilarity of the assemblage (Table 1.9) during the dry season than in the rainy season. Considering that phytophagous bats occur year-round in Lajes, then why A. planirostris and G. soricina had a higher capture rate in dry season than in the rainy season? We believe that this might be explained by sampling bias.
Despite the fact that flowers and fruits for phytophagous bat are abundant in the rainy season, these resources are more “dispersed” in the landscape and therefore captures were lower, for instance in February 2017, January and April 2018 (Fig. 1.7). During the dry season, food resources are found but in low numbers and likely having a higher demand by bats, hence the density of foraging bats near these resources is expected to higher. Since in the dry season these resources were conspicuously found in the sampling area, we arbitrary deployed mist nets near flowering and fructifying trees, in order to increase bat captures. Consequently, the captures rate was higher and hence inflating the abundance values of nectarivores and frugivores during the dry season (Fig 1.7).
Finally, other guilds like animalivores, omnivores and sanguinivores did not presented an evident difference between the season. Bats of this ensembles, with the exception of sanguinivores, may present dietary flexibility. This behavioral adaptation is known to be use by bats in other SDTF seemingly to reduce competition (Stoner and Timm 2004). Gleaning animalivores (T. bidens, T. cirrhosus and M. megalotis) might be having a more omnivorous diet and eating on insects during the rainy season when are more abundant in Caatinga (Vasconcellos et al. 2011), alternating with year- round fruits and opportunistically eating on small vertebrates (Reis et al 2013). We have recorded bird feathers, a small rodent, hundreds of beetle and unidentified insect exoskeletons and moth wings under roosts of T. bidens and T. cirrhosus in two abandoned mines in Lajes. Despite the morphological and behavioral specializations of Phyllostomid bats, they can be opportunistic feeders that include a diet of
73 several trophic levels (Rex et al. 2010). For instance, the nectarivore G. soricina can have an omnivory diet (Clare et al. 2014), and A. planirostris can feed on nectar of flowers of columnar cacti in the Caatinga of Pernambuco (Rocha et al. 2020).
CONCLUSIONS In the Caatinga, key factors that controls the structure and dynamics of the bat assemblages have been attributed to the spatial heterogeneity of many different ecoregions and phytofisiognomies
(Willig 1983, Gregorin et al. 2008, Sá-Neto and Marinho-Filho 2013, Carvalho-Neto et al. 2016) and to the seasonality of rain and pulses of food resource (Novaes et al. 2015, Silva et al. 2015, Rocha et al. 2018, Soares et al. 2018a). In RN, this spatial heterogeneity seem to be more strongly affecting the bat assemblages by presenting particular structure at the species, ensemble (trophic guilds) and assemblage levels that might be related to the spatial characteristics of the landscape, to the vegetational structure of foraging habitats, than to temporal abiotic factors due to year-round food resource found available along the year that drives the assemblage to have less seasonal variation between the rainy and dry season, at least in Lajes. Despite the great advance in the knowledge of the diversity, distribution and ecology of bats in this region of the Brazilian Caatinga, more studies are needed in order to better unravel the diverse bat fauna of this endemic dry forest.
REFERENCES Alvares, C. A., J. L. Stape, P. C. Sentelhas, J. L. De Moraes Gonçalves, and G. Sparovek. 2013. Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22:711–728. Amorim, I. L. de, E. Valadares, de S. Barreto, and E. de Lima. 2009. Fenologia de espécies lenhosas da Caatinga do Seridó, RN. Revista Árvore 33:491–499. Apgaua, D. M. G., R. Santos, D. G. S. Pereira, G. C. de O. Menino, G. G. Pires, M. A. L. Fontes, and Da. Y. P. Tng. 2014. Beta-diversity in seasonally dry tropical forests ( SDTF ) in the Caatinga Biogeographic Domain , Brazil , and its implications for conservation. Biodiversity and Conservation 23:217–232. Bader, E., M. Acácio, and A. Monadjem. 2015. The importance of water bodies for insectivorous bats in a Malagasy dry deciduous forest : A case example from Kirindy (CNFEREF). Malagasy
74
Nature 9:88–96. Barros, M. A. S., C. M. G. Morais, B. M. B. Figueiredo, G. B. de Moura Júnior, F. F. dos S. Ribeiro, D. M. A. Pessoa, F. Ito, and E. Bernard. 2017. Bats (Mammalia, Chiroptera) from the Nísia Floresta National Forest, with new records for the state of Rio Grande do Norte, northeastern Brazil. Biota Neotropica 17. Barton, P. S., S. A. Cunningham, A. D. Manning, H. Gibb, D. B. Lindenmayer, and R. K. Didham. 2013. The spatial scaling of beta diversity. Global Ecology and Biogeography 22:639–647. Basílio, G. H. N., J. P. M. de Araujo, J. C. Vargas-Mena, P. A. Rocha, and M. A. F. Kramer. 2017. Chrotopterus auritus (Peters, 1856) (Chiroptera, Phyllostomidae): first record for the state of Rio Grande do Norte, northeastern Brazil. Check List 13:1–8. Beltrão, M. G., C. G. Zeppelini, M. P. A. Fracasso, and L. C. S. Lopez. 2015. Inventário de morcegos em uma área de Caatinga no Nordeste brasileiro, com uma nova ocorrência para o estado da Paraíba. Neotropical Biology and Conservation 10:15–20. Bento, D. D. M., J. B. Cruz, J. I. Freitas, and U. P. Campos. 2015. Área De Proteção Ambiental Pedra De Abelha : Proposta. 33 Congresso Brasileiro de Espeleologia 2113:51–63. Bernard, E., L. M. S. Aguiar, and R. B. Machado. 2011. Discovering the Brazilian bat fauna: A task for two centuries? Mammal Review 41:23–39. Bobrowiec, P. E. D., M. R. Lemes, and R. Gribel. 2015. Prey preference of the common vampire bat (Desmodus rotundus, Chiroptera) using molecular analysis. Journal of Mammalogy 96:54–63. Braak, C. J. F. ter. 1995. 5. Ordination. Pages 91–212 in R. H. G. Jongman, C. J. F. ter Braak, and O. F. R. Van Tongeren, editors. Data Analysis in Community and Landscape Ecology. Cambridge University Press, New York. Calderón-Patrón, J. M., C. E. Moreno, R. Pineda-lópez, and G. Sánchez-rojas. 2013. Vertebrate Dissimilarity Due to Turnover and Richness Differences in a Highly Beta-Diverse Region : The Role of Spatial Grain Size , Dispersal Ability and Distance. PLoS ONE 8:1–10. Carmignotto, A. P., and D. Astúa. 2017. Mammals of the Caatinga : Diversity , Ecology , Biogeography , and Conservation. Pages 211–254 in J. M. C. da Silva, I. R. Leal, and M. Tabarelli, editors. Caatinga: The Largest Tropical Dry Forest Region in South America. Springer International Publisher, Cham, Switzerland. Carvalho-Neto, F. G., J. R. Da Silva, N. Santos, C. Rohde, A. C. L. Garcia, and M. A. Montes. 2016. The heterogeneity of Caatinga biome: An overview of the bat fauna. Mammalia 81:257–264. Carvalho, W. D., A. C. S. Maas, A. L. Peracchi, and L. A. C. Gomes. 2016. Fruit consumption of Prosopis juliflora ( Fabaceae ) and Anacardium occidentale ( Anacardiaceae ) by Artibeus ( Phyllostomidae ) in the Caatinga biome. Boletim da Sociedade Brasileira de Mastozoologia 77:154–157. 75
Chesson, P., R. L. E. Gebauer, S. Schwinning, N. Huntly, K. Wiegand, M. S. K. Ernest, A. Sher, A. Novoplansky, and J. F. Weltzin. 2004. Resource pulses , species interactions , and diversity maintenance in arid and semi-arid environments. Oecologia 141:236–253. Clare, E. L., H. R. Goerlitz, V. A. Drapeau, M. W. Holderied, A. M. Adams, J. Nagel, E. R. Dumont, P. D. N. Hebert, and M. B. Fenton. 2014. Trophic niche flexibility in Glossophaga soricina : how a nectar seeker sneaks an insect snack. Functional Ecology 28:632–641. Cordero-Schmidt , E. 2020. Interações, mecanismos de persistência e coexistência de morcegos nectarívoros e das plantas das quais se alimentam em uma floresta tropical sazonal seca no Nordeste brasileiro. Dissertação de doutorado. Universidade Federal do Rio Grande do Norte, Natal, Brasil. Pp. 160. Cordero-Schmidt, E., E. Barbier, J. C. Vargas-Mena, P. P. Oliveira, F. D. A. R. Santos, R. A. Medellín, B. R. Herrera, and E. M. Venticinque. 2017. Natural History of the Caatinga Endemic Vieira’s Flower Bat, Xeronycteris vieirai. Acta Chiropterologica 19:399–408. Cordero-Schmidt, E., M. Medeiros-Guimarães, J. C. Vargas-Mena, B. Carvalho, R. L. Ferreira, B. Rodriguez-Herrera, and E. M. Venticinque. 2016. Are leaves a good option in Caatinga’s menu? First record of folivory in Artibeus planirostris (Phyllostomidae) in the semiarid forest, Brazil. Acta Chiropterologica 18:489–497. Costa, L. de M., J. L. Luz, and C. E. Esbérard. 2012. Riqueza de morcegos insetívoros em lagoas no estado do Rio de Janeiro, Brasil. Papéis Avulsos de Zoologia 52:7–19. Denzinger, A., and H. U. Schnitzler. 2013. Bat guilds, a concept to classify the highly diverse foraging and echolocation behaviors of microchiropteran bats. Frontiers in Physiology 4:1–15. Díaz, M. M., S. Solari, L. F. Aguirre, L. M. S. Aguiar, and R. M. Barquez. 2016. Clave de identificación de los murciélagos de Sudamérica. Publicació. Programa de Conservación de los Murciélagos de Argentina (PCMA), Argentina. Diniz, M. T. M., and V. H. C. Pereira. 2015. Climatologia do estado do rio grande do norte, Brasil: sistemas atmosféricos atuantes e mapeamento de tipos de clima. Boletim Goiano de Geografia 35:488–506. Feijó, A., and P. A. da Rocha. 2017. Morcegos da Estação Ecológica Aiuaba, Ceará, Nordeste do Brasil: uma unidade de proteção integral na Caatinga. Mastozoologia Neotropical 24:333–346. Feijó, J. A., and H. L. de F. L. Nunes. 2010. Primeiro registro de Myotis nigricans (Schinz, 1821) para o estado do Rio Grande do Norte, nordeste do Brasil. Chiroptera Neotropical 16:531–534. Ferreira, C. G. T., R. C. Oliveira, J. M. Valls, and M. I. B. de Loiola. 2009. Poaceae da Estação Ecológica do Seridó , Rio Grande do Norte , Brasil. Hoehnea 36:679–707. Gregorin, R., A. P. Carmignotto, and Alexandre R. Percequillo. 2008. Quirópteros do Parque Nacional da Serra das Confusões, Piauí, nordeste do Brasil. Chiroptera Neotropical 14:366–383. 76
Grindal, S. D., J. L. Morissette, and R. M. Brigham. 1999. Concentration of bat activity in riparian habitats over an elevational gradient. Canadian Journal of Zoology 77:972–977. Griz, L. M. S., and I. C. Machado. 2001. Fruiting phenology and seed dispersal syndromes in caatinga , a tropical dry forest in the northeast of Brazil. Journal of Tropical Ecology 17:303–321. Guedes, T. B., R. J. Sawaya, and C. D. C. Nogueira. 2014. Biogeography , vicariance and conservation of snakes of the neglected and Biogeography , vicariance and conservation of snakes of the neglected and endangered Caatinga region , north-eastern Brazil. Journal of Biogeography 41:919–931. Gutiérrez, E. E., and J. Marinho-Filho. 2017. The mammalian faunas endemic to the Cerrado and the Caatinga. ZooKeys 2017:105–157. Hernández, M. I. 2007. Besouros escarabeíneos ( Coleoptera : Scarabaeidae ) da Caatinga paraibana , Brasil. Oecologia Brasiliensis 11:356–364. Hood, C. S., and J. K. Jones Jr. 1984. Noctilio leporinus. Mammalian Species:1–7. Kalko, E. K. V. 1998. Organization and diversity of Tropical bat communities through space and time. Zoology 101:281–297. Korine, C., and B. Pinshow. 2004. Guild structure, foraging space use, and distribution in a community of insectivorous bats in the Negev Desert. Journal of Zoology 262:187–196. Kunz, T. H. 1982. Roosting Ecology of Bats. Pages 1–58 in T. H. Kunz, editor. Ecology of Bats. Plenum Publishing Corporation, New York. Kunz, T. H., and E. D. Pierson. 1994. Bats of the World: An Introduction. Pages 1–46 in R. M. Nowak, editor. Walker’s Bats of the World. John Hopkins University Press. Kunz, T. H., E. B. de Torrez, D. Bauer, T. Lobova, and T. H. Fleming. 2011. Ecosystem services provided by bats. Annals of the New York Academy of Sciences 1223:1–38. López-González, C., S. J. Presley, A. Lozano, R. D. Stevens, and C. L. Higgins. 2014. Ecological biogeography of Mexican bats: The relative contributions of habitat heterogeneity, beta diversity, and environmental gradients to species richness and composition patterns. Ecography 37:1–12. Machado, I. C., L. M. Barros, and E. V. S. B. Sampaio. 1997. Phenology of Caatinga species at Serra Talhada, PE, Northeastern Brazil. Biotropica 29:57–68. Machado, I. C., and A. V. Lopes. 2004. Floral traits and pollination systems in the Caatinga, a brazilian tropical dry forest. Annals of Botany 94:365–376. Machado, W. D. J., A. P. do N. Prata, and A. A. De Mello. 2012. List Floristic composition in areas of Caatinga and Brejo de Altitude in Sergipe state , Brazil. Check List 8:1089–1101. Mares, M. A., M. R. Willig, K. E. Streilein, and T. E. Lacher. 1981. The mammals of northeastern Brazil: a preliminary assessment. Annals of the Carnegie Museum of Natural History 50:81–137. Medellín, R. A., M. Equihua, and M. A. Amin. 2000. Bat Diversity and Abundance as Indicators of 77
Disturbance in Neotropical Rainforests\rDiversidad y Abundancia de Murciélagos como Indicadores de Perturbaciones en Selvas Húmedas Neotropicales. Conservation Biology 14:1666–1675. Moreno, C. E., and G. Halffter. 2001. Spatial and temporal analysis of alpha, beta and gamma diversities of bats in a fragmented landscape. Biodiversity and Conservation 10:367–382. Nogueira, M. R., A. Pol, L. M. Pessôa, J. A. de Oliveira, and A. L. Peracchi. 2015. Small mammals (Chiroptera, Didelphimorphia, and Rodentia) from Jaíba, middle Rio São Francisco, northern Minas Gerais State, Brazil. Biota Neotropica 15:1–18. Norberg, U. M. L., and J. Rayner. 2016. Ecological morphology and flight in bats (Mammalia; Chiroptera): wing adaptations, flight performance, foraging strategy and echolocation. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 316:335–427. Novaes, R. L. M., and R. D. S. Laurindo. 2014. Morcegos da Chapada do Araripe, Nordeste do Brasil. Papeis Avulsos de Zoologia 54:315–328. Novaes, R. L. M., R. D. S. Laurindo, and R. D. F. Souza. 2015. Structure and natural history of an assemblage of bats from a xerophytic area in the Caatinga of northeastern Brazil. Studies on Neotropical Fauna and Environment 50:40–51. Novaes, R. L. M., R. de S. Laurindo, M. de B. Oliveira, C. de R. Barreto, and L. dos S. Avilla. 2013. First record of two molossid bats (Chiroptera: Molossidae) from Piauí state and distributional review for Brazil. Oliveira, J., P. R. Gonçalves, and C. R. Bonvicino. 2003. Mamíferos da Caatinga. Pages 275–334 Ecologia e Conservação da Caatinga. Universidade Federal de Pernambuco, Recife. Paixão, VHF. 2020. Interações entre cactos e vertebrados na Caatinga, floresta tropical seca do nordeste brasileiro. Master degree dissertation. Universidade Federal do Rio Grande do Norte. 77 p. Porto, K. C., J. J. P. Cabral, and M. Tabarelli. 2004. Brejos de Altitude em Pernambuco e Paraíba: História Natural, Ecologia e Conservação. Page Ministerio de Meio Ambiente. Ministerio de Meio Ambiente - Brasil, Brasília. Prado, D. E. 2003. As caatingas da América do Sul. Pages 3–74 in I. R. Leal, M. Tabarelli, and J. M. C. da Silva, editors. Ecologia e Conservação da Caatinga. Universida. Universidade Federal de Pernambuco, Recife. Quirino, Z. M. G., and I. C. Machado. 2014. Pollination syndromes in a Caatinga plant community in northeastern Brazil : seasonal availability of floral resources in different plant growth habits. Brazilian Journal of Biology 74:62–71. Razgour, O., C. Korine, and D. Saltz. 2010. Pond characteristics as determinants of species diversity 78
and community composition in desert bats. Animal Conservation 13:505–513. Reis, N. R. dos, A. L. Peracchi, W. A. Pedro, and I. P. de Lima. 2007. Morcegos do Brasil. Page Morcegos do Brasil. Universidade Estadual de Londrina, Londrina. Rex, K., B. Czaczkes, R. Michener, T. H. Kunz, and C. C. Voigt. 2010. Specialization and omnivory in diverse mammalian assemblages. Ecoscience 17:37–46. Rocha, E. A., A. Domingos-melo, D. C. Zappi, and I. C. Machado. 2020. Reproductive biology of columnar cacti : are bats the only protagonists in the pollination of Pilosocereus , a typical chiropterophilous genus ? Folia Geobot:1–18. Rocha, P. A., J. Ruiz-esparza, and S. F. Ferrari. 2018. Differences in the structure of the bat community between a cloud forest refuge and a surrounding semi-arid Caatinga scrubland in the northeastern Brazil. Journal of Arid Environments 151:41–48. Rodríguez, P., and H. T. Arita. 2004. Beta diversity and latitude in North American mammals : testing the hypothesis of covariation. Ecography 27:547–556. Sá-Neto, R. J., and J. Marinho-Filho. 2013. Bats in fragments of xeric woodland caatinga in Brazilian semiarid. Journal of Arid Environments 90:88–94. Santos, A. J., T. B. Vieira, and K. D. C. Faria. 2016. Effects of vegetation structure on the diversity of bats in remnants of Brazilian Cerrado savanna. Basic and Applied Ecology 17:720–730. Santos, R. M., A. T. Oliveira-filho, P. V. Eisenlohr, L. P. Queiroz, D. Cardoso, and M. J. N. Rodal. 2012. Identity and relationships of the Arboreal Caatinga among other floristic units of seasonally dry tropical forests ( SDTFs ) of north-eastern and Central Brazil. Ecology and Evolution 2:409–428. Sikes, R. S. 2016. 2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. Journal of Mammalogy 97:663–688. Silva, J. M. C. da, I. R. Leal, and M. Tabarelli. 2017. Caatinga: The Largest Tropical Dry Forest Region in South America. Springer International Publisher, Cham, Switzerland. Silva, L. A. M. da. 2007. Comunidades de morcego na Caatinga e Brejo de Altitude, no agreste de Pernambuco. Dissertação de doutorado. Universidade de Brasília, Brasília. Silva, S. S. P. da, D. Dias, M. A. Martins, P. G. Guedes, J. G. de Almeida, A. P. da Cruz, N. M. Serra- Freire, J. dos S. Damascena, and A. L. Peracchi. 2015. Bats (Mammalia: Chiroptera) from the Caatinga scrublands of the Crateus region, northeastern Brazil, with new records for the state of Ceará. Mastozoologia Neotropical 22. Silva, U. B. T. da, M. Delgado-Jaramillo, L. M. Souza Aguiar, and E. Bernard. 2018. Species richness, geographic distribution, pressures, and threats to bats in the Caatinga drylands of Brazil. Biological Conservation 221:312–322. Soares, F. A. M., P. A. da Rocha, A. Bocchiglieri, and S. F. Ferrari. 2018a. Structure of a bat 79
community in the xerophytic Caatinga of the state of Sergipe , Northeastern Brazil. Mammalia 83:125–133. Soares, F., M. Daher, R. Perrelli, José Armando Torres Moreno, and S. F. Ferrari. 2018b. Note on bats (Mammalia, Chiroptera) in a Restinga area of Rio Grande do Note, Brazil. Pesquisa e Ensino em Ciências Exatas e da Natureza 2:17–22. Sousa, M. A. N. de, A. Langguth, and E. A. Gimenez. 2004. Mamíferos dos Brejos de Altitude Paraíba e Pernambuco. Pages 229–254 in K. C. Pôrto, M. Tabarelli, and I. C. Machado, editors. Brejos de altitude em Pernambuco e Paraíba: história natural, ecologia e conservação. MMA/PROBIO/CNPq, Brasília. Straube, F. C., and G. V. Bianconi. 2002. Sobre a grandeza e a unidade utilizada para estimar esforço de captura com utilização de redes-de-neblina. Chiroptera Neotropical 8:150–152. Streilein, K. E. 1982. Ecology of small mammals in the semiarid Brazilian Caatinga. Annals of the Carnegie Museum of Natural History 51:109–126. Vargas-Mena, J. C., K. Alves-Pereira, M. A. S. Barros, E. Barbier, E. Cordero-Schmidt, S. M. Q. Lima, B. Rodríguez-Herrera, and E. M. Venticinque. 2018a. The bats of Rio Grande do Norte state, northeastern Brazil. Biota Neotropica 18:e20170417. Vargas-Mena, J. C., E. Cordero-Schmidt, B. Rodríguez-herrera, R. A. Medellín, D. D. M. Bento, and E. M. Venticinque. 2020. Inside or out ? Cave size and landscape effects on cave-roosting bat assemblages in Brazilian Caatinga caves. Journal of Mammalogy 101:464–475. Vargas-Mena, J. C., E. C. Schmidt, D. D. M. Bento, B. Rodriguez Herrera, R. A. Medellín, and E. M. Venticinque. 2018b. Diversity of cave bats in the Brazilian tropical dry forest of Rio Grande do Norte state. Mastozoologia Neotropical 18:199–212. Velloso, A. L., E. V. S. B. Sampaio, and F. G. C. Pareyn. 2001. Ecoregiões propostas para o bioma Caatinga. Associação. Associação Plantaaas do Nordeste; The Nature Conservancy do Brasil, Recife. Voigt, C. C., and D. H. Kelm. 2006. Host Preference of the Common Vampire Bat (Desmodus Rotundus; Chiroptera) Assessed By Stable Isotopes. Journal of Mammalogy 87:1–6. Voigt, C. C., and T. Kingston. 2016. Bats in the anthropocene: Conservation of bats in a changing world. Springe International Publishing, New York. Willig, M. R. 1983. Composition microgeographic variation and sexual dimorphism in Caatingas and Cerrado bat communities from northeastern Brazil. Bulletin of Carnegie Museum of Natural History 23:1–132. Willig, M. R. 1986. Bat community structure in South America : a tenacious chimera. Revista Chilena de Historia Natural 59:151–168. Willig, M. R., and M. A. Mares. 1989. Mammals from the Caatinga: an updated list and summary of 80
recent research. Willig, M. R., and M. P. Moulton. 1989. The role of stochastic and deterministic processes in structuring neotropical bat communities. Journal of Mammalogy 70:323–329. Zortéa, M., and F. C. D’arc. 2019. Diversity of three bat assemblages of central Brazil. Mastozoología Neotropical 26:1–7.
Figure D. A view of the Serra do Feiticeiro mountains and "Cacti forest" during the rainy season of 2019 in Lajes, Rio Grande do Norte, Brazil. Photo taken by Juan Carlos Vargas-Mena in 2019.
81
SUPPLEMENTARY MATERIALS
Supplementary Material 1.1. Description of Caatinga habitats selected for bat data collection in the Caatinga of Rio Grande do Norte, northeastern Brazil. Habitat Description Medium Caatinga Xerophytic trees of 7-15m tall with a close canopy during rainy season and forest with a variable density in the arboreal layers. Common vegetation are Poincianella pyramidalis, Mimosa tenuiflora, Ziziphus joazeiro, Myracrodruon urundeuva, Auxemma oncocalyx, Jatropha mollisima, , Bauhinia forficata, Cereus jamacaru, Bromelia laciniosa. These forests are rare in RN and restricted to hillsides or canyons and in protected areas. Shrubby Caatinga In general, consists of dispersed trees (3-8m tall) of Aspidosperma pirifolium, Tabebuia impetiginosa, Amburana cearensis in a matrix of bushes of Poincianella pyramidalis, Mimosa tenuiflora, Jatropha sp., Ruellia sp., and Cnidosculus urens, and open areas with annual herbs and grasses like Aristida sp. Cacti are common components like Cereus jamacaru, Melocactus sp., Tacinga inamoena, Pilosocereus gounellei, and P. pachycladus (Facheiro), the latter, a tree-like cacti can found in large densities in some localities (e.g. Lajes); also terrestrial bromeliad Bromelia laciniosa are found. Riparian Caatinga Plant composition varies among localities but, in general, riparian caatingas in RN are a mixture of Shrubby Caatinga with components of medium Caatinga forest. However, presents typical plant species associated to water bodies that are commonly found alongside natural and artificial water bodies like Licania rigida, Tabebuia aurea, Cleome spinosa. Trees of P. pyramidalis, M. tenuiflora, Prosopis juliflora, Z. joazeiro, bushes Jatropha sp., Ruellia sp., and cacti C. jamacaru, P. gounellei and P. pachycladus can be found as well. Copernicia groves Palm stands dominated by Copernicia prunifera (Carnauba) of 10-20m high near river courses, lagoons or lakes with a varzea characteristic during the rainy season.
Rocky outcrops Outcroppings of calcareous or granitic rocks that varies in complexity from simple unbroken rock faces to a complex of many fissured rock faces studded with patches of Caatinga vegetation including cacti (Pilosocereus gounellei), clusters of terrestrial bromeliads (Encholirium spectabile, Bromelia lacinosa), Senna sp. and C. urens bushes, and dispersed trees of P. pyramidalis and Tabebuia aurea trees are commonly found.
82
Humid forest Evergreen and semideciduous forest enclaves found on mountains (>500m enclave altitude) surrounded by Caatinga vegetation with a canopy of 10-20m with trees of Ficus sp., Brosium sp., Copaifera sp., Senegalia polyphylla, Hymenaea sp., Contortisiliquum sp., Anacardium occidentale, Entherolobium sp., Psidium guajava, Spondias sp., Annona squamosa; Syagrus coronata palms, Ruellia sp. bushes, Cereus jamacaru cacti, with Cayoponia sp., Ipomea sp and Mucuna sp vines and epiphyte bromeliads and orchids with non-native species like Mangifera indica, Musa sp., and Artocarpus heterophyllus are found.
Supplementary Material 1.2. Nights sampled, total capture effort (hours [h] of mist nets exposure multiplied by the area [m2] of each mist net, richness, abundance and abundance with effort correction [captures N / (mist netting hours * meters2) * 1000] of bats captured in six areas of Caatinga in Rio Grande do Norte, northeastern Brazil from 2017-2019.
Effort Total Nights Bat corrected Site Effort Richness sampled abundance Bat (h.m2) abundance Açú National Forest (ANF) 6 14198.8 10 76 48.6 Seridó Ecological Station (SES) 10 22612.5 11 96 43.8 Furna Feia National Park (FFNP) 6 14068.8 9 42 22.4 Felipe Guerra (FG) 14 27102.5 16 326 202.4 Martins (MAR) 5 14267.5 11 268 103.2 Lajes (LAJ) 58 150175.0 18 767 107.2 Total 99 242425.0 31 1575
Supplementary Material 1.3. Nights sampled, total capture effort (hours [h] of mist nets exposure multiplied by the area [m2] of each mist net, richness, abundance and abundance with effort correction [captures N / (mist netting hours * meters2) * 1000] of bats captured in seven different habitats of Caatinga in Rio Grande do Norte, northeastern Brazil from 2017-2019.
