Keywords
critical habitat
Haematoxylum campechianum
key species
logwood
Chiroptera
especies clave
hábitat crítico
Haematoxylum campechianum
palo de tinte
How to Cite
Abstract
Introduction: The “tintal” is a type of seasonally inundated forest where the dominant species is Haematoxylum campechianum L. Due to its structural characteristics and the conditions of the areas where it develops, it could work as a critical habitat for many animal species. Objective: This work aimed at describing the regional and local diversity of the chiropterofauna inhabiting tintal along different areas in the Southeastern Mexico. Methods: The research was carried out in eight localities with presence of tintal in the states of Campeche and Tabasco, Mexico. In each site, six mist nets were placed during three nights. The observed and expected richness were calculated for each site, as well as the total abundance. Rank-abundance and species accumulation curves were generated. Similarity analyses between localities were performed and correlated with the geographical distance between them. Results: We recorded 25 bat species distributed in five families, where Phyllostomidae was the most represented. Most registered species were insectivorous (44 % of the total), while frugivorous were the most abundant. Frugivorous Artibeus lituratus and A. jamaicensis were the species recorded in a greater number of localities, and Glossophaga soricina was the most abundant. The highest richness of species was registered in Oxpemul (N= 12), while in Las Bodegas we found the lowest (N= 4), although the latter was the third locality with the highest number of individuals. The estimated richness of species for the whole area varied between 29 and 34. The least equitable communities were Las Bodegas and Tres Brazos. The most similar localities in terms of the structure of the community were La Toza and Las Bodegas and, in terms of the species composition, Oxpemul and Atasta. The similarities between the localities were not correlated with geographical proximity. Conclusions: Most of the researched localities were highly anthropized, but the tolerance of several bat species to these landscape modifications has allowed them to make use of such areas. The high abundance of the frugivorous species registered supports that bats may play a key role in the recovery of tree vegetation in altered areas in Southeastern Mexico, and emphasizes the value of the tintal along this area for the conservation of biodiversity.
References
Aguiar, L.M.S., & Marinho-Filho, J. (2007). Bat frugivory in a remnant of Southeastern Brazilian Atlantic forest. Acta Chiropterologica, 9(1), 251-260.
Álvarez-Castañeda, S.T., Álvarez, T., & González-Ruiz, N. (2015). Guía para la identificación de los mamíferos de México en campo y laboratorio. México D. F., México: Centro de Investigaciones Biológicas del Noroeste, S. C. y Asociación Mexicana de Mastozoología, A. C.
Arita, H.T. (1993). Rarity in Neotropical bats: correlations with phylogeny, diet and body mass. Ecological Applications, 3(3), 506-517.
Baird, A.B., Braun, J.K., Mares, M.A., Morales, J.C., Patton, J.C., Tran, C.Q., & Bickham, J.W. (2015). Molecular systematic revision of tree bats (Lasiurini): doubling the native mammals of the Hawaiian Islands. Journal of Mammalogy, 96(6), 1255-1274.
Baker, R.J., Solari, S., Cirranello, A., & Simmons, N.B. (2016). Higher level classification of phyllostomid bats with a summary of DNA synapomorphies. Acta Chiropterologica, 18(1), 1-38.
Batzer, D.P., & Wissinger, S.A. (1996). Ecology of insect communities in Nontidal wetlands. Annual Review of Entomology, 41(1), 75-100.
Barrios-Gómez, K.M., López-Wilchis, R., Díaz-Larrea, J., & Guevara-Chumacero, L.M. (2019). Spatial distribution of bat richness in Mexico at different taxonomic levels: biogeographical and conservation implications. Therya, 10(1), 11-23.
Bobrowiec, P.E.D., & Gribel, R. (2010). Effects of different secondary vegetation types on bat community composition in Central Amazonia, Brazil. Animal Conservation, 13(2), 204-216.
Boivin, N.L., Zeder, M.A., Fuller, D.Q., Crowther, A., Larson, G., Erlandson, J.M., … Petraglia, M.D. (2016). Ecological consequences of human niche construction: Examining long-term anthropogenic shaping of global species distributions. Proceedings of the National Academy of Sciences, 113(23), 6388-6396.
Bueno, J., Alvarez, F., & Santiago, S. (2005). Biodiversidad del Estado de Tabasco (1a edición). México D.F., México: Comisión Nacional para el Conocimiento y Uso de la Biodiversidad e Instituto de Biología.
