Research Article |
Corresponding author: Rair Sousa Verde ( rair.verde@gmail.com ) Academic editor: Ana Maria Leal-Zanchet
© 2020 Richarlly Costa Silva, Marcos Silveira, Rair Sousa Verde.
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:
Silva RC, Silveira M, Verde RS (2020) Vertical stratification of phyllostomid bats assemblage (Chiroptera, Phyllostomidae) in a forest fragment in Brazilian Southwestern Amazon. Neotropical Biology and Conservation 15(2): 107-120. https://doi.org/10.3897/neotropical.15.e47641
|
Bats represent a key group in tropical forest dynamics, given their participation in ecological interactions that lead the regulation of these forests. They are also sensitive to the heterogeneous vertical gradient in the forest, called stratification. In this study we evaluated the influence of two different forest strata on species composition and bat guild structure. The samplings were carried out over eight nights in a forest fragment located in the southwest of the Amazon; we used mist nets installed in the understory and sub-canopy. A total of 197 captures were distributed in 19 genera and 25 species; they were all representatives of the family Phyllostomidae. In the sub-canopy, 54 individuals and 15 species were captured, with four exclusive species. In the understory, 143 individuals of 21 species were recorded, of which 10 were exclusive of this stratum. The sub-canopy presented a diversity index greater than the understory, with differences between species composition of the two assemblies, due to the presence or absence of some species. We also found a variation in the presence of frugivorous, insectivorous and omnivorous species, which is the result of differences in the foraging methods of these species and also of the habitat preference. Differences were verified in the assemblies studied, demonstrating the effects of vertical stratification on the bats in the studied fragment. Studies that consider more than one vertical stratum in tropical forests are more representative than sampling with only understory mist nets, given the capture of exclusive species.
Chiroptera, diversity, feeding guilds, habitat use, species composition
Bats are one of the most diverse groups of animals in the world, with 18 families, 202 genera and more than 1,300 species and, except for Antarctica, they are found on all continents (
Spatial heterogeneity is an important factor promoting the diversity of animals and plants, especially in tropical forests (
In Central Amazon,
The study was conducted at the Catuaba Experimental Farm, Senador Guiomard, Acre, Brazil, a forest remnant of 1,166 ha (10°04'53"S, 67°37'19"W) located near the intersection of the BR-364 and BR-317 highways, 23 km from the capital, Rio Branco (Fig.
Although the study area is located in an area dominated by Dense Ombrophylous Forest, the vegetation cover of the area is characterized by the predominance of Open Ombrophylous Forest with Bamboo and Open Ombrophylous Forest with Palm, and its surroundings by secondary forests in different successional stages and pastures (
This study used as sample units four plots of uniform distribution of the RAPELD system (
Between May 2014 and January 2015, each plot was sampled twice, one between May and September and one between October and January, and for that purpose, mist nets (12 × 3m, 19mm mesh, Ecotone), eight at ground level for understory sampling and two at sub-canopy sampling. The last two were installed according to
Bats captured under SISBIO license N° 44089-1 were placed in individual cotton bags for weighing, checking of body measurements and identification, remaining in them until the nets closed, thus avoiding the capture of the same individual at the same night or in more than one stratum.
In the field, bats were identified based on the keys proposed by
According to
In order to compare the abundance and number of species among the strata, a rarefaction curve was constructed and, since the sampling effort in the strata was distinct, for any comparisons we used the relative abundance of the species, calculated from the number division of species records by the sampling effort of the treatment. Assembly ordering was performed by using the non-metric multidimensional scaling (NMDS), using the Bray-Curtis distance and the minimum stress value of 0.20, as the stress values above 0.20 mean that the ordering performed is not sufficiently explanatory. In addition to the NMDS, in order to test the patterns of the community structure, a non-parametric permutational multivariate (PERMANOVA) analysis was performed, with 9999 permutations. All analyzes were performed with the “vegan” package of the R 3.0.3 software (
With a total effort of 8,640 m2.h for the sub-canopy nets and 13,824 m2.h for understory nets, 197 captures were taken from at least 25 species distributed in 19 genera. In the sub-canopy, 54 captures were taken from at least 15 species and 143 captures from at least 21 species were recorded in the understory (Table
List of bat species captured in the study area (Fazenda Experimental Catuaba), Senador Guiomard, Acre, Brazil. Values represent the number of captures and capture rate in each strata and total captures.