Total Nights Bat Effort corrected Bat Caatinga Habitat Effort Richness sampled abundance abundance (h.m2) Riparian 43 111406.3 21.0 407 196.0 Shrubby 26 62833.8 17.0 534 224.3 Medium Caatinga Forest 10 25868.8 10.0 86 33.5 Rocky Outcrops 10 18205.0 15.0 188 113.7 Copernicia groves 5 13321.5 10.0 88 31.1 Humid forest enclave 3 7605.0 11.0 235 93.4 Orchards and gardens 2 3185.0 6.0 37 35.2 Total 99 242425.3 31 1575
83
Supplementary Material 1.4. Portrait of all bat species recorded in this study, in the Caatinga of Rio Grande do Norte from 2017-2019. Species number are: Gleaning Animalivores: (1) Micronycteris megalotis, (2) Micronycteris sanborni, (3) Micronycteris schmidtorum, (4) Tonatia bidens, (5) Trachops cirrhosus; Frugivores: (6) Artibeus lituratus, (7) Artibeus planirostris, (8) Carollia perspicillata, (9) Platyrrhinus lineatus, (10) Sturnira lilium; Aerial Insectivores: (11) Peropteryx macrotis, (12) Pteronotus gymnonotus, (13) Eumops sp., (14) Promops nasutus, (15) Molossus molossus, (16) Neoplatymops mattogrossensis, (17) Molossops temminckii, (18) Myotis lavali, (19) Rhogeessa hussoni; Nectarivores: (20) Anoura geoffroyi, (21) Glossophaga soricina, (22) Lonchophylla mordax, (23) Lonchophylla inexpectata, (24) Xeronycteris vieirai; Omnivores: (25) Phyllostomus discolor, (26) Phyllostomus hastatus; Piscivores: (27) Noctilio leporinus; Sanguinivores: (28) Desmodus rotundus, and (29) Diphylla ecaudata.
84
Supplementary Material 1.5. Results of the similarity percentage analysis (SIMPER) for comparisons of the Bray Curtis dissimilarity index between mean abundance of bats in Açú National Forest (ANF), Furna Feia National Park (FFNP), Felipe Guerra (FG), Lajes (LAJ), Martins (MAR), and Seridó Ecological Station (SES) in Rio Grande do Norte State, Brazil. The table indicates average dissimilarity (Av.dissim), percentage of contribution to dissimilarity (Contrib.%), cumulative percentage (Cum. %), and mean abundance of each species per surveyed area. Av. Contrib. Cum. Mean Mean Mean Mean Mean Mean Taxon dissim % % ANF FFNP FG LAJ MAR SES Artibeus planirostris 26.02 41.120 41.12 3.38 1.49 6.98 1.09 12.5 1.5 Myotis lavali 5.305 8.384 49.51 0.563 0.0711 0.0408 0.0333 0 1.55 Desmodus rotundus 4.828 7.631 57.14 0.0704 0.498 2.04 0.593 0.35 0.0442 Glossophaga soricina 3.987 6.301 63.44 0.845 0.213 1.18 0.786 0.701 0 Lonchophylla mordax 3.078 4.865 68.3 0.0704 0 0.735 0.779 0.0701 0.31 Sturnira lilium 2.762 4.365 72.67 0 0 0 0 2.03 0 Carollia perspicillata 1.712 2.706 75.37 0 0.0711 0 0 1.12 0 Platyrrhinus lineatus 1.608 2.542 77.92 0.0704 0 0.0408 0 1.05 0 Phyllostomus discolor 1.439 2.274 82.65 0 0.355 0.286 0.0533 0 0 Xeronycteris vieirai 1.35 2.133 84.78 0 0 0 0.479 0 0 Micronycteris sanborni 1.272 2.010 86.79 0 0 0.0817 0 0 0.398 Peropteryx macrotis 1.147 1.813 88.61 0 0 0.531 0.113 0 0 Trachops cirrhosus 0.9501 1.502 90.11 0.141 0 0.286 0.18 0 0.0442 Diphylla ecaudata 0.9497 1.501 91.61 0.0704 0 0.367 0.127 0 0 Tonatia bidens 0.7403 1.170 92.78 0 0.0711 0.122 0.2 0 0 Neoplatymops mattogrossensis 0.6723 1.063 93.84 0 0 0 0.00666 0 0.221 Pteronotus gymnonotus 0.5745 0.9079 94.75 0.141 0 0.163 0.00666 0 0 Artibeus lituratus 0.5714 0.9031 95.65 0 0 0 0 0.421 0 Noctilio leporinus 0.4898 0.7741 96.43 0 0 0.204 0 0.0701 0.0442 Anoura geoffroyi 0.4762 0.7526 97.18 0 0 0 0 0.35 0 Micronycteris schmidtorum 0.4713 0.7449 97.92 0 0.0711 0.163 0 0 0.0442 Promops nasutus 0.2318 0.3663 98.29 0 0.0711 0 0 0 0 Eumops sp. 0.2318 0.3663 98.66 0 0.0711 0 0 0 0 Phyllostomus hastatus 0.1905 0.3010 98.96 0 0 0 0 0.14 0 Noctilio sp. 0.1717 0.2713 99.23 0 0 0.0408 0 0 0.0442 Rhogeessa hussoni 0.15 0.237 99.47 0 0 0 0.0533 0 0 Molossops temminckii 0.1326 0.2096 99.68 0 0 0 0 0 0.0442 Lonchophylla sp 0.1118 0.1767 99.85 0 0 0.0408 0.02 0 0 Micronycteris megalotis 0.07498 0.1185 99.97 0 0 0 0.0266 0 0 Molossus molossus 0.01874 0.0296 100 0 0 0 0.00666 0 0
85
Supplementary material 1.6. Results of the similarity percentage analysis (SIMPER) for comparisons of the Bray Curtis dissimilarity index between mean abundance values between the Rainy and Dry season in Lajes from 2017-2019 in Rio Grande do Norte State, Brazil. The table indicates average dissimilarity (Av.dissim), percentage of contribution to dissimilarity (Contrib.%), cumulative percentage (Cum. %), and mean abundance of each species per season.
Av. Contrib. Cumulative Taxon Mean RAIN Mean DRY dissim % % Artibeus planirostris 7.542 21.59 21.59 0.555 1.43 Glossophaga soricina 4.722 13.52 35.10 0.72 1.02 Xeronycteris vieirai 3.855 11.03 46.13 0.689 0.527 Lonchophylla inexpectata 3.723 10.66 56.79 0.601 0.649 Desmodus rotundus 3.441 9.849 66.64 0.434 0.714 Trachops cirrhosus 3.013 8.623 75.26 0.469 0.11 Lonchophylla mordax 2.518 7.207 82.47 0.731 0.87 Peropteryx macrotis 1.657 4.743 87.21 0.00813 0.198 Diphylla ecaudata 1.55 4.436 91.65 0.033 0.196 Tonatia bidens 0.887 2.539 94.19 0.15 0.221 Rhogeessa hussoni 0.7997 2.289 96.47 0.00813 0.0853 Phyllostomus discolor 0.4775 1.367 97.84 0.0325 0.0488 Micronycteris megalotis 0.4128 1.182 99.02 0.0336 0.0247 Myotis lavali 0.3413 0.9768 100 0.0163 0.0371
86
Supplementary Material 1.7. Panoramic photographs of the habitat sampled for bats in this study in the Caatinga dry forest of Rio Grande do Norte, Brazil from 2017-2019. Habitats are: Medium Caatinga forests during the rainy (A1) and dry season (A2).
87
Supplementary Material 1.8. Panoramic photographs of the habitat sampled for bats in this study in the Caatinga dry forest of Rio Grande do Norte, Brazil from 2017-2019. Shrubby Caatingas in areas dominated by cacti in the dry season (B1) and in areas dominated by shrubs and grasses in the rainy season are shown.
88
Supplementary Material 1.9. Panoramic photographs of the habitat sampled for bats in this study in the Caatinga dry forest of Rio Grande do Norte, Brazil from 2017-2019. Riparian Caatingas during the rainy (C1) and dry (C2) seasons are shown.
89
Supplementary Material 1.10. Panoramic photographs of the habitat sampled for bats in this study in the Caatinga dry forest of Rio Grande do Norte, Brazil from 2017-2019. Calcareous (D1) and granitic (D2) rocky outcrops or Lajedos are shown.
90
Supplementary Material 1.11. Panoramic photographs of the habitat sampled for bats in this study in the Caatinga dry forest of Rio Grande do Norte, Brazil from 2017-2019. Copernicia Groves or Carnaubais (E1); and Humid Forest enclaves or Brejo de altitude (F1) are shown.
91
Supplementary Material 1.12 Studies on Bat assemblages in the Caatinga from year 1983 to 2020. Caatinga ecoregions are: Northern Sertanejan Depression (NSD), Ibiapaba- Araripe Complex (IAC), Southern Sertanejan Depression (SSD). Trophic guilds acronyms are: frugivores (F), nectarivores (N), omnivores (O), insectivores (I) and sanguinivores (S). Species acronyms are: Artibeus planirostris (Ap), A. lituratus (Al), A. obscurus (Ao), Carollia perspicillata (Cp), Desmodus rotundus (Dr), Glossophaga soricina (Gs), Myotis lavali (Ml), Micronycteris sanborni (Msa), Noctilio leporinus (Nl), Phyllostomus discolor (Pd), Platyrrhinus lineatus (Pl), Pternotus personatus (Ptp), Lonchophylla mordax (Lm), L. inexpectata (Li), Sturnira lilium (Sl), Trachops cirrhosus (Tc), Xeronycteris vieirai (Xv).
Dominant Caatinga Total Abundance Effort Authors Richness Seasonality? trophic Most abundant species Ecoregion captures (m2h) Dry rainy guild Willig 1983 NSD 33 ~5000 N/I N/I N/I F, N -Gs, Cp, Pl, Ap N/I Silva 2007 BH 21 587 214 373 No F, N -Ap Pl Gs N/I Gregorin etal. 2008 IAC 22 191 N/I N/I N/I F, S -Ap, Cp, Sl, Pl, Dr, N/I
Sa-Neto & Marinho-Filho SSD 31 651 N/I N/I N/I F, O, N -Ao, Ap, Pd, Gs 259 200 2013
Novaes & Laurindo 2014 IAC 24 200 N/I N/I N/I F, N, I -Cp, Pl, Gs 48 600 Nogueira et al. 2015 SSD 29 243 N/I N/I N/I S, F, N, O -Dr, Ap, Gs, Pd, Cp N/I Silva et al. 2015 IAC 23 347 107 241 yes F -Cp, Ap, Ptp, Al 185 790 Novaes et al. 2015 IAC 20 126 46 80 yes I, P, F -Ml Nl Ap 48 600 Beltrão et al. 2015 BH 19 126 N/I N/I N/I F, I, -Cp, Pl, Gs 3663 Feijó & Rocha 2017 NSD 26 205 N/I N/I N/I F, N, I -Ap, Cp, Msa, Gs, Ml, Tc 31 500 Soares et al. 2018 SSD 15 104 31 73 yes N, F -Gs, Cp 95 040 Rocha et al. 2018 BH 12 157 69 88 yes F, N, S -Cp, Gs, Dr 185 790 This study (Lajes+Martins) NSD 21 808 N/I N/I N/I F, N, I -Ap, Dr, Gs, Ml 77 982.5 This study BH 24 767 310 457 No N, F, S -Ap, Gs, Lm, Li, Xv, Dr 164442.5 (FFNP+SES+ANF+Felipe Guerra)
92
93
Chapter 2
Seasonal structure and reproductive patterns of cave-dwelling bat assemblages in Caatinga dry forests in northeastern Brazil
Authors: Juan Carlos Vargas-Mena1, Eugenia Cordero-Schmidt1, Bernal Rodríguez- Herrera2, and Eduardo Martins Venticinque1
1 Departamento de Ecologia, Universidade Federal do Rio Grande do Norte, 59078900 Lagoa Nova Natal, RN, Brasil. 2 Escuela de Biología, Universidad de Costa Rica, 2060 Montes de Oca, San José, Costa Rica.
94
ABSTRACT
The Caatinga dry forest is endemic to northeastern Brazil, presents extreme climatic conditions with semiarid characteristics and unique precipitation regime, hence directly influencing the plant phenology of a wide variety of vegetational physiognomies. Caves are an important roost for bats in the Caatingas and some regions harbor large densities of caves in karstic areas like in Rio
Grande do Norte state (RN) with the occurrence of more than 1000 caves. We monitored nine caves in the Caatinga of RN to examine the effects of the seasons and cave size on the richness and species composition of cave-dwelling bats. Using two methods we recorded 17 bat species, captured 2020
(mean: 517 indiv.) and observed 3200 (mean 754) individuals in 61 sampling days. Richness and species composition did not change seasonally and no temporal turnover of species was found.
However, the species composition was different between the large- and small-sized caves. An increase in the overall bat abundance and in some species (insectivores and piscivores) was found mostly at the end of the rainy season. In two caves, peaks of high bat abundance were found from 1-
3 months after peaks of precipitation while during the driest months the abundance decreased. During the rainy season large caves tended to vary more and have higher bat abundance than small caves possibly by a larger load capacity inside large caves than in small. Seasonally abundance increase is likely attributed to reproductive purposes and regional food abundance. Most of the species were reproductively active during the rainy season where their preferred food is more abundant (for frugivores, insectivores and animalivores), while other species that can exploit year-round food resources were reproductive active during both season (sanguinivores, omnivores and unexpectedly nectarivores). Mist nets and direct observation are good complementary methods to detect structural change in diversity and species composition of cave roosting bats but efficient when encountering large bat colonies. The results of this study, besides comparing two traditional methods, provides novel insights of the structural and reproductive patterns of Caatingas’ cave bats and important data to improve conservation actions of these flying mammals in this semiarid tropical dry forest.
95
Key Words: abundance, cave-roosting bats, direct observation, mist nets, richness, species composition
INTRODUCTION
Seasonal Dry Tropical Forest (SDFT) are environments with harsh abiotic factors characterized to be hot, with limited water and an extremely variable but often sparse resources
(Dirzo et al. 2011). In the Caatinga, the largest dry forest of south America, small mammals seems to lack pronounced physiological adaptations and instead exhibit behavioral responses in order to compensate for limiting resources, especially during the dry season (Streilein 1982). The Caatinga dry forest is endemic to northeastern Brazil, presents extreme climatic conditions with semiarid characteristics and unpredictable and unique precipitation regime, hence directly influencing the plant phenology of a wide variety of vegetational physiognomies (Prado 2003, Silva et al. 2017).
Plants in the Caatinga are evergreen and produce flowers and fruits during the short rainy season, while in the long dry season plants are deciduous but some species retain their leaves and can produce flowers and fruits (Leal et al. 2003). Consequently, insects present a seasonal abundance synchronized with the rainy season (Júnior and Schlindwein 2005, Vasconcellos et al.
2010). Thus, bats in the Caatinga are under strong constraints considering the fluctuation on food and water resources throughout the year in this semiarid environment but poor is the knowledge of this behavioral adaptations in Caatinga’s bats and how this affects the structure in the assemblages of this flying mammals (Carmignotto and Astúa 2017).
Caves are an important roost resource for bats in the Caatinga and almost a third of
Caatingas` bats are found to dwell in underground cavities (Guimarães and Ferreira 2014, Nogueira et al. 2014, Oliveira et al. 2018, Silva et al. 2018). Some regions in the Caatinga are known to harbor large densities of caves in karstic areas, such as in the state of Rio Grande do Norte (RN).
Located in the northeasternmost region of Brazil, RN has a high speleological potential and more than 1000 underground cavities has been recorded were large clusters of caves (100-300 caves) can
96 be found in central and western portion of the state (Bento et al. 2013, 2015, 2017). Bat assemblages in these cave clusters in RN has been recently received attention and studies have found a diverse cave bat fauna (16 spp.), with some large bat aggregations (1000-10 000 indiv.), and important roosts for vulnerable and endemic bat species in Brazil (e.g. Lonchorhina aurita,
Natalus macrourus, Furipterus horrens and Xeronycteris vieirai) (Cordero-Schmidt et al. 2017,
Vargas-Mena et al. 2018).
In general, caves and underground cavities are commonly used by a wide array of species due to the permanent and stable roost conditions that provide protection against predators and adverse climate (Kunz 1982). This allows optimal conditions to focus on key social interactions, reproduction and breeding (Kunz 1982). Particularly in the neotropics, caves have been reported hosting more than 10 species and some with large aggregations (Arita 1993, Guimarães and Ferreira
2014, Pérez-Torres et al. 2015, Felix et al. 2016, Vargas-Mena et al. 2018). The reasons of this large diversity of cave bats has been attributed to variables related to size and geomorphology of the cave roost. Larger and more geomorphologically complex caves tend to harbor much more diverse bat assemblages than relatively smaller caves (Arita 1996, Brunet and Medellín 2001, Cardiff 2006,
Niu et al. 2007, Luo et al. 2013, Phelps et al. 2016, Torquetti et al. 2017). As well in karstic landscape with large amount of clustered caves, the species composition of cave bats can vary depending on cave size as well (Vargas-Mena et al. 2020).
Considering that caves are an important roost resource for bats in the Caatinga, studies on this assemblages are scarce but have provided valuable information on species diversity (Trajano and
Gimenez 1998, Gregorin and Mendes 1999, Silva and Guedes 2001, Gregorin et al. 2008, Sbragia and Cardoso 2008), community ecology (Oliveira et al. 2018, Vargas-Mena et al. 2018, 2020,
Otálora-Ardila et al. 2019), natural history (Uieda et al. 1980, Cordero-Schmidt et al. 2016, 2017), and new species records and distribution (Leal et al. 2012, 2018, Rocha et al. 2013, 2014, Basílio et al. 2017). Despite that some of these studies described the reproductive biology for various species
(Trajano and Gimenez 1998, Gregorin and Mendes 1999, Silva and Guedes 2001, Cordero-Schmidt
97 et al. 2017, Gomes et al. 2018), yet poor is the knowledge of the reproduction patterns between the seasons, a seemingly important factor affecting the reproductive patterns of Caatinga’s bats (Willig
1983).
In neotropical bats, patterns of reproductive timing can vary depending on the species (Durant et al. 2013). Some can display aseasonal patterns of reproduction while most species synchronizes their reproduction with periods of more food availability and in some degree to the seasonality of rainfall (Racey and Entwistle 2000). In Caatinga, Willig (1985) found that frugivorous bats (e.g.
Artibeus planirostris) weaned their young primarily during the rainy season, while nectarivores
(e.g. Glossophaga soricina) weaned the first litter during the dry season and the second during the rainy season. The piscivore Noctilio leporinus exhibited unimodal (single annual peak) reproduction in the rainy season while the hematophagous Desmodus rotundus presented an amodal reproduction
(reproductively active year-round). This differences between trophic guilds in their reproductive timing is strongly related to moments of higher availability of food in order to meet the large energy demands of lactation and growth of pups and young (Racey 1982). ). Nevertheless, the knowledge of the reproductive patterns of multiple other species of bats in the Caatinga remains scarce.
The objective of this study is to evaluate the effect of the season and the size of the cave roost in the richness, abundance, species composition of cave-dwelling bats during the dry and rainy season in the Caatinga dry forest of Rio Grande do Norte State, northeastern Brazil, using two different sampling methods. Finally, we wanted to describe and analyze the reproduction patterns of the cave bat assemblages between the rainy and dry seasons. We expect that during the rainy season will be higher 1) the species richness and 2) the overall abundance in the caves. We also expect 3) a variation on the species composition between seasons independently of the cave size. Phytophagous
(frugivorous and nectarivorous), animalivorous and insectivorous bats will present a higher abundance inside caves due to more food availability (e.g. nectar, fruits, insects) during the rainy season in the landscape. Instead, hematophagous bats will present no changes in their abundance since blood is available all year (e.g. Cattle, goats, pigs), as well omnivorous bats will present no
98 seasonal abundance changes due to their food selection flexibility (Ferreyra-García et al. 2018).
Finally, we expect that 4) that both male and females will be reproductive active during only during the rainy season, especially phytophagous, and insectivorous bats, while those who rely in year- round food resource will not have seasonal reproduction patterns.
METHODOLOGY
Study area
From August 2017 to May 2019, we surveyed nine caves distributed in four localities,
Lajes, Felipe Guerra, Martins and Furna Feia National Park (FFNP), all within the Caatinga of Rio
Grande do Norte State (Fig. 2.1). The Caatinga dry forest comprehends almost 90 % of RN’s territory. The climate is predominantly BSh' type (Köppen) characterized by very hot weather and semi-arid. Rainfall is irregular and occur from January to May (can extend to June or July) with highest peaks from march to May and the average annual rainfall ranges from 400 mm in Lajes to
900 mm in Martins (Diniz and Pereira 2015). Extension of dry season is subject to interannual variation with some extensive droughts (Prado 2003).
Of the nine surveyed caves (Table 2.1), six are located in the karstic landscapes of Felipe
Guerra (Gruta do Três Lagos, Gruta do Pau, Gruta da Carrapateira, Caverna do Urubu, Gruta Casa de Homens) and FFNP (Furna Feia). These landscapes are characterized to harbor calcareous rocky outcrops with numerous underground cavities, sinkholes, faults, fractures, among other typical karstic features, thus, high cave densities are found – 200-400 caves in a single region (Bento et al.
2013, 2015). Two caves (Xero Xero and Serrote Preto) in Lajes are granitic and located in the Serra do Feiticeiro, a quartzitic mountain of about 400m of altitude, and one cave (Casa de Pedra) in
Martins found in a marble inselberg. Both areas of Lajes and Martins harbor great diversity of underground as well, but these areas have been less studied in speleological prospections (D. M.
Bento com. pers.). In general, cave are embedded on a matrix composed by mosaics of scrubby vegetation and deciduous forest stands of thorny and xerophytic woody plants, annual herbs in
99 semi- and open areas, many succulents of small and columnar Cacti, and clusters of terrestrial bromeliads that represent most of the vegetational features of the Caatinga dry forest (Prado 2003,
Queiroz et al. 2017).
Figure 2.1. Map of the location A) of the nine caves surveyed in this study, the location of Rio Grande do Norte in Brazil B) and in the Caatinga dry forest C).
Bat data collection
Caves located in Felipe Guerra, FFNP and Martins were surveyed during four days (two in the dry and two in the rainy season) for a total 28 days distributed in 14 days for each season
August 2017 to April 2019. Two caves in Lajes were surveyed once a month (16-17 days each) from September 2017 to February 2019 in a total of 32 sampling days. In each sampling day we conducted to type of methodologies to detect the richness, abundance and species composition – active search through observation and captures of bats, when possible. Although the seasons in
Caatinga can changes in length depending on the region, we arbitrarily determined the rainy season from January to June and the dry season from July to December, based on Diniz and Pereira (2015).
100
Table 2.1. Studied caves from August 2017 - April 2019 in the Caatinga of Rio Grande do Norte, Brazil. Coordinates, cave lithology and number of sampling days per cave is shown.
Coordinates Sampling Locality Cave name Lithology Size Latitude Longitude days Furna Feia Furna Feia -5.036878 -37.560177 National Park Limestone Large 4
Felipe Guerra Gruta dos Três Lagos -5.593288 -37.687155 Limestone Small 4 Gruta do Pau -5.592837 -37.687933 Limestone Small 4 Gruta da Carrapateira -5.560618 -37.663979 Limestone Large 4
Caverna do Urubu -5.573047 -37.65242 Limestone Large 4
Gruta Casa dos Homens -5.576272 -37.573807 Limestone Small 4
Lajes Caverna do Cerrote Preto -5.796675 -36.240747 Granite Small 16
Abrigo Xero-xero -5.797372 -36.240958 Granite Small 17
Martins Casa de Pedra -5.212322 -37.264153 Marble Large 4
In each cave, we applied two methods, during the day we counted bats through direct observation, and during night we used mist nest to capture emerging individuals. The observation method was through an active search where individuals were counted. Counts through direct observation is the most straightforward method for identifying colonies and counting of roosting individuals during a specific period of time in caves and mines and conducting it during the day ensures that all the bats that were found at that moment are using the cave as day roost (Kunz et al.
2009). We carefully and silently toured all the accessible areas of the cave using red-light headlamps, binoculars and digital cameras (Nikon D3300, D5600 and Sony DSC H300). When we encountered colonies of more than 10 individuals, during the first 10 seconds of the encounter, we took pictures with the camera for a more reliable counting on the camera screen. Due to the fact that there are species and individuals that are less tolerant to the nearby human presence, the fact of taking a photograph quickly towards the group, allows us to have a higher certainty of counting a larger number of individuals through the camera, and thus avoid losing individuals that might flee
101 away while counting through direct observation. Cave passages, halls, roofs and walls were counted only once and the active search was effectuated during two to three hours (from 13:00 to 16:00h), depending on cave size and access difficulties.
The capture method was done using mist-nets deployed at cave entrance, or entrances, from
17:30 to 24:00hrs. Deployment of mist nets were only at cave entrances and the number and size (3-
12m) of mist-nets depended on the size of the cave entrance. In multiple entrance caves, entrances were covered with plastic tarp and blocked any other possible exit holes or cracks in order to persuade bats to emerge into the mist-net sites. This strategy was also used in caves with large colonies (>1000 indiv.), but despite the fact that the capture of all individuals of a large colony is not plausible, covering other entrances and possible exit holes or cracks let us to capture a largest sample of individuals of the colony. Captures inside caves was not done due to license restrictions.
Bat species were classified into a trophic guild using the available natural history information about the primary diet of the bats in Brazil (Reis et al., 2007; Reis et al., 2013). Guild categories where based on Hill and Smith (1984). However, we substituted the foliage-gleaning insectivorous and carnivorous guilds for gleaning animalivorous guild since bats belonging to these guilds can have both insectivore and carnivore diet (e.g. Tonatia bidens, Trachops cirrhosus,
Chrotopterus auritus) (Gardner, 2007). Guilds were: aerial insectivores, gleaning animalivores, piscivores, frugivores, nectarivores, omnivores, and sanguinivores.
The reproduction status was obtained only from the captured individuals. For each individual, we collected data of sex, age (adult or juvenile), weight, morphometric measurements
(forearm size, ears, tragus, hind leg) and reproductive status, (Willig 1985a, Simmons and Voss
2009). Age was determined by observing the fusion of epiphysis-shaft of the fourth metacarpal- phalangeal joint (Anthony, 1988). The reproductive condition of males was determined by the position of the testes, considering them reproductive when testicles where in scrotal position
(escrotated) or non-reproductive when they were in abdominal position. The reproductive status of females was classified by observing and touching the belly and nipples to categorize them into:
102 non-reproductive (NR), pregnant (P), lactating (L) and post-lactating (PL) (Racey, 1982).
Observations of female carrying a pup was implied as lactants.
Bat capture and handle protocols followed the guidelines of the American Society of
Mammalogists for the use of wild mammals in research (Sikes 2016). Bats were identified using the identification keys of South American bats (Díaz et al. 2016). Collected individuals were deposited in the Prof. Adalberto Varela Mastozoological Collection (CMAV) of the Universidade Federal do
Rio Grande do Norte. The survey and collection of specimens were allowed by the Brazilian environmental agency (SISBIO license number 48325-2 MMA, IBAMA and ICMBIO). Taxonomy and nomenclature followed (Nogueira et al. 2014).
Surveyed caves where arbitrarily placed into two categories of relatively size (large and small) based on the topographic data available for each cave were taken from the National Register of Speleological Information (Portuguese acronym CANIE, https://www.icmbio.gov.br/cecav/canie.html), a database of the National Center of Research and
Conservation of Caves of Brazil (CECAV). Caves that presented a linear development greater than
200 m where categorized as large while those <200m were set as small caves. The linear development is the distance measured along the axis oriented parallelly of the longitudinal directions of all galleries and continuous depths, whatever their inclinations. We did not use in intermediate size category (e.g. medium size caves) to avoid an unequal distribution in the number of caves in each category due to the small number of caves. Thus, four caves were categorized as large and five as small caves (see table 2.1).
Statistical Analyses
To test if there were differences in the overall richness and abundance between the seasons in all of the caves, we apply a paired T-test. Then, we separated the data obtained from each method and examined separately if a variation in the richness and abundance was related to the cave size and/or the seasons. An ANCOVA was performed to test the effect on the richness and an analysis of variance (ANOVA) for the abundance.
103
To assess if there were a variation in the species composition, we constructed distance matrices based on the proportion of species shared between the nine surveyed caves, between large and small caves and between seasons, using the Bray-Curtis index of similarity. This was done separately for the observation data, the captured data, and with a presence/absence matrix using the detection of both methods. Then for each Bray Curtis matrices, we performed Non-Metric
Multidimensional Scaling (NMDS) checking the stress of the ordination (Kruskal, 1964). The stress is a measure of the fit between the final solution of the analysis and the original distance matrix of the assemblage. To assess the relation of the ecological similarity between the species composition between the surveyed caves, between large and small caves and between the seasons, we performed an analysis of similarities (ANOSIM) with 900 permutations with a significance level of α = 0.05.
This was done for each variable of the capture, observation and presence/absence data. In these analyses we considered only caves with more than 10 captured individuals, and excluded the species that occurred with less than 5 individuals. Then a similarity percentage analysis (SIMPER) was performed for only the matrices that the ANOSIMs indicated a significant dissimilarity. The
SIMPER estimated the weight of each species in the assemblage dissimilarity between each surveyed cave, seasons (dry/rainy), caves size (large/small). Because the caves Serrote Preto and
Abrigo Xero-Xero caves presented a larger number of sampling nights than the others, we calculated the mean abundance per season of each year for each of the methods (captures and observation) in order to standardize the number of samplings between all caves. All analyses were performed separately for each of the applied methods (capture and observations) to see if there were differences in the richness, abundance and species composition patterns between the sampling methods.
