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Bat species diversity from Reserva Ecológica de Guapiaçu, Rio de Janeiro, Brazil: a compilation of two decades of sampling

ABSTRACT

Reserva Ecológica de Guapiaçu (REGUA) is a private, protected area inside a remnant of the Atlantic Forest with high biodiversity. Although the bats of the reserve have been sampled for more than two decades, few studies have been published about them. Based on a compilation of data from several surveys, we present an updated list of the bat species there and compare it with surveys from other locations in the Atlantic Forest. From August 1998 to September 2021, at least 194 sampling nights were carried out at REGUA by different research groups from various institutions, totaling 448,092 m2.h of sampling. A total of 4,069 individuals were captured, belonging to 47 species and six families. Additionally, our results indicate that it is possible that some species that occur at REGUA have not been recorded yet. REGUA has the greatest number of bat species known for the Atlantic Forest. This most likely results from the fact that the reserve includes large areas of mature, continuous forest connected with other protected areas in the State of Rio de Janeiro. Another factor contributing to the high diversity of bat species at REGUA is that the area has been intensely sampled for many years. Given that the bat assemblage there appears to be a good proxy to ascertain the ecological patterns of biodiversity in well-preserved forests, we consider REGUA to be an important area for long-term ecological research. The basic knowledge about the ecological interactions of bats with different food resources and zoonotic microorganisms offers a unique opportunity to carry out research in several areas of knowledge, making it possible to address questions about bat assemblage structure, bat-parasite ecology, competition, niche partitioning, and other related studies.

KEY WORDS:
Atlantic Forest; Chiroptera; long-term monitoring; bat assemblage

INTRODUCTION

Biodiversity surveys are essential to understand regional patterns of biological diversity, and to define the geographic distribution of specific taxa (Soulé and Wilcox 1980Soulé ME, Wilcox BA (1980) Conservation biology: its scope and its challenge. In: Soulé ME, Wilcox BA (Eds) Conservation Biology. Linauer Associates, Massachussetts.). These efforts are also necessary to support the implementation of conservation strategies for species and their habitats (Silveira et al. 2010Silveira LF, Beisiegel BM, Curcio FF, Valdujo PH, Dixo M, Verdade VK, Mattox GMT, Cunningham PTM (2010) What use do fauna inventories serve? Estudos Avançados 24: 173-207. https://doi.org/10.1590/S0103-40142010000100015
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). The results of long-term inventories are a good estimate of the actual faunal community, and enhance our ability to understand the temporal aspects that can affect population dynamics and species diversity due to natural or anthropogenic events (Gannon and Willig 1998Gannon MR, Willig MR (1998) Long-term monitoring protocol for bats: lessons from Luquillo Experimental Forest of Puerto Rico. In: Dallmeier F, Comisky J (Eds) Forest biodiversity in North, Central, and South America and the Caribbean: research and monitoring. The Parthenon Press, Lancashire, 271-291., Meyer et al. 2010Meyer CFJ, Aguiar LMS, Aguirre LF, Baumgarten J, Clarke FM, et al. (2010) Long-term monitoring of tropical bats for anthropogenic impact assessment: Gauging the statistical power to detect population change. Biological Conservation 143: 2797-2807. https://doi.org/10.1016/j.biocon.2010.07.029
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).

A few long-term (> 5 years) bat inventories have been carried out in the Neotropics (Meyer et al. 2010Meyer CFJ, Aguiar LMS, Aguirre LF, Baumgarten J, Clarke FM, et al. (2010) Long-term monitoring of tropical bats for anthropogenic impact assessment: Gauging the statistical power to detect population change. Biological Conservation 143: 2797-2807. https://doi.org/10.1016/j.biocon.2010.07.029
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). Bat surveys in Brazil have been mostly based on rapid faunal assessments and insufficient sampling effort, resulting in species lists that barely represent the real local diversity, and fail to add any information about the ecological dynamics of bat assemblages (Bernard et al. 2011Bernard E, Aguiar LMS, Machado RB (2011) Discovering the Brazilian bat fauna: a task for two centuries? Mammal Review 41: 23-39. https://doi.org/10.1111/j.1365-2907.2010.00164.x
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). With less than 10% of the Brazilian territory minimally sampled (Bernard et al. 2011), it is necessary to increase long-term research efforts in strategic areas, to generate useful scientific knowledge for bat conservation.

