Research Article
Print
Research Article
Bat assemblage at a high diversity locality in the Atlantic Forest
expand article infoJoão Paulo Maires Hoppe, Maria Lavanholle Ventorin, Bruna Malavazi Dell’ Antonio, Carlos Tiago Machel da Silva, Albert David Ditchfield
‡ Universidade Federal do Espírito Santo, Vitória, Brazil
Open Access

Abstract

The Estação Biológica Santa Lúcia (EBSL) is one of the oldest reserves in Brazil, used as a research site since 1939 by the naturalist Augusto Ruschi. It is an Atlantic Forest fragment, and its fauna and flora have been studied throughout the years. However, its chiropteran fauna remains virtually unknown. Here, we aim to provide a bat species list for EBSL. We installed mist-nets over 19 nights from mid-2009 to mid-2010, with a sampling effort of 20 875.5 m2.h. We captured 204 specimens, from two families and 22 species. Ecological analysis reveals a medium to high diversity, heavily dominated by frugivorous species. The collector’s curve and the estimative of species richness suggests that the chiropteran fauna at EBSL remains partially unknown, and we encourage further inventories.

Keywords

Augusto Ruschi, Chiroptera, fragment, southeastern Brazil, species richness

Introduction

Bats play an important ecological role in their ecosystems, especially in pollination and seed dispersal, feeding on fruits, insects, nectar, and other vertebrates as well as blood (Fenton et al. 1992). Of the 181 species recorded in Brazil (Delgado-Jaramillo et al. 2020; Garbino et al. 2020), 83 are known to occur in the state of Espírito Santo (Vela-Ulian et al. in press).

This state is entirely covered by the Atlantic Forest, one of the most diverse and fragmented Brazilian domains, reduced to 11.4% to 16% of its original extension (Ribeiro et al. 2009). Knowledge about bats at the Espírito Santo state began with Maximilian Alexander Philip, the Prince zu Wied-Neuwied. He was a German naturalist explorer, one of the many travelling naturalists who came to the Neotropical Region to catalog the biodiversity (Rocha 1971; Kury 2001). Through his efforts, four bats species were known to occur at Espírito Santo (Schinz 1821; Wied-Neuwied 1826). The nineteenth century had other collections by naturalists, such as Saint-Hilaire and Castelnaeu, until the 1940s, with 11 bat species for the state: Anoura caudifer, Carollia brevicauda, Carollia perspicillata, Centronycteris maximiliani, Desmodus rotundus, Glossophaga soricina, Myotis nigricans, Phyllostomus hastatus, Platyrrhinus lineatus, Rhynchonycteris naso, and Saccopteryx leptura (Lima 1926; Vieira 1942; Ruschi 1951; Mendes et al. 2010).

The Estação Biológica Santa Lúcia (EBSL) reserve is one of the oldest forest reserves in Brazil. The naturalist Augusto Ruschi conducted researches in this area since 1939, mainly on orchids, hummingbirds and bats (Ruschi-Filho 1972). Ruschi conducted his studies on the chiropterofauna of the state of Espírito Santo between 1950 and 1978, publishing a series of papers documenting each species, accompanied by morphological and behavioral data. He also studied the occurrence of rabies on bats, finding positive cases in 19 species (see Ruschi 1978). Following his efforts, Espírito Santo was found to have 37 species of bats. Afterwards, Adriano Peracchi, the first Brazilian specialist in bats, initiated his collections in 1970 in what today is the Floresta Nacional de Goytacazes, reaching a richness of 55 bat species (Peracchi and Albuquerque 1993). Finally, systematic efforts (e.g., Oprea et al. 2007; Vieira et al. 2008; Peracchi et al. 2011) raised to 83 the number of bat species at Espírito Santo state (Vela-Ulian et al. in press).

The EBSL has a convoluted and, even to this day, partially unsolved history. It dates back to, at least, 1939, when an area next to the Timbuí River margins was acquired by the Museu Nacional and the Sociedade de Amigos do Museu Nacional. Ten years later, Augusto Ruschi created the Museu de Biologia Prof. Mello Leitão (MBML), with an acquisition of a second area, bordering the first. These areas were later contested by the Espírito Santo government, due to some irregularities with the paperwork. It endured until 1980, when ownership of the land by the Universidade Federal do Rio de Janeiro (UFRJ) was recognized, with an area of 156 ha. However, a certain imprecision concerning the name, area and perimeter remained. Therefore, MBML decide to name the union of four contiguous areas as “Estação Biológica Santa Lúcia”. The first is the 156 ha aforementioned area, belonging to UFRJ. The second is a 53 ha area belonging to IPHAN (Instituto do Patrimônio Histórico e Artístico Nacional), acquired by Ruschi through the Brazilian State in 1983. A third area, with 129 ha, belongs to the Sociedade de Amigos do Museu Nacional, and was donated to Ruschi at 1972. Finally, there are 103 ha of preserved vacant land, summing up to 440 ha. However, the perimeter is still undefined (Mendes and Padovan 2000).