Cartwright, S.J., Nicoll, M.A.C., Jones, C.G., Tatayah, V., & Norris, K. (2014). Anthropogenic natal environmental effects on life histories in a wild bird population. Current Biology, 24(5), 536-540.
Castro-Luna, A.A., & Galindo-González, J. (2012a). Enriching agroecosystems with fruit-producing tree species favors the abundance and richness of frugivorous and nectarivorous bats in Veracruz, Mexico. Mammalian Biology, 77(1), 32-40.
Castro-Luna, A.A., & Galindo-González, J. (2012b). Seed dispersal by Phyllostomid bats in two contrasting vegetation types in a Mesoamerican Reserve. Acta Chiropterologica, 14(1), 133-142.
Chablé-Vega, M.A., Plasencia-Vázquez, A.H., García-González, A., Ferrer-Sánchez, Y., Riverón-Giró, F.B., & Zamora-Crescencio, P. (2019). Distribución, densidad y estructura dasométrica de Haematoxylum campechianum y Haematoxylum calakmulense en Campeche, México. Ecosistemas y Recursos Agropecuarios, 6(16), 65-77.
Chan, J.K. (2014). The wonderful colors of the hematoxylin-eosin stain in diagnostic surgical pathology. International Journal of Surgical Pathology, 22(1), 12-32.
Chao, A., & Jost, L. (2012). Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology, 93(12), 2533-2547.
Colwell, R.K., Chao, A., Gotelli, N.J., Lin, S.Y., Mao, C.X., Chazdon, R.L., & Longino, J.T. (2012). Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. Journal of Plant Ecology, 5(1), 3-21.
Ellison, A.M. (2010). Partitioning diversity. Ecology, 91(7), 1962-1963.
Escribano-Ávila, G., Lara-Romero, C., Heleno, R., & Traveset, A. (2018). Tropical seed dispersal networks: emerging patterns, biases, and keystone species traits. In W. Dáttilo & V. Rico-Gray (Eds.), Ecological Networks in the Tropics (pp. 93-110). Cham, Switzerland: Springer.
Feinsinger, P. (2003). El Diseño de estudios de campo para la Conservación de la Biodiversidad. Santa Cruz de la Sierra, Bolivia: Editorial FAN.
Fenton, M.B., Acharya, L., Audet, D., Hickey, M.B.C., Merriman, C., Obrist, M.K., … Adkins, B. (1992). Phyllostomid bats (Chiroptera: Phyllostomidae) as indicators of habitat disruption in the Neotropics. Biotropica, 24(3), 440-446.
Fenton, M.B., Whitaker Jr., J.O., Vonhof, M.J., Waterman, J.M., Pedro, W.A., Aguiar, L.M.S., … Zortea, M. (1999). The diet of bats from Southeastern Brazil: the relation to echolocation and foraging behaviour. Revista Brasileira de Zoologia, 16(4), 1081-1085.
Fenton, M.B., & Simmons, N.B. (2014). Bats: a world of science and mystery. Chicago, United States: University of Chicago Press.
Franklin, J.F., & Lindenmayer, D.B. (2009). Importance of matrix habitats in maintaining biological diversity. Proceedings of the National Academy of Sciences, 106(2), 349-350.
Furey, N.M., Mackie, I.J., & Racey, P.A. (2009). The role of ultrasonic bat detectors in improving inventory and monitoring surveys in Vietnamese karst bat assemblages. Current Zoology, 55(5), 327-341.
Galindo-González, J., Guevara, S., & Sosa, V.J. (2000). Bat and bird generated seed rains at isolated trees in pastures in a tropical forest. Conservation Biology, 14(6), 1693-1703.
Galindo-González, J. (2004). Clasificación de los murciélagos de la región de los Tuxtlas, Veracruz, respecto a su respuesta a la fragmentación del hábitat. Acta Zoológica Mexicana (n.s.), 20(2), 239-243.
García-García, J.L., & Santos-Moreno, A. (2014). Efectos de la estructura del paisaje y de la vegetación en la diversidad de murciélagos filostómidos (Chiroptera: Phyllostomidae) de Oaxaca, México. Revista de Biología Tropical, 62(1), 217-239.
García-Morales, R., Chapa-Vargas, L., Galindo-González, J., & Badano, E.I. (2012). Seed dispersal among three different vegetation communities in the Huasteca Region, Mexico, analyzed from bat feces. Acta Chiropterologica, 14(2), 357-367.