In Brazil, most of the long-term bat surveys were carried out in the Atlantic Forest biome, including Southern Bahia (Faria et al. 2006Faria D, Soares-Santos B, Sampaio E (2006) Bats from the Atlantic rainforest of southern Bahia, Brazil. Biota Neotropica 6: bn02406022006. https://doi.org/10.1590/S1676-06032006000200022
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), southern coast of Rio de Janeiro (Gomes and Esbérard 2017Gomes LAC, Esbérard CEL (2017) Long-term bat study on an island in the southeastern Brazilian coast with comparison of richness and composition of species among sites. Studies on Neotropical Fauna and Environment 52: 43-52. https://doi.org/10.1080/01650521.2016.1272168
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), Ilha Grande (Costa et al. 2021Costa LM, Lourenço EC, Damasceno-Júnior DA, Dias D, Esbérard CEL, Jordão-Nogueira T, Melo G, Bergallo HG (2021) Ilha Grande, one of the locations with the most records of bat species (Mammalia, Chiroptera) in Rio de Janeiro state: results of a long-term ecological study. Papéis Avulsos de Zoologia 61: e20216122. https://doi.org/10.11606/1807-0205/2021.61.22
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), Tijuca Forest (Esbérard 2003Esbérard CEL (2003) Diversidade de morcegos m área de Mata Atlântica regenerada no Sudeste do Brasil. Revista Brasileira de Zoociências 5: 189-204.), and Pedra Branca Forest (Tavares et al. 2021Tavares JA, Novaes RLM, Veríssimo I, Kuzel MAA, Costa-Neto SF, et al. (2021) Bats from the Pedra Branca Forest, Rio de Janeiro, Brazil. Biodiversity Data Journal 9: e77400. https://doi.org/10.3897/BDJ.9.e77400
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). These and other efforts have made the Atlantic Forest into the most studied Brazilian biome when it comes to bat diversity. There are more than 100 species currently recorded for the Atlantic Forest, which represents about 35% of the mammal richness known for this biome (Bernard et al. 2011Bernard E, Aguiar LMS, Machado RB (2011) Discovering the Brazilian bat fauna: a task for two centuries? Mammal Review 41: 23-39. https://doi.org/10.1111/j.1365-2907.2010.00164.x
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, Paglia et al. 2012Paglia AP, Fonseca GAB, Rylands AB, Herrmann G, Aguiar LMS, et al. (2012) Annotated checklist of Brazilian mammals. Occasional Papers in Conservation Biology 6: 1-76., Graipel et al. 2017Graipel ME, Cherem JJ, Monteiro-Filho ELA, Carmignotto AP (2017) Mamíferos da Mata Atlântica. In: Monteiro-Filho ELA, Conte CE (Eds) Revisões em Zoologia: Mata Atlântica. Editora da Universidade Federal do Paraná, Curitiba, 391-482., Muylaert et al. 2017Muylaert RL, Stevens RD, Esbérard CEL, Mello MAR, Garbino GST, et al. (2017) Atlantic Bats: a data set of bat communities from the Atlantic Forests of South America. Ecology 98: 3227-3227. https://doi.org/10.1002/ecy.2007
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).

The Reserva Ecológica de Guapiaçu (REGUA) is an important private reserve at the central portion of the state of Rio de Janeiro. The reserve stands out for its high biodiversity (Pimentel and Olmos 2011Pimentel LMS, Olmos F (2011) The birds of Reserva Ecológica Guapiaçu (REGUA), Rio de Janeiro, Brazil. Cotinga 33: 8-24., Almeida-Gomes et al. 2014Almeida-Gomes M, Siqueira CC, Borges-Júnior VNT, Vrcibradic D, Fusinatto LA, Rocha CFD (2014) Herpetofauna of the Reserva Ecológica de Guapiaçu (REGUA) and its surrounding areas, in the state of Rio de Janeiro, Brazil. Biota Neotropica 14: e20130078. https://doi.org/10.1590/1676-0603007813
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, Carvalho et al. 2014Carvalho ID, Oliveira R, Pires AS (2014) Medium and large-sized mammals of the Reserva Ecológica de Guapiaçu, Cachoeiras de Macacu, RJ. Biota Neotropica 14: e20140074. https://doi.org/10.1590/1676-06032014007414
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, Silva et al. 2014Silva JS, Couri MS, Giupponi APL, Alencar J (2014) Mosquito fauna of the Guapiaçu Ecological Reserve, Cachoeiras de Macacu, Rio de Janeiro, Brazil, collected under the influence of different color CDC light traps. Journal of Vector Ecology 39: 384-394. https://doi.org/10.1111/jvec.12114
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) and conservation management actions, which include ecological restoration projects. Several research groups have conducted bat-capturing campaigns there since 1998, as part of ecology and parasitology research projects (e.g., Souza et al. 2015Souza RF, Novaes RLM, Siqueira AC, Sauwen C, Jacob G, et al. (2015) Bats (Mammalia, Chiroptera) in a remnant of Atlantic Forest, Rio de Janeiro, southeastern Brazil. Neotropical Biology and Conservation 10: 9-14. https://doi.org/10.4013/nbc.2015.101.02
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, 2016Souza RF, Novaes RLM, Felix S, Sauwen C, Jacob G, et al. (2016) Morcegos da Reserva Ecológica de Guapiaçu, Cachoeiras de Macacu, estado do Rio de Janeiro, Sudeste do Brasil. In: Santos MG (Ed.) Biodiversidade e sociedade no Leste Metropolitano do Rio de Janeiro. Editora da Universidade do Estado do Rio de Janeiro, São Gonçalo, 95-124., Novaes et al. 2015Novaes RLM, Souza RF, Ribeiro EA, Siqueira AC, Greco AV, Moratelli R (2015a) First evidence of frugivory in Myotis (Chiroptera, Vespertilionidae, Myotinae). Biodiversity Data Journal 3: e6841. https://doi.org/10.3897/BDJ.3.e6841
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a, Rangel et al. 2019Rangel D, Lisboa CV, Novaes RLM, Silva BA, Souza RF, et al. (2019) Isolation and characterization of trypanosomatids, including Crithidia mellificae, in bats from the Atlantic Forest of Rio de Janeiro, Brazil. PLoS Neglected Tropical Diseases 13: e0007527. https://doi.org/10.1371/journal.pntd.0007527
https://doi.org/10.1371/journal.pntd.000...
, Oelbaum et al. 2022Oelbaum PJ, Teixeira TSM, Clare EL, Broders HG (2022) Variation in diet of frugivorous bats in fragments of Brazil’s Atlantic Forest associated with vegetation density. Journal of Mammalogy: gyac024. https://doi.org/10.1093/jmammal/gyac024
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), but no one has compiled a list of species from these efforts.

The main goal of this study is to present an updated list of bat species occurring at REGUA, from the results of fieldwork conducted over two decades. Additionally, we discuss knowledge gaps and propose new objectives and methodological designs to that may result in the addition of new species to the current species list.

