Más Allá de las Orillas: La Influencia de un Río Subterráneo en la Comunidad de Invertebrados de Cueva — Un Estudio de Caso en Niquelândia, Goiás, Brasil
Palabras clave:
Drenaje, Invertebrados, Cuevas, Estructura de Comunidades, Temperatura, HumedadResumen
Los cursos de agua en el interior de las cuevas pueden influir fuertemente en la riqueza y la composición de las comunidades de invertebrados terrestres, al proporcionar humedad y transportar recursos orgánicos desde los hábitats de superficie. Para poner a prueba esta hipótesis, realizamos muestreos en una cueva caliza, comparando dos ambientes distintos: las márgenes de una corriente activa y un conducto superior más seco. Utilizando una metodología estandarizada, establecimos sectores de 30 m² y cuadrantes de 1 m² como unidades de muestreo para registrar invertebrados terrestres y caracterizar los microhábitats del suelo (distancia al curso de agua, temperatura, humedad, diversidad de sustratos, disponibilidad de refugio y de recursos orgánicos). La composición y la riqueza de especies difirieron significativamente entre áreas húmedas y secas, con 35 especies registradas cerca del curso de agua y 27 en zonas más secas. Los cursos de agua subterráneos modifican directamente las condiciones microambientales, como la humedad y la temperatura, además de aumentar la disponibilidad de recursos orgánicos. Asimismo, promueven una mayor heterogeneidad de hábitats al transportar detritos que sirven de refugio y sitios de reproducción. Estos resultados amplían nuestra comprensión sobre el funcionamiento de los ecosistemas subterráneos y ofrecen bases para estrategias de conservación y manejo de estos ambientes.
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ÁLVARES, C. A.; STAPE, J. L.; SENTELHAS, P. C.; GONÇALVES, J. L. M.; SPAROVEK, G. Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift, v. 22, n. 6, p. 711-728, 2013. doi:10.1127/0941-2948/2013/0507
BADINO, G. Underground Meteorology - “What’s the weather underground?”. Acta Carsologica, v. 39, n.3, p. 427–448, 2010. https://doi.org/10.3986/ac.v39i3.74
BASELGA, A. Partitioning the turnover and nestedness components of beta diversity. Global Ecology and Biogeography, v. 19, n. 1, p. 134-143, 2010. https://doi.org/10.1111/j.1466-8238.2009.00490.x
BENTO, D. M.; FERREIRA, R. L.; PROUS, X.; S; SOUZA-SILVA, M.; BELLINI, B. C., & VASCONCELLOS, A. Seasonal Variations in Cave Invertebrate Communities in the Semiarid Caatinga, Brazil. Journal of Cave and Karst Studies, v. 78, p. 61-71, 2016. DOI: 10.4311/2015LSC0111
CALDERÓN-PATRÓN, J. M.; GOYENECHEA, I.; ORTIZ-PULIDO, R.; CASTILLO-CERON, J.; MANRIQUEZ, N.; RAMIREZ-BAUTISTAS, A.; ...; MORENO, C. E. Beta diversity in a highly heterogeneous area: disentangling species and taxonomic dissimilarity for terrestrial vertebrates. PLoS ONE, v. 11, n. 8, p. 1-15, 2016. https://doi.org/10.1371/journal.pone.0160438
CARDOSO, P.; RIGAL, F.; CARVALHO, J. C. BAT–Biodiversity Assessment Tools, an R package for the measurement and estimation of alpha and beta taxon, phylogenetic and functional diversity. Methods in Ecology and Evolution, v. 6, n. 2, p. 232-236, 2015. https://doi.org/10.1111/2041-210X.12310
CASTRO-SOUZA, R. A., JUNTA, V. G. P.; FERREIRA, R. L. Description and ecology of a new species of the cricket genus Endecous (Orthoptera: Grylloidea: Phalangopsidae) in the speleological province of. Zootaxa, v. 4821, n. 2, p. 305–332, 2020. https://doi.org/10.11646/zootaxa.4821.2.4
CHAO, A.; CHIU, C. H.; JOST, L. Unifying Species Diversity, Phylogenetic Diversity, Functional Diversity, and Related Similarity and Differentiation Measures Through Hill Numbers. Annual Review of Ecology, Evolution, and Systematics, v. 45, n. 1, p. 297–324, 2014. https://doi.org/10.1146/annurev-ecolsys-120213-091540
CHOWN, S. L.; SORENSEN, J. G., TERBLANCHE J. S. Water loss in insects: An environmental change perspective. Journal of Insect Physiology, v. 57, n. 8, p. 1070-1084, 2011. https://doi.org/10.1016/j.jinsphys.2011.05.004
CLARKE, K. R.; GORLEY, R. N.; SOMERFELD, P. J.; WARWICK, R. M. Change in marine communities. An approach to statistical analysis and interpretation. PRIMER-E, 2014.