To describe and explore the dynamics of the bat abundance throughout the sampled years, we used only the data from Serrote Preto and Abrigo Xero-Xero caves which were monitored once a month for 16 to 17 months, respectively. We used only the data of the observation method to obtain the mean overall bat abundance of each cave and the mean abundance of the most common
104 species recorded, since we were not able to capture every month. We obtained data of precipitation from the online data base of rainfall of Rio Grande do Norte State from the Empresa de Pesquisa
Agropecuárias do Rio Grande do Norte (EMPARN) from 2017-2019.
(http://meteorologia.emparn.rn.gov.br:8181/monitoramento/monitoramento.php). Then we graphically overlapped the abundance data with the mean monthly precipitation of Lajes in order to explore the abundance of bats in these caves throughout the sampled months.
Finally, the reproductive status patterns were analyzed separately for each trophic guilds and bat species, we used a maximum likelihood significance test, or G-test to see if significative differences were found between seasons. The test was done only for the most common captured species (eleven species) but we included all captured species when testing it by trophic guild. All analyses where done using SYSTAT software version 12.
RESULTS
Effect of season and cave size on richness and abundance
We recorded 17 species in six families (Emballonuridae, Phyllostomidae, Noctilionidae,
Mormoopidae, Natalidae, and Furipteridae) belonging to seven trophic guilds (Table 2.1 and
Supplementary material 2.1). Caves with the highest overall richness were Serrote Preto (10 spp.) and Furna Feia (9) and the lowest was the Abrigo Xero Xero (4) (Supplementary Material 2.2.) The mean richness all caves in the dry season was of 6.33 ± 1.6 species and in the rainy of 6.44 ± 1.7 species. No significant differences in the richness were found between the seasons neither in the capture (F= 0.20106, df = 2, p = 0.81942) nor in the observation methods (F = 0.15677, df = 2, p =
0.85581). As well, the both cave size (Supplementary Material 2.3) and seasons did not affect the species richness neither in the capture nor in the observation methods (Supplementary Material 2.4)
.
105
Table 2.2. Richness, mean abundance and species composition of cave-dwelling bats in nine Caatinga caves in Rio Grande do Norte, Brazil from 2017-2019. Mean abundance data is shown for captures (Capt) and direct observation (Obs). * indicates that the species colony was too large (>5000) to make a visual counting.
Carrapateira Casa Homens Casa Pedra Furna Feia Pau Serrote Preto Tres Lagos Urubu Xero Xero Species Guild Capt Obs Capt Obs Capt Obs Capt Obs Capt Obs Capt Obs Capt Obs Capt Obs Capt Obs Emballonuridae Peropteryx macrotis I 9.2 43.7 13 19 21 2 7.5 3 4.5 2.2 1 1.3 2.5 7.4 Phyllostomidae 88.3 Desmodus rotundus S 12.3 27.2 3.3 2.7 5.3 4 8.7 5.2 1.25 20 99 32 Diphylla ecaudata S 1.7 3.2 2 1.3 1.6 1 2 3 1.75 1 1.7 2 1 1 Glossophaga soricina N 4 2 2.5 3.2 1 1 12.6 2 4.2 2 Lonchophylla inexpectata N 1 Lonchophylla mordax N 1 Xeronycteris vieirai N 1.16 3.2 25.3 Lonchorhina aurita I 2 108.8 1.5 3 * Phyllostomus discolor O 143.8 1 1 >5000 Tonatia bidens A 1 1 67 12 2 Trachops cirrhosus A 9 1 2 Artibeus planirostris F 19 29.3 1.5 17.3 1 3.5 7.2 2 1 1 Carollia perspicillata F 1 Noctilionidae Noctilio leporinus P 7 Mormoopidae * Pteronotus gymnonotus I 98 >9000 Furipteridae Furipterus horrens I 3.2 5.5 30.7 134.7 120.5 1 14.6 1 3 1.5 Natalidae Natalus macrourus I 3 Richness 5 8 6 4 6 9 7 5 10 4 7 6 6 4 6 3 Mean abundance 42.7 100.7 22.7 53.7 181 154.3 147 126.8 7.5 36.8 25 110.75 132 91 6.4 33.5
106
In total we captured 2020 (average: 517 indiv.) and observed 3200 (average: 754) individuals of bats. The bat abundance between the rainy and dry season was significantly different using the observation method (T-test: t = 2.944, df = 13, p = 0.011) and marginally significant with the capture method (t = 1.903, df = 13, p = 0.079). Both methods detected differences in the abundance regarding the cave size (ANOVA, observed: F = 5.94413, df = 1, p = 0.02191; captured:
F= 11.79091, df = 1, p = 0.00201). Both large and small caves presented a higher abundance in the rainy season (Figure 2.2), however large caves tended to vary evidently more than small caves (Fig.
2.4). Moreover, solely on the observation method, a significant interaction between season and cave size was found to affect the bat abundance (F= 6.63524, df = 1, p = 0.01603) (Supplementary
Material 2.4).
Figure 2.2. Abundance of cave bats in large and small caves for each season (rainy and dry) where a) corresponds to captured and b) to observed individuals in nine caves in the Caatinga dry forest of Rio Grande do Norte, Brazil from 2017-2019.
107
Figure 2.3. Graphical ordination of the variation in the abundance of captured and observed bats in small and large caves between the dry and rainy season in nine caves in Rio Grande do Norte, Brazil from 2017-2019.
In caves that were monitored for longer consecutive periods an increase in the abundance was found after one to four months later of the rainiest months in Lajes. In Serrote Preto we found peaks in the overall abundance after two to three months which coincides the rainiest months (Fig.
2.4a). This was consistent for insectivorous bat, where F. horrens (Fig. 2.4c) and P. macrotis (Fig.
2.4d) had the highest abundance (May) after three months of the rainiest month (February).
Similarly, the nectarivore G. soricina (Fig. 2.4e) presented an abundance peaks (June and July) after three to four months of the rainiest months (February-April). The frugivore A. planirostris presented this pattern but only for some abundance peaks (May, August) but other abundance peaks were found in during the middle of the dry season way far from the rainiest months (Fig. 2.4b).
108
Figure 2.4. Mean overall abundance of bats and of the four most abundant species roosting from 2017- 2019 in Serrote Preto cave in Lajes, Rio Grande do Norte, Brazil. Mean monthly precipitation in millimeters (mm).
The Abrigo Xero Xero varied more along the months than in Serrote Preto but still some abundance peaks (in March and May) occurred after one to two three months after the rainiest months (February-March) (Fig. 2.5a). The nectarivore X. vieirai presented abundance peaks
(March, May, June) after one to two three months after the rainiest months (February-March) but two other abundance peaks were found at the end of the dry season (Fig. 2.5b). While P. macrotis
109 did not presented the same patterns as in Serrote Preto cave and abundance fluctuated along the months (Fig 2.5c).
Figure 2.5. Mean overall abundance of bats and of the two most abundant species roosting from 2017- 2019 in Abrigo Xero Xero cave in Lajes, Rio Grande do Norte, Brazil. Mean monthly precipitation in millimeters (mm).
Effect of locality, season and cave size on species composition
Three NMDS ordination were performed, one for the capture method (21% and 22% of the variance in axis 1 and axis 2, respectively; stress = 0.1205;), for the observation method (axis 1 with
44% of variance and axis 2 with 11%; stress = 0.1134) and for the presence/absence (axis 1 with
58% and axis 2 with 11%; stress = 0.1066). Caves were grouped separately in the ordination and assemblages presented different species composition (low polygon overlaps) (Fig. 2.6). The
ANOSIM corroborated the separation of the species composition (capture: R= 0.9593, p < 0.0001; observation: R = 0.8491, p < 0.0001; presence/absence: R= 0.8371, p < 0.0001). In the SIMPER analysis of the observed data (Supplementary Material 2.6), the species F. horrens and D. rotundus contributed the most on the average dissimilarities among the caves with 34.67 % and 30.97%
110
Figure 2.6. NMDS ordination of the species composition of bats in nine caves in the Caatinga of Rio Grande do Norte from 2017-20119, using data of a) observation and b) capture methods, and c) presence/absence data of both methods. Each point represents a cave. ANOSIM’s p-values and ordination stress are shown.
Figure 2.7. NMDS ordination of the species composition of bats between large and small caves in nine caves in the Caatinga of Rio Grande do Norte from 2017-20119, using data of a) observation and b) capture methods, and c) presence/absence data of both methods. Each point represents a cave. ANOSIM’s p-values and ordination stress are shown.
Figure 2.8. NMDS ordination of the species composition of bats between the rainy and dry season in nine caves in the Caatinga of Rio Grande do Norte from 2017-20119, using data of a) observation and b) capture methods, and c) presence/absence data of both methods. Each point represents a cave. ANOSIM’s p-values and ordination stress are shown.
111 respectively (65.64% of the cumulative dissimilarity of all species). Furipterus horrens presented higher mean abundance in Casa de Pedra and Furna Feia caves and D. rotundus in Três Lagos and
Urubu caves.
As for the species composition regarding the categorical sizes of caves (large vs small), the
NMDS ordination show a separation between the sizes (Fig. 2.7) in the capture (ANOSIM: R =
0.2202, p < 0.000), observation (ANOSIM: R = 0.1287, p = 0.0240) and in the presence/absences data (ANOSIM: R = 0.1099, p = 0.0221). In the SIMPER analysis of the captured data
(Supplementary Material 2.7), we found that P. discolor, P. gymnonotus, only occurred in large caves and contributed the most in the dissimilarity with a cumulative percentage of 47.36%. Also,
T. bidens and A. planirostris presented greater abundances in large caves while G. soricina, L. aurita and T. cirrhosus had larger abundances in small caves. With the observation method, the
SIMPER (Supplementary material 2.8) found other species like F. horrens, P. macrotis, D. ecaudata, N. leporinus, and A. planirostris, with greater abundances in large caves, while and X. vieirai, G. soricina, and again T. cirrhosus had larger abundances in small caves.
The species composition between the seasons had no significant differences in none of the methods (Captures: ANOSIM: R= -0.04, p = 0.694; Observation: ANOSIM: R= -0.058, p = 0.9185;
Presence/absence data: ANOSIM: R= -0.03, p = 0.863) (Fig. 2.8). However, differences at species level was found in the abundance between seasons in most of the caves, according to the SIMPER analysis of the observation method (Supplementary material 2.9). The species that contributed the most in the average dissimilarities between seasons were F. horrens (35.11%) and D. rotundus
(29.85 %). The insectivore F. horrens and the piscivore Noctilio leporinus almost tripled their abundance during the rainy season. Seven species (D. rotundus, P. macrotis, A. planirostris,
Xeronycteris vieirai, T. bidens) presented a slighter larger mean abundance in the rainy season.
Trachops cirrhosus and D. ecaudata were the only to doubled their abundance in the dry season.
Other species presented similar mean abundances between the seasons.
112
Reproductive patterns
We found a seasonality in the reproductive activity in three of the six trophic guilds encountered, and in six of the eleven species used in this analysis (Table 2.7). Animalivores presented more pregnant and lactants females in the rainy season (G-test = 22.75, df = 2, p <
0.0001). Frugivores presented more pregnant females in the dry season and more lactant females in the rainy season (A. planirostris, females: G-test = 38.0983, df = 3, p < 0.0001; males: G- test=2.02101, df=1, p=0.15514). Similarly, insectivorous bats presented more pregnant females in the dry season and more lactant females in the rainy season (G-test=125.24, df=2, p<0.0001). this was consistent for L. aurita and P. macrotis, but P. gymnonotus presented more pregnant and lactating females just during the rainy season (G-test=39.6217, df=3, p<0.0001).
Males of most of the guilds were reproductive active in both seasons, except the insectivore
L. aurita (G-test=40.8968, df=2, p<0.0001) where more escrotated males were found in the dry season, while the nectarivore G. soricina presented more escrotated males in the rainy season (G- test=7.69048, df=2, p=0.02138).
Guilds that presented no seasonal reproduction pattern where pregnant and lactant females were found in both seasons corresponded to nectarivores (G-test=1.90, df=4, p <0.75306), sanguinivores (G-test = 4.7343, df = 4, p = 0.31559), and omnivores (G-test=9.00484, df=2, p=0.06098).
113
Table 2.7. The reproduction patterns of trophic guilds and eleven species of bats in nine caves in the Caatinga dry forest of Rio Grande do Norte, Brazil from 2017-2019. Reproductive status for females is: Pregnant (P) and Lactant (L); and for males: escrotated (E). Significant p-values of the maximum likelihood G-test are shown in bold. N/R means that no captured individuals (or less than two) were captured in that reproductive status in that season.
Females Males Species G-test p-value P L G-test p-value E Animalivores 22.75584 <0.0001 Rainy Rainy 1.07227 0.30043 Aseasonal Tonatia bidens 12.67372 0.0054 Rainy N/R 0.7116 0.39891 Aseasonal Trachops cirrhosus 20.7915 0.0001 Rainy Rainy 0.42894 0.51251 Aseasonal
Frugivores 38.0983 <0.0001 Dry Rainy 2.02101 0.15514 Aseasonal Artibeus planirostris 38.0983 <0.0001 Dry Rainy 2.02101 0.15514 Aseasonal
Insectivores 125.24307 <0.0001 Dry Rainy 23.52083 <0.0001 Rainy Lonchorhina aurita 95.0836 <0.0001 Dry Rainy 40.89676 <0.0001 Dry Peropteryx macrotis 35.4390 <0.0001 Dry Rainy 5.54845 0.0624 Rainy Pteronotus gymnonotus 39.62173 <0.0001 Rainy Rainy 0.53284 0.76612 Aseasonal
Nectarivores 1.90589 0.75306 Aseasonal Aseasonal 3.24762 0.19715 Aseasonal Glossophaga soricina 4.2402 0.12002 Rainy Dry 7.69048 0.02138 Rainy Xeronycteris vieirai 6.95857 0.13809 Aseasonal Aseasonal 3.24762 0.19715 Aseasonal
Omnivores 9.00484 0.06098 Aseasonal Aseasonal 1.43624 0.48767 Aseasonal Phyllostomus discolor 9.00484 0.06098 Aseasonal Aseasonal 1.43624 0.48767 Aseasonal
Sanguinivores 4.73493 0.31559 Aseasonal Aseasonal 1.54839 0.67115 Aseasonal Desmodus rotundus 6.2842 0.17891 Aseasonal Aseasonal 1.87293 0.59919 Aseasonal Diphylla ecaudata 1.2750 0.52862 N/R Dry 1.43895 0.23031 Aseasonal
DISCUSSION
Effect of season and cave size on richness
Species richness did not change significantly from one season to another suggesting that
there is not a seasonal increase of species during the rainy season, contrary to our first prediction.
These findings are consistent with cave bat assemblages in Andean foothills in Bolivia (Siles and
Aguirre, 2007), but contrary to what is recorded for some caves in humid forests in Hispaniola
Island (Núnez-Novas et al. 2016). Despite this, the information about seasonal variation in species
114 richness in neotropical caves is scarce and comparison is difficult. More mid and long-term studies are needed in order to better elucidate seasonal richness variation patterns, especially in SDTF.
As well, richness was not affected by caves size, contrary to general findings in other caves systems (Arita 1996, Brunet and Medellín 2001, Cardiff 2006, Niu et al. 2007, Luo et al. 2013,
Phelps et al. 2016, Torquetti et al. 2017). Moreover, in RN, Vargas-Mena et al. (2020) used a similar pool of Caatinga caves (six of the caves used here) and found that larger caves tended to harbor a higher bat richness. However, we found that independently of the size some small caves could be as rich as large caves. For instance, Serrote Preto, a small cave with 10 spp. and Furna
Feia, a large cave with 9 spp. These two caves however presented a very differentiated sampling effort and Serrote Preto was much more sampled than Furna Feia cave (16 vs 4 nights)
It is likely that the fact to have a larger sampling effort in caves is unraveling other factors that might affect as well the overall richness of bats in Caatinga's caves. Due to this larger sampling effort, richness might be more affected by the visit of rare or non-resident species into caves. For instance, in Serrote Preto, only four species formed resident colonies, while few individuals of six species (L. mordax, L. inexpectata, D. rotundus, D. ecaudata, T. cirrhosus, and T. bidens) were solely captured accessing the cave at night, likely using the cave as a night roost. Despite the fact those species are not resident to the cave, the use of the cave as night roost consequently inflates the recorded richness in caves. Night roosts are important for bats because they allow food consumption and digestion and provide a retreat from predators (Kunz 1982). Vargas-Mena et al.
(2020) also found that richness was also affected by the proximity of other caves. When the larger number and proximity of other caves were found nearby, the larger the probability of bats to commute between caves, hence increasing detected richness. This is plausible since all of our studied caves are located in areas with high underground densities.
Effect of season and cave size on abundance
Unlike richness, the overall abundance of the assemblage was significantly higher in the rainy season, consistent with our second prediction, however it was guild and species-specific (e.g. insectivores F. horrens and P. macrotis, nectarivore G. soricina and piscivore N. leporinus) 115
(Supplementary material 2.9). Caves in Lajes (Serrote Preto and Abrigo Xero Xero) showed a fluctuation during the months in their overall abundance (Fig 2.4, 2.5). Different studies have attributed this abundance fluctuation to changes in the abundance of food resources and climatic variables (Torres-Flores et al. 2012, Núñez-Novas et al. 2016, Rocha and Bichuette 2016, Otálora-
Ardila et al. 2019). This is plausible considering the seasonal food resource and climatic changes throughout the Caatinga dry forest (Silva et al. 2017).
Otálora-Ardila et al. (2019) found that in a Caatinga cave occupied by 10 species and large colonies of Mormoopid bats, precipitation was not correlated to changes in the total abundance of bats, and an evident fluctuation in the total abundance was found between months. However, a higher abundance of bats was found at the end of the rainy season that were attributed to regional abundance in food resource. This pattern is similarly to what we found in Serrote Preto in Lajes at the end of the rainy season (May-June) (Fig. 2.3a). For instance, a small colony of the nectarivore
G. soricina (5-10 indiv.) was found year-round in Serrote Preto but a dramatic increase of more than 50 individuals was observed during the transition of the rainy to dry season (June-July), just to return back to the initial colony size in the dry season (Fig. 2.4d). This peak in the abundance coincided with the last flowering peak of the year of three cacti species known to be an important nectar resource for nectarivorous bats in Lajes (see phenological data in Cordero-Schmidt 2020).
This might suggest that individuals are coming from other places to feed on the last flowering peak in the area nearby the Serrote Preto and thus temporally roosting during those months in the cave.
A similar pattern was found for the insectivores F. horrens (Fig. 2.4c) and P. macrotis (Fig.
2.4d). In Serrote Preto, both species had a dramatic increase in their abundance but in May, three months after the rainiest month. Data on seasonal abundance of insects in the Caatinga are scarce but a significant increase after the rainiest months of Coleopterans, Lepidopterans and Dipterans has been found in the Caatinga (Gusmão and Creão-Duarte 2004, Júnior and Schlindwein 2005,
Vasconcellos et al. 2010, Nobre et al. 2012). Although we did not collect data on insect abundance or feces samples, such insect orders are known to be part of the diet of F. horrens and P. macrotis
(Reis et al. 2007) and likely affecting the abundance of this insectivorous bats. Studies on
116 insectivorous bat diet and insect phenology in the Caatinga of Lajes are needed in order to understand better such seasonal dynamic.
Despite the fact that most of the surveyed caves varied in their bat abundance between seasons, the variation presented differences depending on the cave size. Larger caves tended to vary during the rainy season much more in abundance than small caves (Fig 2.3). This is probably because larger caves can have a greater load capacity than small caves by offering more physical space of roosting areas and higher spatial variation in microclimatic roost conditions (temperature and humidity). This might allow larger caves to harbor a wider array of species (Brunet and
Medellín 2001) and to larger number of individuals (Arita 1993, 1996, Kofoky et al. 2007, Niu et al.
2007). In fact, the two largest colonies encountered were found only in relatively large caves, (P. gymnonotus in Furna do Urubu and P. discolor in Furna Feia) (Table 2.1 and 2.2). As well, the largest colonies of F. horrens were found in the largest surveyed caves such as Furna Feia and Casa de Pedra cave (Table 2.2). Nevertheless, monitoring more caves with different sizes are needed in order to better understand if this is a recurrent pattern between the seasons in Caatingas’ cave bats.
Effect of season and cave size on species composition
Our third prediction was partially consistent. We found differences in the species composition between caves and between cave size, regardless of the seasons. We found that there was no variation in the species composition between the rainy and dry seasons and the identity of the species within each assemblage was maintained among the season.
Because the species composition was different between the surveyed caves, this results corroborates the findings of Vargas-Mena et al. (2018), where bat species presented a non-nested distribution in 13 caves (five of which were monitored in this study), with several caves harboring a particular species composition and assemblage structure. The abundant number of caves in these areas of Caatinga in RN are likely offering a large number of potential roosts with different internal structures and microclimates in order to be occupied by a different array of bat species. Indeed, several of these caves harbored year-round colonies of species that were not found elsewhere like
117 the Furna Feia (P. discolor, Natalus macrourus), Casa de Pedra (N. leporinus), Gruta do Urubu (P. gymnonotus), Gruta do Pau (L. aurita) and the Abrigo Xero Xero (X. vieirai).
In the other hand, some species were widespread among caves such as F. horrens and D. rotundus. Interestingly, these two species apparently presented an inverse colony size in the caves they occurred. For instance, in caves with relatively large colonies of F. horrens, D. rotundus either did not occurred or presented small colonies (Supplementary material 2.6). Conversely, in caves with large colonies of D. rotundus, colonies of F. horrens were relatively small. The reason of this patterns is difficult to explain but an antagonistic behavior by D. rotundus might be affecting F. horrens in a way that the species tend to avoid forming large colonies in caves were vampires are abundant.
As well, the species composition was different between the small and large caves and draws the attention that the effect was detected with both capture and observation method (Fig. 2.7). This indicates the size of the cave have an important role structuring the specie composition of cave bats in landscape were caves are abundant, consistent with Vargas-Mena et al (2020). Species like P. discolor, N. macrourus, N. leporinus, P. gymnonotus roosted in relatively large caves while T. cirrhosus and X. vieirai occupied only small ones (Supplementary material 2.7 and 2.8). Because neotropical bat are characterized to have a species-specific preferences in roost microclimatic condition (e.g. temperature and humidity, see Avila-Flores and Medellín 2004), different species can exploit more successfully one type of roost than another species.
Finally, the species composition between the seasons did not change and no seasonal species turnover was found in our studied caves (Fig. 2.8). Concomitantly with the species richness, this seemingly permanence of the same species year-round might be the result of behavioral adaptations that bats present in SDTF such as dietary flexibility (see Cordero-Schmidt 2020), local movements, seasonal changes in forging areas and seasonality in reproduction (Stoner and Timm
2004, 2011). Such adaptations provide advantages to the bats species in the assemblage that makes it unnecessary for most of the individuals of the species to leave or migrate elsewhere.
118
Reproductive patterns
We found a guild -, species - and sex -specific patterns of reproductive activity in the species analyzed herein, where females of the insectivore, frugivores, and animalivores species were active solely active in the rainy season while males of most of the species were active both seasons. In addition, the reproduction activity of the species that presented a seasonality coincided with the increase in their colony size (abundance) like the insectivores F. horrens and P. macrotis, the frugivore A. planirostris and the animalivore T. bidens (Table 2.7 and Supplementary material
2.9). This might provide reproductive benefits since high aggregation increases metabolic rate and roost temperatures that can assists in maintaining conditions necessary for optimum growth of embryos and dependent young (Racey 1982).
Moreover, a fluctuation in the abundance in cave bat species have been attributed to changes in the availability of food resources (Torres-Flores et al. 2012, Núñez-Novas et al. 2016,
Rocha and Bichuette 2016, Otálora-Ardila et al. 2019) which in general entails to a seasonal reproductive activity in bats (Racey 1982, Racey and Entwistle 2000, Kunz et al. 2009). Such seasonal reproductive behavior is to supply the highest moment of energy demand for females, which is lactation and weaning of young (Racey 1982), therefore, species that rely on predictable food availability, like fruits and insects, synchronizes their reproduction activity with moments of high abundance of food resource (Racey and Entwistle 2000).
In Caatinga it has been found that zoochoric plants fructify more during the rainy season
(Machado et al. 1997, Griz and Machado 2001, Amorim et al. 2009), which coincides with the occurrences of more lactating females of the frugivore A. planirostris (Table 2.7). Most of females get pregnant during the dry season and parturition takes place in the rainy season where food abundance is at the highest (Willig 1985). However, in Serrote Preto and Carrapateira caves we observed and captured lactating females with pups during the dry season (Sep, Aug, Nov, Dec).
This suggests that females of A. planirostris can be polyestric and reproduce year round (Willig
1985a, Hollis et al. 2005). The diet of A. planirostris is not restricted to fruits and present a diet flexibility that vary from fruits, pollen, leaves to insects (Hollis et al. 2005, Reis et al. 2007, 119
Cordero-Schmidt et al. 2016). This may allow females to synchronize their reproduction depending on the type of food that is more abundant in a particular time regardless of the season.
Females of the insectivores L. aurita, P. gymnonotus and P. macrotis were also significantly more in lactancy stage during the rainy season (Table 2.7). This coincides with the seasonal increase in insect abundance of Lepidoptera, Coleoptera, Hymenoptera and Diptera orders during the rainy season in the Caatinga (Hernández 2007, Vasconcellos et al. 2010, Bravo and Calor
2014). Both sexes of L. aurita presented a significant seasonality in their reproduction, where pregnancy occurred in the dry and parturition in the rainy season, as indicated by greater number of lactants. While a larger number of males presented evident scrotum in the rainy season. This convergence of escrotated males with pregnant females suggest that the mating activity is seasonal and restricted to the rainy season, consisted with what is known about the species (Lassieur and
Wilson 1989, Reis et al. 2007, Otálora-Ardila et al. 2019). Peropteryx macrotis followed the same pattern with pregnant females in the dry season and lactating in the rainy season (see Yee 2000).
The mormoopid P. gymnonotus presented both pregnant and lactating females restricted to the rainy season consistent with patterns of other species of Pteronotus in the neotropics which present a seasonal unimodal reproduction in the rainy season (Torres-Flores et al. 2012, García et al. 2015,
Vásquez-parra et al. 2015, Núñez-Novas et al. 2016, Otálora-Ardila et al. 2019). Finally, despite the fact that F. horrens were more abundant in the rainy, we were not able to capture enough individuals to infer in its reproduction, however we observed solely during the rainy season (Feb,
Mar, Apr) eight lactating females (carrying pup) and 5 juveniles in Serrote Preto and Casa de
Homens caves, consistent with Uieda et al. (1980) (Fig. E). All of our findings reinforce the fact that insectivorous bats reproduce seasonally during the rainy season in the Caatinga.
Similarly, reproductive females of T. bidens, and T. cirrhosus bats were found only during the rainy season (Table 2.7), consequently the animalivorous guild had the same pattern (Table 2.7), similarly with Willig (1985b) and Feijó and Rocha (2017). A varied diet has been recorded for T. bidens (Esbérard and Bergallo 2004, Felix et al. 2013) and T. cirrhosus (Cramer et al. 2001), thus it is plausible to think that these species in the Caatinga might prey on insects during the rainy season
120 when they are abundant (Vasconcellos et al. 2011) and alternating their diet with year-round fruits and perhaps small vertebrates. Frogs constitute an important diet for T. cirrhosus (Page and Ryan
2005), therefore we believe that in Caatinga the species might feed on this anurans during the rainy season when they are seasonally abundant (Garda et al. 2017). In fact, solely colonies of T. cirrhosus was found in Três Lagos and Pau caves which are next to a small semi perennial wetland found adjacent to the Apodí river in Felipe Guerra. Studies on diet of these and other animalivorous bat species is needed to understand better their seasonal and reproductive patterns in the Caatinga.
Contrary to our prediction, both species of nectarivores recorded herein did not presented a seasonal reproduction (Table 2.7). Even though flowers in the Caatinga are more abundant in the rainy season, studies have indicated that Caatingas’ plant phenology is complex despite the influence of rainfall (Machado et al. 1997), and some species can continuously supply flowers in low number in the dry season (Machado et al. 1997, Griz and Machado 2001, Amorim et al. 2009,
Quirino and Machado 2014, Rocha et al. 2020). Cordero-Schmidt (2020) found in Lajes that plants offered year-round floral (nectar) resources to four species of nectarivorous bats and in addition to morphological differences and their seemingly high diet flexibility (nectar, pollen, insects), these four species are able to coexist during all year. Thus, records of pregnant and lactating females of X. vieirai and G. soricina in both seasons indicates that the floral resources found along the year are abundant enough to supply the energetic demands of this critical reproductive stages.