A number of studies have been conducted at EBSL, including entomological (Azevedo et al. 2003; Barbosa et al. 2014), botanical (Goldenberg and Reginato 2006; Kollmann 2006; Saiter and Thomaz 2014), ornithological (Ruschi 1977; Simon 2000), and mammalian (Passamani 2000; Passamani et al. 2000; Paresque et al. 2004). However, apart from a few isolated records (e.g., Zortéa and Brito 2000; Redondo et al. 2008; Velazco and Patterson 2008), there has been no systematic effort to collect bats at EBSL. Herein, we provide an updated list of bat species present at EBSL.

Materials and methods

Study site

The Estação Biológica Santa Lúcia (EBSL) reserve is a forest fragment located 7 km southeast from the center of the Santa Teresa city, Espírito Santo state, southeastern Brazil (19°57'55"S, 040°32'23"W) (Fig. 1). The EBSL encompasses about 440 hectares of Atlantic Forest, with many trails available. The vegetation is Montane Ombrophilous Dense Forest (Veloso and Goés-Filho 1982), with signs of anthropic action (Mendes and Padovan 2000). There are several disturbances at EBSL, especially agricultural activity. There is significant garbage disposal in the Timbuí River, the main water course crossing EBSL (Mendes and Padovan 2000), and there is an abundant and constant presence of domestic dogs (Srbek-Araujo and Chiarello 2008).

There are many forest fragments within the Santa Teresa city perimeter, most of them of small size. The EBSL is contained in a fragment located in the southeastern region, almost at the boundary with Santa Leopoldina city. There are two conservation units close to EBSL: the Reserva Biológica Augusto Ruschi (3 598 ha), about 5 km north, and Área de Proteção Ambiental do Pico de Goiapaba-Açú (3 740 ha), approximately 5 km northeast. The majority of the forest fragments are contained within the Reserva da Biosfera da Mata Atlântica (Fig. 1). Climate is subtropical humid (Cfa of Köppen), with mean annual temperature of 19.9 °C, ranging from 14.3 to 26.2 °C (Thomaz and Monteiro 1997), and mean annual precipitation of 1 824 mm (SNIRH 2018). The area has a cold and dry season between April and September, and a hot and wet season between October and March, with mean precipitation of 587 mm and 1 237 mm, respectively (SNIRH 2018).

Figure 1. 

Estação Biológica Santa Lúcia (EBSL) location in southeastern Brazil. The state of Espírito Santo is denoted in pink, and Santa Teresa city in gray. EBSL is represented by the hatched area, with the center of Santa Teresa depicted by the black point. Several forest fragments, depicted in green, surround EBSL.

Sampling and analysis

We captured bats with mist nets during 19 nights between May to October 2009, and February to June 2010, which were opened from dusk to dawn (18:00 to 6:00 h) in five different trails (Table 1), during different moon phases and both rainy and dry seasons. We sampled over the course of one to four nights each month, always choosing a different trail each night. All mist nets had a height of 3 m, while the length varied from 6 to 15 m (Table 2). Netting effort was 18 466.5 m2.h, calculated following Straube and Bianconi (2002). Capture efficiency was calculated as the ratio of number of captures by the sampling effort. Identifications followed Gardner (2008) and Díaz et al. (2016).

Table 1.

Sampled trails at Estação Biológica Santa Lúcia (EBSL), southeastern Brazil.

Trail Coordinates Altitude (m) Nights
Indaiá-Açú 19°58'00"S, 040°32'17"W 703 4
Rio (near Augusto Ruschi grave) 19°58'23"S, 040°31'44"W 657 7
Rio (near lodgings) 19°57'55"S, 040°31'38"W 648 4
Sagui 19°58'24"S, 040°32'05"W 813 1
Tapinoã 19°58'08"S, 040°31'43"W 708 3
Table 2.

Number of mist nets used each night, by length, with start and finishing hours, and the resulting sampling effort for bat capturing in an area of Atlantic Forest, southeastern Brazil. All mist nets had a 3 m height.

Nights Trail Length (m) Start Finish Effort (m2.h)
6 7 9 12 15
09/05/2009 Rio, grave 2 0 2 0 0 17:20 23:45 500.50
10/05/2009 Rio, grave 0 0 4 2 1 17:30 0:10 1300.00
11/07/2009 Rio, lodging 0 0 4 1 1 17:00 0:00 1146.60
14/07/2009 Tapinoã 0 0 3 0 1 17:30 0:30 764.40
15/07/2009 Rio, grave 0 0 4 1 0 17:30 21:30 499.20
16/07/2009 Indaiá-Açú 0 0 5 2 1 17:00 0:00 1528.80
11/08/2009 Rio, lodging 0 0 4 0 0 18:30 0:30 561.60
14/08/2009 Indaiá-Açú 0 0 2 1 1 17:30 0:40 838.50
15/08/2009 Tapinoã 0 1 2 1 1 17:30 0:30 946.40
16/08/2009 Rio, lodging 0 0 3 1 0 17:30 0:30 709.80
27/09/2009 Rio, grave 4 1 2 0 0 18:00 6:00 1528.80
28/09/2009 Indaiá-Açú 4 0 2 0 0 18:00 6:00 1310.40
24/10/2009 Tapinoã 2 2 3 1 0 18:00 5:00 1859.00
27/02/2010 Rio, grave 3 0 0 0 0 18:00 6:00 561.60
28/02/2010 Rio, lodging 4 0 0 0 0 18:00 0:45 421.20
19/03/2010 Sagui 7 0 1 0 0 18:00 3:30 1259.70
03/06/2010 Rio, grave 3 0 0 0 0 17:05 0:15 335.40
04/06/2010 Indaiá-Açú 6 0 0 0 0 17:05 5:40 1177.80
05/06/2010 Rio, grave 6 0 0 0 0 17:25 6:25 1216.80