Gardner, T.A., Barlow, J., Chazdon, R., Ewers, R.M., Harvey, C.A., Peres, C.A., & Sodhi, N.S. (2009). Prospects for tropical forest biodiversity in a human-modified world. Ecology Letters, 12(6), 561-582.
Gonçalves, F., Fischer, E., & Dirzo, R. (2017). Forest conversion to cattle ranching differentially affects taxonomic and functional groups of Neotropical bats. Biological Conservation, 210, 343-348.
González Marín, R.M., Gallina, S., Mandujano, S., & Weber, M. (2008). Densidad y distribución de ungulados silvestres en la reserva ecológica El Edén, Quintana Roo, México. Acta Zoológica Mexicana (nueva serie), 24(1), 73-93.
González-Ruiz, N., Ramírez-Pulido, J., & Arroyo-Cabrales, J. (2011). A new species of mastiff bat (Chiroptera: Molossidae: Molossus) from Mexico. Mammalian Biology, 76(4), 461-469.
Gotelli, N.N., & Colwell, R.K. (2001). Quantifying biodiversity: procedures and pitfalls in measurement and comparison of species richness. Ecology Letters, 4, 379-391.
Gotelli, N.N., & Colwell, R.K. (2011). Estimating species richness. In A. Magurran & B.J. McGill (Eds.), Biological Diversity frontiers in measurement and assessment (pp. 39-54). New York, US: Oxford University Press.
Heck, K.L., van Belle, G., & Simberloff, D. (1975). Explicit calculation of the rarefaction diversity measurement and the determination of sufficient sample size. Ecology, 56, 1459-1461.
Henry, M., Cossonb, J., & Pons, J. (2007). Abundance may be a misleading indicator of fragmentation-sensitivity: The case of fig-eating bats. Biological Conservation, 139(3-4), 462-467.
Hill, M.O. (1973). Diversity and evenness: a unifying notation and its consequences. Ecology, 54(2), 427-432.
Hobbs, R.J., Higgs, E., & Harris, J.A. (2009). Novel ecosystems: implications for conservation and restoration. Trends in Ecology & Evolution, 24(11), 599-605.
Hsieh, T.C., Ma, K.H., Chao, A., & McInerny, G. (2016). iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods in Ecology and Evolution, 7(12), 1451-1456. DOI: 10.1111/2041-210X.12613
Hurlbert, S.H. (1971). The nonconcept of species diversity: a critique and alternative parameters. Ecology, 52(4), 577-586.
Jost, L. (2006). Entropy and diversity. Oikos, 113(2), 363-375.
Kalka, M.B., Smith, A.R., & Kalko, E.K.V. (2008). Bats limit arthropods and herbivory in a Tropical Forest. Science, 320(5872), 71.
Kindt, R., & Coe, R. (2005). Tree diversity analysis. A manual and software for common statistical methods for ecological and biodiversity studies. Nairobi, Kenya: World Agroforestry Centre (ICRAF).
Kraker-Castañeda, C., & Echeverría-Tello, J.L. (2012). Riqueza de especies y variabilidad trófica de murciélagos en zonas de riesgo de rabia de origen silvestre en Izabal, Guatemala. Therya, 3(1), 87-99.
Lepczyk, C.A., Aronson, M.F.J., Evans, K.L., Goddard, M.A., Lerman, S.B., & Macivor, J.S. (2017). Biodiversity in the city: fundamental questions for understanding the ecology of urban green spaces for biodiversity conservation. BioScience, 67(9), 799-807.
Lomolino, M.V. (1984). Mammalian island biogeography: effects of area, isolation and vagility. Oecologia, 61(3), 376-382.
MacSwiney, M.C., Clarke, F.M., & Racey, P.A. (2008). What you see is not what you get: the role of ultrasonic detectors in increasing inventory completeness in Neotropical bat assemblages. Journal of Applied Ecology, 45, 1364-1371.
Manly, B.F.J. (1986). Multivariate statistical methods: a primer. London, United Kingdom: Chapman & Hall.
Marinho-Filho, J.S. (1991). The coexistence of two frugivorous bat species and the phenology of their food plants in Brazil. Journal of Tropical Ecology, 7, 59-67.