MATERIAL AND METHODS

Study area

The Reserva Ecológica de Guapiaçu (Guapiaçu Ecological Reserve; REGUA) is a private property, partially protected by a private reserve (Reserva Particular do Patrimônio Natural - RPPN). It is located in the eastern portion of the Guanabara Bay, in the Guapiaçu River sub-basin, Cachoeiras de Macacu municipality, state of Rio de Janeiro, southeastern Brazil (administrative headquarters: 22°27’10”S, 42°46’13”W; Fig. 1). It is part of the Atlantic Forest Mosaic of Corredor Central Fluminense, where it connects with Parque Estadual dos Três Picos and Parque Nacional da Serra dos Órgãos, and it is located in the central portion of Serra do Mar, one of the largest continuous remnants of the Atlantic Forest in Brazil. The climate in the region is tropical, classified as Köppen’s Af (Alvares et al. 2014Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G (2014) Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22: 711-728. https://doi.org/10.1127/0941-2948/2013/0507
https://doi.org/10.1127/0941-2948/2013/0...
), with rainy and hot summers (from October to March) and cold dry winters (April to September). The average annual temperature is 23 °C, and the average annual rainfall is 2,560 mm (Kurtz and Araújo 2000Kurtz BC, Araújo DSD (2000) Composição florística e estrutura do componente arbóreo de um trecho de Mata Atlântica na Estação Ecológica Estadual do Paraíso, Cachoeiras de Macacu, Rio de Janeiro, Brasil. Rodriguésia 51: 69-111. https://doi.org/10.1590/2175-7860200051787903
https://doi.org/10.1590/2175-78602000517...
).

Figure 1
Location of Reserva Ecológica de Guapiaçu (red/white circle) in the context of the Atlantic Forest remnants of Rio de Janeiro (green), Southeastern Brazil. Shapefile of forest coverage is from the Brazilian NGO SOS Mata Atlântica database.

REGUA covers an area of 7,400 hectares. The dominant vegetation there is classified as Dense Ombrophilous Forest, with different structures and typologies such as: Dense Alluvial Ombrophilous Forest in flat relief; Lowland Dense Ombrophilous Forest in soft undulating relief; and Submontane Dense Ombrophilous Forest in highland undulating relief. REGUA has a mosaic of Atlantic Forest at different levels of conservation (Figs 2-6), from secondary forests in their initial stages of succession, to mature and undisturbed forests located at higher altitude areas of difficult access (Rocha et al. 2007Rocha CFD, Vrcibradic D, Kiefer MC, Almeida-Gomes M, Borges-Junior VNT, et al. (2007) A survey of the leaf-litter frog assembly from an Atlantic Forest area (Reserva Ecológica de Guapiaçu) in Rio de Janeiro State, Brazil, with an estimate of frog densities. Tropical Zoology 20: 99-108.). In the surroundings of REGUA there are forest fragments of various sizes, monocultures, and pastures. Since the year 2000, vast areas of anthropic fields have been reforested, and native vegetation was planted on more than 200 ha of the reserve.

Figures 2-6
Forest landscape of Reserva Ecológica de Guapiaçu (2), and some habitat types, as follows: (3) mature forest with riparian vegetation; (4) late secondary forest with lowland flooded areas; (5) patches of initial secondary forest (‘capoeira’) in abandoned pastures; (6) open environment in peridomicile with exotic and native fruit trees. Photographs by Roberto Leonan M. Novaes.

Data collection

Different research groups have surveyed the bat fauna at REGUA. Here, we compile data from fieldwork carried out from August 1998 to September 2021 by Laboratório de Ecologia de Mamíferos at Universidade do Estado do Rio de Janeiro (LEMA, UERJ), Laboratório de Diversidade de Morcegos at Universidade Federal Rural do Rio de Janeiro (LADIM, UFRRJ), Fiocruz Mata Atlântica at Fundação Oswaldo Cruz (FMA, Fiocruz) and Bat Lab from Queen Mary University of London (QMUL). Most of these results are unpublished, except for two partial species’ lists presented by Souza et al. (2015Souza RF, Novaes RLM, Siqueira AC, Sauwen C, Jacob G, et al. (2015) Bats (Mammalia, Chiroptera) in a remnant of Atlantic Forest, Rio de Janeiro, southeastern Brazil. Neotropical Biology and Conservation 10: 9-14. https://doi.org/10.4013/nbc.2015.101.02
https://doi.org/10.4013/nbc.2015.101.02...
, 2016Souza RF, Novaes RLM, Felix S, Sauwen C, Jacob G, et al. (2016) Morcegos da Reserva Ecológica de Guapiaçu, Cachoeiras de Macacu, estado do Rio de Janeiro, Sudeste do Brasil. In: Santos MG (Ed.) Biodiversidade e sociedade no Leste Metropolitano do Rio de Janeiro. Editora da Universidade do Estado do Rio de Janeiro, São Gonçalo, 95-124.).

The data presented here originates from different projects and was obtained with different sampling designs over time. The common elements of these studies are: the bats were captured by 5-12 mist-nets (sizes ranging from 6 × 2.5 m to 12 × 3 m) at night, installed only at the ground level. Mist-nets remained open for either 6 or 12 hours each night after sunset and were set on trails and clearings in the vegetation, close to water bodies and near bat day roosts. Bats were baited in areas varying from initial secondary vegetation to mature native forest, under varying weather conditions and during all seasons and phases of the lunar cycle.