As well, the omnivorous and sanguinivorous bats presented an aseasonal reproductive pattern as we predicted. For instance, in Felipe Guerra, Desmodus rotundus seems to be beneficiated by the year-round resource of blood through the high density of livestock found around caves that allows the species to be reproductive all year, a behavior known for the species in
Caatinga and other disturbed areas (Greenhall et al. 1983, 1984, Willig 1985a).
Regarding the omnivorous P. discolor, an aseasonal reproduction has not been previously recorded for the species and previous studies have reported reproductive activity only in the rainy season but with some geographical variation (Kwiecinski 2006). As mentioned before, the colony of P. discolor in Furna Feia cave is located in a protected Caatinga fragment (~8000 ha) in the
121
Furna Feia National Park which surrounded by large agricultural plantations of mostly mango and banana. These non-native plants have been already recorded as part of P. discolor diet (Kwiecinski
2006), thus these plantations might be providing a year-round food supply for this massive colony.
In addition to the year-round food resource, the large dimension of Furna Feia cave might allow space for the formation of a large aggregation of P. discolor. This factors plus the fact to be located in a protected area, might confound together to create a high reproductive success and explain the exceptional size of this colony (>5000 indiv.). Because such of the large colony size and the big dimension of the cave entrances, we were not able to detect with the applied methods any significant changes in abundance or reproductive pattern, however a larger proportion of lactants and pregnant were found during the rainy season. We encourage studies on diet, population structure and its relation with the landscape using other non-invasive methods (e.g. thermal detection systems, see Otálora-Ardila et al. 2019) to better understand the ecology of this exceptional colony of P. discolor (Fig. F).
Most of males of the species analyzed presented an aseasonal reproduction and there was no synchronization with females. Such asynchrony between periods of high reproductive activity in females and males might indicate that males has concomitantly reproductive activity with females but with stay active during much more time. Females might be determining the moment of reproduction and waiting for favorable ambient conditions (e.g. food) be receptive, while males may be capable of inseminating females for relatively longer periods of time (Handley et al. 1991,
Durant et al. 2013).
Mist netting vs. observation methods to monitor cave-dwelling bats
Even though our replication of data collection was spaced (except in Serrote Preto and Xero
Xero), we were able to detect seasonal patterns in the cave bat assemblages with both methods. We found differences in the methods to detect the richness. The capture method detected more rapidly a higher richness than observation method, especially during the dry season (Supplementary material
2.10). For instance, species like N. macrourus and T. bidens, in numerous times were not observed inside caves but mist net successfully recorded emerging individuals. Similarly, F. horrens for 122 instance, was rarely captured because of its fine echolocation capacity to detect mist-nets, hence only was detected through direct observation. Regarding bat abundance, there was a difference between the two methods and our data suggest that the direct observation method was more sensible than the captures to detect abundance changes between seasons.
However, when encountering large bat colonies, we were not able to reliably estimate the colony size or detect changes in abundance (e.g. P. gymnonotus, P. discolor), therefore other methods are recommended. Using a thermal infrared camera, Otálora-Ardila et al. (2019) found that a large colony of P. gymnonotus (~35 000-100 000) in a Caatinga bat cave, fluctuated monthly with no consistent pattern. This method provides an effective methodology to estimate the number of bats and their emergence patterns more accurately than traditional methods. Overall, the use of mist-nets in cave entrances to capture bats and day active search to obtain bat counting through direct observation, indeed are methods that complement each other. Henceforth, we recommend these methods for studies on temporal structure of cave bat assemblages if colonies are small or medium sized, but in caves with large bat aggregations other methods should be used.
Conservation implications
The results obtained in this study provides important data to be used for future strategies for the conservation and protection of cave-dwelling bats in the Caatinga of RN. We recorded three species vulnerable to extinction, Lonchorhina aurita, Furipterus horrens, and Natalus macrourus
(MMA/ICMBio 2014), one endemic to Caatinga, Lonchophylla inexpectata, and one to
Caatinga/Cerrado, Xeronycteris vieirai. As well, we surveyed three more caves not included in
Vargas-Mena et al. 2018 and recorded two more species of bats dwelling caves – a small colony of
Noctilio leporinus in Casa de Pedra in Martins and the use of Serrote Preto cave in Lajes by L. inexpectata – hence increasing to18 species the total richness of cave bats in RN. Considering the large number of underground cavities in Caatinga, we encourage inventories in more caves in RN that certainly will elevate this number, especially in the area of Felipe Guerra and Lajes.
The Latin American and Caribbean Network for the Conservation of Bats (RELCOM, acronym in Spanish) have settled as areas of importance for the conservation of bats (AICOM, 123 acronym in Spanish) the areas of Felipe Guerra (A-BR-03) and Lajes (A-BR-04). Felipe Guerra is an important area for RN’s underground fauna and cave bats (Bento et al. 2015, Vargas-Mena et al.
2018), harbors vulnerable species like F. horrens, N. macrourus, and the large and only known colony of the vulnerable L. aurita in the state. The area harbors the highest diversity of cave bats in the state bats with 14 species recorded, namely, 87% of the total diversity of cave bats in RN
(Vargas-Mena et al. 2018). Moreover, an area of environmental protection has been proposed to this area and i (Bento et al. 2015). Lajes harbors colonies of F. horrens, the only known colony of the
Caatinga/Cerrado endemic X. veirai, and one of the largest richness of nectar-feeding bats in the
Caatinga (Cordero-Schmidt et al. 2017, Cordero-Schmidt 2020).
Our data corroborates the results of Vargas Mena et al. (2018) that found that the cave bat distribution in RN is non-nested, species are found widespread among different caves, and each cave harbors a different species composition and assemblage structure. Therefore, conservation planning should consider both large and small caves, to adequately protect the largest proportion of cave bats in the state, consistent with the conservation recommendation of Arita (1993) for Mexican cave bats. This way, conservation actions considering cave clusters, considering all cave size, will more accurately protects vulnerable species like N. macrourus, and F. horrens that favored larger caves, or the vulnerable L. aurita and the Brazilian endemic X. vieirai that were found roosting in only in small caves in Felipe Guerra and Lajes, respectively. This is particular important to consider especially in karstic landscapes with numerous cave clusters, such as in the region of Felipe Guerra,
Vargas-Mena et al. (2018, 2020). Fortunately, large cave cluster are integrally protected in the
Furna Feia National Park including the unique large colony of P. discolor and colonies of F. horrens and N. macrourus (Bento et al. 2013, Vargas Mena et al. 2018).
Because in the rainy season we found a seasonal increase in frugivorous, insectivorous and animalivorous bats attributed to reproductive purposes and regional food availability, it is important to avoid the unnecessary visitation to caves in the rainy season. Disturbances during times of reproduction and caring of young, can have critical and negative impact in bat populations (see
124
Furey and Racey 2016). This is of concern especially for vulnerable species with a marked reproductive seasonality such as F. horrens and L. aurita, according to the data presented herein.
Moreover, most of the caves where these two vulnerable species occur, including the endemic X. vieirai, are found in areas under any protection actions (Lajes, Martins and Felipe
Guerra). Thus, these caves are vulnerable to human disturbance. For instance, in RN the underground cavities are known to suffer from several human activities such as illegal mining, petroleum exploration, unorganized rural settlements, agriculture expansion, and disorderly cave visitation (Cruz et al. 2010) Such disturbances are known to be major causes of cave bat population declines around the world (Furey & Racey 2016), and due to their low annual reproductive rates, bat populations are unable to recover quickly after a population decline associated with human disturbances (Racey & Entwistle 2000).
As well, external disturbances in the landscape around caves, like changes in land use (e.g. deforestation and livestock expansion) are known to affect the structure of cave bat assemblages
(see Vargas-Mena et al. 2020). This can cause inside cave roosts a population increase of species favored by human activities– such as vampire bats. The vampire D. rotundus tend to form large colonies in disturbed landscapes favored by the large abundance of livestock around caves (Trajano
1996, Vargas-Mena et al. 2020). As well, our findings related to the occurrence of large colonies of
D. rotundus in caves where F. horrens did not occurred or in low numbers and vice versa, might be an evidence on how external disturbances can affect the integrity of a cave bat assemblage. This relation should be deeply explored because this might have conservation implications, considering that F. horrens is a cave-dependent in Caatinga and is a vulnerable to extinction in Brazil.
We expect that the data presented herein will be useful for future conservation actions in the state in order to accurately protect the largest amount of cave roosts, which are critical for the survival of such diverse cave bats fauna in Rio Grande do Norte.
125
CONCLUSION
The results of this study provide novel insights of the structural and reproductive pattens of cave-roosting bat assemblages in an effort to better understand the ecology of these flying mammals in the semi-arid landscape of Caatingas’ dry forests. Patterns of assemblage structure and reproduction were complex and our predictions were partially consistent. Species richness did not change significantly from one season to another suggesting that there is not a seasonal increase of species during the rainy season, as we initially predicted. The species composition was different between caves including among large and small-sized caves. No temporal turnover of species was found between seasons, and just like with the richness, the same species were resident year-round regardless of the season. However, the overall bat abundance did increase significantly in the rainy season, especially at the end of this season but was guild and species-specific. Large caves tended to vary positively much more in abundance than small caves in the rainy season, despite small caves varied seasonally as well. This seasonally increase of those species is likely attributed to reproductive purposes and regional food availability. Most of the species were reproductively active during the rainy season were their preferred food seems to be abundant (frugivores, insectivores and animalivores), while others that rely on year-round available food resources were active during both season (sanguinivores, omnivores and unexpectedly nectarivores). The data provided herein demonstrates different patterns in the structure and reproduction of cave bat assemblages of what is expected in a highly seasonal environment and provides insights of a general year-round adaptation of the cave bat fauna in this part of the unique but threatened Caatinga Dry Forest.
REFERENCES
Amorim, I. L. de, E. Valadares, de S. Barreto, and E. de Lima. 2009. Fenologia de espécies lenhosas da Caatinga do Seridó, RN. Revista Árvore 33:491–499. Arita, H. T. 1993. Conservation Biology of the Cave Bats of Mexico. Journal of Mammalogy 74:693–702. Arita, H. T. 1996. The conservation of cave-roosting bats in Yucatan, Mexico. Biological Conservation 76:177–185. 126
Avila-Flores, R., and R. A. Medellín. 2004. Ecological, taxonomic, and physiological correlates of cave use by mexican bats. Journal of Mammalogy 85:675–687. Basílio, G. H. N., J. P. M. de Araujo, J. C. Vargas-Mena, P. A. Rocha, and M. A. F. Kramer. 2017. Chrotopterus auritus (Peters, 1856) (Chiroptera, Phyllostomidae): first record for the state of Rio Grande do Norte, northeastern Brazil. Check List 13:1–8. Bento, D. D. M., J. B. Cruz, J. I. Freitas, U. P. Campos, and A. F. de Oliveira. 2017. A Mais de 1000 ! O patrimônio espeleológico potiguar após a descoberta da milésima Caverna. 34 Congresso Brasileiro de Espeleologia 2113:227–237. Bento, D. D. M., J. B. Cruz, D. J. dos Santos, J. I. Freitas, U. P. Campos, and R. F. de R. Souza. 2013. Parque Nacional da Furna Feia - o parque nacional com a maior quantidade de cavernas no Brasil. Pages 31–43 ANAIS do 32° Congresso Brasileiro de Espeleologia. Bento, D. de M., J. B. Cruz, J. I. Freitas, and U. P. Campos. 2015. Área de Proteção Ambiental Pedra de Abelha: proposta para a conservação da maior concentração de cavernas do Rio Grande do Norte. 33 Congresso Brasileiro de Espeleologia 2113:51–63. Bravo, F., and A. Calor. 2014. Artrópodes do Semiárido: biodiversidade e conservação. Printmídia, Feira de Santana. Brunet, A. K., and R. A. Medellín. 2001. The species–area relationship in bat assemblages of tropical caves. Journal of Mammalogy 82:1114–1122. Cardiff, S. G. 2006. Bat cave selection and conservation in Ankarana, northern Madagascar. Columbia University, New York. Carmignotto, A. P., and D. Astúa. 2017. Mammals of the Caatinga : diversity, ecology, biogeography, and conservation. Pages 211–254 in J. M. C. da Silva, I. R. Leal, and M. Tabarelli, editors. Caatinga: The Largest Tropical Dry Forest Region in South America. Springer International Publisher, Cham, Switzerland. Charles O. Handley Jr., D. E. Wilson, and A. L. Gardner. 1991. Demography and natural history of the common fruit bat, Artibeus jamaicensis , on Barro Colorado island, Panama. Smithsonian Contributions to Zoology:1–184. Cordero-Schmidt , E. 2020. Interações, mecanismos de persistência e coexistência de morcegos nectarívoros e das plantas das quais se alimentam em uma floresta tropical sazonal seca no Nordeste brasileiro. Dissertação de doutorado. Universidade Federal do Rio Grande do Norte, Natal, Brasil. Pp. 160. Cordero-Schmidt, E., E. Barbier, J. C. Vargas-Mena, P. P. Oliveira, F. D. A. R. Santos, R. A. Medellín, B. R. Herrera, and E. M. Venticinque. 2017. Natural history of the Caatinga endemic Vieira’s flower bat, Xeronycteris vieirai. Acta Chiropterologica 19:399–408. Cordero-Schmidt, E., M. Medeiros-Guimarães, J. C. Vargas-Mena, B. Carvalho, R. L. Ferreira, B. Rodriguez-Herrera, and E. M. Venticinque. 2016. Are leaves a good option in Caatinga’s
127
menu? First record of folivory in Artibeus planirostris (Phyllostomidae) in the semiarid forest, Brazil. Acta Chiropterologica 18:489–497. Cramer, M. J., M. R. Willig, and C. Jones. 2001. Trachops cirrhosus. Mammalian Species:1–6. Cruz, J. B., D. D. M. Bento, F. H. R. Bezerra, J. I. Freitas, U. P. Campos, and D. J. dos Santos. 2010. Diagnóstico espeleológico do Rio Grande do Norte. Revista Brasileira de Espeleologia 1:1–24. Díaz, M. M., S. Solari, L. F. Aguirre, L. M. S. Aguiar, and R. M. Barquez. 2016. Clave de identificación de los murciélagos de Sudamérica. Publicació. Programa de Conservación de los Murciélagos de Argentina (PCMA), Argentina. Diniz, M. T. M., and V. H. C. Pereira. 2015. Climatologia do estado do Rio Grande do Norte, Brasil: sistemas atmosféricos atuantes e mapeamento de tipos de clima. Boletim Goiano de Geografia 35:488–506. Dirzo, R., H. S. Young, H. A. Mooney, and G. Ceballos. 2011. Seasonally Dry Tropical Forests: ecology and conservation. Island Press, Washington. Durant, K. A., R. W. Hall, L. M. Cisneros, R. M. Hyland, and R. Michael. 2013. Reproductive phenologies of phyllostomid bats in Costa Rica Reproductive phenologies of phyllostomid bats in Costa Rica. Journal of Mammalogy 94:1438–1448. Esbérard, C. E. L., and H. G. Bergallo. 2004. Aspectos sobr e a biologia de T onatia bidens ( Spix ) no estado do sobre Rio de J aneir o , sudeste do Br asil ( Mammalia , Chir opter a , Ph yllostomidae ) Brasil Chiropter Phyllostomidae ) Janeir 21:253–259. Feijó, A., and P. A. da Rocha. 2017. Morcegos da Estação Ecológica Aiuaba, Ceará, Nordeste do Brasil: uma unidade de proteção integral na Caatinga. Mastozoologia Neotropical 24:333–346. Felix, S., R. L. M. Novaes, R. de F. Souza, and R. T. Santori. 2013. Diet of Tonatia bidens ( Chiroptera , Phyllostomidae ) in an Atlantic Forest area , southeastern Brazil : first evidence for frugivory. Mammalia 77:451–454. Felix, S., R. L. M. Novaes, R. F. Souza, and L. S. Avilla. 2016. Bat assemblage in a karstic area from northern Brazil: Seven new occurrences for Tocantins state, including the first record of Glyphonycteris sylvestris Thomas, 1896 for the Cerrado. Check List 12:1–16. Ferreyra-García, D., R. A. Saldaña-Vázquez, and J. E. Schondube. 2018. La estacionalidad climática no afecta la fenología de murciélagos cavernícolas con dieta omnívora. Revista Mexicana de Biodiversidad 89:488–496. Furey, N. M., and P. A. Racey. 2016. Conservation Ecology of Cave Bats. Pages 463–500 in C. C. Voigt and T. Kingston, editors. Bats in the Anthropocene: Conservation of Bats in a Changing World. Springe International Publisher, London. García, G. J., D. Araujo-Reyes, O. Vásquez-Parra, H. Brito, and M. Machado. 2015. Bats (Mammalia: Chiroptera) associados com una cuerva en el Parque Nacional Yurubí, Sierra de
128
Aroa , Yaracuy State , Venezuela. Zoología 37:381–391. Garda, A. A., M. G. Stein, R. B. Machado, M. B. Lion, F. A. Juncá, and M. F. Napoli. 2017. Ecology , Biogeography , and Conservation of Amphibians of the Caatinga. Pages 133–149 in J. M. C. da Silva, I. R. Leal, and M. Tabarelli, editors. Caatinga: The Largest Tropical Dry Forest Region in South America. Springer International Publisher, Cham, Switzerland. Gomes, L. A. C., A. C. S. Maas, M. S. M. Godoy, M. A. Martins, A. R. Pedrozo, and A. L. Peracchi. 2018. Ecological considerations on Xeronycteris vieirai : An endemic bat species from the Brazilian semiarid macroregion. Mastozoología Neotropical 25:81–88. Greenhall, A. M., G. Joermann, and U. Schmidt. 1983. Desmodus rotundus. Mammalian Species:1– 6. Greenhall, A. M., U. Schmidt, and G. Joermann. 1984. Diphylla ecaudata. Mammalian Species:1–3. Gregorin, R., A. P. Carmignotto, and Alexandre R. Percequillo. 2008. Quirópteros do Parque Nacional da Serra das Confusões, Piauí, nordeste do Brasil. Chiroptera Neotropical 14:366– 383. Gregorin, R., and L. de F. Mendes. 1999. On Chiroptera (Emballonuridae, Phyllostomidae, Natalidae) of two caves at Chapada Diamantina, Bahia, Brazil. Iheringia Serie Zoologia 86:121–124. Griz, L. M. S., and I. C. Machado. 2001. Fruiting phenology and seed dispersal syndromes in caatinga , a tropical dry forest in the northeast of Brazil. Journal of Tropical Ecology 17:303– 321. Guimarães, M. M., and R. L. Ferreira. 2014. Morcegos cavernícolas do Brasil: novos registros e desafios para conservação. Revista Brasileira de Espeleologia 2:1–33. Gusmão, M. A. B., and A. J. Creão-Duarte. 2004. Diversidade e análise faunística de Sphingidae (Lepidoptera) em área de brejo e caatinga no Estado da Paraíba. Revista Brasileira de Zoologia 21:491–498. Hernández, M. I. 2007. Besouros escarabeíneos ( Coleoptera : Scarabaeidae ) da Caatinga paraibana , Brasil. Oecologia Brasiliensis 11:356–364. Hollis, L., A. Spix, and F. F. Bat. 2005. Artibeus planirostris. Mammalian Species 1410:1–6. Júnior, J. A. D., and C. Schlindwein. 2005. The highly seasonal hawkmoth fauna (Lepidoptera: Sphingidae) of the Caatinga of northeast Brazil: a case study in the state of Rio Grande do Norte. Journal of the Lepidopterists’ Society 59:212–218. Kofoky, A., D. Andriafidison, F. Ratrimomanarivo, H. J. Razafimanahaka, D. Rakotondravony, P. A. Racey, and R. K. B. Jenkins. 2007. Habitat use , roost selection and conservation of bats in Tsingy de Bemaraha National Park, Madagascar. Biodiversity and Conservation 16:1039– 1053. Kunz, T. H. 1982. Roosting Ecology of Bats. Pages 1–58 in T. H. Kunz, editor. Ecology of Bats.
129
Plenum Publishing Corporation, New York. Kunz, T. H., M. Betke, N. I. Hristov, and M. J. Vonhof. 2009. Methods for assessing colony size, population size, and relative abundance of bats. Pages 133–157 in T. H. Kunz and S. Parsons, editors. Ecological and Behavioral Methods for the Study of Bats [2nd. Ed.]. John Hopkins University Press, Baltimore. Kwiecinski, G. G. 2006. Phyllostomus discolor. Mammalian Species 801:1–11. Lassieur, S., and D. E. Wilson. 1989. Lonchorhina aurita. Mammalian Species 347:1–4. Leal, E. S. B., F. F. Gomes-Silva, D. de Q. G. Filho, S. M. De Azevedo, R. M. De Lyra-Neves, and W. R. Telino-Junior. 2018. Update of the distribution of Lonchorhina aurita ( Chiroptera ), a vulnerable cave-dwelling bat in Brazil. Neotropical Biology and Conservation 13:254–267. Leal, E. S. B., D. D. F. Ramalho, B. G. Miller, P. D. B. P. Filho, J. G. D. P. Neto, F. V. P. V. Nova, R. M. De Lyra-Neves, G. J. B. De Moura, and W. R. Telino-Junior. 2012. Primeiro registro da família Natalidae (Mammalia : Chiroptera) para a Caatinga do Estado da Paraíba , Nordeste do Brasil. Revista Brasileira de Zoociencias 14:243–253. Leal, I. R., M. Tabarelli, and J. M. C. da Silva. 2003. Ecologia e Conservação da Caatinga. Editora Un. Universidade Federal de Pernambuco, Recife. Luo, J., T. Jiang, G. Lu, L. Wang, J. Wang, and J. Feng. 2013. Bat conservation in China: Should protection of subterranean habitats be a priority? Oryx 47:526–531. Machado, I. C., L. M. Barros, and E. V. S. B. Sampaio. 1997. Phenology of Caatinga species at Serra Talhada, PE, Northeastern Brazil. Biotropica 29:57–68. MMA/ICMBio - Ministério de Meio Ambiente/Instituto Chico Mendes de Conservação da Biodiversidade. 2014. Lista Nacional Oficial de Espécies da Fauna Ameaçadas de Extinção. Diário Oficial da União, Portaria MMA nº 444, de 17 de dezembro de 2014. Niu, H., N. Wang, L. Zhao, and J. Liu. 2007. Distribution and underground habitats of cave- dwelling bats in China. Animal Conservation 10:470–477. Nobre, C. E. B., L. Iannuzzi, and C. Schlindwein. 2012. Seasonality of fruit-feeding butterflies (Lepidoptera, Nymphalidae) in a Brazilian semiarid area. International Scholarly Research Network Zoology 2012:1–8. Nogueira, M. R., I. P. de Lima, R. Moratelli, V. da C. Tavares, R. Gregorin, and A. L. Peracchi. 2014. Checklist of Brazilian bats, with comments on original records. Check List 10:808–821. Núñez-Novas, M. S., Y. M. León, J. Mateo, and L. M. Dávalos. 2016. Records of the cave-dwelling bats (Mammalia: Chiroptera) of Hispaniola with an examination of seasonal variation in diversity. Acta Chiropterologica 18:269–278. Oliveira, H. F. M. de, M. Oprea, and R. I. Dias. 2018. Distributional patterns and ecological determinants of bat occurrence inside caves: A broad scale meta-analysis. Diversity 10:1–14. Otálora-Ardila, A., J. M. Torres, E. Barbier, N. T. Pimentel, E. S. B. Leal, and E. Bernard. 2019. 130
Thermally-assisted monitoring of bat abundance in an exceptional cave in Brazil ’ s Caatinga drylands. Acta Chiropterologica 21:411–423. Page, R. A., and M. J. Ryan. 2005. Flexibility in assessment of prey cues : frog-eating bats and frog calls. Proceedings of the Royal Society B: Biological Sciences 272:841–847. Pérez-Torres, J., D. Martínez-Medina, M. Peñuela-Salgado, M. C. Ríos-Blanco, S. Estrada-Villegas, and L. Martínez-Luque. 2015. Macaregua: the cave with the highest bat richness in Colombia. Check List 11:1–7. Phelps, K., R. Jose, M. Labonite, and T. Kingston. 2016. Correlates of cave-roosting bat diversity as an effective tool to identify priority caves. Biological Conservation 201:201–209. Prado, D. E. 2003. As caatingas da América do Sul. Pages 3–74 in I. R. Leal, M. Tabarelli, and J. M. C. da Silva, editors. Ecologia e Conservação da Caatinga. Universidade Federal de Pernambuco, Recife. Queiroz, L. P. De, D. Cardoso, M. F. Fernandes, and M. F. Moro. 2017. Diversity and Evolution of Flowering Plants of the Caatinga Domain. Pages 23–63 in J. M. C. da Silva, I. R. Leal, and M. Tabarelli, editors. Caatinga: The Largest Tropical Dry Forest Region in South America. Springer International Publisher, Cham, Switzerland. Quirino, Z. M. G., and I. C. Machado. 2014. Pollination syndromes in a Caatinga plant community in northeastern Brazil : seasonal availability of floral resources in different plant growth habits. Brazilian Journal of Biology 74:62–71. Racey, P. A. 1982. Ecology of Bat Reproduction. Pages 52–104 in T. H. Kunz, editor. Ecology of Bats. Plenum Publishing Corporation. Racey, P. A., and A. C. Entwistle. 2000. Life-history and Reproductive strategies of Bats. Pages 363–414 in E. G. Crichton and Phillip H. Krutzsch, editors. Reproductive Biology of Bats. Academic Press. Reis, N. R. dos, A. L. Peracchi, W. A. Pedro, and I. P. de Lima. 2007. Morcegos do Brasil. Page Morcegos do Brasil. Universidade Estadual de Londrina, Londrina. Rocha, A. D., and M. E. Bichuette. 2016. Influence of abiotic variables on the bat fauna of a granitic cave and its surroundings in the state of São Paulo, Brazil. Biota Neotropica 16:1–8. Rocha, E. A., A. Domingos-melo, D. C. Zappi, and I. C. Machado. 2020. Reproductive biology of columnar cacti : are bats the only protagonists in the pollination of Pilosocereus , a typical chiropterophilous genus ? Folia Geobot:1–18. Rocha, P. A. da, J. S. Mikalauskas, A. Bocchiglieri, J. Anderson, and S. F. Ferrari. 2013. An update on the distribution of Natalus macrourus (Gervais, 1856) (Mammalia, Chiroptera), with new records from the Brazilian Northeastern. Check List 9:675–679. Rocha, P. A., M. A. Pedroso, A. Feijó, N. G. Filho, B. A. T. P. Campos, and S. F. Ferrari. 2014. Update on the distribution of Diphylla ecaudata Spix, 1823 (Mammalia, Chiroptera): New
131
records from the Brazilian northeast. Check List 10:1541–1545. Sbragia, I. A., and A. Cardoso. 2008. Quirópterofauna (Mammalia: Chiroptera) cavernícola da Chapada Diamantina, Bahia, Brasil. Chiroptera Neotropical 14:360–365. Sikes, R. S. 2016. 2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. Journal of Mammalogy 97:663–688. Silva, J. M. C. da, I. R. Leal, and M. Tabarelli. 2017. Caatinga: The Largest Tropical Dry Forest Region in South America. Springer International Publisher, Cham, Switzerland. Silva, S. S. P. da, and P. G. Guedes. 2001. Levantamento preliminar dos morcegos do Parque Nacional Ubajara (Mammalia, Chiroptera), Ceará, Brasil. Revista Brasileira de Zoologia 18:139–144. Silva, U. B. T. da, M. Delgado-Jaramillo, L. M. Souza Aguiar, and E. Bernard. 2018. Species richness, geographic distribution, pressures, and threats to bats in the Caatinga drylands of Brazil. Biological Conservation 221:312–322. Simmons, N. B., and R. S. Voss. 2009. Collection , Preparation , and Fixation of Specimens and Tissues. Page in T. H. Kunz and S. Parsons, editors. Ecological and behavioral methods for the study of bats. John Hopkins University Press. Stoner, K. E., and R. M. Timm. 2004. Tropical Dry Forest mammals of Palo Verde. Pages 48–66 in G. W. Frankie, A. Mata, and S. B. Vinson, editors. Biodiversity conservation in Costa Rica: Learning the lessons in the seasonal dry forest2. University of California Press, Berkeley. Stoner, K. E., and R. M. Timm. 2011. Seasonally Dry Tropical Forest Mammals : Adaptations and Seasonal Patterns. Pages 85–106 in R. Dirzo, H. S. Young, H. A. Mooney, and G. Ceballos, editors. Seasonally Dry Tropical Forests: Ecology and Conservation. Island Press, Washington. Streilein, K. E. 1982. Ecology of small mammals in the semiarid Brazilian Caatinga. Annals of the Carnegie Museum of Natural History 51:109–126. Torquetti, C. G., M. X. Silva, and S. Talamoni. 2017. Differences between caves with and without bats in a Brazilian karst habitat. Zoologia 34:1–7. Torres-Flores, J. W., R. Lopez-Wilchis, and A. Soto-Castruita. 2012. Population dynamics, roost selection and reproductive patterns of some cave bats from Western of Mexico. Revista De Biologia Tropical 60:1369–1389. Trajano, E. 1996. Movements of cave bats in southeastern Brazil, with emphasis on the population ecology of the Common vampire bat, Desmodus rotundus (Chiroptera). Biotropica 28:121. Trajano, E., and E. A. Gimenez. 1998. Bat community in a cave from eastern Brazil , including a new record of Lionycteris (Phyllostomidae, Glossophaginae). Studies on Neotropical Fauna and Environment 33:69–75. Uieda, W., I. Sazima, and A. Storti-Filho. 1980. Aspectos da Biologia do Morcego Furipterus
132
horrens (Mammalia, Chiroptera, Furipteridae). Revista Brasileira de Biologia 40:59–66. Vargas-Mena, J. C., E. Cordero-Schmidt, B. Rodríguez-herrera, R. A. Medellín, D. D. M. Bento, and E. M. Venticinque. 2020. Inside or out ? Cave size and landscape effects on cave-roosting bat assemblages in Brazilian Caatinga caves. Journal of Mammalogy 101:464–475. Vargas-Mena, J. C., E. C. Schmidt, D. D. M. Bento, B. Rodriguez Herrera, R. A. Medellín, and E. M. Venticinque. 2018. Diversity of cave bats in the Brazilian tropical dry forest of Rio Grande do Norte state. Mastozoologia Neotropical 18:199–212. Vasconcellos, A., R. Andreazze, A. M. Almeida, H. F. P. Araujo, E. S. Oliveira, and U. Oliveira. 2010. Seasonality of insects in the semi-arid Caatinga of northeastern Brazil. Revista Brasileira de Entomologia 54:471–476. Vásquez-parra, O., F. J. García, D. Araujo-Reyes, H. Brito, and M. Machado. 2015. Dinámica poblacional de Pteronotus parnellii y Anoura geoffroyi (Mammalia: Chiroptera) en Venezuela. Ecotrópicos 28:27–37. Willig, M. R. 1983. Composition microgeographic variation and sexual dimorphism in Caatingas and Cerrado bat communities from northeastern Brazil. Bulletin of Carnegie Museum of Natural History 23:1–132. Willig, M. R. 1985a. Reproductive patterns of bats from Caatingas and Cerrado biomes in northeast Brazil. Journal of Mammalogy 66:668–681. Willig, M. R. 1985b. Reproductive activity of female bats northeast Brazil. Bat Research News 26:17–20. Yee, D. A. 2000. Peropteryx macrotis. Mammalian Species 643:1–4.
