Bat fauna in an ore extraction area in Central Brazil

Daiany Folador Sotero1

https://orcid.org/0000-0002-5549-818X

Daniela de Melo e Silva1

https://orcid.org/0000-0003-0362-0988

Arthur Angelo Bispo de Oliveira1

https://orcid.org/0000-0002-3375-1471

Marcelino Benvindo-Souza1*

https://orcid.org/0000-0001-9008-6087

* Contato principal

1 Universidade Federal de Goiás/UFG, Goiânia/GO, Brasil. <daianyfolador@gmail.com, danielamelosilva@ufg.br, tucobispo@gmail.com, marcelinobenvindo@gmail.com>.

Recebido em 10/03/2024 – Aceito em 01/11/2024

ABSTRACT – Opencast mining often causes considerable changes to the landscape, including habitat fragmentation and impact on bat activities. The present study aimed to survey the composition of bats in an open pit-mining region in Barro Alto, Goiás. During 20 days of sampling in the rainy season between October (2021) and February (2022), 174 bats of 15 species were sampled. All animals belonged to the Phyllostomidae family of seven subfamilies and 13 genera. Carollia perspicillata was the dominant species corresponding to 70.69% of captures. The captured animals had a variety of eating habits, categorized as nectarivore, hematophagous, frugivore, insectivore, and omnivore. According to the national and international lists, none of the species are endangered. Finally, new research is encouraged to leverage knowledge of the bats diversity in the region and relate it to the impacts of mining.

Keywords: Chiroptera; inventory; ferronickel; conservation.

Fauna de morcegos em área de extração de minério no Brasil Central

RESUMO – A mineração a céu aberto geralmente provoca mudanças consideráveis na paisagem, incluindo a fragmentação de habitat e impacto nas atividades dos morcegos. O presente estudo teve como objetivo levantar a composição de morcegos em uma região de mineração a céu aberto no município de Barro Alto, Goiás. Durante 20 dias de amostragens no período chuvoso entre o final de outubro (2021) e fevereiro (2022) foram amostrados 174 morcegos de 15 espécies. Todos os animais pertenciam à família Phyllostomidae de sete subfamílias e 13 gêneros. Carollia perspicillata foi a espécie dominante correspondendo 70,69% das capturas. Os animais capturados possuíam uma variedade de hábitos alimentares categorizados como nectarívoro, hematófago, frugívoro, insetívoro e onívoro. Nenhuma das espécies encontra-se ameaçada de extinção, conforme as listas nacional e internacional. Finalmente, novas pesquisas na área são encorajadas para alavancar o conhecimento da diversidade de morcegos na região e, sobretudo relacionar com os impactos da mineração.

Palavras-chave: Chiroptera; inventário; ferroníquel; conservação.

Fauna de murciélagos en un área de extracción de minerales en el centro de Brasil

RESUMEN – La minería a cielo abierto a menudo provoca grandes cambios en el paisaje, incluida la fragmentación del hábitat y el impacto en las actividades de los murciélagos. El presente estudio tuvo como objetivo relevar la composición de los murciélagos en una región minera a cielo abierto en el municipio de Barro Alto, Goiás. Durante 20 días de muestreo en época de lluvias entre finales de octubre (2021) y febrero (2022) se muestrearon 174 murciélagos de 15 especies. Todos los animales pertenecían a la familia Phyllostomidae de siete subfamilias y 13 géneros. Carollia perspicillata fue la especie dominante correspondiendo al 70,69% de las capturas. Los animales capturados tenían una variedad de hábitos alimenticios categorizados como nectarívoros, hematófagos, frugívoros, insectívoros y omnívoros. Ninguna de las especies encontradas amenazadas según la lista nacional e internacional. Finalmente, se impulsan nuevas investigaciones en el área para aprovechar el conocimiento de la diversidad de murciélagos de la región y, sobre todo, relacionarlo con los efectos del proyecto.

Palabras clave: Quirópteros; inventario; ferroníquel; conservación.