After capture, we assessed individual weight, sex, reproductive condition, forearm length and feeding guild based on the categories proposed by Schnitzler and Kalko (2001). The first of each species, and those with uncertain identification on the field were collected as vouchers, under license 14592-1937 (IBAMA). The vouchers were first fixed in formaldehyde, then fluid-preserved in 70% alcohol, with the skull removed and cleaned and liver tissue extracted. Vouchers were deposited in the Mammalian Collection at Universidade Federal do Espírito Santo (UFES-MAM) (see Appendix 1). We built a species accumulation curve, estimated the species richness using the first-order Jackknife estimator, and calculated the species diversity index using the probability of interspecific encounter (PIE) (Hurlbert 1971). PIE is metric that can be interpreted as “what is the probability that two species of a community, taken at random, belong to two different species?” It is the complement of the Simpson’s diversity index (D), a metric that asks the chance of, in the aforementioned scenario, being of the same species (PIE = 1 – D), and sometimes is called the Gini-Simpson index (Jost 2007; Chase and Knight 2013). We chose PIE because it is more sensitive to species evenness, and is rather insensitive to species richness, after a certain threshold has been surpassed, around 10 species (Hurlbert 1971). The index ranges from 0 to 1, with 0 a completely uneven community (e.g., a monoculture), and 1 a perfectly even community. A moderately uneven community has values around .75, and a highly uneven has .5 or lower. In order to provide a species diversity comparison, we compiled inventories of bat species conducted at the Atlantic Forest, tracking the study area size, species richness, and calculating PIE through available abundance data. All analysis was conducted using the software R 3.5.3 (R Core Team 2019), with the vegan package (Oksanen et al. 2019).

A few sporadic captures were made at EBSL before this study, with vouchers deposited at two collections: the Instituto Nacional da Mata Atlântica (INMA), and the aforementioned UFES-MAM. We checked records of bats in these collections through the speciesLink platform (speciesLink 2020).

Results

We captured a total of 204 individuals, from 22 species of two families, Phyllostomidae and Vespertilionidae (Table 3). Capture efficiency was 0.011 bats/m2.h. Phyllostomidae accounted for the largest number of species (18 spp.) and individuals, representing over 95% of captured specimens, with Vespertilionidae representing four species and 5% of all individuals captured. Almost 75% of captures were represented by three species, Carollia perspicillata, Artibeus lituratus and Artibeus fimbriatus.

We found slightly more females than males in our study, with 111 females and 85 males (8 specimens lack this data). Regarding the reproductive state, we found seven lactating and one post-lactating female, from the species Carollia perspicillata, Artibeus lituratus, Artibeus fimbriatus and Sturnira tildae. We also found 19 pregnant females, from Artibeus fimbriatus (N = 5), Artibeus lituratus (N = 4), Artibeus obscurus (N = 1), Carollia perspicillata (N = 8), and Myotis ruber (N = 1). We found 13 males with descended testes: Anoura geoffroyi (N = 1), Artibeus lituratus (N = 5), Carollia perspicillata (N = 6), and Myotis riparius (N = 1).

The species accumulation curve did not reach an asymptote (Fig. 2B). The first-order Jackknife estimated 29.6 species for EBSL, and the species diversity was PIE = .731. We registered five of the ten trophic guilds. Frugivores represented approximately 88% of the captures. The sanguivores represented less than 1% of the captures. We found 18 species based on museum vouchers, with six of them not found in our sampling: Micronycteris minuta, Lonchophylla mordax, Carollia brevicauda, Platyrrhinus lineatus, Eptesicus diminutus, and Lasiurus blossevillii (Table 3).

We found 119 bat species inventories conducted at the Atlantic Forest containing sufficient data to calculate the area PIE index. We excluded 28 of those inventories before analysis, as they lacked the study area size, or were areas sampled more than once, where we considered the higher species richness (see Suppl. material 1: Table S1).

Figure 2. 

