in

A multifaceted approach to understanding bat community response to disturbance in a seasonally dry tropical forest

[adace-ad id="91168"]
  • 1.

    Naeem, S., Duffy, J. E. & Zavaleta, E. The functions of biological diversity in an age of extinction. Science 336, 1401–1406 (2012).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 2.

    Curtis, P. G., Slay, C. M., Harris, N. L., Tyukavina, A. & Hansen, M. C. Classifying drivers of global forest loss. Science 361, 1108–1111 (2018).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 3.

    Ewers, R. M. & Didham, R. K. Confounding factors in the detection of species responses to habitat fragmentation. Biol. Rev. 81, 117–142 (2006).

    PubMed  Article  Google Scholar 

  • 4.

    Jones, G., Jacobs, D. S., Kunz, T. H., Willig, M. R. & Racey, P. A. Carpe noctem: the importance of bats as bioindicators. Endanger. Species Res. 8, 93–115 (2009).

    Article  Google Scholar 

  • 5.

    Rocha, R. et al. Design matters: an evaluation of the impact of small man-made forest clearings on tropical bats using a before-after-control-impact design. For. Ecol. Manag. 401, 8–16 (2017).

    Article  Google Scholar 

  • 6.

    Wood, J. R. et al. No single driver of biodiversity: divergent responses of multiple taxa across land use types. Ecosphere 8, e01997 (2017).

    Article  Google Scholar 

  • 7.

    Coutinho Cunto, G. C. & Bernard, E. Neotropical bats as indicators of environmental disturbance: what is the emerging message?. Acta Chiropterologica 14, 143–151 (2012).

    Article  Google Scholar 

  • 8.

    Medellín, R. A., Equihua, M. & Amin, M. A. Bat diversity and abundance as indicators of disturbance in neotropical rainforest. Conserv. Biol. 14, 1666–1675 (2000).

    Article  Google Scholar 

  • 9.

    Russo, D., Bosso, L. & Ancillotto, L. Novel perspectives on bat insectivory highlight the value of this ecosystem service in farmland: research frontiers and management implications. Agric. Ecosyst. Environ. 266, 31–38 (2018).

    Article  Google Scholar 

  • 10.

    Avila-Cabadilla, L. D., Stoner, K. E., Henry, M. & Alvarez Añorve, M. Y. Composition, structure and diversity of phyllostomid bat assemblages in different successional stages of a tropical dry forest. For. Ecol. Manag. 258, 986–996 (2009).

    Article  Google Scholar 

  • 11.

    Castro-Luna, A. A., Sosa, V. J. & Castillo-Campos, G. Quantifying phyllostomid bats at different taxonomic levels as ecological indicators in a disturbed tropical forest. Acta Chiropterologica 9, 219–228 (2007).

    Article  Google Scholar 

  • 12.

    García-Morales, R., Badano, E. I. & Moreno, C. E. Response of neotropical bat assemblages to human land use. Conserv. Biol. 27, 1096–1106 (2013).

    PubMed  Article  Google Scholar 

  • 13.

    Meyer, C. F. J. & Kalko, E. K. V. Bat assemblages on neotropical land-bridge islands: nested subsets and null model analyses of species co-occurrence patterns. Divers. Distrib. 14, 644–654 (2008).

    Article  Google Scholar 

  • 14.

    Farneda, F. Z. et al. Predicting biodiversity loss in island and countryside ecosystems through the lens of taxonomic and functional biogeography. Ecography 43, 97–106 (2020).

    Article  Google Scholar 

  • 15.

    Cisneros, L. M., Fagan, M. E. & Willig, M. R. Season-specific and guild-specific effects of anthropogenic landscape modification on metacommunity structure of tropical bats. J. Anim. Ecol. 84, 373–385 (2015).

    PubMed  Article  Google Scholar 

  • 16.

    Peña-Cuellar, E., Stoner, K. E., Avila-Cabadilla, L. D., Martínez-Ramos, M. & Estrada, A. Phyllostomid bat assemblages in different successional stages of tropical rain forest in Chiapas, Mexico. Biodivers. Conserv. 21, 1381–1397 (2012).

    Article  Google Scholar 

  • 17.

    Fenton, A. M. B. et al. Phyllostomid bats (Chiroptera: Phyllostomidae) as indicators of habitat disruption in the Neotropics. Biotropica 24, 440–446 (1992).

    Article  Google Scholar 

  • 18.

    Avila-Cabadilla, L. D. et al. Local and landscape factors determining occurrence of phyllostomid bats in tropical secondary forests. PLoS ONE 7, e35228 (2012).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 19.

