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Seasonal Variations in Cave Invertebrate Communities in the Semiarid Caatinga, Brazil

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Seasonal Variations in Cave Invertebrate Communities in the Semiarid Caatinga, Brazil D. de M. Bento, R.L. Ferreira, X. Prous, M. Souza-Silva, B.C. Bellini, and A. Vasconcellos – Seasonal variations in cave invertebrate communities in the semiarid Caatinga, Brazil. Journal of Cave and Karst Studies, v. 78, no. 2, p. 61–71. DOI: 10.4311/2015LSC0111 SEASONAL VARIATIONS IN CAVE INVERTEBRATE COMMUNITIES IN THE SEMIARID CAATINGA, BRAZIL DIEGO DE M. BENTO1*,RODRIGO L. FERREIRA2,XAVIER PROUS2,MARCONI SOUZA-SILVA2, BRUNO CAVALCANTE BELLINI3, AND ALEXANDRE VASCONCELLOS4 Abstract: The Brazilian semiarid region has a clear distinction between the dry season, which can last up to nine months, and the rainy season. Caves are connected to different extents to surface ecosystems, although they are idealized as stable environments due to their isolation. Furthermore, little is known about the effects of wet and dry seasonal variations on underground biological assemblages. Invertebrate communities were analyzed during dry and rainy seasons in 24 caves in the semiarid region of northeastern Brazil. We also investigated whether the environmental stability of caves attenuates the effects of seasonality in this particular region. Morphospecies richness and abundance and the diversity indexes of caves were significantly higher during the rainy season. In addition, more stable caves showed less variation in the community composition between seasons. Our data point to a clear influence of the surface ecosystems on the caves in Caatinga. However, the intensity of this influence apparently depends on the environmental stability of the cave, and the most stable caves present smaller changes in the structure of their invertebrate communities during different seasons. INTRODUCTION may increase during the rainy season for some weeks or months (Culver and White, 2005; Souza-Silva et al., The underground environment has distinct features in 2011a). The availability may also decrease because of comparison to adjacent surface ecosystems: a permanent intense leaching that might follow the organic resources lack of light, except in areas near the entrances, and a higher importation (Souza-Silva et al., 2007; Souza-Silva et al., tendency toward stable environmental conditions such as 2011a). temperature and moisture (Culver, 1982). The size of the The Brazilian semiarid region has a relatively predict- oscillation of these climatic parameters will depend substan- able seasonality, with a dry season that may last for more tially on the morphological complexity of the cave and on than nine months (Sampaio, 1995). The effects of climatic the amplitude of climatic variations on the surface (Culver variables in the ecoregion of Caatinga on several inverte- and White, 2005). brate taxa in epigean ecosystems have already been investi- The permanent absence of light inside caves prevents the gated. Some of the sampled taxa were Apoidea (Aguiar and existence of photoautotrophic organisms. Therefore, food Martins, 1997), Sphingidae (Gusmão and Creão-Duarte, sources available for the resident fauna usually have 2004), Buprestidae (Iannuzzi et al., 2006), Scarabeidae (Her- allochthonous origin (Schneider et al., 2011; Souza-Silva nández, 2007), Scorpiones (Araújo et al., 2010a), and ants et al., 2011a). Such resources are imported from the external (Medeiros et al., 2012), besides some studies on larger environments continuously or temporarily by physical and groups like Hexapoda (Vasconcellos et al., 2010) and soil biological agents (Culver, 1982; Howarth, 1983; Ferreira macroarthopods (Araújo et al., 2010b). The vast majority and Martins, 1999). Hence, cave ecosystems are generally, of these studies have shown a positive relation between pop- to a greater or lesser extent, connected to surface ecosys- ulation size and rainfall. tems, whose environmental variations affect the communi- Other studies of seasonality in caves are scarce and ties of cave invertebrates (Culver, 1982; Culver and White, restricted to a few groups such as mites in Belgium 2005; Souza-Silva et al., 2011a; Simões et al., 2015). The general features of numbers, positions, distribution, and extents of the entrances and their relation with the length * Corresponding author: [email protected] 1 Centro Nacional de Pesquisa e Conservação de Cavernas, Base Avançada Compar- of caves are factors that can act directly on the maintenance tilhada no Rio Grande Do Norte, Instituto Chico Mendes de Conservação da Biodi- of microclimate in underground environments (Ferreira, versidade. 59015-350 Natal, Rio Grande do Norte, Brasil. 2004; Simões et al., 2015). 