Figure E. An exceptional large colony of the omnivore Phyllostomus discolor in Furna Feia cave at the Furna Feia National Park, in western Rio Grande do Norte, Brazil. Photo by Juan Carlos Vargas-Mena in 2019. 133
SUPPLEMENTARY MATERIALS
Supplementary material 2.1. Richness of cave-dwelling bats recorded in nine caves in the Caatinga of Rio Grande do Norte from 2017-2019. Trophic guilds and species are Sanguinivores: Desmodus rotundus (a), Diphylla ecaudata (b); Nectarivores: Glossophaga soricina (c), Lonchophylla inexpectata (d), Lonchophylla mordax (e), Xeronycteris vieirai (f); Frugivores: Artibeus planirostris (g), Carollia perspicillata (h); Piscivores: Noctilio leporinus (i); Animalivores: Tonatia bidens (j), Trachops cirrhosus (m); Omnivorous: Phyllostomus discolor (k), Phyllostomus discolor with total leucism (l); Insectivores: Lonchorhina aurita (n), Peropteryx macrotis (o), Pteronotus gymnonotus (p), Natalus macrourus (q) and Furipterus horrens (r). Vulnerable species and Caatinga endemics are shown.
134
Supplementary material 2.2 Richness of cave-dwelling per season in nine caves in the Caatinga of Rio Grande do Norte from 2017-2019.
Richness Cave Rainy Dry Carrapateira 7 6 Casa de Homens 5 5 Casa de Pedra 6 6 Furna Feia 9 8 Pau 5 5 Serrote Preto 8 10 Três Lagos 8 7 Urubu 6 5 Xero Xero 4 3
Supplementary material 2.3. Results of the analysis of covariance (ANCOVA) of the relation of richness with seasons with A) captures with mist-nets and the B) observations through direct observation of cave bats in nine caves in the Caatinga of Rio Grande do Norte, Brazil from 2017- 2019.
A) Captured Dependent Variable richness N 28 Multiple R 0.16209 Squared Multiple R 0.02627
Type III Mean Source df F-ratio p-value SS Squares Seasons 0.65637 1 0.65637 0.1439 0.70777 Abundance_Captures 1.6917 1 1.6917 0.37087 0.54825 Seasons*Abundance_Captures 0.00706 1 0.00706 0.00155 0.96894 Error 109.47479 24 4.56145
B) Observed Dependent Variable richness N 30 Multiple R 0.51867 Squared Multiple R 0.26902
Type III Mean Source df F-ratio p-value SS Squares Season 3.31951 1 3.31951 2.19892 0.15013 Abundance_Observation 14.15923 1 14.15923 9.37939 0.00505 Seasons*Abundance_Observation 7.23509 1 7.23509 4.79268 0.03775 Error 39.24988 26 1.50961
135
Supplementary material 2.4. Results of the analysis of covariance (ANCOVA) of the relation of richness with abundance, seasons and cave size of the data obtain with the A) capture with mist-nets and the B) observations through direct observation of cave bats in nine caves in the Caatinga of Rio Grande do Norte, Brazil from 2017-2019.
A) Dependent Variable Richness Captures N 28 Multiple R 0.30162 Squared Multiple R 0.09097
Mean Source Type III SS df F-ratio p-value Squares Abundance_Capture 2.62874 1 2.62874 0.54015 0.4705 Season 3.36406 1 3.36406 0.69124 0.4151 Cave size 5.2893 2 2.64465 0.54342 0.58871 Season*Cave size 1.95701 2 0.97851 0.20106 0.81942 Error 102.20063 21 4.8667
Dependent Variable Richness Observation N 30 Multiple R 0.43094 Squared Multiple R 0.18571
B) Mean Source Type III SS df F-ratio p-value Squares Season 0.08605 1 0.08605 0.04527 0.83339 Cave size 1.52729 2 0.76365 0.4017 0.67378 Abundance_Observation 2.36079 1 2.36079 1.24185 0.27662 Season*Cave size 0.59604 2 0.29802 0.15677 0.85581 Error 43.7235 23 1.90102
136
Supplementary material 2.5. Results of the analysis of variance (ANOVA) of the relation of abundance with seasons and cave size of the data obtain with the A) observations through direct observation and the B) capture with mist-nets the of cave bats in nine caves in the Caatinga of Rio Grande do Norte, Brazil from 2017-2019.
A) Dependent Observed
Variable abundance N 30 Multiple R 0.62132 Squared Multiple R 0.38603
Mean Source Type III SS df F-ratio p-value Squares Cave size 30154.89867 1 30154.89867 5.94413 0.02191 Season 33660.95238 1 33660.95238 6.63524 0.01603 Cave size*Season 15971.66667 1 15971.66667 3.14833 0.08772 Error 131899.4743 26 5073.0567
B) Dependent Captured
Variable abundance N 30 Multiple R 0.61545 Squared Multiple R 0.37878
Mean Source Type III SS df F-ratio p-value Squares Cave size 39261.97624 1 39261.97624 11.79091 0.00201 Season 9329.9653 1 9329.9653 2.80192 0.10614 Cave size*Season 5988.77127 1 5988.77127 1.79851 0.19149 Error 86576.12667 26 3329.85103
137
Supplementary Material 2.6. Results of the similarity percentage analysis (SIMPER) for comparisons of the Bray Curtis dissimilarity index between mean abundance of the eleven most abundant observed bats in each surveyed cave in Rio Grande do Norte State, Brazil from 2017-2019. Average dissimilarity was 78.09%. Caves acronyms are: Serrote Preto (SP), Abrigo Xero-Xero (AXX), Casa de Homens (CH), Urubu (UR), Carrapateira (CA), Casa de Pedra (CP), Furna Feia (FF), and Três Lagos (TL) The table indicates average dissimilarity (Av.dissim), percentage of contribution to dissimilarity (Contrib.%), cumulative percentage (Cum. %), and mean abundance of each species per surveyed cave. Av. Contrib. Cumulative Taxon SP AXX CH UR CA CP FF TL dissim % % Furipterus horrens 27.07 34.67 34.67 24 2.4 30.7 1.5 5.5 144 121 0.5 Desmodus rotundus 24.18 30.97 65.64 0 0 2.67 132 27.3 4 8.75 122 Peropteryx macrotis 9.012 11.54 77.18 9.82 8.7 19 1 43.8 21 9.75 2.25 Xeronycteris vieirai 7.113 9.109 86.29 0 29.1 0 0 0 0 0 0 Artibeus planirostris 5.293 6.779 93.07 7.38 0 0 0 26.5 13 0 0 Glossophaga soricina 2.88 3.689 96.76 12 0 0 0 0.5 0 3.25 4.25 Diphylla ecaudata 0.9405 1.204 97.96 0 0 1.33 0.5 3.25 1.25 1 1.75 Lonchorhina aurita 0.5328 0.6823 98.65 0 0 0 0 0.5 0 0 3.75 Tonatia bidens 0.4949 0.6338 99.28 0 0 0 0 0.25 0 6 0 Noctilio leporinus 0.3719 0.4763 99.76 0 0 0 0 0 4.75 0 0 Trachops cirrhosus 0.1912 0.2449 100 0 0 0 0 0 0 0 1.5
Supplementary Material 2.7. Results of the similarity percentage analysis (SIMPER) for comparisons of the Bray Curtis dissimilarity index between mean abundance of the eleven most abundant captured bat species between large and small caves from 2017-2019 in the Caatinga of Rio Grande do Norte State, Brazil. The table indicates average dissimilarity (Av.dissim), percentage of contribution to dissimilarity (Contrib.%), cumulative percentage (Cum. %), and mean abundance of each species per surveyed cave. Average dissimilarity was 88.29%.
Av. Contrib. Cumulative Mean Mean Taxon dissim % % Large Small Phyllostomus discolor 22.78 25.80 25.80 48.00 0.00 Pteronotus gymnonotus 19.04 21.57 47.36 32.80 0.00 Lonchorhina aurita 14.89 16.86 64.23 0.00 30.40 Desmodus rotundus 11.02 12.48 76.71 15.40 6.23 Artibeus planirostris 8.66 9.81 86.52 6.42 1.55 Peropteryx macrotis 4.90 5.55 92.06 2.92 3.12 Glossophaga soricina 1.67 1.89 93.95 0.75 1.32 Trachops cirrhosus 1.49 1.69 95.64 0.00 2.85 Tonatia bidens 1.38 1.57 97.21 1.67 0.66 Diphylla ecaudata 0.84 0.95 98.16 0.92 0.92 Furipterus horrens 0.82 0.93 99.10 0.00 0.85 Xeronycteris vieirai 0.80 0.90 100.00 0.00 0.69
138
Supplementary Material 2.8. Results of the similarity percentage analysis (SIMPER) for comparisons of the Bray Curtis dissimilarity index between mean abundance of the eleven most abundant observed bat species between large and small caves from 2017-2019 in the Caatinga of Rio Grande do Norte State, Brazil. The table indicates average dissimilarity (Av.dissim), percentage of contribution to dissimilarity (Contrib.%), cumulative percentage (Cum. %), and mean abundance of each species per surveyed cave. Average dissimilarity was 77.39%.
Taxon Av. dissim Contrib. % Cumulative % Mean Large Mean Small Furipterus horrens 29.52 38.14 38.14 77.3 12.6 Desmodus rotundus 22.19 28.68 66.82 30.2 30.9 Peropteryx macrotis 9.178 11.86 78.68 21.4 9.3 Xeronycteris vieirai 5.956 7.696 86.37 0 9.11 Artibeus planirostris 5.62 7.262 93.63 11.3 1.84 Glossophaga soricina 2.326 3.005 96.64 1.07 4.07 Diphylla ecaudata 1.013 1.309 97.95 1.64 0.688 Tonatia bidens 0.438 0.5659 99.25 0.143 0.938 Lonchorhina aurita 0.5711 0.738 98.69 1.79 0 Noctilio leporinus 0.4289 0.5542 99.81 1.36 0 Trachops cirrhosus 0.1502 0.1941 100 0 0.375
Supplementary Material 2.9. Results of the similarity percentage analysis (SIMPER) for comparisons of the Bray Curtis dissimilarity index between mean abundance of the eleven most abundant observed bats in each season (Dry and Rainy) from 2017-2019 in the Caatinga of Rio Grande do Norte State, Brazil. The table indicates average dissimilarity (Av.dissim), percentage of contribution to dissimilarity (Contrib.%), cumulative percentage (Cum. %), and mean abundance of each species per surveyed cave. Average dissimilarity was 72.57%.
Taxon Av. dissim Contrib. % Cumulative %Mean Dry Mean Rainy Furipterus horrens 25.48 35.11 35.11 20.9 59.5 Desmodus rotundus 21.66 29.85 64.96 24.4 35.3
Peropteryx macrotis 8.561 11.8 76.76 13.1 16.4 Xeronycteris vieirai 6.681 9.206 85.96 4.25 5.32 Artibeus planirostris 5.027 6.927 92.89 5.73 6.65
Glossophaga soricina 2.728 3.759 96.65 2.77 2.59 Diphylla ecaudata 0.9171 1.264 97.91 1.62 0.765 Lonchorhina aurita 0.5185 0.7144 98.63 0.769 0.412
Tonatia bidens 0.4623 0.637 99.27 0 1.47 Noctilio leporinus 0.3504 0.4828 99.75 0.308 0.882 Trachops cirrhosus 0.1828 0.2519 100 0.308 0.118
139
Supplementary material 2.10. Comparison of the detection of richness and abundance of cave bats using two methods in nine Caatinga caves in Rio Grande do Norte, Brazil from 2017-2019. Methods are a) capture with mist nets and b) direct observation.
Figure E. A lactating female of the vulnerable Thumbless bat (Furipterus horrens) with a pup during the rainy season at the Gruta Casa de Homens cave in Felipe Guerra, western Rio 140 Grande do Norte, Brazil. Photo by Juan Carlos Vargas-Mena in 2017.
141
Chapter 3
The bats of Rio Grande do Norte, northeastern Brazil.
Juan Carlos Vargas-Mena1, Kleytone Alves Pereira2, Marília A. S. Barros3, Eder Barbier3, Eugenia Cordero-Schmidt1, Sergio Maia Queiroz Lima 4, Bernal Rodríguez- Herrera5, and Eduardo Martins Venticinque1
1 Departamento de Ecologia, Universidade Federal do Rio Grande do Norte, Centro de Biociências, Campus Lagoa Nova, 59072-970, Natal, Rio Grande do Norte, Brazil [Correspondence: [email protected]].
2 Departamento de Psicobiologia, Universidade Federal do Rio Grande do Norte, Centro de Biociências, Campus Lagoa Nova, 59072-970, Natal, Rio Grande do Norte, Brazil.
3 Laboratório de Ciência Aplicada à Conservação da Biodiversidade, Programa de Pós- graduação em Biologia Animal, Departamento de Zoologia, Universidade Federal de Pernambuco, Rua Professor Nelson Chaves s/n, Cidade Universitária, 50670-420, Recife, Pernambuco, Brazil.
4 Departamento de Botânica e Zoologia, Universidade Federal do Rio Grande do Norte, Centro de Biociências, Campus Lagoa Nova, 59072-970, Natal, Rio Grande do Norte, Brazil
5 Escuela de Biología, Universidad de Costa Rica, 2060 Montes de Oca, San José, Costa Rica.
Published in the journal Biota Neotropical: Vargas-Mena, Juan Carlos, Alves-Pereira, Kleytone, Barros, Marília Abero Sá, Barbier, Eder, Cordero-Schmidt, Eugenia, Lima, Sergio Maia Queiroz, Rodríguez-Herrera, Bernal, & Venticinque, Eduardo Martins. (2018). The bats of Rio Grande do Norte state, northeastern Brazil. Biota Neotropica, 18(2), e20170417. Epub April 16, 2018.https://dx.doi.org/10.1590/1676-0611-bn-2017-0417
142
RESUMO:
O Rio Grande do Norte (RN) é um dos menores estados do Brasil, mas possui grande diversidade de ecossistemas, incluindo vegetação de Caatinga, Mata Atlântica, habitats costeiros, manguezais e grandes áreas cársticas com cavernas. No entanto, a fauna de quirópteros é pouco conhecida, e o estado contém lacunas importantes sobre a ocorrência e distribuição de morcegos no Brasil. Para reduzir essa lacuna de informação, com base em uma revisão da literatura científica e coleções regionais de mamíferos, listamos 42 espécies de morcegos, incluindo novas ocorrências para 13 espécies e discusões sobre seu estado de conservação. Os resultados mostram que mais de metade (54%) das espécies registradas são morcegos filostomídeos e cerca de um terço dos morcegos no estado se abrigam em cavidades subterrâneas. A Caatinga abrigou a maior riqueza de morcegos no estado, incluindo a ocorrência de quatro espécies vulneráveis (Furipterus horrens, Lonchorhina aurita, Natalus macrourus e Xeronycteris vieirai). A Mata Atlântica precisa ser mais amostradas, incluindo manguezais, habitats costeiros e áreas de Caatinga principalmente na região central do estado (planalto da Borborema), que são virtualmente inexplorados. Embora o recente aumento das investigações no estado em relação aos morcegos, estudos futuros devem complementar os métodos convencionais de captura com procura ativa de abrigos e monitoramento bioacústico para obter melhores dados na tarefa de desvendar a diversidade de morcegos do Rio Grande do Norte.
Palavras-chave: Caatinga, Chiroptera, Espécies vulneráveis, distribuição de espécies, Mata Atlântica.
143
INTRODUCTION About one-quarter of the Brazilian mammal species are bats (Paglia et al. 2012), currently comprising 183 known species (Nogueira et al. 2014, Feijó et al. 2015a, Fischer et al. 2015, Moratelli & Dias 2015, Gregorin et al. 2016, Rocha et al. 2016). Considering that
Brazil harbors one of the largest mammal diversities in the world, its bat fauna is poorly known. Bat records indicate that less than 10% of the Brazilian territory can be considered minimally sampled, and about 60% has no single formal record of bat species (Bernard et al.
2011).
The state of Rio Grande do Norte (RN) represents a conspicuous gap of bat information in
Brazil (Bernard et al. 2011). The earliest records of bats in RN date back to the past century, when
Sanborn (1937), Goodwin (1959), Webster (1993), and Jones & Hood (1993) reported few bat records from the coastal region of the state (municipality of Natal) and deposited the specimens in biological collections in United States. Studies on bats in RN slowly began to increase in this century, with new records and distributional expansions (Feijó & Nunes 2010, Barros 2014, Basílio et al. 2017), ecology and natural history (Cordero-Schmidt et al. 2016, Cordero-Schmidt et al.
2017), community diversity (Barros et al. 2017, Vargas-Mena et al. 2018), and subterranean fauna inventories (Ferreira et al. 2010); including a bilbliographic review on the bat fauna in northeastern
Brazil by Garcia et al. (2014). Such studies together have recorded a richness of 38 species of bats in the state.
Despite the recent efforts in describing the bat fauna of RN, there are still gaps of knowledge.
In addition, bat diversity and species distribution are poorly known in the state, and it is important for conservation strategies and policies (Costa et al. 2005). Therefore, we present an updated list of bat species based on available mammal collections and literature review in order to describe the bat species composition, distribution and richness that occur within the state’s political boundaries and discuss conservation concerns based on the available data. We expect that this study will inform the scientific community, government agencies, non-governmental organizations, and general society about the diversity of bats that occurr in RN; will point out sites that need increased research
144 efforts; and will be a reference baseline for ecological and diversity assessments, including those for environmental impact studies, to be carried out in the state.
MATERIAL AND METHODS
Study Site
The state of Rio Grande do Norte (RN) is located in the northeastern region of Brazil between the latitudes 4°49'53'' S and 6°58'57" S and longitudes 35°58'03" W and 38°36'12" W. It is limited to the north and the east by the Atlantic Ocean; to the west by the Ceará State, and the south with the state of Paraíba (Fig 3.1). RN has a territorial extension of 52,797 km² and is composed of 167 municipalities, being one of the smallest states in Brazil (IDEMA 2015).
The 95% of the state is characterized by a semiarid climate where the Caatinga domain occurs
(IDEMA 2015). According to Köppen classification, the climate in this portion of the state is BShw
(hot and dry), with a mean annual rainfall of less than 800 mm (Alvares et al., 2013). The Caatinga is a seasonally dry tropical forest composed by mosaics of xeric spiny shrub lands, columnar cacti, succulents, and deciduous woody forest stands (arboreal caatingas) (Leal et al. 2003). Physiognomy and plant composition variations determine eight different ecoregions in the Caatinga; however, only two occur in RN: the Northern Sertaneja Depression (NSD) and the Borborema Highlands
(BH) (see Velloso et al. 2002). The NSD is characterized by extensive low plains, with elevations varying from 20-500 meters. The vegetation type is spiny shrub lands with herbaceous plants and remnants of arboreal Caatinga on slopes and low mountain ranges, and on main river valleys there are ciliary remnants of Carnaúba palms (Copernicia prunifera). The BH ecoregion is mountainous with steep slopes and rugged relief, with rocky outcrops of granite. The altitude varies from 150-
650 m and the vegetation is characterized by a shrubby-arboreal Caatinga with columnar cacti and arboreal Caatingas in more humid areas on the tops of the mountains.
On the east coast of the state, according to Köppen classification, the climate type is Aw with precipitations varying from 700-1500 mm (Alvares et al., 2013). This region harbors the northernmost distribution of the Atlantic Forest in Brazil (IDEMA 2015). The RN’s Atlantic Forest
145 is composed of remnants of evergreen and semi-evergreen forests stands, dunes, short bushy-forests on fixed dunes (known as “restingas”), and mangroves (INPE/SOS Mata Atlântica 2014). Ecotones occur in contact areas of Caatinga and Atlantic Forest.
Finally, RN contains an important speleological heritage with the occurrence of extensive calcareous outcrops or “lajedos” that harbors numerous caves. Most of caves occur in the northern and western region of the state in the Caatinga (Cruz et al. 2010), with the majority of caves located in the NSD ecoregion. RN has the fourth highest number of underground cavities in Brazil with more than 1000 recorded caves (Bento et al. 2017).
Data collection
To find bat records within the political boundaries of RN, we searched in regional mammal collections (as primary data) and specialized bibliographic reviews (as secondary data). Primary data consisted of bat records in the mammal collections of the Universidade Federal de Pernambuco
(UFPE) and the Universidade Federal of Rio Grande do Norte (UFRN) (Coleção Mastozoológica
Adalberto Varela, CMAV). We only considered specimens with voucher number and location
(geographic coordinates and municipality). We examined all bat specimens (N = 166) currently deposited at CMAV (except one specimen without specific collection site data), and all bat specimens deposited at UFPE (N = 128) that where collected in RN. The species were identified using taxonomic keys of Neotropical bats, such as Simmons (1996), Gardner (2008), Gregorin &
Taddei (2002) and Díaz et al. (2016), as well as the original description of species on scientific articles. Specimens with doubtful identifications were confirmed by experts.
Secondary data were obtained from academic online databases (Google Scholar, Periódicos
Capes, ScieELO, Science Direct, and Web of Science) using “Atlantic Forest”, “bat”, “Caatinga”,
“Chiroptera”, “Mata Atlântica”, “morcego”, “quiróptero”, and “Rio Grande do Norte” as keywords.
Also, we consulted books and book chapters that deal with the subject. We compiled all the information available about bats in the state of RN and then selected only records originally published in peer-reviewed literature and books. Among the bat records from peer-reviewed literature and books, we selected only those supported by voucher specimens deposited in public 146 scientific collections. Only the records that met both requirements (publication in peer-reviewed literature/books and availability of vouchers) were included in our list. However, all the bat records found in RN, regardless of presence of voucher specimens, are included in the Supplementary
Material.
The species nomenclature and taxonomic arrangement followed Nogueira et al. (2014) and
Phyllostomidae species followed Baker et al. (2016). We recognized Lonchophylla inexpectata
Moratelli & Dias, 2015 as a different species from Lonchophylla mordax Thomas, 1903 (see
Moratelli & Dias 2015). Finally, we assigned for each species its current international and national conservation status following the IUCN Red List of Threatened Species (IUCN 2016) and Brazil
Red Book of Threatened Species of Fauna (ICMBio/MMA 2016) respectively; its region (Caatinga and Atlantic Forest) of occurrence; locality(ies) of record(s); literature reference(s) and/or collection number(s) when available.
RESULTS
We found 75 published records, of which 38 satisfied our criteria (peer-reviewed literature/books with voucher specimens), plus 66 unpublished records (CMAV and UFPE collections), totalizing 104 bat records included in the final species list (Table 3.1) from 141 bat records inspected (Appendix 2). We found records of 50 bat species among the 141 records
(Appendix 2) and just 42 species according to our criteria for inclusion in the RN list (Table 3.1).
These 42 species represented eight families: Phyllostomidae (23 species), Molossidae (6),
Vespertilionidae (5), Emballonuridae (3), Noctilionidae (2), Furipteridae (1), Mormoopidae (1), and
Natalidae (1). Eight species cited in the literature did not entered in the official list due to absence of voucher specimens, Peropteryx kappleri Peters, 1867; Saccopteryx canescens Thomas, 1901; S. leptura Thomas, 1901; Anoura caudifer (É. Geoffroy, 1818); Artibeus fimbriatus Gray, 1838;
Chiroderma villosum Peters, 1860; Myotis riparius Handley 1960 and M. simus Thomas, 1901.
Records were reported in 21 localities, 18 in the Caatinga and three in the Atlantic Forest
(Figure 2). All localities in the Caatinga corresponded to the NSD, with no records for the BH. The
147 state’s Caatinga presented an accumulated richness of 32 bat species whereas the Atlantic Forest did
22 species. Nineteen species were exclusive to the Caatinga and nine to the Atlantic Forest (Table
3.1). The species with the highest number of collected specimens (with voucher numbers) were
Myotis lavali (31 specimens), Pteronotus gymnonotus (30), Molossus molossus (28), Artibeus planirostris (26), and Glossophaga soricina (22). The species found in more than one locality were
G. soricina (eight localities), Peropteryx macrotis (seven), Myotis lavali (six); and Desmodus rotundus, Carollia perspicillata, and Molossus molossus (four) (Table 3.1).
Regarding the conservation status, 31 species are categorized as Least Concern (LC), three as
Data Deficient (DD), two as Not Evaluated (NE), and only Natalus macrourus is regarded as Near
Threatened (NT) in the IUCN Red List of Threatened Species (UICN, 2016). In the Brazil Red
Book of Threatened Species of Fauna), 34 species are regarded as LC, two as DD, two as NE, and four species are considered Vulnerable (VU) Furipterus horrens, Lonchorhina aurita, Natalus macrourus and Xeronycteris vieira.
Of the 42 species of bats presented herein, 13 are new records for RN which are listed below.
Family Emballonuridae Gervais, 1856
Rhynchonycteris naso (Wied-Neuwied, 1820)
The only known records of this species in the state are two specimens collected close to water in the Poço Branco dam (5°37'48.96" S, 35°39'8.31" W) at 65 m.a.s.l. on 16 November 1990 in a transition area between the Atlantic Forest and Caatinga. Specimens presented pointed and elongated snout, two light and weak stripes on back and forearms (35.9-37.8 mm) with whitish tufts. Specimens are deposited in CMAV. Specimens examined: CMAV 105, 106.