FARIAS-MARTINS, F.; SPERBER, C. F.; ALBENY-SIMÕES, D.; BREAUX, J. A.; FIANCO, M.; SZINWELSKI, N. Forest litter crickets prefer higher substrate moisture for oviposition: Evidence from field and lab experiments. PLoS ONE, v. 12, n. 10, e0185800. 2017. https://doi.org/10.1371/journal.pone.0185800
FERREIRA, R. L. A medida da complexidade ecológica e suas aplicações na conservação e manejo de ecossistemas subterrâneos. 2004. Tese (Doutorado em Ecologia) - Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, 2004.
FERREIRA, T.; RASBAND, W. ImageJ user guide IJ 1.42 r. National Institute of Health, 2012.
FURTADO-OLIVEIRA, L., FERREIRA, R. L.; FERNÁNDEZ, R. J. I.; SOUZA-SILVA, M. Recreational caving impacts of visitors in a high-altitude cave in Bolivian Andes: main effects on microhabitat structure and faunal distribution. International Journal of Speleology, v. 51, n. 2, p. 93–103. 2022. https://doi.org/10.5038/1827-806X.51.2.2418
HARTING, F. DHARMa: Diagnóstico Residual para Hierárquico Modelos de regressão (multinível/mistos) (versão 0.4.6). 2022. Pacote R. https://CRAN.R-project.org/package=DHARMa
HERTL P. T.; BRANDENBURG, R. L.; BARBERCHECK, M. E. Effect of soil moisture on ovipositional behavior in the southern mole cricket (Orthoptera: Gryllotalpidae). Environmental Entomology, v. 30, n. 3, p. 466-473, 2001. https://doi.org/10.1603/0046-225X-30.3.466
HOWARTH, F. G. Why the delay in recognizing terrestrial obligate cave species in the tropics?. International Journal of Speleology, v. 52, n. 1, p. 3, 2023. https://doi.org/10.5038/1827-806X.52.1.2446
JUNTA, V. G. P.; SOUZA-SILVA, M.; VAZ, G. A. S.; FERREIRA, R. L. One cave, multiple worlds: cave zonation, habitat selection and conservation of cave-dwelling fauna in a new hotspot of subterranean biodiversity in South America. Community Ecology, v. 26, p. 287-302, 2025. https://doi.org/10.1007/s42974-025-00235-8
LEGENDRE, P.; GALLAGHER, E. D. Ecologically meaningful transformations for ordination of species data. Oecologia, v. 129, n. 2, p. 271-280, 2001.
LÜDECKE, D.; BEN-SHACHAR, M.; PATIL I. et al. Performance: an R package for assessment, comparison and testing of statistical models. Journal of Open Source Software, v. 6, p. 3139, 2021. https://doi.org/10.21105/joss.03139
MAGURRAN, A. E. Measuring biological diversity. Oxford: Blackwell Science, 256 p. 2004.
MAMMOLA, S. Finding answers in the dark: caves as models in ecology fifty years after Poulson and White. Ecography, v. 42, n. 7, p. 1331-1351, 2019. https://doi.org/10.1111/ecog.03905
MAMMOLA, S.; CARDOSO, P.; ANGYAL, D.; BALÁZS, G.; BLICK, T.; BRUSTEL, H.; ...; ISAIA, M. Local-versus broad-scale environmental drivers of continental β-diversity patterns in subterranean spider communities across Europe. Proceedings of the Royal Society B, v. 286, 2019. https://doi.org/10.1098/rspb.2019.1579
MONRO, A. K.; BYSTRIAKOVA, N.; FU, L.; WEN, F.; WEI, Y. Discovery of a diverse cave flora in China. PLoS ONE, v. 13, n. 2, e0190801, 2018. https://doi.org/10.1371/journal.pone.0190801
MYERS, N.; MITTERMEIER, R.; MITTERMEIER, C.; et al. Biodiversity hotspots for conservation priorities. Nature, v. 403, p. 853–858, 2000. https://doi.org/10.1038/35002501
OLIVER, L.; BEATTIE, A. J. Designing a Cost-Effective Invertebrate Survey: A Test of Methods for Rapid Assessment of Biodiversity. Ecological Applications, v. 6, n. 2, p. 594-607, 1996b. https://doi.org/10.2307/2269394
OLIVER, L.; BEATTIE, A. J. Invertebrate morphospecies as surrogates for species: a case study. Conservation Biology, v. 10, n. 1, p. 99-109, 1996a. https://doi.org/10.1046/j.1523-1739.1996.10010099.x
PELLEGRINI, T.; VENDAS, L. P.; AGUIAR, P.; & FERREIRA, R. L. Linking spatial scale dependence of land-use descriptors and invertebrate cave community composition. Subterranean Biology, v. 18, p. 17-38, 2016. doi: 10.3897/subtbiol.18.8335
POULSON, T. L.; WHITE, W. B. The Cave Environment: Limestone caves provide unique natural laboratories for studying biological and geological processes. Science, v. 165, n. 3897, p. 971-981, 1969. DOI: 10.1126/science.165.3897.971
R CORE TEAM. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Viena, Áustria, 2023.