Bat assemblages in an area of Atlantic Forest, southeastern Brazil. A. Species richness and PIE values from 90 inventories of bats. EBSL is highlighted by the red dot. Area of the locality is represented by the dot size. Blue line depicts a fitted model of expected PIE values due to species richness. See Suppl. material 1: Table S1 for details. B. Species accumulation curves based on first-order Jackknife richness estimator. Dashed line are the accumulated average number of species, after randomizations, and dotted line depicts the number of species estimated by Jackknife.

Table 3.

List of bat species captured at Estação Biológica Santa Lúcia (EBSL), southeastern Brazil, with abundance (by trail and total), and the feeding guild. Museum indicates if the record is based on a voucher deposited in an institution. ANI: Gleaning animalivore, BAI: aerial insectivore, FRU: frugivore, NEC: nectarivore, SAN: sanguivore, I: Indaiá-Açú, II: Rio (near Augusto Ruschi grave), III: Rio (near lodgings), IV: Sagui, V: Tapinoã.

Family Species Guild Museum I II III IV V Total
Phyllostomidae Micronycteris microtis ANI 0 0 0 1 0 1
Micronycteris minuta ANI X
Desmodus rotundus SAN X 0 0 2 0 0 2
Mimon bennettii ANI 0 1 0 0 0 1
Phyllostomus hastatus ANI 0 0 0 1 0 1
Trachops cirrhosus ANI X 1 0 0 0 0 1
Anoura caudifer NEC X 0 2 0 0 1 3
Anoura geoffroyi NEC X 2 1 1 0 1 5
Lonchophylla mordax NEC X
Lonchophylla peracchii NEC X 0 1 0 0 0 1
Carollia brevicauda FRU X
Carollia perspicillata FRU X 22 25 14 8 26 95
Rhinophylla pumilio FRU X 0 1 2 5 1 9
Artibeus fimbriatus FRU X 3 3 2 3 5 16
Artibeus lituratus FRU X 6 10 10 1 14 41
Artibeus obscurus FRU X 1 4 2 1 0 8
Dermanura cinerea FRU 0 1 1 0 0 2
Platyrrhinus lineatus FRU X
Platyrrhinus recifinus FRU X 0 0 0 0 1 1
Sturnira lilium FRU X 1 0 2 0 0 3
Sturnira tildae FRU 0 1 0 0 1 2
Vampyressa pusilla FRU 1 0 0 1 0 2
Vespertilionidae Eptesicus brasiliensis BAI 0 0 1 0 0 1
Eptesicus diminutus BAI
Lasiurus blossevillii BAI X
Myotis nigricans BAI X 0 0 1 0 0 1
Myotis riparius BAI 0 1 2 2 0 5
Myotis ruber BAI 0 1 0 1 1 3

Discussion

The family Phyllostomidae was the best represented in this Atlantic Forest locality, following a trend depicted by many other studies conducted in the Neotropical Region (e.g., Portfors et al. 2000; Esbérard 2003; Sampaio et al. 2003; Laurindo et al. 2016; Novaes et al. 2017). This pattern is explained by two factors: the wide distribution and high number of species, and especially by sampling bias due to using mist nets at ground level (Fleming 1986; Fenton et al. 1992). Employment of mist nets at canopy level and bioacoustics survey are recommended for a more effective sampling of aerial insectivore bats, such as the Emballonuridae, Molossidae and Vespertilionidae (Carvalho et al. 2013; Marques et al. 2016; Gregorin et al. 2017; Hintze et al. 2020).

Frugivores were the most abundant trophic guild in our sample (Table 3). Three species – Carollia perspicillata, Artibeus lituratus and Artibeus fimbriatus – represented almost 75% of all captured individuals, a pattern observed at the Atlantic Forest (e.g., Esbérard 2003; Lima et al. 2016; Novaes et al. 2017). The observed species diversity index (PIE) indicates a moderately uneven community, close to what is expected for an Atlantic Forest locality of similar observed species richness (Fig. 2A). This can be seen in the composition of the community: almost 75% of occurrences are of three species, while the remaining display a similar number of captured individuals (Table 3). Members of the genus Artibeus show a preference for Ficus, while Carollia consume mostly Piper fruits. These botanical genus are abundant throughout the Neotropical Region, providing a homogeneous and available food source (Parolin et al. 2016). In addition, the environmental disturbance at EBSL (Mendes and Padovan 2000) could have caused a reduction of ecological niches, especially most specialized ones, such as gleaning animalivores (e.g., Lophostoma, Lonchorhina, Chrotopterus), frugivorous (Chiroderma) and specialized nectarivorous (Lionycteris), that are known to occur in this region (Woodman and Timm 2006; Scabello et al. 2009; Mendes et al. 2014).

The species accumulation curve did not reach an asymptote (Fig. 2B). Accordingly, the first-order Jackknife estimated a species richness of 30 species, suggesting that our sampling recorded about 73% of the local richness, and the chiropteran fauna at EBSL remains partially undiscovered. It was demonstrated that species richness tends to stabilize, for the Phyllostomidae at the Atlantic Forest, around 1 000 captures (Bergallo et al. 2003). We had 194 phyllostomid captures in our sampling, so these results are expected.