The captured bats were kept in cotton bags and identified in the field based on morphological characters. After triage, biometrics, and other biological information necessary for each project (e.g., sex, reproductive stage, age), the bats were released back at the capture site. Few specimens were collected (N = 74) to confirm their identifications or to obtain biological samples, and these specimens are deposited as vouchers at the Museu Nacional, Universidade Federal do Rio de Janeiro (Appendix 1 Appendix 1 Bats from Reserva Ecológica de Guapiaçu deposited in the mammal collection of Museu Nacional da Universidade Federal do Rio de Janeiro (MN, Rio de Janeiro). Phyllostomidae: Anoura caudifer (MN 79859, 83041, 83044); Anoura geoffroyi (MN 79860, 79918, 83042); Artibeus cinereus (MN 79875); Artibeus fimbriatus (MN 79861, 79862, 79919, 79920); Artibeus lituratus (MN 78125, 78126, 79863, 79864, 79865); Artibeus obscurus (MN 79866); Carollia perspicillata (MN 79867, 79868, 79869, 79870, 79871, 79872, 80334); Chiroderma villosum (MN 79873); Chrotopterus auritus (MN 79874); Desmodus rotundus (MN 79876, 80349); Diaemus youngii (MN 79877); Glossophaga soricina (MN 79882, 79883, 83043); Lonchophylla peracchii (MN 78404); Micronycteris minuta (MN 79884, 79885, 79886, 79887, 79888, 79889, 79890, 79917); Mimon bennettii (MN 79891; 79892); Phyllostomus hastatus (MN 79903); Platyrrhinus recifinus (MN 79904, 79905, 79921); Sturnira lilium (MN 79906, 79907, 79908, 79922); Sturnira tildae (MN 79909); Tonatia bidens (MN 80343, 80350); Trachops cirrhosus (MN 79911); Vampyressa pusilla (MN 79912, 79913); Vampyrodes caraccioli (MN 79914, 79915). Molossidae: Eumops glaucinus (MN 79881); Molossus fluminensis (MN 79894); Molossus molossus (MN 79893, 79916). Vespertilionidae: Eptesicus diminutus (MN 79878, 79879); Eptesicus furinalis (MN 79880); Myotis nigricans (MN 79895, 79896, 79897, 79898, 79900, 79901, 79902); Myotis riparius (MN 79899). ). Two occasional observations of species that were not sampled in mist nets were recorded: one individual of Noctilio leporinus (Linnaeus, 1758) foraging on a lake, and three Thyroptera tricolor Spix, 1823 individuals roosting in a rolled leaf of a banana tree. In this study, these species were included in the species list, but they were not included in the total number of individuals captured and in ecological analyses. All field and laboratory procedures followed ethical precepts (q.v., Sikes and Animal Care and Use Committee of the ASM 2016Sikes RS, Animal Care and Use Committee of the American Society of Mammalogists (2016) Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. Journal of Mammalogy 97: 663-688. https://doi.org/10.1093/jmammal/gyw078
https://doi.org/10.1093/jmammal/gyw078...
) and were authorized by governmental agencies under research licenses (1985/89-DIFAS/DEVIS; SISBio 3893-1/28717; SISBio 19037-1; SISBio 74191-3; SISBio 12548-1; SisGen A46B0E1; CEUA/IBRAG/UERJ nº 009/2021; CEUA/Fiocruz LM-2/18).

Data analysis

We followed the taxonomic arrangement in Garbino et al. (2020Garbino GST, Gregorin R, Lima IP, Loureiro L, Moras LM, Moratelli R, Nogueira MR, Pavan AC, Tavares VC, Nascimento MC, Peracchi AL (2020) Updated checklist of Brazilian bats: versão 2020. Comitê da Lista de Morcegos do Brasil, Sociedade Brasileira para o Estudo de Quirópteros (SBEQ). https://www.sbeq.net/lista-de-especies.
https://www.sbeq.net/lista-de-especies...
). Genera and species are presented in alphabetical order. The classification into trophic guilds followed Kalko et al. (1996Kalko EKV, Handley CO, Handley D (1996) Structure, diversity, and long-term dynamics of a Neotropical bat community. In: Cody ML, Smallwood JA (Eds) Long-term studies of vertebrate communities. Academic Press, New York, 503-553.). We calculated the sampling effort following Straube and Bianconi (2002Straube F, Bianconi GV (2002) Sobre a grandeza e a unidade utilizada para estimar esforço de captura com utilização de redes-de-neblina. Chiroptera Neotropical 8: 150-152.) and capture efficiency was calculated by dividing the number of captures by the sampling effort employed. To test the effect of sampling effort and number of captures on accumulated bat species richness, we performed linear regression analyses using the ‘Stats v.3.5.0’ package in the R platform (R Core Team 2021R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at Available at https://www.R-project.org [Accessed: 12/11/2021]
https://www.R-project.org...
).

We built a species accumulation curve and from it we extrapolated an estimate of the species richness following Chao et al. (2014Chao A, Gotelli NJ, Hsieh TC, Sander EL, Ma KH, Colwell RK, Ellison AM (2014) Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecological Monographs 84: 45-67. http://doi.org/10.1890/13-0133.1
http://doi.org/10.1890/13-0133.1...
). This approach uses rarefaction and extrapolation in an integrated way, based on the first three Hill numbers (q = 0, species richness; q = 1, Shannon diversity; q = 2, Simpson diversity; q.v., Chao et al. 2014Chao A, Gotelli NJ, Hsieh TC, Sander EL, Ma KH, Colwell RK, Ellison AM (2014) Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecological Monographs 84: 45-67. http://doi.org/10.1890/13-0133.1
http://doi.org/10.1890/13-0133.1...
). We used the extrapolation curve to predict how much the number of species could increase if we doubled the sampling effort. We also estimated a 95% confidence interval using the bootstrap method. These analyses were performed using the ‘iNEXT’ package in R platform (Hsieh et al. 2016Hsieh TC, Ma KH, Chao A (2016) Interpolation and extrapolation for species diversity. Available at https://cran.r-project.org/web/packages/iNEXT/iNEXT.pdf
https://cran.r-project.org/web/packages/...
). We estimated the maximum species richness that could be recorded using the Chao-1 index, implemented in the PAST 4 software (Hammer et al. 2001Hammer O, Harper DAT, Ryan PD (2001) PAST: Paleontological Statistics Software package for education and data analysis. Palaeontologia Electronica 4(1): 1-9.)

