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Cross-habitat spillover may be the outcome of a process of habitat loss or degradation where the receiving habitat serves as a refuge for organisms. Once surface habitats are lost or degraded, animals can find underground refuge in caves. This paper is focused on testing whether taxonomic order richness inside caves is positively affected by the loss of the native vegetation cover surrounding caves; whether degradation of native vegetation cover predicts cave community composition; and whether there is a pattern of cave community clusters delimited by similarity in the effects of habitat degradation on animal communities. We gathered a comprehensive speleological dataset consisting of occurrence data of thousands of invertebrates and vertebrates sampled in 864 iron caves in the Amazon, to test the effects of both variables measured inside caves and surrounding landscapes on spatial variation in richness and composition of animal communities. We show that caves can work as refuges for the fauna in landscapes where the native vegetation cover surrounding them was degraded, which was evidenced by landcover change increasing the richness of cave communities and clustering caves by similarity in community composition. Therefore, habitat degradation on the surface should be a key variable when characterizing cave ecosystems for conservation prioritization and offset planning. Habitat degradation causing a cross-habitat spillover effect highlights the importance of maintaining the connection between caves by the surface, especially large caves. Our study can help guide industry and stakeholders working on the complex conciliation between land use and biodiversity conservation.
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Animais Selvagens , Ecossistema , Animais , Brasil , BiodiversidadeRESUMO
Understanding the factors underpinning species abundance patterns in space and time is essential to implement effective cave conservation actions. Yet, the methods employed to monitor cave biodiversity still lack standardization, and no quantitative assessment has yet tried to optimize the amount and type of information required to efficiently identify disturbances in cave ecosystems. Using a comprehensive monitoring dataset for tropical iron caves, comprising abundance measurements for 33 target taxa surveyed across 95 caves along four years, here we provide the first evidence-based recommendations to optimize monitoring programs seeking to follow target species abundance through time. We found that seasonality did not influence the ability to detect temporal abundance trends. However, in most species, abundance estimates assessed during the dry season resulted in a more accurate detection of temporal abundance trends, and at least three surveys were required to identify global temporal abundance trends. Finally, we identified a subset of species that could potentially serve as short-term disturbance indicators. Results suggest that iron cave monitoring programs implemented in our study region could focus sampling efforts in the dry season, where detectability of target species is higher, while assuring data collection for at least three years. More generally, our study reveals the importance of long-term cave monitoring programs for detecting possible disturbances in subterranean ecosystems, and for using the generated information to optimize future monitoring efforts.
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Coleoptera presents most of the cave fauna biodiversity, with several troglobite species belonging to the aquatic family Dytiscidae. However, very little is known on both genetic and genomic diversity traits of Neotropical cave beetles. Thus, here we present the complete mitochondrial genome sequence of five specimens of Desmopachria collected in a ferruginous cave from Serra dos Carajás in Parauapebas (Pará, Brazil, Eastern Amazon). Besides the general characteristics of the mitogenome of the analyzed specimens, we present their phylogenetic position within the family, considering the available genome sequences of different subfamilies within Dytiscidae.
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We report the complete mitochondrial genome sequence of Glomeridesmus spelaeus, the first sequenced genome of the order Gomeridesmida. The genome is 14,825 pb in length and encodes 37 mitochondrial (13 PCGs, 2 rRNA genes, 22 tRNA) genes and contains a typical AT-rich region. The base composition of the mitogenome was A (40.1%), T (36.4%), C (15.8%), and G (7.6%), with an GC content of 23.5%. Our results indicated that G. spelaeus is only distantly related to the other Diplopoda species with available mitochondrial genomes in the public databases. As the broadest genetic characterization of a Glomeridesmida species available to date, the mitogenome of G. spelaeus will help understanding the evolution of such a little-known millipede group. Also, our data will be important for the characterization and conservation of the diverse invertebrate troglofauna of the Amazonian caves.