2 Centro de Estudos em Biologia Subterrânea, Setor de Zoologia Geral, Departa- mento de Biologia (DBI), Universidade Federal de Lavras (UFLA), Minas Gerais, Caves located in semiarid ecosystems are generally subject CEP: 37200-000, Brasil. to seasonal variations in the external environment with a clear 3 Departamento de Botânica, Ecologia e Zoologia, Centro de Biociências, Universi- alternation between dry and rainy seasons. The structure of dade Federal do Rio Grande do Norte, CEP 59072-970, Natal, Rio Grande do Norte, Brazil. cave communities may suffer alterations due to climate 4 Laboratório de Termitologia, Departamento de Sistemática e Ecologia, Universi- changes on the surface, given that the resource availability dade Federal da Paraíba, 58051-900, João Pessoa, Paraíba, Brazil. Journal of Cave and Karst Studies, August 2016 .61 SEASONAL VARIATIONS IN CAVE INVERTEBRATE COMMUNITIES IN THE SEMIARID CAATINGA,BRAZIL (Ducarme et al., 2004), crickets in North America (Lavoie conducted on each cave between December 2009 and et al., 2007), and even a single species of spider in southern August 2010, one at the end of the dry season and other at Brazil (Ferreira et al., 2005). In caves at Caatinga, most oth- the end of the rainy season, with a six-month interval er studies were focused solely on the characterization of between visits. invertebrate communities, without regard to season (Tra- We carried out the sampling by visually searching across jano, 1987; Ferreira and Martins, 1998; Ferreira et al., 2010). all the same accessible parts of each cave during both events, The present study aimed to evaluate changes in the struc- prioritizing organic matter such as debris, carcasses, and ture of invertebrate communities between the dry and rainy guano and microhabitats such as humid soil, cracks, spe- seasons in limestone caves from five municipalities in the leothems, and spaces under rocks. Manual collections were semiarid region of Brazil. In addition, we also investigated made with the aid of tweezers, brushes, and entomological if the environmental stability of these caves can mitigate nets (Souza-Silva et al., 2011b). Invertebrates were collected the effects of seasonal variations on invertebrate communi- from water bodies with the aid of forceps, hand nets, and ties. In this context, due to the strong seasonality on the sur- creels, in accordance with Ferreira et al. (2010). face and the connection between epigean and hypogean The collection team was always composed of the same environments, we expected changes in the structure of the four biologists with experience in caving and manual collec- cave invertebrate community between dry and rainy sea- tion of invertebrates, as recommended by Weinstein and sons, and that caves with greater environmental stability Slaney (1995). This methodology is effective for collections would have less fluctuation in the composition of the inver- and reduces the impact generated by other kinds of sam- tebrate community throughout the year. pling, such as the installation of pitfall traps, which are notorious for causing population disturbances in caves (Weinstein and Slaney, 1995; Sharratt et al., 2000). To MATERIAL AND METHODS ensure that the sampling was as standardized as possible, the sampling time was approximately one hour per 50 m2 The study was conducted in 24 caves in the municipali- cave area for each biologist. ties of Baraúna, Felipe Guerra, Governador Dix-Sept All invertebrates were identified to the lowest possible Rosado, Apodi, and Mossoró, Rio Grande do Norte state, taxonomic level and grouped in morphospecies for all statis- northeastern Brazil (Figure 1; Table 1). These caves are tical analysis (Oliver and Beattie, 1996a; Derraik et al., embedded in the limestones of the Jandaíra Formation, 2002; Ward and Stanley, 2004; Derraik et al., 2010; which is the most extensive area of carbonate outcrops of Souza-Silva et al. 2011b). Oliver and Beattie (1996a) showed Phanerozoic age in Brazil. Deposited between the Meso- that morphospecies identified by non-specialists can provide Turonian and Eocampanian, the rocks of Jandaíra Forma- estimates of richness and turnover consistent with those gen- tion are a carbonate ramp that crops out in almost all the erated using species identified by taxonomic specialists. The onshore portion of the Potiguar Basin. This carbonate use of morphospecies or corrected morphospecies invento- ramp was submitted, during and after deposition, to various ries in the analyses generally provides results concordant episodes of uplift that led to a subaerial exposure and ero- with conventional species inventories (Oliver and Beattie, sion, resulting in intense epigenetic karstification (Bezerra 1996b). et al., 2007). All the invertebrate morphospecies found on each cave Most caves in the area occur as clusters in limestone out- had some specimens collected. The individuals observed crops locally called lajedos. The sampled caves were ran- during the collections
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