    Falcão, L. A. D., do Espírito-Santo, M. M., Fernandes, G. W. & Paglia, A. P. Effects of habitat structure, plant cover, and successional stage on the bat assemblage of a tropical dry forest at different spatial scales. Diversity 10, 1–11 (2018).

    Article  Google Scholar 

  • 20.

    Avila-Cabadilla, L. D. et al. Phyllostomid bat occurrence in successional stages of neotropical dry forests. PLoS ONE 9, e84572 (2014).

    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 21.

    Falcão, L. A. D., do Espírito-Santo, M. M., Leite, L. O., Garro, R. N. S. L., Avila-Cabadilla, L. D. & Stoner, K. E. Spatiotemporal variation in phyllostomid bat assemblages over a successional gradient in a tropical dry forest in southeastern Brazil. J. Trop. Ecol. 30, 123–132 (2014).

    Article  Google Scholar 

  • 22.

    Zarazúa-Carbajal, M., Avila-Cabadilla, L. D., Alvarez-Añorve, M. Y., Benítez-Malvido, J. & Stoner, K. E. Importance of riparian habitat for frugivorous bats in a tropical dry forest in western Mexico. J. Trop. Ecol. 33, 74–82 (2017).

    Article  Google Scholar 

  • 23.

    Meyer, C. F. J., Struebig, M. J. & Willig, M. R. Responses of tropical bats to habitat fragmentation, logging, and deforestation. In Bats in the Anthropocene: conservation of bats in a changing world (eds. Voigt, C. C. & Kingston, T.) 63–103 (Springer International Publishing) doi:https://doi.org/10.1007/978-3-319-25220-9 (2016).

  • 24.

    Estrada, A. & Coates-Estrada, R. Bats in continuous forest, forest fragments and in an agricultural mosaic habitat-island at Los Tuxtlas, Mexico. Biol. Conserv. 103, 237–245 (2002).

    Article  Google Scholar 

  • 25.

    Galindo-González, J. Clasificación de los murciélagos de la región de Los Tuxtlas, Veracruz, respecto a su respuesta a la fragmentación del hábitat. Acta Zoológica Mex. 20, 239–243 (2004).

    Google Scholar 

  • 26.

    Gorrensen, M. & Willing, M. R. Landscape responses of bats to habitat fragmentation in Atlantic forest of Paraguay. J. Mammal. 85, 688–697 (2004).

    Article  Google Scholar 

  • 27.

    de Oliveira, H. F. M., de Camargo, N. F., Gager, Y. & Aguiar, L. M. S. The response of bats (Mammalia: Chiroptera) to habitat modification in a neotropical savannah. Trop. Conserv. Sci. 10, 1–14 (2017).

    Article  Google Scholar 

  • 28.

    de la Peña-Cuéllar, E., Benítez-Malvido, J., Avila-Cabadilla, L. D., Martínez-Ramos, M. & Estrada, A. Structure and diversity of phyllostomid bat assemblages on riparian corridors in a human-dominated tropical landscape. Ecol. Evol. 5, 903–913 (2015).

    PubMed  PubMed Central  Article  Google Scholar 

  • 29.

    García-Morales, R. et al. Deforestation impacts on bat functional diversity in tropical landscapes. PLoS ONE 11, 1–16 (2016).

    Article  CAS  Google Scholar 

  • 30.

    Daniel, S., Korine, C. & Pinshow, B. Central-place foraging in nursing, arthropod-gleaning bats. Can. J. Zool. 86, 623–626 (2008).

    Article  Google Scholar 

  • 31.

    Galindo-González, J. & Sosa, V. J. Frugivorous bats in isolated trees and riparian vegetation associated with human-made pastures in a fragmented tropical landscape. Southwest. Nat. 48, 579–589 (2003).

    Article  Google Scholar 

  • 32.

    Chazdon, R. L. et al. Rates of change in tree communities of secondary neotropical forests following major disturbances. Philos. Trans. R. Soc. B Biol. Sci. 362, 273–289 (2007).

    Article  Google Scholar 

  • 33.

    Brito, J., Camacho, M. A., Romero, V. & Vallejo, A. F. Mamíferos del Ecuador. Versión 2019.0. Museo de Zoología, Pontificia Universidad Católica del Ecuador. https://bioweb.bio/faunaweb/mammaliaweb (2019).

  • 34.

    Tirira, D. A field guide to the mammals of Ecuador. Asociación Ecuatoriana de Mastozoología and Murciélago Blanco Publishing House (2017).

  • 35.