Taxon | Sub-canopy | Understory | Total captures (%) |
---|---|---|---|
Carolliinae | |||
Carollia spp. | 26 (0.752) | 93 (0.673) | 119 (60.40) |
Desmodontinae | |||
Desmodus rotundus (E. Geoffroy, 1810) | 2 (0.057) | 1 (0.007) | 3 (1.52) |
Gardnerycterinae | |||
Gardnerycteris crenulatum (E. Geoffroy, 1810) | 2 (0.057) | 1 (0.007) | 3 (1.52) |
Glossophaginae | |||
Glossophaga soricina (Pallas, 1766) | 1 (0.028) | 4 (0.029) | 5 (2.54) |
Glyphonycterinae | |||
Glyphonycteris sylvestris (Thomas, 1896) | – | 2 (0.014) | 2 (1.02) |
Micronycterinae | |||
Lampronycteris brachyotis (Dobson, 1879) | 1 (0.028) | 4 (0.029) | 5 (2.54) |
Micronycteris hirsuta (Peters, 1869) | – | 3 (0.022) | 3 (1.52) |
Phyllostominae | |||
Lophostoma brasiliense (Peters, 1866) | – | 1 (0.007) | 1 (0.51) |
Lophostoma silvicolum (d’Orbigny, 1836) | 1 (0.028) | 5 (0.036) | 6 (3.05) |
Phyllostomus elongatus (E. Geoffroy, 1810) | 2 (0.057) | 3 (0.022) | 5 (2.54) |
Phyllostomus hastatus (Pallas, 1767) | 5 (0.144) | 1 (0.007) | 6 (3.05) |
Tonatia saurophila Koopman &Williams, 1951 | 3 (0.035) | 3 (0.022) | 6 (3.05) |
Trachops cirrhosus (Spix, 1823) | – | 2 (0.014) | 2 (1.02) |
Stenodermatinae | |||
Artibeus lituratus (Olfers, 1818) | 1 (0.028) | 4 (0.029) | 5 (2.54) |
Artibeus obscurus Schinz, 1821 | 1 (0.028) | – | 1 (0.51) |
Artibeus planirostris (Spix, 1823) | 2 (0.057) | 4 (0.029) | 6 (3.05) |
Dermanura cinerea Gervais, 1856 | – | 2 (0.014) | 2 (1.02) |
Dermanura cf. glauca Thomas, 1893 | 5 (0.144) | – | 5 (2.54) |
Mesophylla macconnelli Thomas, 1901 | – | 2 (0.014) | 2 (1.01) |
Platyrrhinus brachycephalus (Rouk & Carter, 1972) | 1 (0.028) | – | 1 (0.51) |
Sturnira lilium (E. Geoffroy, 1810) | – | 1 (0.007) | 1 (0.51) |
Sturnira tildae de la Torre, 1959 | – | 4 (0.029) | 4 (2.03) |
Uroderma bilobatum Peters, 1866 | 1 (0.028) | – | 1 (0.51) |
Vampyressa thyone Thomas, 1909 | – | 1 (0.007) | 1 (0.51) |
Vampyriscus bidens Dobson, 1878 | – | 2 (0.014) | 2 (1.02) |
Number of captures | 54 (0.015) | 143 (0.010) | 197 |
Richness | 15 | 21 | 25 |
Exclusive species | 4 | 10 | – |
Effort (m2h) | 3456 | 13824 | 22464 |
The rarefaction curve by individuals showed that the richness of bats at the point of intersection of 54 individuals was of 15 species for the sub-canopy and 14 species in the understory (Fig.
Individuals-based species accumulation curves for captures in in the study area. The gray line represent captures in sub-canopy and the black line represent captures in understory strata, dashed lines represent 95% CI. The vertical dashed line highlights the intersection point of 54 individuals.
The most abundant taxa were Carollia spp. with 119 records, representing 60.40% of total catches, with a greater abundance in the understory (78%) than in the sub-canopy (22%). Artibeus planirostris (Spix, 1823), Phyllostomus hastatus (Pallas, 1767), Tonatia saurophila Koopman & Williams, 1951 and Lophostoma silvicolum d’Orbigny, 1836, with six records each, representing 12.20% of the captures; 16 species had less than six catches and five were caught only once (Table
Fifteen species were captured in the sub-canopy, among them, Artibeus obscurus, Dermanura cf. glauca, Platyrrhinus brachycephalus and Uroderma bilobatum were exclusive and represent 37.5% of the richness of this stratum. Among the 21 species found in the understory, 10 (47.6% of the species) were exclusive: Dermanura cinerea, Glyphonycteris sylvestris, Lophostoma brasiliense, Mesophylla macconnelli, Micronycteris hirsuta, Sturnira lilium, Sturnira tildae, Trachops cirrhosus, Vampyressa thyone and Vampyriscus bidens.
The assembly ordering in two dimensions (stress = 0.07) revealed a clear separation between understory and sub-canopy (Fig.
Our results indicate that species composition are different between understory and sub-canopy, indicating differences on forage pattern and vertical stratification; ten species were exclusive in understory and four were captured only in sub-canopy. Most of the studies involving bats and vertical stratification carried out in Amazon compare understory and canopy (
All categories of guilds proposed by
In studies carried out in central Amazon,
Species of the genus Artibeus, considered as canopy frugivorous, are more captured in the canopy than in the understory, mainly because they feed on fruits that are common in the canopy (ex. Ficus), using the understory during periods of drought to compensate for the low availability of fruits in the higher strata (
Members of the genus Sturnira, here represented by S. lilium and S. tildae, are classified as understory specialists (
Bats from the genus Carollia have high capture rates in studies conducted in the Amazon (see
The preliminary results reported here demonstrate that the vertical structure of the forest functions as an environmental filter, regulating the species richness of bats in the southwest of the Amazon, given the exclusivity of some species to the forest strata. Therefore, more studies that contemplate several vertical strata should be performed, since they allow the capture of species that are not frequently captured in the understory, allowing to generate more precise conclusions on the environmental factors that are being approached.
Even though our effort may not be enough to answer questions about vertical stratification for all species, we suggest that the main limitation in relation to our results is the uneven sampling effort between the platforms and the need for a longer sampling period to be able to record a relatively considerable number of unusual species. On the other hand, this is the first attempt to test the vertical stratification of bat assemblies in the far west of the Brazilian Amazon; in addition, we find evidence of vertical stratification patterns that are similar to those found in other studies in the Amazon (see
We thank Programa de Pesquisa em Biodiversidade (PPBio), PPBio Núcleo regional Acre and Fundação de Amparo à Pesquisa do Estado do Acre (FAPAC) for the financial support, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Programa de Pós Graduação em Ecologia e Manejo de Recursos Naturais (PPG-EMRN), for the logistic support. We also thank Robson, Aline Reis, Cyntia Nascimento, Luciano Nascimento, Luiz Borges, Marcos Lima, Salatiel Clemente, Sérgio Oliveira and Thais Braga for support in field activities and André Botelho, Luiz Borges and several reviewers who improved the manuscript.