148
Figure 3.1. Map showing site localities where at least one bat has been sampled within the state of Rio Grande do Norte, northeastern Brazil. Coordinates of localities are: Natal (5°50'16.77" S, 35°12'7.38" W), Macaíba (5°51'19.17" S, 35°12'7.38" W), Maxaranguape (5°26'23.35" S, 35°21'19.26" W), Ceará-Mirim (5°37'40.82" S, 35°26'4.45" W), Taipu (5°36'52.07" S, 35°35'38.54" W), João Câmara (5°31'48.98" S, 35°49'59.06" W), Guamaré (5°7’35.42” S, 36°21’38.56” W), Galinhos (5°5’28.63” S, 36°16’54.60” W), Jandaíra (5°22'47.46" S, 36° 8'45.14" W), Nísia Floresta National Forest, Nísia Floresta (6°5'5.44." S, 35°11'2.65" W), Lagoa Salgada (6° 8'59.54" S, 35°31'23.24" W), Nova Cruz (6°26'41.54" S, 35°24'7.17" W), Poço Branco (5°37'48.96" S, 35°39'8.31" W), Lajes (5°51'7.17" S, 36° 9'31.45" W), Seridó Ecological Station, Serra Negra do Norte (6°34'55.46" S, 37°15'9.91" W), Mossoró (5°12'29.13" S, 37°20'50.97" W), Furna Feia National Park, Baraúna/Mossoró (5°3'24.13" S, 37°30'54.03" W), Governador Dix-Sept Rosado (5°23'37.14" S, 37°34'8.54" W), Felipe Guerra (5°34'38.75" S, 37°39'57.03" W), Caraúbas (5°41'10.09" S, 37°35'38.00" W), and Martins (6°2'54.68" S, 37°53'43.99" W).
Family Phyllostomidae Gray, 1825
Subfamily Micronycterinae
Micronycteris megalotis (Gray, 1842)
One specimen collected in a small calcareous outcrop surrounded by scrubby Caatinga vegetation close to the Porco do Mato cave in the Furna Feia National Park, Mossoró-Baraúna municipalities 5°3'24.13" S, 37°30'54.03" W) at 131 m.a.s.l. It presented notch in ear band shallow; 149 similar ventral and dorsal fur coloration; calcar longer than foot; and length of hair on the inner edge of the ear >4 mm. Specimen examined: CMAV 134.
Micronycteris schmidtorum Sanborn, 1935
Known from only one locality in Sítio Santa Rosa in Lajes municipality, where two individuals were captured in a riparian Caatinga close to a water dam (05°49'56.2"S, 36°12'16.0"W) at 295 m.a.s.l. Both specimens presented ventral fur very pale gray to almost white and calcar (10.2
-10.4mm) longer than the foot (6.5-8.5 mm) which differentiates it from other Micronycteris bats with pale ventral fur (Fig 3.3A). Specimens examined: CMVA 140, 145.
Micronycteris sanborni Simmons, 1996
Only one recorded site in the Seridó Ecological Station in Serra Negra do Norte municipality (6°34'55.4" S, 37°15'9.91” W) at 200 m.a.s.l. One adult male, and two females were collected at the edge of a natural lake in Caatinga vegetation. Specimens presented diagnostic characteristics of M. sanborni: gap between I2 and canine, length of calcar similar or shorter (6.6-
8.0 mm) than foot (7.6-8.1 mm), thumb shorter than 7.5 mm (6.8-7.7 mm) and pure white color in ventral fur (Fig 3.3B). Specimens examined: UFPE 3436, 3439, 3440.
Subfamily Glossophaginae
Anoura geoffroyi Gray, 1838
One male collected in Sítio Joazeiro at 230 m above sea level (a.s.l.) at the foothill of the
Serra do Feiticeiro in a semi-open area with patches of scrubby caatinga vegetation, cacti, and some woody trees in Lajes municipality (05º45'55.7"S, 36º12'55.7"W). The specimen presented diagnostic characteristics of A. geoffroyi with no lower incisors, short semicircular uropatagium, and forearm length of 40.2mm. (A. caudifer has forearm of 34-39mm). Specimens examined:
CMAV 144.
Subfamily Lonchophyllinae
Lonchophylla inexpectata Moratelli & Dias, 2015
This recently described species was recorded only at the Serra do Feticeiro in Lajes municipality (5°51'7.1"S, 36° 9'31.4"W) at 325 m.a.s.l. Six specimens were collected and identified
150 as L. inexpectata by their pale-greyish ventral fur on the throat and abdomen that differs from L. mordax which has pale-brownish ventral fur as indicated by Moratelli & Dias (2015) (Fig. 3.4A).
Specimens examined: CMAV 121, 123, 141, 142, 146, 167.
Family Noctilionidae Gray, 1821
Noctilio albiventris Desmarest, 1818
One adult female collected in the Seridó Ecological Station, Serra Negra do Norte on the edge of a natural lake (6°34'55.4" S, 37°15'9.91” W) at 200 m.a.s.l. We also captured an adult in
Sítio Santa Rosa, Lajes municipality (05º49'56.2" S, 36º12'16.0" W) in a drying water reservoir on
10 May 2015, but only biometrical data and photographs data were taken. Specimens presented forearm length less than 70 mm (55.7 mm) which differentiates it from the similar but larger N. leporinus (FA: >70 mm) Specimens examined: UFPE 3427.
Noctilio leporinus (Linnaeus, 1758)
Collected only in two localities of Caatinga. The first record is of an adult male collected and deposited in CMAV on 17 January 1990 in Taipu municipality (5°36'52.07" S, 35°35'38.54"
W) in an ecotone area close to the BR-404 highway with no habitat specification at 30 m of altitude.
The second record corresponds to an adult male captured near a lake (6°34'55.4" S, 37°15'9.91” W) on 18 July 2012 in the Seridó Ecological Station, Serra Negra do Norte municipality at 200 m.a.s.l.
The specimens presented diagnostic characteristics of N. leporinus, forearm length of >70 mm
(82.5-85.4 mm) and legs length exceeding head length that differentiates it from the smaller N. albiventris. Specimens examined: CMAV 037; UFPE 3426.
Family Molossidae Gervais, 1856
Molossops temminckii (Burmeister, 1854)
One adult female captured on 9 March 2013 in a semi-open area in the Seridó Ecological
Station (6°34'55.4" S, 37°15'9.91” W) at 200 m.a.s.l. It presented triangular ears, semi-squared antitragus and forearm less than 34 mm (30.2 mm), which differentiates it from its congener in
Brazil (M. neglectus) that has a forearm greater than 36 mm. Specimen examined: UFPE 3433.
Neoplatymops mattogrossensis (Vieira, 1942)
151
This molossid bat has been captured only in the Seridó Ecological Station in open areas near a natural lake (6°34'55.4" S, 37°15'9.91” W) at 200 m.a.s.l. All six captured specimens presented flattened head, upper incisors separated by a space and granulations or small protrusion in forearms; these characteristics separate N. mattogrossensis from other Neotropical small flat-headed molossids. Specimen examined: UFPE 3421, 3422, 3435, 3437, 3438, 3441.
Nyctinomops macrotis (Gray, 1840)
One adult female found dead on the ground at a wind farm in a coastal Caatinga in
Guamaré municipality, north coast of the state (5°7’35.42” S, 36°21’38.56” W) near sea level. The bat presented damages on head, neck and dorsal area probably caused by a direct collision with the turbine blades. The specimen presented deeply wrinkled lips; joined ears; incisors 1/2, upper incisors parallel to each other; and forearm greater than 55mm (FA= 58.2 mm), characteristic that differentiates it from other smaller Nyctinomops bats in Brazil (FA<55mm). Specimen examined:
CMAV 156.
Family Vespertilionidae Gray, 1821
Eptesicus furinalis (d’Orbigny & Gervais, 1847)
Two specimens collected in different localities. An adult male captured in a house roof in
Galinhos municipality in the coastal Caatinga (5°5’28.63” S, 36°16’54.60” W) at sea level and another adult male captured in garden area on the campus of the Federal University of Rio Grande do Norte (5°50'16.77"S, 35°12'7.38"W), at 45 m.a.s.l. Despite specimens presented forearms lengths of 40.1-41.0 mm that overlaps with smaller individuals of E. brasiliensis (forearm length of
E. furinalis = 37.0 - 41.0 mm and E. brasiliensis = 40-46 mm), both presented characteristics of E. furinalis, narrow but not tapered tragus, short fur (5-6 mm), lower teeth row length less than 6.3 mm, and skull length less than 16.3 mm. Specimens examined: CMAV 150, 164.
Lasiurus ega (Gervais, 1856)
One adult male found dead at a wind farm in Guamaré municipality (5°7’35.42” S,
36°21’38.56” W) near sea level. The bat had damages on the head and dorsal region, probably caused by a collision with turbine blades; however, the skull suffered no damages. The specimen
152 was identified as L. ega due to its olive-yellowish coloration in ventral and dorsal region; hairs covering down to the half of the uropatagium on the dorsal side; and single upper premolars.
Specimen examined: CMAV 151.
DISCUSSION
Species richness
The richness of bats in RN is greater than previously known. Of the 38 species of bats previously reported in RN (Feijó & Nunes 2010, Ferreira et al. 2010, Barros 2014, Garcia et al.
2014, Cordero-Schmidt et al. 2016, Basílio et al. 2017, Cordero-Schmidt et al. 2017, Vargas-Mena et al. 2018) we found vouchers for only 29 species. However, by adding the 13 new species records that we present herein, the number of species with confirmed occurrence in the state is 42 (Table
3.1).
Compared to the neighboring states of Ceará and Paraíba, RN presents a lower bat richness. The state of Paraíba, with a diversity of 58 species (Feijó & Langguth 2011, Ferreira et al. 2013, Nunes et al. 2013, Leal et al. 2014, Beltrão et al. 2015, Vilar et al. 2015), is similar to RN in size and proportion of Caatinga and Atlantic Forest, however, it has been more sampled (Bernard et al.
2011). Similarly, the state of Ceará contains a richer bat diversity (66 species) (Gurgel-Filho et al.
2015, Silva et al. 2015), but its bat fauna has been more studied than for RN, including the firsts surveys on Caatingas’ mammal communities (e.g., Mares et al. 1981, 1985, Willig 1983).
The bat richness found in RNs’ Caatinga was higher than in the states’ Atlantic Forest, probably because of the lower number of collection sites in the latter (Fig 3.1). Since all of sites in
Caatinga are in the NSD, our study contributes to fill the knowledge gap in this part of the ecoregion by adding 15 new localities of bat data collection in relation to the records reported by
Carvalho-Neto et al. (2016). Previous authors, after reviewing the bat species richness in the
Caatinga, warned that the eastern part of the NSD and the north of the BH have not been comprehensively investigated. Based on Velloso et al. (2002) ecoregions of Caatinga, our map (Fig.
3.2) does not show records in the Borborema Highlands, thus the bat fauna of the northern distribution of this ecoregion is poorly known. 153
Table 3.1: List of bat species recorded in the state of Rio Grande do Norte, northeastern Brazil, including conservation status according to International Union for Conservation of Nature (IUCN) and Brazilian Ministry of Environment (Ministério do Meio Ambiente, MMA), localities, voucher numbers and references of original records. Conservation status: LC ‒ Least Concern; DD ‒ Data Deficient; NE ‒ Not Evaluated; NT ‒ Near Threatened. Ecoregions are Atlantic Forest (AF) and Caatinga (Caat). Localities are: Natal (1), Macaíba (2), Maxaranguape (3), Ceará-Mirim (4), Taipu (5), João Câmara (6), Guamaré (7), Galinhos (8), Jandaíra (9), Nísia Floresta National Forest, Nísia Floresta (10), Lagoa Salgada (11), Nova Cruz (12), Poço Branco (13), Lajes (14), Seridó Ecological Station, Serra Negra do Norte (15), Mossoró (16), Furna Feia National Park, Baraúna/Mossoró (17), Governador Dix-Sept Rosado (18), Felipe Guerra (19), Caraúbas (20), and Martins (21); coordinates are found in Figure 1. Voucher specimens presented in collection number column correspond to the oldest specimen recorded in each locality. All collection numbers of revised specimen are found in Supplementary table. References in the original record column corresponds to the study who first recorded the species in the state. Collections abbreviations: CAS ‒ California Academy of Science; CMAV ‒ Coleção de Mamíferos Adalberto Varela, Universidade Federal do Rio Grande do Norte; CMUFS ‒ Coleção de Mamíferos da Universidade Federal de Sergipe; MZUSP ‒ Museu de Zoologia da Universidade de São Paulo; UFPB ‒ Coleção de Mamíferos da Universidade Federal da Paraíba; UFPE ‒ Coleção de Mamíferos da Universidade Federal de Pernambuco; USNM ‒ United States National Museum. New species records are indicated with an asterisk (*).
Ecoregion Family / Subfamily / IUCN / Localities Collection number Original record Species MMA AF Caat
Emballonuridae Gervais, 1856
Emballonurinae
Peropteryx leucoptera LC X 10 UFPE 3193 Barros et al. 2017 Peters, 1867
Peropteryx macrotis LC X X 1, 9, 13, 14, USNM (not informed), Sanborn 1937; Vargas- (Wagner, 1843) 18, 19, 20 CMAV 111, CMAV 107, Mena et al. 2018; This CMAV 122, CMAV 130, study CMAV 129, CMAV 131
Rhynchonycteris naso LC X 13 CMAV 105 This study (Wied-Neuwied, 1820) *
Phyllostomidae Gray, 1825
Micronycterinae
Micronycteris megalotis LC X 17 CMAV 134 This study (Gray, 1842) *
Micronycteris schmidtorum DD X 15 CMAV 140, CMAV 145 This study Sanborn, 1935 *
Micronycteris sanborni LC X 14 UFPE 3436 This study Simmons, 1996 *
Desmodontinae
Desmodus rotundus (É. LC X X 6, 10, 13, CMAV 117, UFPE 3306, Barros et al. 2017; This Geoffroy, 1810) 17 CMAV 038, CMAV 070 study
154
Diphylla ecaudata Spix, LC X 20 CMAV 135 Vargas-Mena et al. 2018 1823
Lonchorhininae
Lonchorhina aurita Tomes, LC / VU X 19 CMAV 128 Vargas-Mena et al. 2018 1863
Phyllostominae
Chrotopterus auritus LC X 21 CMUFS 259 Basílio et al. 2017 (Peters, 1856)
Lophostoma brasiliense LC X 10 UFPE 2181 Barros et al. 2017 Peters, 1866
Phyllostomus discolor LC X X 2, 5, 10 CMAV 018, CMAV 039, Barros et al. 2017; This (Wagner, 1843) UFPE 3247 study
Phyllostomus hastatus LC X 10 UFPE 3225 Barros et al. 2017 (Pallas, 1767)
Tonatia bidens (Spix, 1823) DD X 20 CMAV 138 Vargas-Mena et al. 2018
Trachops cirrhosus (Spix, LC X X 10, 14 UFPE 3266, CMAV 069 Barros et al. 2017; This 1823) study
Glossophaginae
Anoura geoffroyi Gray, LC X 14 CMAV 144 This study 1838 *
Glossophaga soricina LC X X 1, 4, 5, 10, CAS (not informed Barros et al. 2017; (Pallas, 1766) 12, 14, 15, number), CMAV 015, Vargas-Mena et al. 2018; 16 CMAV 061, UFPE 3257, Webster 1993; This study CMAV 002, CMAV 124, UFPE 3423, CMAV 147
Lonchophyllinae
Lonchophylla mordax NT / LC X 15 CMAV 142, UFPE 3424 This study Thomas, 1903*
Lonchophylla inexpectata NE X 14, 16 CMAV 121, CMAV 149 Vargas-Mena et al. 2018; Moratelli & Dias, 2015 * This study
Xeronycteris vieirai DD / VU X 14 CMAV 143 Cordero-Schmidt et al. Gregorin & Ditchfield, 2005 2017
Carollinae
Carollia perspicillata LC X X 5, 6, 10, 17 CMAV 044, CMAV 120, Barros et al. 2017; This (Linnaeus, 1758) UFPE 3290, CMAV 136 study
155
Subfamily Stenodermatinae
Artibeus lituratus (Olfers, LC X 1, 10 CMAV 159, UFPE 3288 Barros et al. 2017; This 1818) study
Artibeus planirostris (Spix, LC X X 1, 5, 10, 15 CMAV 004, CMAV 067, Barros et al. 2017; This 1823) UFPE 3200, UFPE 3083 study
Dermanura cinerea LC X 1, 10 USNM (not informed Barros et al. 2017; Gervais, 1856 number), UFPE 3299 Handley 1987
Platyrrhinus lineatus (É. LC X 1, 10 CMAV 012, UFPE 3208 Barros et al. 2017; This Geoffroy, 1810) study
Sturnira lilium (É. LC X 1, 10 CMAV 161, UFPE 3265 Barros et al. 2017; This Geoffroy, 1810) study
Mormoopidae Saussure, 1860
Pteronotus gymnonotus LC X 6, 19 CMAV 075, CMAV 125 Vargas-Mena et al. 2018; (Wagner, 1843) This study
Noctilionidae Gray, 1821
Noctilio albiventris LC X 15 UFPE 3427 This study Desmarest, 1818 *
Noctilio leporinus LC X 5, 15 CMAV 037, UFPE 3426 This study (Linnaeus, 1758) *
Furipteridae Gray, 1866
Furipterus horrens (Cuvier, LC / VU X 17, 20 CMAV 137, CMAV 132 Vargas-Mena et al. 2018 1828)
Natalidae Gray, 1866
Natalus macrourus NT / VU X X 1, 16, 19 USNM 242830, CMAV Goodwin 1959; Vargas- (Gervais, 1856) 148, CMAV 126 Mena et al. 2018
Molossidae P. Gervais, 1856
Molossinae
Molossops temminckii LC X 15 UFPE 3433 This study (Burmeister, 1854) *
Molossus molossus (Pallas, LC X X 1, 2, 8, 11 CMAV 001, CMAV 023, Barros 2014; This study 1766) CMAV 152, UFPE 3068
156
Neoplatymops LC X 15 UFPE 3421 This study mattogrossensis (Vieira, 1942) *
Nyctinomops aurispinosus LC X 3 USNM 3726 Shamel 1931 (Peale, 1848)
Nyctinomops macrotis LC X 7 CMAV 156 This study (Gray, 1840) *
Promops nasutus (Spix, LC X X 7, 10 CMAV 154, UFPE 3218 Barros et al. 2017; This 1823) study
Vespertilionidae Gray, 1821
Vespertilioninae
Eptesicus furinalis LC X X 1, 8 CMAV 164, CMAV 150 This study (d’Orbigny & Gervais, 1847) *
Lasiurus blossevillii LC X 10 UFPE 3199 Barros et al. 2017 ([Lesson, 1826])
Lasiurus ega (Gervais, LC X 7 CMAV 151 This study 1856) *
Myotinae
Myotis lavali Moratelli, NE X X 1, 2, 6, 8, CMAV 010, CMAV 043, Barros et al. 2017; This Peracchi, Dias & Oliveira, 10, 15 CMAV 005, CMAV 153, study 2011 UFPE 3181, UFPE 3442
Myotis nigricans (Schinz, LC X 12 UFPB 1631 Feijó & Nunes 2010 1821)
Although the Atlantic Forest showed only three localities of bat collections, the richness
difference with the Caatinga is not large – a difference of 10 species. Considering that the Atlantic
Forest in Brazil is richer in bat species than the Caatinga (Paglia et al. 2012), it is likely that an
increase in research in this region will yield a higher richness than what was found in this study.
Phyllostomid bats represented more than half of the species records (54%). This proportion is
similar to other Brazilian states, with the occurrence of Atlantic forest and Caatinga, like in Paraíba
(Feijó & Langguth 2011) and Sergipe (Leal et al. 2013). Such dominance was expected since
157
Phyllostomidae is the richest family in Brazil (Nogueira et al. 2014) and in the Neotropics (Solari &
Martínez-Arias 2014).
Furthermore, all bat studies in RN were done using mist nets, a type of methodology heavily biased towards the capture of phyllostomids than species of other families (Barnett et al. 2006).
Consequently, the diversity of aerial insectivorous bats, such as members of the Emballonuridae,
Molossidae, and Vespertilionidae families, are poorly known in RN, probably because all of the studies conducted in RN used mainly mist-nets. Acoustic samplings (recordings of bat echolocation calls) detect aerial insectivores not sampled by conventional capture methods (Simmons & Voss
1998) and, thus, this method should be used together with bat captures to increase inventory completeness (MacSwiney et al. 2008). Moreover, in Neotropical dry forests where nearly half of the species are open-space insectivores, Silva & Bernard (2017) found that different bat species were detected using solely mist nets or bioacoustics, therefore authors conclude that a combination of both techniques is essential to achieve the local bat diversity in Caatinga areas.
The search for day roosts is another good alternative to increase the knowledge on bat species richness of the state. Caves are an important roost for local bat populations considering the high number of underground cavities that occur in RN. Inventories in such areas are likely to provide new species occurrences, and to contribute to a better understanding of the bat species distribution in the state. For instance, 17 species of bats have been already recorded to roost in RN’s caves
(Vargas-Mena et al. 2016, Cordero-Schmidt et al. 2017), this is one-third of the total bat species presented here.
The bat diversity in Brazil is still being discovered as recent taxonomic revisions of specimens in the biological collections have led to the description of new bat species. For instance, of these recently described species, Myotis lavali (Moratelli et al. 2011) and Lonchophylla inexpectata occur in RN. Myotis lavali was recently described from the Myotis nigricans (Schinz,
1821) complex after specimens’ revision in biological collections. We revised M. nigricans specimens from CMAV and UFPE that occur in RN and all of them corresponded to M. lavali. The only record of M. nigricans in the state was provided by Feijó & Nunes (2010) from Nova Cruz
158 municipality, close to Paraíba state; however, we did not have access to the collected specimen to confirm the taxon. Similarly, L. inexpectata was described from L. mordax by Moratelli & Dias
(2015) after specimens’ revision in biological collection, and is currently endemic to Caatinga.
The confirmation of the species that we found in the literature review without vouchered specimens is needed. Of those seven non-confirmed species, for Peropteryx kappleri we did not find any locality or record whatsoever, despite Garcia et al. (2014) record it in the state. The remaining six species were recorded by Farias (2009) (see Supplementary Material) in a small
Atlantic Forest patch in the Jiquí Public Park in Parnamirim municipality. Considering the possible presence of these species in the state, we call the attention to future bat studies in the Atlantic Forest to collect and confirm their occurrence.
1. New species records
Here, we presented 13 bat species with no previous record in RN, which increases our knowledge on the occurrence and distribution of the chiropteran fauna of RN and Brazil. Species such as Rhynchonycteris naso, Micronycteris megalotis, M. sanborni, Anoura geoffroyi, Noctilio albiventris, N. leporinus, Molossops temminckii, Neoplatymops mattogrossensis, Eptesicus furinalis, and Lasiurus ega have been already recorded in the neighboring states of Paraíba (Feijó &
Langguth 2011) and Ceará (Gurguel-Filho et al. 2015), therefore, their occurrence was expected in
RN.
Two pale-bellied species of Micronycteris (M. schmidtorum and M. sanborni) were found to occur in the state (Fig. 3.2). Both records represent a northward expansion of the distribution of these species in Brazil. Micronycteris schmidtorum has a wide distribution in Brazil but records in the Caatinga are scarce (Rocha et al. 2017) and the closest locality is from Exu, Pernambuco State
(Ascorra et al. 1991) – about 430 km from our record in Lajes. However, there is a closer record about 146 km southeast from Lajes in the Atlantic Forest in Guaribas Biological Reserve in Paraíba
State (Rocha et al. 2017). M. sanborni is endemic to Brazil and known from 10 scattered localities
(Feijó et al. 2015b). We only found it in the Seridó Biological Station and its closest previous record is from 42.6 km south in Patos in the Caatinga of Paraíba State (Feijó et al. 2015b).
159
However, M. sanborni might be more common than previously thought because it is difficult to differentiate from other sympatric pale-bellied Micronycteris bats in Brazil. We encourage special attention when identifying this bat species to avoid misidentification and to better understand their distribution and habitat preferences.
Figure 3.2. Ventral pelage of A Micronycteris schmidtorum (CMAV 145) and B Micronycteris sanborni (UFPE 3440). Note very pale gray almost white color of the ventral fur of A that differs from pure white color of B. Lengths of foots, calcars and thumbs of A and B are found in results. Scale bar 10 mm
The record of L. inexpectata in RN, specifically at the Serra do Feticeiro in Lajes, expands the distribution of the species northeastwards about 430 km from the closest record in Exu,
Pernambuco State (Moratelli & Dias 2015). This record is noteworthy since the species has been registered only in the states of Bahia and Pernambuco (Moratelli & Dias 2015), where it is considered endemic to Caatinga (Gutiérrez & Marinho-Filho 2017). However, sympatry in certain areas of the Caatinga of L. inexpectata with L. mordax can be found – L. mordax occurs along the eastern border of the Caatinga and the Atlantic Forest-Caatinga ecotone. We found both species in sympatry in Lajes, however its differentiation in the field is fuzzy which difficult identification (R.
Moratelli pers. comm.). Although these two species can be differentiated by mandibular length
160
(MAL) and ventral fur color (VFC) (L. mordax, MAL 15.5-17.0 mm, VFC pale brown; L. inexpectata MAL 14.1-16.3 mm, VFC whitish or pale gray on neck and abdomen), the six analyzed specimens of Lonchophylla of Lajes presented overlapping MAL (15.4-16.2 mm). Therefore, external characters for differentiating these species were restricted to the VFC (Fig. 3.3).
Regarding Nyctinomops macrotis, the species has been recorded mainly in the Atlantic Forest but as well in other regions; in Caatinga it is known for just one locality (Rocha et al. 2015).
However, the record of N. macrotis in Guamaré expands the species distribution northeastward about 740 km from the closest record in Boqueirão da Onça in Bahia State (Rocha et al. 2015). This second record suggest that the species might occur in other areas of the Caatinga, thus, acoustic surveys should be done in order to detect this or other molossid bats in RN.
Figure 3.3. Ventral pelage of A Lonchophylla inexpectata (CMAV 167) and B Lonchophylla mordax (CMAV 149). Note the pale-greyish ventral fur on the throat and abdomen of A that differs from the pale-brownish ventral fur of B. Scale bar 10 mm.
Conservation panorama
Four threatened bat species in Brazil occur in RN, corresponding to the 57% of the
Brazilian threatened bat species (see ICMBio/MMA 2016). Furipterus horrens, Natalus macrourus,
Lonchorhina aurita and Xeronycteris vieirai are vulnerable species (VU), a high extinction risk 161 category (ICMBio/MMA 2016). Moreover, F. horrens and L. aurita roost mainly in caves (Reis et al. 2007), N. macrourus is cave-dependent (Tejedor & Davalos 2016) and, X. vieirai, is only known to roost in caves (Cordero-Schmidt et al. 2017). Therefore, their conservation status is linked to their dependence on cave roosts (Sagot & Chaverri 2015). Bats species that rely on a single roost type are linked to higher extinction risks, and management actions to preserve such species should prioritize the protection of roosting sites (e.g., cave-dependent species) (Sagot & Chaverri 2015).
Consequently, the possible presence of these species should be considered when biospeleological inventories and cave-use licensing is carried out in the states’ caves.
On the other hand, according to the IUCN international criteria, all bats that occur in RN are at lower risk of extinction, where just N. macrourus and L. mordax are near threatened (NT). This categorization was different from what we found at national level. Such a mismatch between these assessments, where species are considered nationally but not globally threatened, represents cases of globally common and stable species that are rather rare or declining at a local or regional level
(Brito et al. 2010). However, L. mordax, previously classified as least concern (LC), is categorized as NT because now its distribution is restricted to just in three localities in eastern Brazil as consequence of its separation with L. inexpectata (Sampaio et al. 2016). Regarding this latter species, the IUCN has not yet evaluated its conservation status in Brazil, and it was therefore not included in threatened species lists (Gutiérrez & Marinho-Filho 2017). Given the endemic condition of L. inexpectata (Caatinga) and L. mordax (Eastern Brazil) their extinction risks should be assessed soon at the national and global level.
The evaluation of the distribution and analysis of pressures and threats to these vulnerable species is needed to assess their conservation needs. For instance, the vulnerable N. macrourus has already lost 54% of its habitat in Brazil, and only 4% of its potential distribution of the species is located within fully protected areas (Delgado-Jaramillo et al. 2017). In RN, only F. horrens and N. macrourus have populations integrally protected in the Furna Feia National Park in Baraúna and
Mossoró municipalities (Vargas-Mena et al. in press), while X. vieirai and L. aurita occur in no protected areas. The natural vegetation in RN has suffered substantial human impacts, only the 11%
162 the state is under some protected area (Bento et al. 2013). The Atlantic Forest has been reduced by agricultural activities and urban expansion in coastal areas (INPE/SOS Mata Atlântica 2014), whereas Caatinga has suffered deforestation for human use and cattle activities that make it susceptible to desertification (Santos et al. 2011). Such human activities are already known to negatively affect the integrity of bat communities and their populations around the world (Furey &
Racey 2016). Furthermore, RN has currently 125 wind farms, being the largest producer of wind energy in Brazil (ABBEólica 2017). Wind turbine facilities can cause high mortality among aerial insectivore bats (Barros et al. 2015, Schuster et al. 2015, Hein & Schirmacher 2016, O'Shea et al.