    Jara-Guerrero, A., Maldonado Riofrío, D., Espinosa, C. I. & Duncan, D. H. Beyond the blame game: a restoration pathway reconciles ecologists’ and local leaders’ divergent models of seasonally dry tropical forest degradation. Ecol. Soc. 24, 22 (2019).

    Article  Google Scholar 

  • 36.

    Cueva Ortiz, J. et al. Influence of anthropogenic factors on the diversity and structure of a dry forest in the central part of the Tumbesian region (Ecuador-Perú). Forests 10, 1–22 (2019).

    Article  Google Scholar 

  • 37.

    Medina, A., Harvey, C. A., Sánchez Merlo, D., Vílchez, S. & Hernández, B. Bat diversity and movement in an agricultural landscape in Matiguás, Nicaragua. Biotropica 39, 120–128 (2007).

    Article  Google Scholar 

  • 38.

    Davies, K. F., Margules, C. R. & Lawrence, J. F. Which traits of species predict population declines in experimental forest fragments?. Ecology 81, 1450–1461 (2000).

    Article  Google Scholar 

  • 39.

    Henle, K., Davies, K. F., Kleyer, M., Margules, C. & Settele, J. Predictors of species sensitivity to fragmentation. Biodivers. Conserv. 13, 207–251 (2004).

    Article  Google Scholar 

  • 40.

    Medellin, R. A. Chrotopterus auritus. Mamm. Species 343, 1–5 (1989).

    Google Scholar 

  • 41.

    Aguirre, L. F., Lens, L., Van Damme, R. & Matthysen, E. Consistency and variation in the bat assemblages inhabiting two forest islands within a neotropical savanna in Bolivia. J. Trop. Ecol. 19, 367–374 (2003).

    Article  Google Scholar 

  • 42.

    Stoner, K. E. Phyllostomid bat community structure and abundance in two contrasting tropical dry forests. Biotropica 37, 591–599 (2005).

    Article  Google Scholar 

  • 43.

    Gotelli, N. J. & Colwell, R. K. Estimating species richness. In Biological diversity: frontiers in measurement and assessment (eds. Magurran, A. & McGill, B. J.) 39–54 (Oxford University Press, 2011).

  • 44.

    Moreno, C. E. & Halffter, G. Assessing the completeness of bat biodiversity inventories using species accumulation curves. J. Appl. Ecol. 37, 149–158 (2000).

    Article  Google Scholar 

  • 45.

    Colwell, R. K. & Coddington, J. A. Estimating terrestrial biodiversity through extrapolation. Philos. Trans. Biol. Sci. 345, 101–118 (1994).

    ADS  CAS  Article  Google Scholar 

  • 46.

    Baselga, A. Partitioning the turnover and nestedness components of beta diversity. Glob. Ecol. Biogeogr. 19, 134–143 (2010).

    Article  Google Scholar 

  • 47.

    Baselga, A. Separating the two components of abundance-based dissimilarity: balanced changes in abundance vs. abundance gradients. Methods Ecol. Evol. 4, 552–557 (2013).

    Article  Google Scholar 

  • 48.

    Mena, J. L. & Williams de Castro, M. Diversidad y patrones reproductivos de quirópteros en un área urbana de Lima, Perú. Ecol. Apl. 1, 1–8 (2002).

    Article  Google Scholar 

  • 49.

    Pacheco, V., Cadenillas, R., Salas, E., Tello, C. & Zeballos, H. Diversidad y endemismo de los mamíferos del Perú. Rev. Peru. Biol. 16, 5–32 (2009).

    Google Scholar 

  • 50.

    Pinto, C. M., Marchán-Rivadeneira, M. R., Tapia, E. E., Carrera, J. P. & Baker, R. J. Distribution, abundance and roosts of the fruit bat Artibeus fraterculus (Chiroptera: Phyllostomidae). Acta Chiropterologica 15, 85–94 (2013).

    Article  Google Scholar 

  • 51.

    Homyack, J. A. Evaluating habitat quality of vertebrates using conservation physiology tools. Wildl. Res. 37, 332–342 (2010).

    Article  Google Scholar 

  • 52.

    Carrasco-Rueda, F. & Loiselle, B. A. Do riparian forest strips in modified forest landscapes aid in conserving bat diversity?. Ecol. Evol. 9, 4192–4209 (2019).

    PubMed  PubMed Central  Article  Google Scholar 

  • 53.

    Lewis, S. E. Roost fidelity of bats: a review. Am. Soc. Mammal. Roost 76, 481–496 (1995).

    Google Scholar 

  • 54.