We recorded a few noteworthy species in this study. Gleaning animalivores feed mainly on animals, though a few species ingest more fruit and pollen than animals, such as Phyllostomus hastatus and Phyllostomus discolor (Giannini and Kalko 2004). Members of this guild are found more often in forested rather than in deforested areas, and are considered suitable indicators of habitat disruption caused by deforestation (Fenton et al. 1992). We captured four species of gleaning animalivores – Micronycteris microtis, Mimon bennettii, Phyllostomus discolor, and Trachops cirrhosus – at EBSL, each represented by a single individual, with a fifth (Micronycteris minuta) known to occur by voucher specimens. This can be explained by the relatively low sampling size of our collection, but it may also reflect an impact at EBSL. In fact, it has vegetation of late stages of ecological succession, with signs of anthropic disturbance in areas of old agriculture activity (Mendes and Padovan 2000).

We captured a single Lonchophylla peracchii specimen, already known to occur in the Espírito Santo state (Pimenta et al. 2010). Until recently, this species was lumped with Lonchophylla bokermanni, but a morphological analysis revealed the existence of two species, with Atlantic Forest populations reassigned to Lonchophylla peracchii (Dias et al. 2013, Cláudio et al. 2018). This is the one of the Atlantic Forest endemic bat species, among Eptesicus taddeii, Histiotus alienus, Lasiurus ebenus and Myotis levis (Delgado-Jaramillo et al. 2020). While Lonchophylla peracchii is classified as Least Concern by the IUCN (Solari 2017), it is considered as Data Deficient in the last assessment of the state of Espírito Santo fauna (Costa et al. 2019). Another species with that classification registered in the present study is Micronycteris microtis. Furthermore, Myotis ruber is listed as a Near Threatened by the IUCN (Solari 2019).

Conclusion

Our research describes an assemblage of bats within the Atlantic Forest of Espírito Santo, southeast Brazil, in one of the oldest Brazilian conservation areas. Despite the dominance by common frugivorous species, the EBSL has a medium to high diversity, and we expect that further inventories will find more species.

Acknowledgements

The authors have declared that no competing interests exist. The authors are grateful to “Seu” Molino for the hospitality at EBSL; to all colleagues for help during field and laboratory work. CTMS is grateful to CAPES for the undergraduate PIIC scholarship. Marlon Zortéa, Roberto Leonan Novaes, Daniella Bôlla and an anonymous reviewer made valuable suggestions that greatly improved the manuscript.