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The edaphic fauna plays an important role in the organic matter dynamics of the soil. Millipeds (Diplopoda),centipeds (Chilopoda) and isopods (Isopoda) are among the main components of the soil fauna. Vegetationstructure represents one of the main factors influencing composition and diversity of these species that inhabitleaf litter and soil, what is particularly important in the Amazon Forest, where there are several singular ve-getation types. Savannah and forest areas stand out in ferruginous hills, which represents one of the most poorlyknown and highly threatened ecosystems in the Amazon. However, sampling the edaphic fauna in high diversitysites represents a challenging task. Studies have shown that sampling method may influence observed patterns ofdiversity. From this perspective, the present study aimed to (i) investigate whether assemblages of Chilopoda,Diplopoda and Isopoda differ between vegetation types in the Amazon, (ii) indicate how biological parametersbehave in such communities, (iii) identify which method or combination of methods is better suited to samplespecies richness and (iv) quantify the efficiency of each method regarding time of work and cost. Sampling wasconducted by means of hand collection, leaf litter collection, hay-bait traps and soil sampling in four patches,two in the savannah (also called canga) and two in the forest. Richness was higher in forest habitats forChilopoda and Diplopoda, while for Isopoda there was no significant difference. Species composition also dif-fered between vegetation types for Chilopoda and Isopoda, but not for Diplopoda. Beta diversity between ve-getation types was mainly determined by nestedness and balancing, while turnover was the main beta diversitycomponent responsible for differences among methods. Soil sampling and hand collection added more species tothe samples, therefore, this combination was the most efficient to access diversity. Our results support thehypothesis that differences in the soil cover promoted by distinct vegetation types influence the species diversityand composition of edaphic fauna. The differences were mainly determined by nestedness and balancing, in-dicating that the fauna sampled in the canga represents a subset of those present in the surrounding forest. In thissense, even in ecosystems with distinct vegetation types, the combination of soil and surface sampling methods isrecommended. Lastly, the present study proposes a set of decision rules and a key to select the most appropriatemethod to sample the studied taxonomic groups
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The edaphic fauna plays an important role in the organic matter dynamics of the soil. Millipeds (Diplopoda),centipeds (Chilopoda) and isopods (Isopoda) are among the main components of the soil fauna. Vegetationstructure represents one of the main factors influencing composition and diversity of these species that inhabitleaf litter and soil, what is particularly important in the Amazon Forest, where there are several singular ve-getation types. Savannah and forest areas stand out in ferruginous hills, which represents one of the most poorlyknown and highly threatened ecosystems in the Amazon. However, sampling the edaphic fauna in high diversitysites represents a challenging task. Studies have shown that sampling method may influence observed patterns ofdiversity. From this perspective, the present study aimed to (i) investigate whether assemblages of Chilopoda,Diplopoda and Isopoda differ between vegetation types in the Amazon, (ii) indicate how biological parametersbehave in such communities, (iii) identify which method or combination of methods is better suited to samplespecies richness and (iv) quantify the efficiency of each method regarding time of work and cost. Sampling wasconducted by means of hand collection, leaf litter collection, hay-bait traps and soil sampling in four patches,two in the savannah (also called canga) and two in the forest. Richness was higher in forest habitats forChilopoda and Diplopoda, while for Isopoda there was no significant difference. Species composition also dif-fered between vegetation types for Chilopoda and Isopoda, but not for Diplopoda. Beta diversity between ve-getation types was mainly determined by nestedness and balancing, while turnover was the main beta diversitycomponent responsible for differences among methods. Soil sampling and hand collection added more species tothe samples, therefore, this combination was the most efficient to access diversity. Our results support thehypothesis that differences in the soil cover promoted by distinct vegetation types influence the species diversityand composition of edaphic fauna. The differences were mainly determined by nestedness and balancing, in-dicating that the fauna sampled in the canga represents a subset of those present in the surrounding forest. In thissense, even in ecosystems with distinct vegetation types, the combination of soil and surface sampling methods isrecommended. Lastly, the present study proposes a set of decision rules and a key to select the most appropriatemethod to sample the studied taxonomic groups
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Plants living above and around caves represent an important, albeit poorly studied, resource within cave ecosystems. The presence of plant material (root-like structures or rhizothemes, saplings, seeds, and seedlings) correlates positively with the biodiversity of the cave dwelling animals as shown for iron-ore caves in Carajás, Pará, Brazil. Plant material collected in caves has proven to be difficult to identify by traditional botanical methods, thus this research aims to provide a qualitative insight into the taxonomy and morphology of rhizothemes and other plant fragments found in the caves. The identification process used a combination of different molecular markers (ITS2, rbcL, and trnH-psbA) followed by a comparison of the sequences obtained against publicly available databases. The rhizothemes were submitted to micromorphological analysis to ascertain their putative root or stem origin and to compare their anatomy with known patterns found in the plant families or genera recovered through molecular matches. All studied samples were Angiosperms, mostly belonging to subclass Rosideae, within four orders: Malpighiales (Euphorbiaceae, Hypericaceae), Sapindales (Anacardiaceae and Sapindaceae), Myrtales (Myrtaceae), Fabales (Fabaceae), and only two belonging to subclass Asteridae, order Gentianales (Apocynaceae). Some of the samples were matched to generic level, with ITS2 being the best marker to identify the fragments because it shows high degree of sequence variation even at specific level and result reliability. All rhizothemes turned out to be roots, and correspondence was found between the existing literature and the individual anatomical patterns for the families and genera retrieved. DNA barcode has proved to be a useful tool to identify plant fragments found in this challenging environment. However, the existence of well curated, authoritatively named collections with ample biological information has proven to be essential to achieve a reliable identification.