We estimated the species diversity with the Shannon index (H’) and species dominance with the 1-Simpson index (D’) using the PAST 4 software (Hammer et al. 2001Hammer O, Harper DAT, Ryan PD (2001) PAST: Paleontological Statistics Software package for education and data analysis. Palaeontologia Electronica 4(1): 1-9.) in order to compare the bat assemblage structure in REGUA with assemblages from other localities in the Brazilian Atlantic Forest. In these analyses, we excluded all captures that were made in roosts, to avoid bias in the results. Although aerial insectivorous bats are more difficult to capture using ground-level mist-nets (Mancini et al. 2022Mancini MCS, Hintze F, Laurindo RS, Mello RM, Gregorin R (2022) Tradition vs. innovation: comparing bioacoustics and mist-net results to bat sampling. Bioacoustics 31(5): 575-593. https://doi.org/10.1080/09524622.2021.2008494
https://doi.org/10.1080/09524622.2021.20...
)-the main method used in this study- we chose to keep them in the analyses because the capture probabilities of bats in this guild were the same throughout the entire sampling.

To test the significance of differences in species composition between the bat assemblage from REGUA and other localities, we used an analysis of variance (ANOVA) with a binary matrix of presence or absence. Pairwise comparisons were performed using the Mann-Whitney test and the p-value was corrected by the Bonferroni procedure (Kaufmann and Schering 2014Kaufmann J, Schering AG (2014) Analysis of Variance ANOVA. Wiley StatsRef: Statistics Reference Online. John Wiley & Sons, Inc. https://doi.org/10.1002/9781118445112.stat06938
https://doi.org/10.1002/9781118445112.st...
) on the PAST 4 software (Hammer et al. 2001Hammer O, Harper DAT, Ryan PD (2001) PAST: Paleontological Statistics Software package for education and data analysis. Palaeontologia Electronica 4(1): 1-9.).

RESULTS

The bat samplings carried out at REGUA between 1998 and 2008 were sporadic, and the sampling effort of each study was relatively low. In 2011, a continuous sampling using a comparatively high sampling effort (Table 1) was initiated. The total number of sampling nights carried out at REGUA was at least 194, and the total sampling effort was 448,092 m2.h (Table 2). As a result, 4,069 individuals of 47 species and six families were captured. Linear regressions recover a positive correlation between the accumulated species richness and number of captures (r2 = 0.669) or sampling effort (r2 = 0.874). However, this last metric performed better (Figs 7, 8).

Figures 7-8
Linear regressions of the accumulated species on: the sampling effort (7), and number of captures (8) in bat inventories at Reserva Ecológica de Guapiaçu, Brazil.

Table 1
Bat sampling conducted at Reserva Ecológica de Guapiaçu during almost two decades, including a detailed information of sampling effort, number of species recorded, and the total accumulated species throughout the research periods.

Table 2
Bats from Reserva Ecológica de Guapiaçu, including a simplified trophic guild classification; type of record (RC = roost capture; MN = mist net capture; FO = foraging observation); and number of individuals captured (N).

The species accumulation curve has not reached its asymptote, despite showing a tendency to stabilization (Fig. 9). Looking at the extrapolation from this curve, we expect that four additional species will be recorded if we double the sampling effort (Fig. 9). The estimated richness at REGUA is 53 species, according to the Chao-1 index. Our analysis shows that the number of species in our list represents about 89% of the estimated bat richness for this area.

Figure 9
Estimated species accumulation curves (solid line) and extrapolated (dotted line) of bat assemblage at the Reserva Ecológica de Guapiaçu. The dotted line is a representation of the doubled number of captures. The shaded area represents the 95% confidence interval.

Phyllostomidae was the richest family at REGUA, with 30 species, followed by Vespertilionidae (10 spp.), Molossidae (3 spp.), Emballonuridae (2 spp.), Noctilionidae (1 sp.), and Thyropteridae (1 sp.). The most abundant species were Carollia perspicillata (Linnaeus, 1758) (49% of all captures), Artibeus lituratus (Olfers, 1818) (23%), and Sturnira lilium (É. Geoffroy, 1810) (11%). All trophic guilds recognized for Neotropical bats were recorded, with a marked dominance of frugivorous species (86% of all captures). Excluding individuals captured in roosts, aerial insectivorous bats accounted for only 1.6% of all captures. The aerial insectivorous bats Peropteryx macrotis (Wagner, 1843), Saccopteryx leptura (Schreber, 1774), Eumops glaucinus (Wagner, 1843), and Molossus sp. were captured exclusively while leaving their roosts. Three species are endemic to the Atlantic Forest (Lonchophylla peracchii Dias, Esbérard & Moratelli, 2013, Platyrrhinus recifinus (Thomas, 1901), and Myotis ruber (É. Geoffroy, 1806)) and another three are strongly associated with the Atlantic Forest (Vampyressa pusilla (Wagner, 1843), Molossus fluminensis Lataste, 1891, and Myotis levis (I. Geoffroy, 1824)), although there are sporadic records of them in other ecoregions. Some species in our list have been rarely recorded in the Atlantic Forest, such as S. leptura, Lonchorhina aurita Tomes, 1863, Vampyrodes caraccioli (Thomas, 1889), and E. glaucinus.

REGUA has a highly diverse bat assemblage, with low species dominance when compared with other locations in the Atlantic Forest, while very similar to other large Atlantic Forest remnants, such as Tijuca Forest, Ilha Grande, and Tinguá Biological Reserve (Table 3). However, there is a significant difference in species composition between the bat assemblage of REGUA and other localities, except Tijuca Forest and Ilha Grande (F = 5.123, p < 0.0001; Table 4).

Table 3
Localities in the Atlantic Forest with long-term studies of bat assemblage, including the sampling effort (SE - m2.h), number of species recorded (Nsp), number of captures (Ncap), species diversity by Shannon index (H’), species dominance by 1-Simpson index (D’), and the reference of the published study (Source). REGUA = Reserva Ecológica de Guapiaçu.