2016, Frick et al. 2017). Bat occurrences in the areas of wind farms, as well as the possible impacts of wind turbines on bats, are still unknown (Bernard et al. 2014). For instance, some of the new species records presented herein (e.g., N. macrotis and L. ega) are based on single specimens found dead probably by wind turbines in wind parks.
Main knowledge gaps
Although this study updates information regarding the bat fauna of RN, several gaps of knowledge on the distribution of bat species still remains in the state (Fig 3.1). Therefore, we propose additional effort of research and inventories in the following areas:
▪ The Northern Sertaneja Depression: all records of bats in the states’ Caatinga are in this
ecoregion. According to the distribution of the bat records, however the central region
presented the most evident gap, and bat inventories are encouraged in such area. Moreover,
most of protected areas of the state are found in this ecoregion and the Seridó Ecological
Station in Serra Negra do Norte, the Açu National Forest in Açu and the Furna Feia
National Park in Mossoró-Baraúna are areas where the bat fauna is poorly known and
should be priorities for inventories in the state.
▪ The Borborema Highlands and other mountainous ranges in the central and southwestern
region: this mountain ranges (ranging from 400–800 m of altitude), characterized by more
humid areas with Caatinga vegetations, are virtually unexplored regarding bats, and
particular assemblages are expected to occur in these areas. For instance, in the Serra do 163
Feticeiro in Lajes do Cabugi, all five species of nectar feeding bats registered in the state
are found in this sierra, including endemic and vulnerable species such as Xeronycteris
vieirai and Lonchophylla inexpectata (Cordero-Schmidt et al., 2017). Considering that no
conservation units are found in BH and other mountainous ranges, the sierras in the
municipalities of Serra de Santana, Cerro Corá, Coronel Ezequiel, São Tomé Martins,
Portalegre, Serrinha dos Pintos, and Luís Gomes, should be explored.
▪ Transitional areas of Caatinga with mangroves and coastal habitats all along the north coast
such as in the municipalities of Dunas do Rosado, Galinhos, and Caiçara do Norte are
unique ecotones with no data regarding bats, including the State Sustainable Development
Reserve (RDS) Ponta do Tubarão, in Macau and Guamaré municipalities.
▪ Ecotone areas alongside the contact of Caatinga and Atlantic Forest are known as
“Agreste”, where bat communities may contain a mixture of species of both ecoregions.
▪ The southeastern region where there are remnants of Atlantic Forest; some of them in
protected areas such as Private Reserve of Natural Heritage Mata da Estrela, in Baía
Formosa municipality (the largest Atlantic Forest patch of RN), the northern part of the
Nísia Floresta National Forest, in Nísia Floresta municipality (Barros et al. 2017), the
Environmental Protection Area (APA) Jenipabú in Natal and Extremoz municipalities, and
the Dunas State Park in Natal, one of the biggest urban park in Brazil.
▪ The Mangrove in the east and north coast are also unexplored.
▪ Finally, the karstic areas located in Mossoró, Baraúna, Felipe Guerra, Apodi, Governador
Dix-Sept Rosado, and Jandaíra municipalities are sites with high density of underground
cavities and potential sites to roost a wide diversity of bats. For instance, the Furna Feia
cave located in the Furna Feia National Park harbors up to 10 species, the richest in the
state (Vargas-Mena et al. 2018).
Despite the small size of RN, the state has a potential to be an important refuge for bat diversity in northeastern Brazil, as long as bat inventories and specimens’ collection increases in the future. Finally, bat inventories, including those for environmental impact studies, should
164 complement conventional capture methods with bioacoustical monitoring and active searching of roost places to obtain a complete understanding of the bat fauna of Rio Grande do Norte.
REFERENCES
ABBEÓLICA. 2017. Dados Mensais da Associação Brasileira de Energia Eólica – abril de 2017. São Paulo, ABEEólica. Available in: http://www.abeeolica.org.br/wp- content/uploads/2017/04/Dados-Mensais-ABEEolica-04.2017.pdf
ALVARES, C.A., STAPE, J.L., SENTELHAS, P.C., DE MORAES, G., LEONARDO, J. & SPAROVEK, G. 2013. Köppen's climate classification map for Brazil. Meteorol. Z. 22(6), 711– 728.
ASCORRA, C. F., WILSON, D. E., & GARDNER, A. L. 1991. Geographic distribution of Micronycteris schmidtorum sanborn (Chiroptera: phyllostomidae). P. Biol. Soc. Wash. 104(2):351– 355.
BAKER, R.J., SOLARI, S., CIRRANELLO, A. & SIMMONS, N. B. 2016. Higher level classification of phyllostomid bats with a summary of DNA synapomorphies. Acta Chiropterol. 18(1):1–38.
BARNETT, A.A., SAMPAIO, E.M., KALKO, E.K.V., SHAPLEY, R.L., FISCHER, E., CAMARGO, G. & RODRÍGUEZ-HERRERA, B. 2006. Bats of Jaú National Park, central Amazonia, Brazil. Acta Chiropterol. 8: 103–128.
BARROS, M.A.S. 2014. First record of Molossus molossus (Pallas, 1766) (Mammalia: Chiroptera) in the state of Rio Grande do Norte, northeastern Brazil. Check List 10(6):1520–1524.
BARROS, M.A., MAGALHÃES, R.G. & RUI, A.M. 2015. Species composition and mortality of bats at the Osório Wind Farm, southern Brazil. Stud. Neotrop. Fauna E. 50(1):31–39.
BARROS, M.A., MORAIS, C.M.G., FIGUEIREDO, B.M.B., MOURA JÚNIOR, G.B.D., RIBEIRO, F.F.D.S., PESSOA, D.M.A., ITO, F. & BERNARD, E. 2017. Bats (Mammalia, Chiroptera) from the Nísia Floresta National Forest, with new records for the state of Rio Grande do Norte, northeastern Brazil. Biota Neotrop. 17(2): e20170351.
BASÍLIO, G.H.N., ARAUJO, J.P.M., VARGAS-MENA, J.C., ROCHA, P.A. & KRAMER, M.A.F. 2017. Chrotopterus auritus (Chiroptera, Phyllostomidae): first record for the state of Rio Grande do Norte, northeastern Brazil. Check List. 13(3): 2110.
BENTO DM, JC BRANDÃO, DJ DOS SANTOS, JIM FREITAS, UP CAMPOS & RFR SOUZA. 2013. Parque Nacional da Furna Feia: o parque nacional com a maior quantidade de cavernas do brasil. In Congresso Brasileiro de Espeleologia (M.A. Rasteiro & L. Morato, coord.). Sociedade Brasileira de Espeleologia Barreiras, Bahia, p.31–43.
BENTO, D.M., CRUZ, J.B., FREITAS, J.I.M., CAMPOS, U.P. & OLIVEIRA, A.F. 2017. A mais de 1000! O patrimônio espeleológico potiguar após a descoberta da milésima caverna. In Congresso Brasileiro de Espeleologia (R.M. Rasteiro, C.M. Teixeira-Silva, S.G. Lacerda, coord.). Sociedade Brasileira de Espeleologia, Ouro Preto, p.227–237. 165
BELTRÃO, M.G., ZEPPELINI, C.G., FRACASSO, M.P.A. & LOPEZ, L.C.S. 2015. Bat inventory in a Caatinga area in Northeastern Brazil, with a new occurrence in the state of Paraíba. Neotrop. Biol. Conserv. 10(1):15–20.
BERNARD, E., AGUIAR, L. & MACHADO, R.B. 2011. Discovering the Brazilian bat fauna: a task for two centuries? Mammal Rev. 41:23–39.
BERNARD, E., PAESE, A., MACHADO, R.B. & DE SOUZA AGUIAR, L.M. 2014. Blown in the wind: bats and wind farms in Brazil. Nat. Conservação 12(2):106–111.
BRITO, D., AMBAL, R.G., BROOKS, T., DE SILVA, N., FOSTER, M., HAO, W., HILTON- TAYLOR, C., PAGLIA, A., RODRÍGUEZ, J.P. & RODRÍGUEZ, J.V. 2010. How similar are national red lists and the IUCN Red List? Biol. Conserv. 143(5):1154–1158.
CARVALHO-NETO, F.G., DA SILVA, J.R., SANTOS, N., ROHDE, C., GARCIA, A.C.L. & MONTES, M.A. 2017. The heterogeneity of Caatinga biome: an overview of the bat fauna. Mammalia, 81(3):257–264.
CORDERO-SCHMIDT, E., MEDEIROS-GUIMARÃES, M., VARGAS-MENA, J.C., CARVALHO, B., FERREIRA, R.L., RODRIGUEZ-HERRERA, B. & VENTICINQUE, E.M. 2016. Are leaves a good option in Caatinga's menu? First record of folivory in Artibeus planirostris (Phyllostomidae) in the semiarid forest, Brazil. Acta Chiropterol. 18(2):489–497.
CORDERO-SCHMIDT, E., BARBIER, E., VARGAS-MENA, J.C., OLIVEIRA, P.P., SANTOS, F.A.R., MEDELLÍN, R.A., RODRIGUEZ-HERRERA, B. & VENTICINQUE, E.M. in press. Natural history of the Caatinga endemic Vieira’s Flower Bat, Xeronycteris vieirai. Acta Chiropterol. 19(2):399-408.
COSTA, L.P., LEITE, Y.L.R., MENDES, S.L. & DICHTFIELD, A.D. 2005. Conservação de Mamíferos no Brasil. Megadiversidade 1(1):103–112.
CRUZ, J.B., BENTO, D.M., BEZERRA, F.H.R., FREITAS, J.I. & CAMPOS, U.P. 2010. Diagnóstico Espeleológico do Rio Grande do Norte. Rev. Bras. Espeleo. 1:1–24.
DELGADO-JARAMILLO, M., BARBIER, E. & BERNARD, E. 2017. New records, potential distribution, and conservation of the Near Threatened cave bat Natalus macrourus in Brazil. Oryx 1–8 doi:10.1017/S0030605316001186.
DÍAZ, M.M., SOLARI, S., AGUIRRE, L.F., AGUIAR, L. & BARQUEZ, R.M. 2016. Clave de identificación de los murciélagos de Sudamérica/Chave de identificação dos morcegos da América do Sul. Publicación Especial 2, Programa de Conservación de los Murciélagos de Argentina, Tucumán, Argentina, p.160.
FARIAS, F.H.C. 2009. Caracterização biológica e zoneamento ambiental do Parque Estadual do Jiquí/RN, Brasil: subsídios ao plano de manejo. Master thesis, Animal biology department, Science faculty, Lisbon University, Lisbon, Portugal.
FEIJÓ, J.A. & NUNES, H.L. 2010. Primeiro registro de Myotis nigricans (Schinz, 1821) para o estado do Rio Grande do Norte, nordeste do Brasil. Chiropt. Neotrop. 16(1):531–534.
FEIJÓ, J.A. & LANGGUTH, A. 2011. Lista de quirópteros da Paraíba, Brasil com 25 novos registros. Chiropt. Neotrop. 17(2):1055–1062.
166
FEIJÓ, A., ROCHA, P.A. & ALTHOFF, S.L. 2015a. New species of Histiotus (Chiroptera: Vespertilionidae) from northeastern Brazil. Zootaxa 4048(3):412–427.
FEIJÓ, A., ROCHA, P.A. & FERRARI, S. F. 2015b. How do we identify Micronycteris sanborni Simmons, 1996 (Chiroptera, Phyllostomidae) reliably and where we can find this species in South America? Pap. Avulsos de Zool. (São Paulo) 55(20).
FERREIRA, R.P., PROUS, X., BERNARDI, L.O.F. & SOUZA-SILVA, M. 2010. Fauna subterrânea do estado do Rio Grande do Norte: caracterização e impactos. Rev. Bras. Espeleo. 1(1):25–51.
FERREIRA, A.P., CARVALHO-MELO, D. & LOURES-RIBEIRO, A. 2013. Diclidurus albus Wied-Neuwied, 1820 (Chiroptera: Emballonuridae): first record of the species in the state of Paraíba, Brazil. Check List 9(4):793–796.
FISCHER, E., SANTOS, C.F., CARVALHO, L.F.A.C., CAMARGO, G., CUNHA, N.L., SILVEIRA, M., BORDIGNON, M.O. & SILVA, C.L. 2015. Bat fauna of Mato Grosso do Sul, southwestern Brazil. Biota Neotrop. 15(2):e20140066. http://dx.doi.org/10.1590/1676- 06032015006614 (last access on 25/Apr/2017).
FRICK, W.F., BAERWALD, E.F., POLLOCK, J.F., BARCLAY, R.M.R., SZYMANSKI, J.A., WELLER, T.J., RUSSELL, A.L., LOEB, S.C., MEDELLIN, R.A. & MCGUIRE, L.P. 2017. Fatalities at wind turbines may threaten population viability of a migratory bat. Biol. Conserv. 209:172–177.
FUREY, N. & RACEY, P.A. 2016. Conservation ecology of cave bats. In Bats in the Anthropocene: Conservation of bats in a changing world (C.C. Voigt and T. Kingston eds.). Springer, USA, p.606.
GARCIA, A.C.L., LEAL, E.S., ROHDE, C., CARVALHO-NETO, F.G. & MONTES, M.A. 2014. The bats of northeastern Brazil: a panorama. Anim. Biol. 64(2):141–150.
GARDNER, A.L. 2008. Mammals of South America - Volume 1: Marsupials, Xenarthrans, Shrews, and Bats. Chicago and London, The University of Chicago Press.
GOODWIN, G.G. 1959. Bats of the subgenus Natalus. Am. Mus. Novit. 1977:1–22.
GREGORIN, R. & TADDEI, V.A. 2002. Chave artificial para a identificação de molossídeos brasileiros (Mammalia, Chiroptera). Mastozool. Neotrop. 9(1):13–32.
GREGORIN, R., MORAS, L.M., ACOSTA, L.H., VASCONCELLOS, K.L., POMA, J.L., DOS SANTOS, F.R. & PACA, R.C. 2016. A new species of Eumops (Chiroptera: Molossidae) from southeastern Brazil and Bolivia. Mamm. Biol. 81(3):235–246.
GURGEL-FILHO, N.M., FEIJÓ, A. & LANGGUTH, A. 2015. Pequenos Mamíferos do Ceará (Marsupiais, Morcegos e Roedores sigmodontineos) com discussão taxonômica de algumas espécies. Rev. Nordestina Biol. 23(3):3–150.
GUTIÉRREZ, E. & MARINHO-FILHO, J. 2017. The mammalian faunas endemic to the Cerrado and the Caatinga. ZooKeys 644:105–157
HEIN, C.D. & SCHIRMACHER, M.R. 2016. Impact of wind energy on bats: a summary of our current knowledge. Hum-Wildl. Interact. 10(1):19–27.
167
ICMBio/MMA – Instituto Chico Mendes de Conservação da Biodiversidade/Ministério de Meio Ambiente. 2016. Sumário Executivo do Livro Vermelho da Fauna Ameaçada de Extinção. Distrito Federal, Brasília, Brazil, p. 1–17.
IUCN – International Union for Conservation of Nature. 2016. The IUCN Red List of Threatened Species. Version 2016–3. http://www.iucnredlist.org (last access on 17/Apr/2017).
IDEMA - Instituto De Desenvolvimento Sustentável e Meio Ambiente. 2015. Anuário estatístico 2015. Rio Grande do Norte: Governo do Rio Grande do Norte. http://www.idema.rn.gov.br/Conteudo.asp?TRAN=ITEM&TARG=1357&ACT=null&PAGE=0&P ARM=null&LBL=Socioecon%C3%B4micos (last access on 15/Dec/2016).
INPE/SOS MATA ATLANTICA. 2014. Atlas dos remanescentes florestais da Mata Atlântica período 2011-2012 - relatório técnico. Fundação SOS Mata Atlântica, Instituto Nacional de Pesquisas Espaciais -INPE, São Paulo, p.1–60.
JONES, J.K. & HOOD, C.S. 1993. Synopsis of South American bats of the family Emballonuridae. Occas. Pap. Tex. Tech. Univ. Mus. 155:1–32.
LEAL, I.R., TABARELLI, M. & SILVA, J.M.C. 2003. Ecologia e conservação da Caatinga. 3 ed. Editora Universitária da Universidade Federal de Pernambuco, Recife, Brasil.
LEAL, E.S.B., AZEVÊDO-JÚNIOR, S.M., NOVA, F.V.P.V., QUEIRÓZ-GUERRA, D. & TELINO-JÚNIOR, W.R. 2013. Updated compilation of bat species (Chiroptera) for the Brazilian state of Sergipe, including new records. Chiropt. Neotrop. 19(1):1163–1178.
LEAL, E.S.B., SILVA, D.Q., FIGUEIREDO-RAMALHO, D., MILLER, B.G., PASSOS-FILHO, P.B., PRADO-NETO, J.G., QUEIRÓZ-GUERRA, D., MOURA, G.J.B., LYRA-NEVES, R.M. & TELINO-JÚNIOR, W.R. 2014. Extension of the geographical distribution of Lonchophylla dekeyseri Taddei, Vizotto and Sazima, 1983 (Chiroptera: Phyllostomidae): new record in northeastern Brazil. Chiropt. Neotrop. 19(2):1220–1225.
MACSWINEY, G., CRISTINA, M., CLARKE, F.M. & RACEY, P.A. 2008. What you see is not what you get: the role of ultrasonic detectors in increasing inventory completeness in Neotropical bat assemblages. J. Appl. Ecol. 45(5):1364–1371.
MARES, M.A., WILLIG, M.R., SRTEILEIN, K.E. & LACHER JR. T.E. 1981.The mammals of northeastern Brazil: a preliminary assessment. Ann. Carnegie Mus. 50:81–137.
MARES, M.A., WILLIG, M.R. & LACHER JR, T.E. 1985. The Brazilian Caatinga in South American zoogeography: tropical mammals in a dry region. J. Biogeogr. 12:57–69.
MORATELLI, R., PERACCHI, A. L., DIAS, D. & DE OLIVEIRA, J. A. 2011. Geographic variation in South American populations of Myotis nigricans (Schinz, 1821) (Chiroptera, Vespertilionidae), with the description of two new species. Mamm. Biol. 76(5): 592–607.
MORATELLI, R. & DIAS, D. 2015. A new species of nectar-feeding bat, genus Lonchophylla, from the Caatinga of Brazil (Chiroptera, Phyllostomidae). ZooKeys 514:73–91.
NOGUEIRA, M.R., LIMA, I.P., MORATELLI, R., TAVARES, V.C., GREGORIN, R. & PERACCHI, A.L. 2014. Checklist of Brazilian bats, with comments on original records. Check List 10(4):808–821.
168
NUNES, H.L., FEIJÓ, J.A., BELTRÃO, M., LOPEZ, L.C.S. & FRACASSO, M.P.A. 2013. First and easternmost record of Molossops temminckii (Burmeister, 1854) (Chiroptera: Molossidae) for the state of Paraíba, northeastern Brazil. Check List 9(2):436–439.
O'SHEA, T.J., CRYAN, P.M., HAYMAN, D.T., PLOWRIGHT, R.K. & STREICKER, D.G. 2016. Multiple mortality events in bats: a global review. Mammal Rev. 46(3):175–190.
PAGLIA, A.P., FONSECA, G.A.B., RYLANDS, A.B., HERRMANN, G., AGUIAR, L.M.S., CHIARELLO, A.G., LEITE, Y.L.R., COSTA, L.P., SICILIANO, S., KIERULFF, M.C.M., MENDES, S.L., TAVARES. V.C., MITTERMEIER, R.A. & PATTON, J.L. 2012. Lista Anotada dos Mamíferos do Brasil. 2 ed. Occ. Pap. In Conservat. Biology.
REIS, N.R., PERACCHI, A.L., PEDRO, W.A. & LIMA, I.P. 2007. Morcegos do brasil. Universidade Estadual de Londrina, Londrina, Brazil.
ROCHA, P.A., FEIJÓ, A., PEDROSO, M.A., & FERRARI, S.F. 2015. First record of the big free- tailed bat, Nyctinomops macrotis (chiroptera, molossidae), for the semi-arid caatinga scrublands of northeastern Brazil. Mastoz. Neotrop. 22(1):195–200.
ROCHA, P.A., BRANDÃO, M.V., GARBINO, G.S.T., CUNHA, I.N. & AIRES, C.C. 2016. First record of Salvini’s big-eyed bat Chiroderma salvini Dobson, 1878 for Brazil. Mammalia 80(5):573–578.
ROCHA, P.A., SOARES, F.A., DIAS, D., MIKALAUSKAS, J.S., VILAR, E.M., FEIJÓ, A., & DAHER, M. R. 2017. New records of Micronycteris schmidtorum Sanborn, 1935 (Phyllostomidae, Chiroptera) for northeastern Brazil. Mastoz. Neotrop. 24:1–8.
SAGOT, M. & CHAVERRI, G. 2015. Effects of roost specialization on extinction risk in bats. Conserv. Biol. 29(6):1666–1673.
SAMPAIO, E., LIM, B. & PETERS, S. 2016. Lonchophylla mordax. The IUCN Red List of Threatened Species 2016. e.T12267A22038521. http://dx.doi.org/10.2305/IUCN.UK.2016- 3.RLTS.T12267A22038521.en.
SANBORN, C.C. 1937. American bats of the subfamily Emballonuridae. Field Mus. Nat. Hist. Zool. Series 29(24):321–354.
SANTOS, J.C., LEAL, I.R., ALMEIDA-CORTEZ, J.S., FERNANDES, G.W. & TABARELLI, M. 2011. Caatinga: the scientific negligence experienced by a dry tropical forest. Trop. Conserv. Sci. 4(3):276–286.
SCHUSTER, E., BULLING, L. & KÖPPEL, J. 2015. Consolidating the state of knowledge: a synoptical review of wind energy’s wildlife effects. Environ. Manage. 56(2):300–331.
SILVA, S.S., DIAS, D., MARTINS, M.A., GUEDES, P.G., DE ALMEIDA, J.C., CRUZ, A.P., SERRA-FREIRE, N.M., DAMASCENA, J.S. & PERACCHI, A.L. 2015. Bats (Mammalia: Chiroptera) from the caatinga scrublands of the Crateús region, northeastern Brazil, with new records for the state of Ceará. Mastozool. Neotrop. 22(2):335–348.
SILVA, C.R. & BERNARD, E. 2017. Bioacoustics as an important complementary tool in bat inventories in the Caatinga drylands of Brazil. Acta Chiropterol. 19(2):409-418.
169
SIMMONS, N.B. 1996. A new species of Micronycteris (Chiroptera, Phyllostomidae) from northeastern Brazil: with comments on phylogenetic relationships. Am. Mus. Novit. 3158:1–34.
SIMMONS, N.B. & VOSS, R.S. 1998. The mammals of Paracou, French Guiana, a Neotropical lowland rainforest fauna. Part 1, Bats. Bull. Am. Mus. Nat. Hist. 237:1–219.
SOLARI, S. & MARTÍNEZ-ARIAS, V. 2014. Cambios recientes en la sistemática y taxonomía de murciélagos Neotropicales (Mammalia: Chiroptera). Therya 5(1):167–196.
TEJEDOR, A. & DAVALOS, L. 2016. Natalus espiritosantensis. The IUCN Red List of Threatened Species 2016: e.T136448A21983924. http://dx.doi.org/10.2305/IUCN.UK.2016- 2.RLTS.T136448A21983924.en (last access on 15/Feb/2017).
VARGAS-MENA, J.C., CORDERO-SCHMIDT, E., BENTO, D.M., RODRÍGUEZ-HERRERA, B., MEDELLÍN, R.A., VENTICINQUE, E.M. 2018. Diversity of cave bats in the Brazilian tropical dry forest of Rio Grande do Norte State. Mastozool. Neotrop. 25(1):199-212. https://doi.org/10.31687/saremMN.18.25.1.0.16
VELLOSO, A.L., SAMPAIO, E.V.S.B. & PAREIN, F.G.C. 2002. Ecorregiões propostas para o bioma Caatinga – Resultado do Seminário de Planejamento Ecorregional da Caatinga. Associação Plantas do Nordeste, Instituto de Conservação Ambiental, The Nature Consercancy, Recife, p. 1– 76.
VILAR, E.M., NUNES, H., NASCIMENTO, J.L. & ESTRELA, P.C. 2015. Distribution extension of Ametrida centurio Gray, 1847 (Chiroptera, Phyllostomidae): first record in the Brazilian Atlantic Forest. Check List 11(1):1503.
WEBSTER, W.D. 1993. Systematics and evolution of bats of the genus Glossophaga. Tex. Tech. Univ. Mus. Spec. Publ. 36:1–184.
WILLIG, M.R. 1983. Composition, microgeographic variation and sexual dimorphism in Caatingas and Cerrado bat communities from northeast Brazil. Bull. Carnegie Mus. Nat His. 23:1–131
Figure G. Front portrait of the Funnel-eared bat (Natalus macrourus), a cave dependent and vulnerable species in Rio Grande do Norte and Brazil. Photo by Juan Carlos Vargas- 170 Mena. GENERAL CONCLUSIONS
HOW?
• The structure regarding richness (alpha) and species composition (spatial beta
diversity) of bat assemblages in the studied sites is composed of seven trophic
guilds in six taxonomical families of 31 species, ranging from 9 to 18 species per
surveyed sites, from 1575 individuals captured in 99 sampling nights using a
capture effort of 242 425 hm2. Additionally, in nine cave roosts we recorded 17 bat
species of 2020 captured and 3200 observed individuals in 61 sampling days.
• The assemblages had a structure that differed at the species- and ensemble-level
(trophic guilds) between different studied areas. This was found as well between
the seven different habitats of Caatinga. Species and trophic guilds have specific
preference to occur in specific landscape characteristics and preferred to forage
depending on the vegetational structure of the differed surveyed Caatinga
phytofisiognomies, despite bats high vagile ability.
•
WHEN? • Richness and species composition presented no evident seasonal variation between
season in the region of Lajes. Likely, food resource found along the year may be
the key factor that sustain a similar structure of the bat assemblage year-round.
• Similarly, in caves the species richness and species composition did not change
seasonally and no temporal turnover of species was found. However, bat abundance
did increase significantly for some species in the rainy season. In Lajes’ caves,
peaks of abundance were found in the end of the rainy season attributed to regional
availability of food resources and reproduction activity.
171
WHAT?
• The effect of season in the reproductively active varied between guilds of cave-
dwelling bats. During the rainy season frugivores, insectivores and animalivores
were reproductive active where their preferred food seems to be abundant, while
sanguinivores, omnivores that rely on year-round available food were active during
both seasons, including nectarivores, unexpectedly.
• There was an interaction between seasons and cave size and large caves tended to
vary positively in abundance much more than small caves in the rainy season by
bats. As well, the species composition was different between all studied caves,
including between large and small-sized caves.
WHO?
• From the scientific literature and mammal collections revision, we offically list 42
species of bats in Rio Grande do Norte (RN). More than half (54%) of species in
RN are phyllostomid bats, and about one third of the RN’s bats are cave-dwelling.
The Caatinga harbored the highest bat richness in the state, including the
occurrence of three vulnerable species (Furipterus horrens, Lonchorhina aurita,
Natalus macrourus), one endemics to Caatinga (Lonchophylla inexpectata), and
one to Cerrado/Caatinga (Xeronycteris vieirai).
• Captures yielded two species new records for the state (Eumops cf. glaucinus, and
Rhogeessa sp.).
• Overall, in this thesis I captured 3705 individuals and more than 3700 observed
bats in 161 sampling days of 32 species, that is the 72.7% of the gamma diversity
of bats in Rio Grande do Norte (44 species).
The results of this thesis in an effort to describe and to have a deeper insight into the natural history and ecology of the poorly known bat fauna of the seasonal Caatinga dry
172 forest in Brazil. The data provided herein provides novel insights of different patterns in the structure and reproduction of cave bat assemblages of what is expected in a highly seasonal environment and provides insights of a general year-round adaptation of the fauna in this semiarid landscape. I expect that the data generated in this thesis could be used for more accurate protection actions for the conservation of bats, their foraging areas of Caatinga and critical cave roosts in this semiarid tropical dry forest of Rio Grande do Norte state.
MSc. Juan Carlos Vargas Mena
173
APPENDIX 1 List of bats (Chiroptera) in taxonomical order recorded in different foraging areas and in cave roosts using mist nets and direct observation in the six areas of Caatinga from 2017-2019 in Rio Grande do Norte State. Number in parenthesis correspond to number of species per family.