References

  • Azevedo C, Corrêa M, Gobbi F, Kawada R, Lanes G, Moreira A, Redighieri E, Santos L, Waichert C (2003) Perfil das famílias de vespas parasitóides (Hymenoptera) em uma área de Mata Atlântica da Estação Biológica de Santa Lúcia, Santa Teresa, ES, Brasil. Boletim do Museu de Biologia Mello Leitão 16: 39–46. http://inma.gov.br/downloads/boletim/arquivos/16/Azevedo_ET_AL.pdf
  • Barbosa LS, Cunha AM, Couri MS, Maia VC (2014) Muscidae, Sarcophagidae, Calliphoridae e Mesembrinellidae (Diptera) da Estação Biológica de Santa Lúcia (Santa Teresa, Espírito Santo, Brasil). Boletim do Museu de Biologia Mello Leitão 33: 131–140. http://inma.gov.br/downloads/boletim/arquivos/33/33_06.pdf
  • Bergallo HG, Esbérard CEL, Mello MAR, Lins V, Mangolin R, Melo GGS, Baptista M (2003) Bat species richness in Atlantic Forest: What is the minimum sampling effort? Biotropica 35: 278–288. https://doi.org/10.1646/02033
  • Carvalho F, Fabián ME, Menegheti JO (2013) Vertical structure of an assemblage of bats (Mammalia: Chiroptera) in a fragment of Atlantic Forest in Southern Brazil. Zoologia 30(5): 491–498. https://doi.org/10.1590/S1984-46702013000500004
  • Chase JM, Knight TM (2013) Scale-dependent effect sizes of Ecological drivers on biodiversity: Why standardized sampling is not enough. Ecology Letters 16: 17–26. https://doi.org/10.1111/ele.12112
  • Cláudio VC, Silveira GC, Farias SG, Maas AS, Oliveira MB, Lapenta MJ, Martín RA, Dias D, Moratelli R (2018) First record of Lonchophylla bokermanni (Chiroptera, Phyllostomidae) for the Caatinga Biome. Mastozoología Neotropical 25(1): 43–51. https://doi.org/10.31687/saremMN.18.25.1.0.05
  • Costa LP, Bergallo HG, Caldara V Jr, Evaldt BHC, Fagundes V, Geise L, Kierulff CM, Leite YLR, Mayorga LFSP, Mendes SL, Moreira DO, Paglia AP, Passamani M, Secco HQC, Srbek-Araujo AC, Paresque R, Siciliano S, Sousa-Lima RS, Tavares VC, Zanin M, Zortéa M (2019) Mamíferos ameaçados de extinção no estado no Espírito Santo. In: Fraga CN, Formigoni MH, Chaves FG (Eds) Fauna e flora ameaçadas de extinção no estado do Espírito Santo. Instituto Nacional da Mata Atlântica, Santa Teresa, 314–341.
  • Delgado-Jaramillo M, Aguiar LMS, Machado RB, Bernard E (2020) Assessing the distribution of a species-rich group in a continental-sized megadiverse country: Bats in Brazil. Diversity & Distributions 26(5): 632–643. https://doi.org/10.1111/ddi.13043
  • Dias D, Esbérard CEL, Moratelli R (2013) A new species of Lonchophylla (Chiroptera, Phyllostomidae) from the Atlantic Forest of southeastern Brazil, with comments on L. bokermanni. Zootaxa 3722(3): 347–360. https://doi.org/10.11646/zootaxa.3722.3.4
  • Díaz MM, Solari S, Aguirre LF, Aguiar LMS, Barquez RM (2016) Clave de identificación de los murciélagos de Sudamérica. Publicación Especial N° 2, PCMA (Programa de Conservación de los Murciélagos de Argentina), 160 pp.
  • Fenton MB, Acharya L, Audet D, Hickey MBC, Merriman C, Obrist MK, Syme DM, Adkins B (1992) Phyllostomid bats (Chiroptera: Phyllostomidae) as indicators of habitat disruption in the Neotropics. Biotropica 24(3): 440–446. https://doi.org/10.2307/2388615
  • Fleming TH (1986) The structure of Neotropical bat communities: A preliminary analysis. Revista Chilena de Historia Natural 59: 135–150.
  • Garbino GST, Gregorin R, Lima IP, Loureiro L, Moras LM, Moratelli R, Nogueira MR, Pavan AC, Tavares VC, Peracchi AL (2020) Updated Checklist of Brazilian bats: versão 2020. Comitê da Lista de Morcegos do Brasil – CMLB. Sociedade Brasileira para o Estudo de Quirópteros (Sbeq). https://www.sbeq.net/lista-de-especies
  • Goldenberg R, Reginato M (2006) Sinopse da família Melastomataceae na Estação Biológica de Santa Lúcia, Santa Teresa, Espírito Santo. Boletim do Museu de Biologia Mello Leitão 20: 33–58.
  • Gregorin R, Bernard E, Lobão KW, Oliveira LF, Machado FS, Gil BB, Tavares VC (2017) Vertical stratification in bat assemblages of the Atlantic Forest of south-eastern Brazil. Journal of Tropical Ecology 33(5): 299–308. https://doi.org/10.1017/S026646741700027X
  • Hintze F, Arias-Aguilar A, Dias-Silva L, Delgado-Jaramillo M, Silva CR, Jucá T, Mischiatti FL, Almeida M, Bezerra B, Aguiar LMS, Pereira MJR, Bernard E (2020) Molossid unlimited: Extraordinary extension of range and unusual vocalization patterns of the bat, Promops centralis. Journal of Mammalogy 101(2): 417–432. https://doi.org/10.1093/jmammal/gyz167
  • Kollmann LJC (2006) Begoniaceae da Estação Biológica de Santa Lúcia, município de Santa Teresa, estado do Espírito Santo, Brasil. Boletim do Museu de Biologia Mello Leitão 20: 7–25.
  • Laurindo RDS, Bonilha LM, Ratz SVS, Novaes RLM (2016) Estrutura de comunidade de morcegos em remanescentes de Mata Atlântica ripária do Rio Pardo, Sudeste do Brasil. Boletim da Sociedade Brasileira de Mastozoologia 77: 97–104.
  • Lima JL (1926) Os morcegos da colecção do Museu Paulista. Revista do Museu Paulista 14: 43–127.
  • Lima IP, Nogueira MR, Monteiro LR, Peracchi AL (2016) Frugivoria e dispersão de sementes por morcegos na Reserva Natural Vale, sudeste do Brasil. In: Rolim SG, Menezes LFT, Sberk-Araujo AC (Eds) Floresta Atlântica de Tabuleiro: diversidade e endemismo na Reserva Natural Vale. Editora Rupestre, Belo Horizonte, 433–452.
  • Marques JT, Pereira MJR, Palmeirim JM (2016) Patterns in the use of rainforest vertical space by Neotropical aerial insectivore bats: All the action is up in the canopy. Ecography 39(5): 476–486. https://doi.org/10.1111/ecog.01453
  • Mendes PL, Vieira TB, Oprea M, Pimenta VT, Ditchfield AD (2014) Diferentes métodos de regeneração florestal podem interferir na comunidade local de morcegos? Mastozoología Neotropical 21(2): 231–240.
  • Mendes PL, Vieira TB, Oprea M, Lopes SR, Ditchfield AD, Zortéa M (2010) O conhecimento sobre morcegos (Chiroptera: Mammalia) do Estado do Espírito Santo, sudeste do Brasil. Papéis Avulsos de Zoologia 50(22): 363–373. https://doi.org/10.1590/S0031-10492010002200001
  • Novaes RLM, Souza RF, Felix S, Siqueira AC, Laurindo RS, Menezes LF, Shapiro JT (2017) Seasonality and habitat influence on bat assemblage structure in an urban Atlantic Forest remnant from Southeastern Brazil. Mammalia 81(3): 265–274. https://doi.org/10.1515/mammalia-2015-0115
  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PT, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2019) vegan: Community ecology package. R package version 2.5-4. https://CRAN.R-project.prg/package=vegan