Como citar:

Sotero DF, Silva DM, Oliveira AAB, Benvindo-Souza M. Bat fauna in an ore extraction area in Central Brazil. Biodivers. Bras. [Internet]. 2024; 14(4): 1-9. doi: 10.37002/biodiversidadebrasileira.v14i4.2385

Introduction

The order Chiroptera comprises 1474 species of bats [1], 22% of the world’s mammals. These animals are the second most diverse group of mammals on the planet, surpassed only by rodents. In Brazil, the country with the world’s second-highest diversity of bats, 186 species of 68 genera and nine families are recognized [2][3]. For the Cerrado, 118 species are listed [4]; that is, 65% of the bat richness in the country is found in this biome. Linked to their diversity, the bats have varied eating habits, one of the mechanisms that allow them to survive in different places [5][6]. These animals feed on insects, and others consume fruits and nectar, but there are also carnivorous bats that feed on fish and small crustaceans such as scorpions and the well-known vampire bats that feed on blood [7].

However, bats are under several pressures around the world. Among the main ones are fungi that cause white-nose syndrome [8], wind turbines [9], habitat loss [10], climate change [11], run over on roads [12], and contamination by chemical agents [13][14]. Regarding chemical agents, mining areas are particularly noteworthy for their potential to harm biodiversity and impact human health. Although mining is economically significant, open-pit mining, in particular, causes sudden and extensive changes to the landscape, including habitat fragmentation and disruption of bat activities [15], this effect can then generate complications in their health, having effects on the sustainability of their populations and the survival of the species.

For example, liver metal bioaccumulation and DNA damage in insectivorous bats was observed in coal mining animals in the Santa Catarina Carboniferous Basin, southern Brazil [16]. Another study in the area of coal mining indicated that chronic exposure of bats to environments filled with ore dust particles causes histological and oxidative damage [17]. In a Ferronickel mining area in Goiás, the location of the present study, bats were observed with a high frequency of DNA damage [18][19]. Finally, iron mining pollution in fruit bats in the Atlantic Forest also showed greater hepatic accumulation of aluminum, calcium, iron, and barium; muscular accumulation of Ca and Fe, in addition, they detected oxidative stress in the brain, hepatic and renal oxidative damage associated with liver fibrosis and renal inflammation [20], indicating the susceptibility of these animals to pollutants generated by mining companies that can compromise its survival.

Although these works have highlighted the ecotoxicological impact, primary studies, such as fauna inventories in mining areas, remain scarce for open-pit mining. In contrast, the bat fauna in underground mining is well-documented in several regions around the world [21][22][23]. In this context, the present study aimed to survey the composition of bats in an open-pit mining region in Barro Alto, Goiás, to know the diversity of local animals. To our knowledge, this is the first study, at least in the state of Goiás, to inventory bats within a ferronickel mining area.

Material and Methods

Sampling

Bats were sampled in Barro Alto, Goiás, between October 2021 and February 2022, ten days in each period, Barro Alto, the city where the study was carried out, has had an industrial ferronickel production plant since 2011 [18]; being one of the main areas of metal extraction in the country. Ten mist nets were used in fragments of cerrado in the ore extraction area with points up to 100 meters from the excavation zones and peripheral regions, totaling ten sampling sites (Figure 1). The mist nets were open for the first four hours of activities [21][24], between 6:00pm and 10:00pm and inspected every 30 minutes, totaling 19,200m2h of nets. Each animal was packed in a cotton bag, sorted, and released in the same capture area. Biological samples were obtained from some species and have been published elsewhere [18]. The species identification criterion was used by Reis et al. [25] in addition to checking the list of bats in Goiás [26] and the list of the Sociedade Brasileira de Estudos de Chiroptera [2]. The project was licensed by the Chico Mendes Institute under number 75819-1 and by the Ethics Committee of the Federal University of Goias (nº 004/21).