Caatinga Family/subfamily Taxon Cave roost habitats Emballonuridae (1) Peropteryx macrotis x x Phyllostomidae (20) Micronycterinae Micronycteris megalotis x Micronycteris sanborni x Micronycteris schmidtorum x Desmodontinae Desmodus rotundus x x Diphylla ecaudata x x Lonchorhininae Lonchorhina aurita x Phyllostominae Phyllostomus discolor x x Phyllostomus hastatus x Tonatia bidens x x Trachops cirrhosus x x Glossophaginae Anoura geoffroyi x Glossophaga soricina x x Lonchophyllinae Lonchophylla inexpectata x x Lonchophylla mordax x x Xeronycteris vieirai x x Carolliinae Carollia perspicillata x x Stenodermatinae Artibeus lituratus x Artibeus planirostris x x Platyrrhinus lineatus x Sturnira lilium x
Noctilionidae (2) Noctilio leporinus x x
Mormoopidae (1) Pteronotus gymnonotus x x
Furipteridae (1) Furipterus horrens x
Natalidae (1) Natalus macrourus x
Molossidae (5) Eumops cf. glaucinus x Molossops temminckii x Molossus molossus x Neoplatymops mattogrossensis x Promops nasutus x
Vespertilionidae (2) Myotis lavali x Rhogeessa hussoni x 174
APPENDIX 2
List of bat records (Mammalia, Chiroptera) in the state of Rio Grande do Norte, northeastern Brazil, based on review of literature and specimens in collections. Abbreviations: CAS ‒ California Academy of Science; CMAV ‒ Coleção de Mamíferos Adalberto Varela, Universidade Federal do Rio Grande do Norte; CMUFS ‒ Coleção de Mamíferos da Universidade Federal de Sergipe; MZUSP ‒ Museu de Zoologia da Universidade de São Paulo; UFPB ‒ Coleção de Mamíferos da Universidade Federal da Paraíba; UFPE ‒ Coleção de Mamíferos da Universidade Federal de Pernambuco; USNM ‒ United States National Museum.
Included in the Species Locality Municipality Voucher Voucher number Original record Cited in final list?
Emballonuridae
Emballonurinae
Peropteryx kappleri ? ? ? ? Not found Garcia et al. 2014 no
Peropteryx leucoptera Nísia Floresta National Nísia Floresta yes UFPE 3193 Barros et al. 2017 _ yes Forest
Peropteryx macrotis Casa dos Homens Cave Caraúbas yes CMAV 131, 133 Vargas-Mena et _ yes al. In press
Carrapateira Cave Felipe Guerra no _ Ferreira et al. Garcia et al. 2014 no 2010; Vargas- Mena et al. In press
175
Urubu Cave Felipe Guerra no _ Vargas-Mena et _ no al. in press
Três Lagos Cave Felipe Guerra yes CMAV 129 Vargas-Mena et _ yes al. in press
Lajedo Grande Cave Governador Dix- yes CMAV 130 Vargas-Mena et _ yes Sept Rosado al. in press
Capoeira do João Carlos Governador Dix- no _ Vargas-Mena et _ no Cave Sept Rosado al. in press
Apertar da Hora Cave Jandaíra yes CMAV 111, 112, 113, Present study _ yes 114, 115, 116
Santa Rosa Farm Lajes yes CMAV 122 Present study _ yes
Furna Feia Cave, Furna Mossoró/Barauna no _ Vargas-Mena et _ no Feia National Park al. in press
Pedra Lisa Cave, Furna Mossoró/Barauna no _ Vargas-Mena et _ no Feia National Park al. in press
Furna Nova Cave, Furna Mossoró/Barauna no _ Vargas-Mena et _ no Feia National Park al. in press
Porco do Mato 1 Cave, Mossoró/Barauna no _ Vargas-Mena et _ no Furna Feia National Park al. in press
Gruta dos Trinta Cave Mossoró no _ Vargas-Mena et _ no al. in press
176
Not informed Natal yes USNM (not informed Sanborn 1937 Jones & Hood 1993; yes number) Oliveira et al. 2005; Gardner 2008; Garcia et al. 2014
Alagamar Beach Natal yes CMAV 007 Present study _ yes
Poço Branco Dam Poço Branco yes CMAV 107, 108, 109, Present study _ yes 110
Rhynchonycteris naso Poço Branco Dam Poço Branco yes CMAV 105, 106 Present study _ yes
Saccopteryx canescens Jiquí State Park Parnamirim no _ Farias 2009 Garcia et al. 2014 no
Saccopteryx leptura Jiquí State Park Parnamirim no _ Farias 2009 Garcia et al. 2014 no
Phyllostomidae
Micronycterinae
Micronycteris megalotis Furna Feia National Park Baraúna/Mossoró yes CMAV 134 Present study _ yes
Micronycteris sanborni Seridó Ecological Station Serra Negra do yes UFPE 3436, UFPE Present study _ yes 3439, UFPE 3440 Norte
Micronycteris schmidtorum Açude Santa Rosa Lajes yes CMAV 140 Present study _ yes
Santa Rosa Farm Lajes yes CMAV 145 Present study _ yes
Desmodontinae
177
Desmodus rotundus Roncador Apodi no _ Ferreira et al. Garcia et al. 2014 no 2010
Casa dos Homens Cave Caraúbas no _ Vargas-Mena et _ no al. in press
Urubu Cave Felipe Guerra no _ Vargas-Mena et _ no al. in press
Boa Cave Felipe Guerra no _ Vargas-Mena et _ no al. in press
Carrapateira Cave Felipe Guerra no _ Vargas-Mena et _ no al. in press
Gruta dos Três Lagos Felipe Guerra no _ Vargas-Mena et _ no al. in press
Lajedo Grande Cave Governador Dix- no _ Vargas-Mena et _ no Sept Rosado al. in press
Furna Feia Cave, Furna Mossoró/Barauna no _ Ferreira et al. Garcia et al. 2014 no Feia National Park 2010; Vargas- Mena et al. in press
Pedra Lisa Cave, Furna Mossoró/Barauna no _ Vargas-Mena et _ no Feia National Park al. in press
Furna Nova Cave, Furna Mossoró/Barauna no _ Vargas-Mena et _ no Feia National Park al. in press
178
Porco do Mato 1 Cave, Mossoró/Barauna no _ Vargas-Mena et _ no Furna Feia National Park al. in press
Gruta dos Trinta Cave Mossoró no _ Vargas-Mena et _ no al. in press
Nísia Floresta National Nísia Floresta yes UFPE 3306 Barros et al. 2017 _ yes Forest
Cave between Bento Poço Branco yes CMAV 038, 045, 046, Present study _ yes Fernandes and Poço 047, 048, 049, 050, Branco 051, 052, 053, 054, 055, 056, 057
Diphylla ecaudata
Casa dos Homens Cave Caraúbas yes CMAV 135 Vargas-Mena et _ yes al. in press
Urubu Cave Felipe Guerra no _ Vargas-Mena et _ no al. in press
Boa Cave Felipe Guerra no _ Vargas-Mena et _ no al. in press
Carrapateira Cave Felipe Guerra no _ Vargas-Mena et _ no al. in press
Três Lagos Cave Felipe Guerra no _ Vargas-Mena et _ no al. in press
179
Lajedo Grande Cave Governador Dix- no _ Vargas-Mena et _ no Sept Rosado al. in press
Capoeira do João Carlos Governador Dix- no _ Vargas-Mena et _ no Cave Sept Rosado al. in press
Furna Nova Cave, Furna Mossoró/Barauna no _ Vargas-Mena et _ no Feia National Park al. in press
Porco do Mato 1 Cave, Mossoró/Barauna no _ Vargas-Mena et _ no Furna Feia National Park al. in press
Furna Feia Cave, Furna Mossoró/Barauna no _ Ferreira et al. Garcia et al. 2014 no Feia National Park 2010; Vargas- Mena et al. in press
Lonchorhininae
Lonchorhina aurita Três Lagos Cave Felipe Guerra no _ Ferreira et al. Garcia et al. 2014 no 2010
Três Lagos Cave Felipe Guerra yes CMAV 128 Vargas-Mena et _ yes al. in press
Phyllostominae
Chrotopterus auritus Carrapateira Cave Felipe Guerra no _ Basílio et al. _ no 2017
180
Três Inchu Cave Martins yes CMUFS 259 Basílio et al. _ yes 2017
Lophostoma brasiliense Nísia Floresta National Nísia Floresta yes UFPE 2181, 3272, Barros et al. 2017 _ yes Forest 3273, 3274, 3275, 3278, 3279, 3282
Phyllostomus discolor Mangabeira Farm Macaíba yes CMAV 018, 019, 020, Present study _ yes 021
Boa Cave Felipe Guerra no _ Vargas-Mena et _ no al. in press
Nísia Floresta National Nísia Floresta yes UFPE 3247, 3248, Barros et al. 2017 _ yes Forest 3249, 3250, 3251, 3252, 3253, 3254, 3255, 3256
Furna Nova Cave, Furna Mossoró/Barauna no _ Vargas-Mena et _ no Feia National Park al. in press
Furna Feia Cave, Furna Mossoró/Barauna no _ Vargas-Mena et _ no Feia National Park al. in press
Not informed Taipu yes CMAV 039, 040, 041, Present study _ yes 042
181
Phyllostomus hastatus Nísia Floresta National Nísia Floresta yes UFPE 3225, 3226, Barros et al. 2017 _ yes Forest 3261, 3262, 3263, 3264
Tonatia bidens Casa dos Homens Cave Caraúbas yes CMAV 138 Vargas-Mena et _ yes al. in press
Urubu Cave Felipe Guerra no _ Vargas-Mena et _ no al. in press
Boa Cave Felipe Guerra no _ Vargas-Mena et _ no al. in press
Capoeira do João Carlos Governador Dix- no _ Vargas-Mena et _ no Cave Sept Rosado al. in press
Furna Feia Cave, Furna Mossoró/Barauna no _ Ferreira et al. Garcia et al. 2014 no Feia National Park 2010; Vargas- Mena et al. in press
Pedra Lisa Cave, Furna Mossoró/Barauna no _ Vargas-Mena et _ no Feia National Park al. in press
Furna Nova Cave, Furna Mossoró/Barauna no _ Vargas-Mena et _ no Feia National Park al. in press
Porco do Mato 1 Cave, Mossoró/Barauna no _ Vargas-Mena et _ no Furna Feia National Park al. in press
182
Trachops cirrhosus Três Lagos Cave Felipe Guerra no _ Vargas-Mena et no al. in press
Pedra Vermelha Farm Lajes yes CMAV 069 Present study _ yes
Casa de Pedra Cave Martins no _ Ferreira et al. Garcia et al. 2014 no 2010
Nísia Floresta National Nísia Floresta yes UFPE 3266 Barros et al. 2017 _ yes Forest
Glossophaginae
Anoura caudifer Jiquí State Park Parnamirim no _ Farias 2009 Garcia et al. 2014 no
Anoura geoffroyi Juazeiro Farm Lajes yes CMAV 144 Present study _ yes
Glossophaga soricina Muriú Beach Street Ceará Mirim yes CMAV 015, 016, 058 Present study _ yes
Carrapateira Cave Felipe Guerra no _ Vargas-Mena et _ no al. in press
Capoeira do João Carlos Governador Dix- no _ Vargas-Mena et _ no Cave Sept Rosado al. in press
Santo Antonio Farm Lajes yes CMAV 124 Present study _ yes
Açude Santa Rosa Lajes yes CMAV 139 Present study _ yes
Furna Nova Cave, Furna Mossoró/Barauna no _ Vargas-Mena et _ no Feia National Park al. in press
183
Porco do Mato 1 Cave, Mossoró/Barauna no _ Vargas-Mena et _ no Furna Feia National Park al. in press
Pedra Lisa Cave, Furna Mossoró/Barauna no _ Vargas-Mena et _ no Feia National Park al. in press
Furna Feia Cave, Furna Mossoró/Barauna no _ Ferreira et al. Garcia et al. 2014 no Feia National Park 2010
Furna Feia Cave, Furna Mossoró/Barauna no _ Vargas-Mena et _ no Feia National Park al. in press
Not informed Natal yes CAS (not informed Webster 1993 Oliveira et al. 2005; yes number) Garcia et al. 2014
UFRN campus Natal yes CMAV 162, 166 Present study _ yes
Nísia Floresta National Nísia Floresta yes UFPE 3257, 3258, Barros et al. 2017 _ yes Forest 3259, 3260, 3276, 3277, 3280, 3283, 3284, 3285
UERN Advanced Campus Nova Cruz yes CMAV 002 Present study _ yes
Jiquí State Park Parnamirim no _ Farias 2009 Garcia et al. 2014 no
Seridó Ecological Station Serra Negra do yes UFPE 3423 Present study _ yes
Norte
Farm Taipu yes CMAV 061, 062, 063 Present study _ yes
Lonchophyllinae
184
Lonchophylla mordax Muriú Beach Ceará Mirim no _ Varela-Freire _ no 1997
Santo Antônio Farm Lajes yes CMAV 142 Present study _ yes
Jiquí State Park Parnamirim no _ Farias 2009 Garcia et al. 2014 no
Seridó Ecological Station Serra Negra do yes UFPE 3424 Present study _ yes Norte
Lonchophylla inexpectata Amarante Lajes yes CMAV 167 Present study _ yes
Santa Rosa Farm Lajes yes CMAV 123 Present study _ yes
Santo Antonio Farm Lajes yes CMAV 121, 141 Present study _ yes
Juazeiro Farm Lajes yes CMAV 146 Present study _ yes
Dos Trinta Cave Mossoró yes CMAV 149 Vargas-Mena et _ yes al. in press
Xeronycteris vieirai Santo Antonio Farm Lajes yes CMAV 143 Cordero-Schmidt _ yes et al. in press
Carolliinae
Carollia perspicillata Furna Feia National Park Baraúna/Mossoró yes CMAV 136 Present study _ yes
Farm João Câmara yes CMAV 120 Present study _ yes
Nísia Floresta National Nísia Floresta yes UFPE 3290, 3291, Barros et al. 2017 _ yes Forest 3292, 3293, 3294, 3295, 3296, 3297, 3298
185
Jiquí State Park Parnamirim no _ Farias 2009 Garcia et al. 2014 no
Not informed Taipu yes CMAV 044, 072 Present study _ yes
Farm Taipu yes CMAV 059, 060, 064, Present study _ yes 065, 066
Stenodermatinae
Artibeus fimbriatus Potengi Natal no _ Vilela et al. 2010 Garcia et al. 2014 no
Artibeus lituratus UFRN campus Natal yes CMAV 159 Present study _ yes
Nísia Floresta National Nísia Floresta yes UFPE 3288, 3289 Barros et al. 2017 _ yes Forest
Jiquí State Park Parnamirim no _ Farias 2009 Garcia et al. 2014 no
Furna Feia Cave, Furna Mossoró/Barauna no _ Vargas-Mena et no Feia National Park al. in press
Artibeus planirostris Casa dos Homens Cave Caraúbas no _ Cordero-Schmidt _ no et al. 2016
Carrapateira Cave Felipe Guerra no _ Ferreira et al. Garcia et al. 2014 no 2010
Carrapateira Cave Felipe Guerra no _ Cordero-Schmidt _ no et al. 2016; Vargas-Mena et al. in press
186
Urubu Cave Felipe Guerra no _ Vargas-Mena et _ no al. in press
Lajedo Grande Cave Governador no _ Cordero-Schmidt _ no Dix-Sept Rosado et al. 2016; Vargas-Mena et al. in press
Capoeira de João Carlos Governador no _ Cordero-Schmidt _ no Cave Dix-Sept Rosado et al. 2016; Vargas-Mena et al. in press
Serrote Preto Cave Lajes no _ Cordero-Schmidt _ no et al. 2016
Furna Feia Cave, Furna Mossoró/Barauna no _ Vargas-Mena et _ no Feia National Park al. in press
Porco do Mato 1 Cave, Mossoró/Barauna no _ Vargas-Mena et _ no Furna Feia National Park al. in press
Building in Ponta Negra Natal yes CMAV 009 Present study _ yes
Ponta Negra Natal no _ Varela-Freire _ no 1997
Praia de Pirangi street, Natal yes CMAV 004 Present study _ yes Ponta Negra
187
UFRN campus Natal yes CMAV 157, 158 Present study _ yes
Via Costeira Natal yes CMAV 073 Present study _ yes
Nísia Floresta National Nísia Floresta yes UFPE 3200, 3201, Barros et al. 2017 _ yes Forest 3202, 3203, 3204, 3228, 3229, 3230, 3231, 3232
Seridó Ecological Station Serra Negra do yes UFPE 3083, 3084, Present study _ yes 3419, 3420, 3425, Norte 3429, 3431, 3432, 3434
Farm Taipu yes CMAV 067, 068 Present study _ yes
Chiroderma villosum Jiquí State Park Parnamirim no _ Farias 2009 Garcia et al. 2014 no
Dermanura cinerea Not informed Natal yes USNM (not informed Handley 1987 Gardner 2008; Garcia yes number) et al. 2014
Dunas State Park Natal yes CMAV 074 Present study _ yes
Near IBGE Natal yes CMAV 103, 104 Present study _ yes
Nísia Floresta National Nísia Floresta yes UFPE 3299, 3300, Barros et al. 2017 _ yes Forest 3301, 3302, 3303, 3304, 3305
Jiquí State Park Parnamirim no _ Farias 2009 Garcia et al. 2014 no
188
Platyrrhinus lineatus Ponta Negra Natal no _ Varela-Freire _ no 1997
Ponta Negra Natal yes CMAV 012 Present study _ yes
Petrópolis Natal yes CMAV 013, 014, 017 Present study _ yes
Nísia Floresta National Nísia Floresta yes UFPE 3208, 3209, Barros et al. 2017 _ yes Forest 3210, 3211, 3212, 3213, 3214, 3215, 3216, 3217
Jiquí State Park Parnamirim no _ Farias 2009 Garcia et al. 2014 no
Sturnira lilium UFRN campus Natal yes CMAV 161 Present study _ yes
Nísia Floresta National Nísia Floresta yes UFPE 3265, 3267, Barros et al. 2017 _ yes Forest 3268, 3269, 3270, 3271
Jiquí State Park Parnamirim no _ Farias 2009 Garcia et al. 2014 no
Mormoopidae
Pteronotus gymnonotus Urubu Cave Felipe Guerra yes CMAV 125, 127 Vargas-Mena et _ yes al. in press
Riacho Seco Farm João Câmara yes CMAV 075, 076, 077, Present study _ yes 078, 079, 080, 081, 082, 083, 084, 085, 086, 087, 088, 089,
189
090, 091, 092, 093, 094, 095, 096, 097, 098, 099, 100, 101, 102
Noctilionidae
Noctilio albiventris ? ? ? ? Not found Garcia et al. 2014 no
Seridó Ecological Station Serra Negra do yes UFPE 3427 Present study _ yes
Norte
Noctilio leporinus Seridó Ecological Station Serra Negra do yes UFPE 3426 Present study _ yes Norte
BR 406 Road Taipu yes CMAV 037 Present study _ yes
Furipteridae
Furipterus horrens Casa dos Homens Cave Caraúbas yes CMAV 132 Vargas-Mena et _ yes al. in press
Carrapateira Cave Felipe Guerra no _ Vargas-Mena et _ no al. in press
Três Lagos Cave Felipe Guerra no _ Vargas-Mena et _ no al. in press
Arapuá Cave Felipe Guerra no _ Vargas-Mena et _ no al. in press
190
Capoeira do João Carlos Governador Dix- no _ Vargas-Mena et _ no Cave Sept Rosado al. in press
Porco do Mato 1 Cave, Mossoró/Barauna no _ Vargas-Mena et _ no Furna Feia National Park al. in press
Furna Feia Cave, Furna Baraúna/Mossoró yes CMAV 071 Present study _ yes Feia National Park
Pedra Lisa Cave, Furna Baraúna/Mossoró yes CMAV 137 Vargas-Mena et _ yes Feia National Park al. in press
Natalidae
Natalus macrourus Boa Cave Felipe Guerra yes CMAV 126 Vargas-Mena et _ yes al. in press
Gruta dos Trinta Cave Mossoró yes CMAV 148 Vargas-Mena et _ yes al. in press
Furna Feia Cave, Furna Mossoró/Barauna no _ Ferreira et al. Garcia et al. 2014 no Feia National Park 2010; Vargas- Mena et al. in press
Furna Nova Cave, Furna Mossoró/Barauna no _ Vargas-Mena et _ no Feia National Park al. in press
Not informed Natal yes USNM 242830 Goodwin 1959 Gardner 2008 yes
191
Guano Cave Pedra Grande no _ Ferreira et al. Garcia et al. 2014 no 2010
Molossidae
Molossinae
Molossops temminckii Seridó Ecological Station Serra Negra do yes UFPE 3433 Present study _ yes Norte
Molossus molossus House roof Galinhos yes CMAV 152, 155 Present study _ yes
Urban area, Patrícia Carla Lagoa Salgada yes UFPE 3068, 3069, Barros 2014 _ yes Pereira da Costa 3070, 3071, 3072, Municipal School 3073, 3074, 3075, 3076, 3077
Sítio Mangabeira Macaíba yes CMAV 023, 024, 025, Present study _ yes 026, 027, 028, 029, 030, 031, 032, 033, 034, 035, 036
Lagoa Nova Natal yes CMAV 001, 006 Present study _ yes
Morro Branco Natal no _ Varela-Freire _ no 1997
Neoplatymops mattogrossensis Seridó Ecological Station Serra Negra do yes UFPE 3421, 3422, Present study _ yes Norte 3435, 3437, 3438, 3441
192
Nyctinomops aurispinosus Ship offshore (160 km near Maxaranguape yes USNM 3726 Shamel 1931 Bianconi et al. 2009; yes from Cabo de São Roque) Garcia et al. 2014
Nyctinomops macrotis Alegria Wind Farm Guamaré yes CMAV 156 Present study _ yes
Promops nasutus Alegria Wind Farm Guamaré yes CMAV 154 Present study _ yes
Nísia Floresta National Nísia Floresta yes UFPE 3218 Barros et al. 2017 _ yes Forest
Vespertilionidae
Vespertilioninae
Eptesicus furinalis House roof Galinhos yes CMAV 150 Present study _ yes
UFRN campus Natal yes CMAV 164 Present study _ yes
Lasiurus blossevillii Nísia Floresta National Nísia Floresta yes UFPE 3199 Barros et al. 2017 _ yes Forest
Lasiurus ega Alegria Wind Farm Guamaré yes CMAV 151 Present study _ yes
Myotinae
Myotis lavali House roof Galinhos yes CMAV 153 Present study _ yes
APRN Residence João Câmara yes CMAV 005 Present study _ yes
Granja Cerveira Macaíba yes CMAV 043 Present study _ yes
UFRN campus Natal yes CMAV 010, 011, 160, Present study _ yes 163
193
Nísia Floresta National Nísia Floresta yes UFPE 3181, 3182, Barros et al. 2017 _ yes Forest 3183, 3184, 3185, 3189, 3191, 3195, 3197, 3198
Near Seridó Ecological Serra Negra do yes CMAV 008 Present study _ yes Station Norte
Seridó Ecological Station Serra Negra do yes CMAV 022; UFPE Present study _ Yes Norte 3442, 3443, 3444, 3445, 3446, 3447, 3448, 3449, 3450, 3451, 3452, 3453
Myotis nigricans UFRN campus Natal no _ Varela-Freire _ No 1997
Lapa Farm Nova Cruz yes UFPB 1631, 1635, Feijó & Nunes Garcia et al. 2014 Yes 1639 2010
Myotis riparius Jiquí State Park Parnamirim no _ Farias 2009 Garcia et al. 2014 No
Myotis simus Jiquí State Park Parnamirim no _ Farias 2009 Garcia et al. 2014 No
194
References
BARROS, M.A.S. 2014. First record of Molossus molossus (Pallas, 1766) (Mammalia: Chiroptera) in the state of Rio Grande do Norte, northeastern Brazil. Check List 10(6):1520-1524.
BARROS, M.A., MORAIS, C.M.G., FIGUEIREDO, B.M.B., MOURA JÚNIOR, G.B.D., RIBEIRO, F.F.D.S., PESSOA, D.M.A., ITO, F. & BERNARD, E. 2017. Bats (Mammalia, Chiroptera) from the Nísia Floresta National Forest, with new records for the state of Rio Grande do Norte, northeastern Brazil. Biota Neotrop. 17(2): e20170351.
BASÍLIO, G.H.N., ARAUJO, J.P.M., VARGAS-MENA, J.C., ROCHA, P.A. & KRAMER, M.A.F. 2017. Chrotopterus auritus (Chiroptera, Phyllostomidae): first record for the state of Rio Grande do Norte, northeastern Brazil. Check List. 13(3): 2110.
BIANCONI, G.V., GREGORIN, R. & CARNEIRO, D.C. 2009. Range extension of the peale’s free-tailed bat Nyctinomops aurispinosus (Molossidae in Brazil). Biota Neotrop. 9(2): 267-270.
CORDERO-SCHMIDT, E., MEDEIROS-GUIMARÃES, M., VARGAS-MENA, J.C., CARVALHO, B., FERREIRA, R.L., RODRIGUEZ-HERRERA, B. & VENTICINQUE, E.M. 2016. Are leaves a good option in Caatinga's menu? First record of folivory in Artibeus planirostris (Phyllostomidae) in the semiarid forest, Brazil. Acta Chiropterol. 18(2):489-497.
CORDERO-SCHMIDT, E., BARBIER, E., VARGAS-MENA, J.C., OLIVEIRA, P.P., SANTOS, F.A.R., MEDELLÍN, R.A., RODRIGUEZ-HERRERA, B. & VENTICINQUE, E.M. in press. Natural history of the Caatinga endemic Vieira’s Flower Bat, Xeronycteris vieirai. Acta Chiropterol.
FARIAS, F.H.C. 2009. Caracterização biológica e zoneamento ambiental do Parque Estadual do Jiquí/RN, Brasil: subsídios ao plano de manejo. Master thesis, Animal biology department, Science faculty, Lisbon University, Lisbon, Portugal.
FEIJÓ, J.A. & NUNES, H.L. 2010. Primeiro registro de Myotis nigricans (Schinz, 1821) para o estado do Rio Grande do Norte, nordeste do Brasil. Chiropt. Neotrop. 16(1):531-534.
FERREIRA, R.P., PROUS, X., BERNARDI, L.O.F. & SOUZA-SILVA, M. 2010. Fauna subterrânea do estado do Rio Grande do Norte: caracterização e impactos. Rev. Bras. Espeleo. 1(1):25-51.
195
GARCIA, A.C.L., LEAL, E.S., ROHDE, C., CARVALHO-NETO, F.G. & MONTES, M.A. 2014. The bats of northeastern Brazil: a panorama. Anim. Biol. 64(2):141-150.
GARDNER, A.L. 2008. Mammals of South America - Volume 1: Marsupials, Xenarthrans, Shrews, and Bats. Chicago and London, The University of Chicago Press.
GOODWIN, G.G. 1959. Bats of the subgenus Natalus. Am. Mus. Novit. 1977:1-22.
HANDLEY JR., C.O. 1987. New species of mammals from northern South America: Fruit-eating bats, genus Artibeus Leach. In: Studies in Neotropical mammalogy, essays in honor of Philip Hershkovitz (B.D. Patterson & R.M. Timm, eds). Fieldiana, Zoology, 39, p. 163–172
JONES, J.K. & HOOD, C.S. 1993. Synopsis of South American bats of the family Emballonuridae. Occas. Pap. Tex. Tech. Univ. Mus. 155:1-32.
OLIVEIRA, J.A., GONÇALVES, P.R. & BONVICINO, C.R. 2005. Mamíferos da Caatinga, pp. 275-303. In: Ecologia e Conservação da Caatinga (I.R. Leal, M. Tabarelli & J.M.C. Silva, eds). Universidade Federal de Pernambuco, Recife, Brasil, p. 275-302
SANBORN, C.C. 1937. American bats of the subfamily Emballonuridae. Field Mus. Nat. Hist. Zool. Series 29(24):321-354.
SHAMEL, H.H. 1931. Notes on the American bats of the genus Tadarida. Proc. U. S. Nat. Mus. 78:1-27.
VARGAS-MENA, J.C., CORDERO-SCHMIDT, E., BENTO, D.M., RODRÍGUEZ-HERRERA, B., MEDELLÍN, R.A., VENTICINQUE, E.M. in press. Diversity of cave bats in the Brazilian tropical dry forest of Rio Grande do Norte State. Mastozool. Neotrop.
VILELA, F.C., SOUTO, M.C.S. & NETO, J.C.F. 2010. Descrição do 1º caso de raiva em morcego frugívoro relatado pelo Centro de Controle de Zoonoses de Natal, estado do Rio Grande do Norte, Nordeste do Brasil. Chiropt. Neotrop. 6(1a): 167-168.
VARELA-FREIRE, A.A. 1997. Fauna Potiguar Vol. 1 – A fauna das dunas costeiras da cidade do Natal e do litoral oriental do Rio Grande do Norte. Editora da Universidade Federal do Rio Grande do Norte, Natal, Rio Grande do Norte, Brasil. DUFRN, p.174. WEBSTER, W.D. 1993. Systematics and evolution of bats of the genus Glossophaga. Tex. Tech. Univ. Mus. Spec. Publ. 36:1-18
196
197