  • Oprea M, Mendes P, Vieira TB, Pimenta VT, Brito D, Ditchfield AD (2007) Mammalia, Chiroptera, Phyllostomidae, Phyllostomus hastatus and Pygoderma bilabiatum: First occurrence in the Brazilian coastal shrubland ecosystem. Check List 3(3): 175–179. https://doi.org/10.15560/3.3.175
  • Parolin LC, Bianconi GV, Mikich SB (2016) Consistency in fruit preferences across the geographical range of the frugivorous bats Artibeus, Carollia and Sturnira (Chiroptera). Iheringia. Série Zoologia 106(0): e2016010. https://doi.org/10.1590/1678-4766e2016010
  • Passamani M (2000) Análise da comunidade de marsupiais em Mata Atlântica de Santa Teresa, Espírito Santo. Boletim do Museu de Biologia Mello Leitão 11: 215–228. http://boletim.sambio.org.br/pdf/11_13.pdf
  • Peracchi AL, Albuquerque ST (1993) Quirópteros do município de Linhares, Estado do Espírito Santo, Brasil (Mammalia, Chiroptera). Revista Brasileira de Biologia 53: 575–581.
  • Peracchi AL, Nogueira MR, Lima IP (2011) Novos achegos à lista dos quirópteros do município de Linhares, estado do Espírito Santo, sudeste do Brasil (Mammalia, Chiroptera). Chiroptera Neotropical 17: 842–852.
  • Pimenta VT, Machel CT, Ditchfield AD (2010) First occurrence of Lonchophylla bokermanni Sazima, Vizotto & Taddei, 1978 (Phyllostomidae) in Espírito Santo State, Southeastern Brazil. Chiroptera Neotropical 16: 740–742.
  • Portfors CV, Fenton MB, Aguiar LMS, Baumgarten JE, Vonhof MJ, Bouchard S, Faria DM, Pedro WA, Rauntenbach NIL, Zortéa M (2000) Bats from Fazenda Intervales, Southeastern Brazil: Species account and comparison between different sampling methods. Revista Brasileira de Zoologia 17(2): 533–538. https://doi.org/10.1590/S0101-81752000000200022
  • R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
  • Redondo RAF, Brina LPS, Silva RF, Ditchfield AD, Santos FR (2008) Molecular systematics of the genus Artibeus (Chiroptera: Phyllostomidae). Molecular Phylogenetics and Evolution 49(1): 44–58. https://doi.org/10.1016/j.ympev.2008.07.001
  • Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM (2009) The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation 142(6): 1141–1153. https://doi.org/10.1016/j.biocon.2009.02.021
  • Rocha L (1971) Viajantes Estrangeiros no Espírito Santo. Ebrasa, Brasília, 190 pp.
  • Ruschi A (1951) Morcegos do estado do Espírito Santo – Introdução e considerações gerais. Boletim do Museu de Biologia Mello Leitão 1: 1–16.
  • Ruschi A (1977) A ornitofauna da estação biológica do Museu Nacional. Boletim do Museu de Biologia Mello Leitão 88: 1–10.
  • Ruschi A (1978) Morcegos das reservas biológicas do E.E. Santo e algumas observações novas – considerações sobre algumas descobertas publicadas em 1952-53. Boletim do Museu de Biologia Mello Leitão 91: 1–6.
  • Ruschi-Filho A (1972) O conservacionismo no Estado do Espírito Santo. Boletim do Museu de Biologia Mello Leitão 40: 1–21.
  • Saiter FZ, Thomaz LD (2014) Revisão da lista de espécies arbóreas do inventário de Thomaz & Monteiro (1997) na Estação Biológica de Santa Lúcia: o mais importante estudo fitossociológico em florestas montanas do Espírito Santo. Boletim do Museu de Biologia Mello Leitão 34: 101–128. http://antigo.inma.gov.br/downloads/boletim/arquivos/34/34_06.pdf
  • Sampaio EM, Kalko EKV, Bernard E, Rodríguez-Herrera B, Handley CO (2003) A biodiversity assessment of bats (Chiroptera) in a tropical lowland rainforest of Central Amazonia, including methodological and conservation considerations. Studies on Neotropical Fauna and Environment 38: 17–31. https://doi.org/10.1076/snfe.38.1.17.14035
  • Scabello M, Oliveira LF, Cipriano RS, Carvalho RC, Ditchfield AD, Gregorin R, Martins RL (2009) Mammalia, Chiroptera, Phyllostomidae, Chiroderma doriae: First record for the state of Espírito Santo, Brazil, and distribution map. Check List 5(3): 539–541. https://doi.org/10.15560/5.3.539
  • Schinz HR (1821) Das Thierreich eingetheilt nach dem Bau der Thiere als Grandlage ihrer Naturgeschichte und der vergleichenden Anatomie von dem Herrn Ritter von Cuvier. Erster Band. Säugethiere und Vögel. J.G. Cotta`schen Buchhandlung, Stuttgart und Tübingen, 894 pp.
  • speciesLink (2020) Rede de dados speciesLink.
  • Srbek-Araujo AC, Chiarello AG (2008) Domestic dogs in Atlantic forest preserves of south-eastern Brazil: A camera-trapping study on patterns of entrance and site occupancy rates. Brazilian Journal of Biology 68(4): 771–779. https://doi.org/10.1590/S1519-69842008000400011
  • Straube FC, 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.
  • Thomaz LD, Monteiro R (1997) Composição florística da mata atlântica de encosta da Estação Biológica de Santa Lúcia, município de Santa Teresa-ES. Boletim do Museu de Biologia Mello Leitão 7: 3–48. http://boletim.sambio.org.br/pdf/07_01.pdf
  • Vela-Ulian CM, Hoppe JPM, Ditchfield AD (in press) New records of bats (Mammalia: Chiroptera) in the Atlantic Forest of Espírito Santo, southeastern Brazil. Mammalia. https://doi.org/10.1515/mammalia-2019-0109
  • Velazco PM, Patterson BD (2008) Phylogenetics and biogeography of the broad-nosed bats, genus Platyrrhinus (Chiroptera: Phyllostomidae). Molecular Phylogenetics and Evolution 49(3): 749–759. https://doi.org/10.1016/j.ympev.2008.09.015
  • Veloso HP, Goés-Filho L (1982) Classificação Fisionômico-Ecológica da Vegetação Neotropical. Boletim Técnico Projeto Radambrasil, Salvador, 85 pp.
  • Vieira CC (1942) Ensaio monográfico sobre os quirópteros do Brasil. Arquivos de Zoologia 3: 219–471.
  • Vieira TB, Mendes P, Coutinho RZ, Oprea M, Ditchfield AD (2008) New records for three species of the genus Myotis Kaup for the state of Espírito Santo, southeastern Brazil. Chiroptera Neotropical 14: 415–418.
  • Wied-Neuwied MP (1826) Beiträge zur Naturgeschichte von Brasilien. Verzeichniss der Amphibien, Säugethiere und Vögel, welche auf einer Reise dem 13ten und dem 23sten Grade südlicher Breite im östlichen Brasilien beobachtet wurden. II Band. II. Abtheilung. Mammalia. Säugethiere. Gr. H. S. priv. Landes-Industrie-Comptoirs, Weimar, 622 pp. https://doi.org/10.5962/bhl.title.48512
  • Woodman N, Timm RM (2006) Characters and phylogenetic relationships of nectar-feeding bats, with descriptions of new Lonchophylla from western South America (Mammalia: Chiroptera: Phyllostomidae: Lonchophyllini). Proceedings of the Biological Society of Washington 119(4): 437–476. https://doi.org/10.2988/0006-324X(2006)119[437:CAPRON]2.0.CO;2

