Research Article |
Corresponding author: João Paulo Maires Hoppe ( jpmhoppe@gmail.com ) Academic editor: Ana Maria Leal-Zanchet
© 2020 João Paulo Maires Hoppe, Maria Lavanholle Ventorin, Bruna Malavazi Dell’ Antonio, Carlos Tiago Machel da Silva, Albert David Ditchfield.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Hoppe JPM, Ventorin ML, Dell’ Antonio BM, da Silva CTM, Ditchfield AD (2020) Bat assemblage at a high diversity locality in the Atlantic Forest. Neotropical Biology and Conservation 15(4): 487-501. https://doi.org/10.3897/neotropical.15.e55986
|
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.
Augusto Ruschi, Chiroptera, fragment, southeastern Brazil, species richness
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 (
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 (
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 (
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 (
A number of studies have been conducted at EBSL, including entomological (
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.
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.
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.
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
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 |
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
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
We captured a total of 204 individuals, from 22 species of two families, Phyllostomidae and Vespertilionidae (Table
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.
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
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
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 |
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.,
Frugivores were the most abundant trophic guild in our sample (Table
The species accumulation curve did not reach an asymptote (Fig.
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 (
We captured a single Lonchophylla peracchii specimen, already known to occur in the Espírito Santo state (
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.
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.
Vouchers deposited at the Mammalian Collection of Universidade Federal do Espírito Santo (
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.
Table S1. Locality, species richness, and calculated Shannon, Pielou and PIE diversity indexes from 119 bat species inventories at the Atlantic Forest, southeastern Brazil
Data type: species data