Data analysis

The diversity index was conducted following Shannon-Wiener, and the Equitability index using the H/Hmax ratio. A richness estimation curve was constructed based on 1,000 randomizations, and the estimator used was the first-order Jackknife. Finally, the conservation status of all species was assessed according to the Brazilian list of endangered fauna from the Ministry of the Environment [27] and the IUCN international list [28].

Results and Discussion

The present study sampled 174 bats of 15 species in Barro Alto, Goiás. The study sampled 13% of bats from the Cerrado and 8% when considering the Brazilian territory. All captured animals belonged to the Phyllostomidae family, comprising seven subfamilies and 13 genera (Table 1). However, it is important to note that the mist net method favors the capture of the Phyllostomidae family [29]. Additionally, given that the sampling was conducted over 20 nights with 4 hours per night, these results are still preliminary for the study area.

The diversity index in the region was H’ = 1.294, and the uniformity of J = 0.478. The rarefaction curve did not tend to an asymptote, indicating four more species in the area (Figure 2). Although it did not occur in a mining area, a previous study on a farm in the municipality of Barro Alto, Zortéa and D’arc [30] sampled 116 bats from 14 species. The diversity (H’ = 1.657) and uniformity (J = 0.628) indices were higher in the study by Zortéa and D’arc [30]. In contrast to the present study, it’s likely that our high capture abundance, particularly for Carollia perspicillata, contributed to this difference, despite the presence of one additional species. In a study conducted in an iron and manganese mining area in Corumbá, Mato Grosso do Sul, 83 bats representing nine species were captured, all of which belonged to the Phyllostomidae family. This finding supports the notion that the mist net method tends to be more biased toward capturing species within this family.

Carollia perspicillata was the dominant species corresponding to 70.69% of the total number of captured animals, corroborating Zortéa and D’arc [30], followed by Glossophaga soricina with 6.32%. The significant representation in captures of G. soricina has also been evidenced in studies from Goiás [31][30]. This species is a generalist and opportunistic, and its capture is widespread [32][33][34][35]. In addition to these common species, it is worth highlighting those less captured in the present study, such as Artibeus planirostris, Platyrrhinus incarum, Lionycteris spurrelli, Tonatia maresi, and Micronycteris sp. Future studies in the same investigated areas may answer whether such species are rare in the respective locations, although seasonality affects the abundance and composition of species [36][37].

Bats were represented by five trophic guilds (Figure 3). Frugivores had the highest species richness (n = 7) and abundance (n = 142; 82%). The prominent representatives were from the subfamily Stenodermatinae and Carolliinae. Stenodermatinae are bats that generally have facial stripes, and some species have stripes on the back [25], which are evident or barely perceptible. In Brazil, there are 35 species [2]. Carolliinae, the species belonging to this subfamily, was C. perspecillata. For hematophagous, the typical vampire bat, Desmodus rotundus, was captured. However, in the state of Goiás, there is still the occurrence of the other two species of bats that feed on blood, Diaemus youngi and Diphylla ecaudata [26]. Desmodus rotundus is a species of interest for public and rural health in Tropical America because it is an essential transmitter of the rabies virus [38].

The omnivores were represented by the species Phyllostomus discolor. This species can be found in forest environments and altered by plantations and urban areas [25]. As for the nectarivorous species, Anoura caudifer, Glossophaga soricina, and Lionycteris spurrelli were captured. The insectivores were Lophostoma silvicola, Tonatia maresi, and Micronycteris sp., which corresponded to 5% of the total abundance. Bats with an insect-based diet suppress populations of pests in agricultural ecosystems [39], which generates income for farmers [40]. Therefore, in a state where the leading economy is based on agriculture, it is essential to consider these animals as partners in crops and natural pest controllers, which is highly beneficial to environmental health. Typical and exclusively insectivorous bat families such as Molossidae and Vespertilionidae were not sampled, although they are rarely sampled in the fog network. However, in the review by Hannibal et al. [26], the authors listed 12 species of Vespertilionidae and 14 of Molossidae for the state of Goiás.