    Voss, R. S., Fleck, D. W., Strauss, R. E., Velazco, P. M. & Simmons, N. B. Roosting ecology of Amazonian bats: evidence for guild structure in hyperdiverse mammalian communities. Am. Museum Novit. 3870, 1–43 (2016).

    Article  Google Scholar 

  • 55.

    Hylander, K. & Ehrle, J. The mechanisms causing extinction debts. Trends Ecol. Evol. 28, 341–346 (2013).

    PubMed  Article  Google Scholar 

  • 56.

    Willig, M. R. et al. Guild-level responses of bats to habitat conversion in a lowland Amazonian rainforest: species composition and biodiversity. J. Mammal. 100, 223–238 (2019).

    PubMed  PubMed Central  Article  Google Scholar 

  • 57.

    Meyer, C. F. J. Methodological challenges in monitoring bat population- and assemblage-level changes for anthropogenic impact assessment. Mamm. Biol. 80, 159–169 (2015).

    Article  Google Scholar 

  • 58.

    Gibb, R., Browning, E., Glover-Kapfer, P. & Jones, K. E. Emerging opportunities and challenges for passive acoustics in ecological assessment and monitoring. Methods Ecol. Evol. 10, 169–185 (2019).

    Article  Google Scholar 

  • 59.

    Sikes, R. S. & the Animal Care and Use Committee of the American Society of Mammalogists. 2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. J. Mammal. 97, 663–688 (2016).

  • 60.

    Espinosa, C. I. et al. Bosques tropicales secos de la región Pacífico Ecuatorial: diversidad, estructura, funcionamiento e implicaciones para la conservación. Ecosistemas 21, 167–179 (2012).

    Google Scholar 

  • 61.

    García-Cervigón, A. I., Camarero, J. J. & Espinosa, C. I. Intra-annual stem increment patterns and climatic responses in five tree species from an Ecuadorian tropical dry forest. Trees 31, 1057–1067 (2017).

    Article  Google Scholar 

  • 62.

    Jara-Guerrero, A., De la Cruz, M. & Méndez, M. Seed dispersal spectrum of woody species in South Ecuadorian dry forests: environmental correlates and the effect of considering species abundance. Biotropica 43, 722–730 (2011).

    Article  Google Scholar 

  • 63.

    Vázquez, M., Larrea, M. & Ojeda, P. Biodiversidad en los bosques secos del suroccidente de la provincia de Loja (EcoCiencia, 2001).

    Google Scholar 

  • 64.

    Tapia-Armijos, M. F., Homeier, J., Espinosa, C. I., Leuschner, C. & De La Cruz, M. Deforestation and forest fragmentation in south Ecuador since the 1970s-losing a hotspot of biodiversity. PLoS ONE 10, e133701 (2015).

    Google Scholar 

  • 65.

    Cueva Ortiz, J. & Chalán, L. A. Cobertura vegetal y uso actual del suelo de la provincia de Loja. Informe Técnico (2010).

  • 66.

    Kalka, M. & Kalko, E. K. V. Gleaning bats as underestimated predators of herbivorous insects: diet of Micronycteris microtis (Phyllostomidae) in Panama. J. Trop. Ecol. 22, 1–10 (2006).

    Article  Google Scholar 

  • 67.

    Espinosa, C. I., Valle, D., Armijos, D., Jara-Guerrero, A. & Griffith, D. M. Bat abundance data from Zapotillo, Ecuador 2013–2017. Knowl. Netw. Biocomplexity https://doi.org/10.5063/F1765CQJ (2020).

    Article  Google Scholar 

  • 68.

    Barwell, L. J., Isaac, N. J. B. & Kunin, W. E. Measuring β-diversity with species abundance data. J. Anim. Ecol. 84, 1112–1122 (2015).

    PubMed  PubMed Central  Article  Google Scholar 

  • 69.

    Jakob, E. M., Marshall, S. D. & Uetz, G. W. Estimating fitness: a comparison of body condition indices. Oikos 77, 61–67 (1996).

    Article  Google Scholar 

  • 70.

    Reist, J. D. An empirical evaluation of several univariate methods that adjust for size variation in morphometric data. Can. J. Zool. 63, 1429–1439 (1985).

    ADS  Article  Google Scholar 

  • 71.

    Oksanen, J. et al. vegan: Community Ecology Package. R package version 2.5-6. https://CRAN.R-project.org/package=vegan (2019).

  • 72.

    R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/ (2018).


  • Source: Ecology - nature.com

    Growing support for valuing ecosystems will help conserve the planet

    Visualizing a climate-resilient MIT