Table 4
P-values from ANOVA pairwise comparisons between six bat assemblages. Values statistically significant (p < 0.05) are in boldface indicating differences in species composition from different areas. REGUA = Reserva Ecológica de Guapiaçu.

DISCUSSION

REGUA is among the richest places for bat species in the Atlantic Forest (Esbérard 2003Esbérard CEL (2003) Diversidade de morcegos m área de Mata Atlântica regenerada no Sudeste do Brasil. Revista Brasileira de Zoociências 5: 189-204., Faria et al. 2006Faria D, Soares-Santos B, Sampaio E (2006) Bats from the Atlantic rainforest of southern Bahia, Brazil. Biota Neotropica 6: bn02406022006. https://doi.org/10.1590/S1676-06032006000200022
https://doi.org/10.1590/S1676-0603200600...
, Dias et al. 2008Dias D, Esbérard CEL, Peracchi AL (2008) Riqueza, diversidade de espécies e variação altitudinal de morcegos na Reserva Biológica do Tinguá, estado do Rio de Janeiro, Brasil (Mammalia, Chiroptera). In: Reis NR, Peracchi AL, Santos GASD (Eds) Ecologia de morcegos. Technical Books, Rio de Janeiro, 125-142., Gomes and Esbérard 2017Gomes LAC, Esbérard CEL (2017) Long-term bat study on an island in the southeastern Brazilian coast with comparison of richness and composition of species among sites. Studies on Neotropical Fauna and Environment 52: 43-52. https://doi.org/10.1080/01650521.2016.1272168
https://doi.org/10.1080/01650521.2016.12...
, Delciellos et al. 2018Delciellos AC, Motta A, Dias D, Almeida B, Rocha-Barbosa O (2018) Bats of the Serra da Bocaina National Park, southeastern Brazil: an updated species list and a distribution extension for Trinycteris nicefori (Sanborn, 1949). Biota Neotropica 18: e20180537. https://doi.org/10.1590/1676-0611-BN-2018-0537
https://doi.org/10.1590/1676-0611-BN-201...
, Cronemberguer et al. 2019Cronemberguer C, Delciellos AC, Barros CS, Gentile R, Weksler M, Braz AG, et al. (2019) Mamíferos do Parque Nacional da Serra dos Órgãos: atualização da lista de espécies e implicações para a conservação. Oecologia Australis 23: 191-214. https://doi.org/10.4257/oeco.2019.2302.02
https://doi.org/10.4257/oeco.2019.2302.0...
, Hoppe et al. 2020Hoppe JPM, Ventorin ML, Dell’Antonio BM, Silva TM, Ditchfield AD (2020) Bat assemblage at a high diversity locality in the Atlantic Forest. Neotropical Biology and Conservation 15: 484-501. https://doi.org/10.3897/neotropical.15.e55986
https://doi.org/10.3897/neotropical.15.e...
, Costa et al. 2021Costa LM, Lourenço EC, Damasceno-Júnior DA, Dias D, Esbérard CEL, Jordão-Nogueira T, Melo G, Bergallo HG (2021) Ilha Grande, one of the locations with the most records of bat species (Mammalia, Chiroptera) in Rio de Janeiro state: results of a long-term ecological study. Papéis Avulsos de Zoologia 61: e20216122. https://doi.org/10.11606/1807-0205/2021.61.22
https://doi.org/10.11606/1807-0205/2021....
, Tavares et al. 2021Tavares JA, Novaes RLM, Veríssimo I, Kuzel MAA, Costa-Neto SF, et al. (2021) Bats from the Pedra Branca Forest, Rio de Janeiro, Brazil. Biodiversity Data Journal 9: e77400. https://doi.org/10.3897/BDJ.9.e77400
https://doi.org/10.3897/BDJ.9.e77400...
), with 47 species, which is equivalent to about 46% of the bat richness known for the Brazilian Atlantic Forest (Graipel et al. 2017Graipel ME, Cherem JJ, Monteiro-Filho ELA, Carmignotto AP (2017) Mamíferos da Mata Atlântica. In: Monteiro-Filho ELA, Conte CE (Eds) Revisões em Zoologia: Mata Atlântica. Editora da Universidade Federal do Paraná, Curitiba, 391-482., Muylaert et al. 2017Muylaert RL, Stevens RD, Esbérard CEL, Mello MAR, Garbino GST, et al. (2017) Atlantic Bats: a data set of bat communities from the Atlantic Forests of South America. Ecology 98: 3227-3227. https://doi.org/10.1002/ecy.2007
https://doi.org/10.1002/ecy.2007...
). It is possible that this high bat diversity there can be explained by the large area of continuous mature forest connected with other forested areas, and by the time span of the sampling effort, over two decades. However, some results indicate that the species list has not yet reached its maximum, as the species accumulation curve has yet to reach its asymptote. Furthermore, some specimens sampled were not identified to species, and it is possible that they represent unrecorded taxa.