REIS-VENÂNCIO, P. C.; FERREIRA, R. L.; SOUZA-SILVA, M. From the front door to the basement: Invertebrate communities' structure as a proxy for determining cave zonation in Neotropics. Biotropica, v. 56, n. 4, p. e13356, 2024. https://doi.org/10.1111/btp.13356
REIS-VENÂNCIO, P. C.; RABELO, L. M.; PELLEGRINI, T. G.; FERREIRA, R. L. From light to darkness: the duality of influence of habitat heterogeneity on Neotropical terrestrial cave invertebrate communities. Studies on Neotropical Fauna and Environment, v. 59, n. 2, p. 255-264, 2022. https://doi.org/10.1080/01650521.2022.2095832
ROCHA MELO, L. M.; FERREIRA, R. L.; SILVA, M. S. A review of the factors influencing invertebrate community structure in subterranean habitats. Community Ecology, p. 1-15, 2025.
SARBU, S. M.; KANE, T. C.; & KINKLE, B. K. A Chemoautotrophically Based Cave Ecosystem. Science, v. 272, n. 5270, p. 1953–1955, 1996. DOI: 10.1126/science.272.5270.1953
SIMÕES, M. H.; SOUZA-SILVA, M.; FERREIRA, R. L. Cave physical attributes influencing the structure of terrestrial invertebrate communities in Neotropics. Subterranean Biology, v. 16, p. 103-121, 2015. doi: 10.3897/subtbiol.16.5470
SIMÕES, M. H.; SOUZA-SILVA, M.; FERREIRA, R. L. Species-area relationship and richness persistence as a proxy of environmental carrying capacity: A case study in a neotropical show cave. Acta Oecologica, v. 116, p. 103848, 2022. https://doi.org/10.1016/j.actao.2022.103848
SOUZA-SILVA, M.; MARTINS, R. P.; FERREIRA, R. L. Cave lithology determining the structure of the invertebrate communities in the Brazilian Atlantic Rain Forest. Biodiversity and Conservation, v. 20, n. 8, p. 1713-1729, 2011. https://doi.org/10.1007/s10531-011-0057-5
SOUZA-SILVA, M., CERQUEIRA, R. F. V., PELLEGRINI, T. G., & FERREIRA, R. L. Habitat selection of cave-restricted fauna in a new hotspot of subterranean biodiversity in Neotropics. Biodiversity and Conservation, v. 30, n. 14, p. 4223–4250, 2021. https://doi.org/10.1007/s10531-021-02302-8
SOUZA-SILVA, M., DE OLIVEIRA BERNARDI, L. F., MARTINS, R. P., & FERREIRA, R. L. Transport and consumption of organic detritus in a neotropical limestone cave. Acta Carsologica, v. 41, n. 1, 2012. https://doi.org/10.3986/ac.v41i1.54
SOUZA-SILVA, M.; FERREIRA, R. L. Dinâmica Trófica em Ambientes de Cavernas. In: ZAMPAULO, R. A.; PROUS, X. (Eds.) Fauna Cavernícola do Brasil. Belo Horizonte, MG: Rupestre, 2022. Cap. 2, p. 59-81.
WEINSTEIN, P. Behavioural ecology of tropical cave cockroaches: preliminary field studies with evolutionary implications. Australian Journal of Entomology, v. 33, n. 4, p. 367-370, 1994. https://doi.org/10.1111/j.1440-6055.1994.tb01249.x
WYNNE, J. J.; HOWARTH, F. G.; SOMMER, S.; DICKSON, B. G. Fifty years of cave arthropod sampling: techniques and best practices. International Journal of Speleology, v. 48, n. 1, p. 33-48, 2019. https://doi.org/10.5038/1827-806X.48.1.2231
ZUUR, A. F.; LENO, E. N.; WALKER, N. J.; SAVELIEV, A. A.; SMITH, G. M. Mixed effects models and extensions in ecology with R. 1st edition. New York: Springer, 2009. 574p.