Ultimately, in mining areas, the stressors on bats include noise pollution generated by machinery, which could impact the foraging behavior of certain species. Moreover, the presence of vehicles results in a notable decrease in bat activity near roads, largely attributable to elevated noise levels [41]. Theobald et al. [15] noted that distance from the mine is considered an essential predictor of bat species richness and activity levels, with the effect on richness extending to approximately 900 m from the site and the effect on activity potentially extending beyond the sampling area (1,200 m). In this study, some sampling points were conducted in forest remnants over 100 meters from the ore extraction area. For Lonchophylla dekeyseri an endemic species of the Brazilian Cerrado, deforestation and mining are acknowledged as significant threats [42]. Moreover, studies in the field of ecotoxicology have raised alarms regarding bat contamination by metals in mining areas on a global scale [16][43][20].

Conclusion

The richness and diversity of bats were evaluated in a mining company in Barro Alto, Goiás, in the Central Plateau, Brazil. The study surveyed 15 species of bats, which represents 17% of the total recorded in the state of Goiás. Considering that basic biology studies, such as inventories in Brazilian mining areas, are scarce. There is limited understanding of the bat composition in mining areas. We acknowledge that our study was not exhaustive in identifying all potential species in the area, and further research is warranted. Future studies in mining areas could explore bat composition across various sampling sites and compare them with reference (control) areas. Additionally, evaluating different stations would provide insights into the impact of mining activities on bat composition, thus enhancing our understanding of their ecological dynamics in these environments.

Acknowledgements

We thank the Coordination for Higher Education Personnel Training (CAPES), and Anglo American. D.M.S. thanks the National Council for Scientific and Technological Development (CNPq) for a scholarship.

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Figure 1 – Bat sampling region in Barro Alto, Goiás.

Table 1 – Bats sampled in Barro Alto Goiás in Central Brazil.

Táxons

Abundance

Guild

Status

Absolute

Relative

MMA

IUCN

Phyllostomidae

Glossophaginae

Anoura caudifer

2

1.15%

N

LC

Glossophaga soricina

11

6.32%

N

LC

Desmodontinae 

Desmodus rotundus

6

3.45%

H

LC

Stenodermatinae

Artibeus lituratus

5

2.87%

F

LC

Artibeus planirostris

1

0.57%

F

LC

Artibeus cinereus

2

1.15%

F

LC

Platyrrhinus lineatus

6

3.45%

F

LC

Platyrrhinus incarum

1

0.57%

F

LC

Sturnira lilium

4

2.30%

F

LC

Carolliinae

Carollia perspicillata

123

70.69%

F

LC

Lonchophyllinae

Lionycteris spurrelli

1

0.57%

N

LC

Phyllostominae 

Lophostoma silvicola

6

3.45%

I

LC

Tonatia maresi

1

0.57%

I

*

Phyllostomus discolor

4

2.30%

O

LC

Micronycterinae

Micronycteris sp.

1

0.57%

I

*

Abundância

174

Riqueza

 ١٥

 

Shannon H

1.294

Equitabilidade J

0.478

Trophic Guild: N) Nectarivore, H) Hematophage, F) Frugivore, I) Insectivore and O) Omnivore. LC) Least concern. No species at risk for MMA. * Not found. MMA) Ministry of the Environment, IUCN) International Union for Conservation of Nature and Natural Resources.

Figure 2 – Species accumulation curve. Dark blue line indicates the observed richness, while the light blue line is the expected richness (Jackknife 1). The test was performed with a 95% confidence interval for the association with the estimate.

Figure 3 – Bat trophic guild. Inner circle indicates the abundance and the peripheral circle species richness.

Biodiversidade Brasileira – BioBrasil.

Fluxo Contínuo e Edição Temática:

Ecologia do Fogo e Conservação do Bioma Pantanal

n.4, 2024

http://www.icmbio.gov.br/revistaeletronica/index.php/BioBR

Biodiversidade Brasileira é uma publicação eletrônica científica do Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) que tem como objetivo fomentar a discussão e a disseminação de experiências em conservação e manejo, com foco em unidades de conservação e espécies ameaçadas.

ISSN: 2236-2886