In almost 20 years of research with bats at REGUA, the only sampling method used in a standardized way was ground level mist-nets. Therefore, it is most likely that the bat assemblage at REGUA is undersampled, since aerial insectivorous bats, especially molossids, vespertilionids and embalonurids are not efficiently captured by ground-level mist-nets, because they are able of more accurate echolocation, and they fly at the highest strata of the forest (Portfors et al. 2000Portfors CV, Fenton MB, Aguiar LMS, Baumgarten JE, Vonhof MJ, et al. (2000) Bats from Fazenda Intervales, Southeastern Brazil - species account and comparison between different sampling methods. Revista Brasileira de Zoologia 17: 533-538. https://doi.org/10.1590/S0101-81752000000200022
https://doi.org/10.1590/S0101-8175200000...
, Kalko and Handley 2001Kalko EKV, Handley CO (2001) Neotropical bats in the canopy: diversity, community structure, and implications for conservation. Plant Ecology 153: 319-333. https://doi.org/10.1023/A:1017590007861
https://doi.org/10.1023/A:1017590007861...
, Mancini et al. 2022Mancini MCS, Hintze F, Laurindo RS, Mello RM, Gregorin R (2022) Tradition vs. innovation: comparing bioacoustics and mist-net results to bat sampling. Bioacoustics 31(5): 575-593. https://doi.org/10.1080/09524622.2021.2008494
https://doi.org/10.1080/09524622.2021.20...
). The number of species in this guild recorded from REGUA are lower when compared to other areas where alternative methods were used (q.v., Mancini et al. 2022Mancini MCS, Hintze F, Laurindo RS, Mello RM, Gregorin R (2022) Tradition vs. innovation: comparing bioacoustics and mist-net results to bat sampling. Bioacoustics 31(5): 575-593. https://doi.org/10.1080/09524622.2021.2008494
https://doi.org/10.1080/09524622.2021.20...
). Consequently, future studies with bats should consider the adoption of new sampling methods, such as bioacoustics and active search of bat roosts. We expect that these methods will increase the number of species from REGUA and its surroundings, especially when we consider the occurrence of different bat species in localities close to REGUA (e.g., Micronycteris hirsuta, Macrophyllum macrophyllum, Myotis izecksohni; Novaes et al. 2015Novaes RLM, Rosa DTC, Vrcibradic D, Avilla LS (2015b) Bat assemblages from three Atlantic Forest fragments in Rio de Janeiro state, Southeastern Brazil. Biodiversity Data Journal 3: e4404. https://doi.org/10.3897/BDJ.3.e4404
https://doi.org/10.3897/BDJ.3.e4404...
b, Cronemberger et al. 2019Cronemberguer C, Delciellos AC, Barros CS, Gentile R, Weksler M, Braz AG, et al. (2019) Mamíferos do Parque Nacional da Serra dos Órgãos: atualização da lista de espécies e implicações para a conservação. Oecologia Australis 23: 191-214. https://doi.org/10.4257/oeco.2019.2302.02
https://doi.org/10.4257/oeco.2019.2302.0...
, Louzada et al. 2021Louzada NSV, Nogueira MR, Pessôa LM (2021) First record of Macrophyllum macrophyllum (Schinz, 1821) in Brazilian mangroves, with comments on bat diversity in this region. Notas sobre Mamíferis Sudamericanos 3: 1-3. http://doi.org/10.31687/saremNMS.21.6.2
http://doi.org/10.31687/saremNMS.21.6.2...
).

The number of specimens from REGUA deposited as vouchers in biological collections (N = 74) is low, considering that bats were sampled for a number of years, and that not all species are represented. Some individuals were not identified to species level during the fieldwork, nor were they collected for further examination. This raises questions about the real number of bat species in the region. Future studies should increase the representation of local species in biological collections, particularly those not yet represented (see Moratelli 2014Moratelli R (2014) Wildlife biologists are on the right track: a mammalogist’s view of specimen collection. Zoologia (Curitiba) 31: 413-417. https://doi.org/10.1590/S1984-46702014000500001
https://doi.org/10.1590/S1984-4670201400...
).

Long-term studies are valuable for a better characterization of the local biodiversity, but it can also provide accurate information about population fluctuations in response to climatic variations, landscape modifications, and other ecological disturbances (Callahan 1984Callahan JT (1984) Long-term ecological research. BioScience 34: 363-367. https://doi.org/10.2307/1309727
https://doi.org/10.2307/1309727...
, Havstad and Herrick 2010Havstad KM, Herrick JE (2010) Long-term ecological monitoring. Arid Land Research and Management 17: 389-400. https://doi.org/10.1080/713936102
https://doi.org/10.1080/713936102...
). In relation to tropical bats, Meyer et al. (2010Meyer CFJ, Aguiar LMS, Aguirre LF, Baumgarten J, Clarke FM, et al. (2010) Long-term monitoring of tropical bats for anthropogenic impact assessment: Gauging the statistical power to detect population change. Biological Conservation 143: 2797-2807. https://doi.org/10.1016/j.biocon.2010.07.029
https://doi.org/10.1016/j.biocon.2010.07...
) indicated that long-term monitoring programs of bat assemblages for more than 20 years can potentially detect a 5% annual change in abundance for a suite of bat species from different ensembles. Nevertheless, this requires a rigorous sampling design and conceptual framework to allow robust statistical modeling to answer long-term ecological questions (Lindenmayer and Likens 2009Lindenmayer DB, Likens GE (2009) Adaptive monitoring: a new paradigm for long-term research and monitoring. Trends in Ecology and Evolution 24: 482-486. https://doi.org/10.1016/j.tree.2009.03.005
https://doi.org/10.1016/j.tree.2009.03.0...
). In this sense, REGUA is a great candidate to host long-term bat monitoring programs, considering all basic knowledge about its bat fauna accumulated in these two decades of research. We suggest that new research projects should be based on a collaborative and multi-institutional protocol that aims to standardize efforts on a temporal and geographic scale that can meet short-term objectives, while aggregating data for continuous and long-term monitoring.