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The degradation of subterranean habitats is believed to represent a serious threat for the conservation of obligate subterranean dwellers (troglobites), many of which are short-range endemics. However, while the factors influencing cave biodiversity remain largely unknown, the influence of the surrounding landscape and patterns of subterranean connectivity of terrestrial troglobitic communities have never been systematically assessed. Using spatial statistics to analyze the most comprehensive speleological database yet available for tropical caves, we first assess the influence of iron cave characteristics and the surrounding landscape on troglobitic communities from the Eastern Amazon. We then determine the spatial pattern of troglobitic community composition, species richness, phylogenetic diversity, and the occurrence of frequent troglobitic species, and finally quantify how different landscape features influence the connectivity between caves. Our results reveal the key importance of habitat amount, guano, water, lithology, geomorphology, and elevation in shaping iron cave troglobitic communities. While mining within 250 m from the caves influenced species composition, increasing agricultural land cover within 50 m from the caves reduced species richness and phylogenetic diversity. Troglobitic species composition, species richness, phylogenetic diversity, and the occurrence of frequent troglobites showed spatial autocorrelation for up to 40 km. Finally, our results suggest that the conservation of cave clusters should be prioritized, as geographic distance was the main factor determining connectivity between troglobitic communities. Overall, our work sheds important light onto one of the most overlooked terrestrial ecosystems, and highlights the need to shift conservation efforts from individual caves to subterranean habitats as a whole.
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ABSTRACT Amblypygids are among the main predators in the ferriferous caves in Carajás National Forest, state of Pará (Amazon region of Brazil). One of the most common amblypygid species in this region is Heterophrynus longicornis (Butler 1873), and its most frequent prey are crickets of the family Phalangopsidae, which are abundant in the caves of Pará. Because they are primarily predators, necrophagy by amblypygids is not frequent in nature, and there are only two literature records of necrophagy of bats by Amblypygi. On December 11th, 2013, we observed an individual H. longicornis eating a bat carcass in a Pará ferriferous cave. The amblypygid exhibited considerable interest in the bats carcass, and it did not interrupt its meal even when lamps or a cameras flash were pointed in its direction. The availability of nutrients in the carcass must promote this opportunistic behavior in caves, especially considering the habitual scarcity of trophic resources in underground environments when compared to epigean environments.
RESUMO Amblipígios são considerados um dos principais predadores em cavernas de litologia ferrífera localizadas na Floresta Nacional de Carajás no estado do Pará (região da Amazônia brasileira). Uma das espécies de amblipígios mais comuns nesta região é Heterophrynus longicornis (Butler 1873), e uma das presas mais frequentes são grilos da família Phalangopsidae, abundantes nas cavernas do Pará. Por serem predadores, a necrofagia em amblipígeos foi pouco observada na natureza, sendo que existem dois registros na literatura sobre necrofagia de morcegos por amblipígios. Em 11 de dezembro de 2013, observamos um H. longicornis se alimentando da carcaça de um morcego em uma caverna de litologia ferrífera da Floresta Nacional de Carajás. Aparentemente, havia um interesse considerável pela carcaça do morcego por parte do amblipígio, uma vez que o indivíduo não interrompeu sua alimentação, mesmo quando iluminado por lanternas e o flash da câmera. A abundância de nutrientes na carcaça deve favorecer este comportamento oportunístico em cavernas, especialmente quando se considera a habitual escassez de recursos tróficos destes ambientes subterrâneos, quando comparados a ambientes epígeos.
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Animais , Cadeia Alimentar , Quirópteros/metabolismo , Quirópteros/sangueRESUMO
Caves pose significant challenges for mining projects, since they harbor many endemic and threatened species, and must therefore be protected. Recent discussions between academia, environmental protection agencies, and industry partners, have highlighted problems with the current Brazilian legislation for the protection of caves. While the licensing process is long, complex and cumbersome, the criteria used to assign caves into conservation relevance categories are often subjective, with relevance being mainly determined by the presence of obligate cave dwellers (troglobites) and their presumed rarity. However, the rarity of these troglobitic species is questionable, as most remain unidentified to the species level and their habitats and distribution ranges are poorly known. Using data from 844 iron caves retrieved from different speleology reports for the Carajás region (South-Eastern Amazon, Brazil), one of the world's largest deposits of high-grade iron ore, we assess the influence of different cave characteristics on four biodiversity proxies (species richness, presence of troglobites, presence of rare troglobites, and presence of resident bat populations). We then examine how the current relevance classification scheme ranks caves with different biodiversity indicators. Large caves were found to be important reservoirs of biodiversity, so they should be prioritized in conservation programs. Our results also reveal spatial autocorrelation in all the biodiversity proxies assessed, indicating that iron caves should be treated as components of a cave network immersed in the karst landscape. Finally, we show that by prioritizing the conservation of rare troglobites, the current relevance classification scheme is undermining overall cave biodiversity and leaving ecologically important caves unprotected. We argue that conservation efforts should target subterranean habitats as a whole and propose an alternative relevance ranking scheme, which could help simplify the assessment process and channel more resources to the effective protection of overall cave biodiversity.