Appendix 1

Vouchers deposited at the Mammalian Collection of Universidade Federal do Espírito Santo (UFES-MAM), Brazil.

Anoura caudifer: 3964, 3965, 3966. Anoura geoffroyi: 3260, 3261, 3262, 3263, 3264, 3265. Artibeus fimbriatus: 3827. Artibeus lituratus: 4376, 4379, 4532. Artibeus obscurus: 4377, 4378, 4380. Carollia perspicillata: 3716, 3717, 3718, 3719, 3720, 3721, 3722, 3723, 3724, 3725, 3726, 3727, 3730. Dermanura cinerea: 4150, 4248, 4381. Desmodus rotundus: 4287. Lonchophylla peracchii: 3225. Micronycteris microtis: 3943. Mimon bennettii: 3178. Phyllostomus hastatus: 3525. Platyrrhinus recifinus: 4311. Rhinophylla pumilio: 4087, 4088, 4089, 4090, 4091, 4092, 4093. Sturnira lilium: 3547. Sturnira tildae: 4206, 4207. Trachops cirrhosus: 3776. Vampyressa pusilla: 4210, 4211. Eptesicus brasiliensis: 3269. Myotis riparius: 4239, 4240, 4241, 4242, 4243. Myotis ruber: 4041.

Supplementary material

Supplementary material 1 

Table S1. Locality, species richness, and calculated Shannon, Pielou and PIE diversity indexes from 119 bat species inventories at the Atlantic Forest, southeastern Brazil

João Paulo Maires Hoppe, Maria Lavanholle Ventorin, Bruna Malavazi Dell’ Antonio, Carlos Tiago Machel da Silva, Albert David Ditchfield

Data type: species data

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Download file (84.50 kb)