Because of its high bat diversity, associated with large forest remnants in an agricultural matrix and its location close to the urban center of Rio de Janeiro city, REGUA is an important area for long-term research. Studies there can potentially address questions about bat assemblage structure, populational fluctuations, bat-parasite ecology, competition, niche partitioning, effects of habitat quality, and other related topics. In addition, basic knowledge about the ecological interactions of bats with different food resources (Novaes et al. 2015Novaes RLM, Souza RF, Ribeiro EA, Siqueira AC, Greco AV, Moratelli R (2015a) First evidence of frugivory in Myotis (Chiroptera, Vespertilionidae, Myotinae). Biodiversity Data Journal 3: e6841. https://doi.org/10.3897/BDJ.3.e6841
https://doi.org/10.3897/BDJ.3.e6841...
a, Oelbaum et al. 2022Oelbaum PJ, Teixeira TSM, Clare EL, Broders HG (2022) Variation in diet of frugivorous bats in fragments of Brazil’s Atlantic Forest associated with vegetation density. Journal of Mammalogy: gyac024. https://doi.org/10.1093/jmammal/gyac024
https://doi.org/10.1093/jmammal/gyac024...
) and zoonotic microorganisms (Rangel et al. 2019Rangel D, Lisboa CV, Novaes RLM, Silva BA, Souza RF, et al. (2019) Isolation and characterization of trypanosomatids, including Crithidia mellificae, in bats from the Atlantic Forest of Rio de Janeiro, Brazil. PLoS Neglected Tropical Diseases 13: e0007527. https://doi.org/10.1371/journal.pntd.0007527
https://doi.org/10.1371/journal.pntd.000...
, Speer et al. 2022Speer KA, Teixeira TSM, Brown AM, Perkins SL, Dittmar K, et al. (2022) Cascading effects of habitat loss on ectoparasite-associated bacterial microbiomes. ISME Communications 2: a67. https://doi.org/10.1038/s43705-022-00153-0
https://doi.org/10.1038/s43705-022-00153...
) offers a unique opportunity to carry out research in several areas of knowledge, with direct implications for biodiversity conservation and public health management. Therefore, we suggest that bat sampling in REGUA continues in the form of a new bat monitoring program.

ACKNOWLEDGMENTS

André C. Siqueira, Camila Sant’Anna, Carlos Eduardo L. Santos, Cristal Sauwen, Edvandro A. Ribeiro, Gabriella Jacob, Letícia Moraes, Raíssa F. Souza, Saulo Felix, Isabela Belizzi, for helping with fieldwork. Davor Vrcibradic, Nicholas Locke and REGUA’s staff provide support for the field activities. Rafael S. Laurindo for helping in the statistical analyses. LMC and ECL thank Programa de Apoio à Pesquisa e Docência (PAPD) for the benefit granted by the Universidade do Estado do Rio de Janeiro (UERJ). HGB has received support from Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ; E-26/200.913/2021) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; 306585/2018-9). PSMA received support from environmental compensation from Vale S.A. managed by the National Center for Research and Conservation of Caves (CECAV/ICMBio) and destined to the Sociedade Brasileira para o Estudo de Quirópteros (SBEQ), as part of the Small Scholarship Program in Biology, Ecology and Conservation of Bats; grant from Bat Conservation International (SS2102) and scholarship from FAPERJ (E-26/200.485/2020). CELE has received support from CNPq (151029/2004-0) and FAPERJ (E-26/102.201/2009). RM has received support from FAPERJ (E-26/200.967/2021); RLMN has received support from FAPERJ (E-26/204.243/2021).

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ADDITIONAL NOTES

  • Zoobank register

    https://zoobank.org/D47425AE-909B-4007-8768-6DEE1D721157
  • How to cite this article

    Pires RSA, Soares G, Souza RF, Teixeira TSM, Monteiro-Alves PS, Lourenço EC, Bergallo EG, Costa LM, Santori RT, Esbérard CEL, Moratelli R, Novaes RLM (2022) Bat species diversity from the Reserva Ecológica de Guapiaçu, Rio de Janeiro, Brazil: a compilation of two decades of sampling. Zoologia (Curitiba) 39: e22032. https://doi.org/10.1590/S1984-4689.v39.e22032
  • Published by

    Sociedade Brasileira de Zoologia at Scientific Electronic Library Online (https://www.scielo.br/zool)

Appendix 1

Bats from Reserva Ecológica de Guapiaçu deposited in the mammal collection of Museu Nacional da Universidade Federal do Rio de Janeiro (MN, Rio de Janeiro).

Phyllostomidae: Anoura caudifer (MN 79859, 83041, 83044); Anoura geoffroyi (MN 79860, 79918, 83042); Artibeus cinereus (MN 79875); Artibeus fimbriatus (MN 79861, 79862, 79919, 79920); Artibeus lituratus (MN 78125, 78126, 79863, 79864, 79865); Artibeus obscurus (MN 79866); Carollia perspicillata (MN 79867, 79868, 79869, 79870, 79871, 79872, 80334); Chiroderma villosum (MN 79873); Chrotopterus auritus (MN 79874); Desmodus rotundus (MN 79876, 80349); Diaemus youngii (MN 79877); Glossophaga soricina (MN 79882, 79883, 83043); Lonchophylla peracchii (MN 78404); Micronycteris minuta (MN 79884, 79885, 79886, 79887, 79888, 79889, 79890, 79917); Mimon bennettii (MN 79891; 79892); Phyllostomus hastatus (MN 79903); Platyrrhinus recifinus (MN 79904, 79905, 79921); Sturnira lilium (MN 79906, 79907, 79908, 79922); Sturnira tildae (MN 79909); Tonatia bidens (MN 80343, 80350); Trachops cirrhosus (MN 79911); Vampyressa pusilla (MN 79912, 79913); Vampyrodes caraccioli (MN 79914, 79915).

Molossidae: Eumops glaucinus (MN 79881); Molossus fluminensis (MN 79894); Molossus molossus (MN 79893, 79916).

Vespertilionidae: Eptesicus diminutus (MN 79878, 79879); Eptesicus furinalis (MN 79880); Myotis nigricans (MN 79895, 79896, 79897, 79898, 79900, 79901, 79902); Myotis riparius (MN 79899).

Edited by

Editorial responsibility

Guilherme S.T. Garbino

Publication Dates

  • Publication in this collection
    25 Nov 2022
  • Date of issue
    2022

History

  • Received
    06 July 2022
  • Accepted
    02 Sept 2022
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