Medellín, R.A., Equihua, M., & Amín, M.A. (2000). Bat diversity and abundance as indicators of disturbance in Neotropical rainforest. Conservation Biology, 14(6), 1666-1675.
Medellín, R.A., Arita, H.T., & Sánchez, H.O. (2008). Identificación de los Murciélagos de México. Clave de Campo (2ª. Ed.). México, D. F., México: Instituto de Ecología y Universidad Nacional Autónoma de México.
Meyer, C.F.J., & Kalko, E.K.V. (2008) Bat assemblages on Neotropical land-bridge islands: nested subsets and null model analyses of species co-occurrence patterns. Diversity and Distributions, 14, 644-654.
Meyer, C.F.J., Aguiar, L.M.S., Aguirre, L.F., Baumgarten, J., Clarke, F.M., Cosson, J.F., … Kalko, E. K. V. (2011). Accounting for detectability improves estimates of species richness in tropical bat surveys. Journal of Applied Ecology, 48(3), 777-787.
Montiel, S., Estrada, A., & León, P. (2006). Bat assemblages in a naturally fragmented ecosystem in the Yucatan Peninsula, Mexico: species richness, diversity and spatio-temporal dynamics. Journal of Tropical Ecology, 22, 267-276.
Moreno, C.E., Arita, H.T., & Solis, L. (2006). Morphological assembly mechanisms in Neotropical bat assemblages and ensembles within a landscape. Oecologia, 149, 133-140.
Moreno, C.E., Barragán, F., Pineda, E., & Pavón, N.P. (2011). Reanálisis de la diversidad alfa: alternativas para interpretar y comparar información sobre comunidades ecológicas. Revista Mexicana de Biodiversidad, 82(4), 1249-1261.
Morrison, D.W. (1978). Foraging ecology and energetics of the frugivorous bat Artibeus jamaicensis. Ecology, 59, 716-723.
Muñoz-Jiménez, O., Villegas-Patraca, R., Mac Swiney, M.C., & López-Acosta, J.C. (2016). Importancia de los elementos de un paisaje antropizado para la retención de diversidad de murciélagos en el Istmo de Tehuantepec, Oaxaca, México. En A. Ramírez-Bautista & R. Pineda-López (Eds.), Fauna nativa en ambientes antropizados (pp. 115-122). Querétaro, México: Consejo Nacional de Ciencia y Tecnología, Universidad Autónoma de Querétaro.
Muscarella, R., & Fleming, T.H. (2007). The Role of frugivorous bats in Tropical Forest succession. Biological Reviews, 82(4), 573-590.
Oksanen, J., Guillaume Blanchet, F., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., … Wagner, H. (2017). Vegan: Community Ecology Package. R package version 2.4-3. Retrieved from https://CRAN.R-project.org/package=vegan
Olea-Wagner, A., Lorenzo, C., Naranjo, E., Ortiz, D., & León-Paniagua, L. (2007). Diversidad de frutos que consumen tres especies de murciélagos (Chiroptera: Phyllostomidae) en la selva Lacandona, Chiapas, México. Revista Mexicana de Biodiversidad, 78(1), 191-200.
Olímpio, A.P.M., Ventura, M.C.S., Mascarenhas, M.J.O., Nascimento, D.C., Andrade, F.A.G., Fraga, E.C., & Barros, M.C. (2016). Bat fauna of the Cerrado savanna of Eastern Maranhão, Brazil, with new species occurrences. Biota Neotropica, 16(3), e20150089. DOI: http://dx.doi.org/10.1590/1676-0611-BN-2015-0089
Oporto, S., Arriaga-Weiss, S.L., & Castro-Luna, A.A. (2015). Diversidad y composición de murciélagos frugívoros en bosques secundarios de Tabasco, México. Revista Mexicana de Biodiversidad, 86(2), 431-439.
Pinto, N., & Keitt, T.H. (2008). Scale-dependent responses to forest cover displayed by frugivore bats. Oikos, 117, 1725-1731.
Plasencia-Vázquez, A.H., Villegas, P., Ferrer-Sánchez, Y., & Zamora-Crescencio, P. (2017). Distribución histórica de las especies del género Haematoxylum (Leguminosae) en la Península de Yucatán, México, basada en ejemplares de herbario. Acta Botánica Mexicana, 119, 51-68.
R Core Team. (2017). R: A Language and Environment for Statistical Computing. Vienna, Austria: The R Development Core Team. Retrieved from https://www.R-project.org
Ramírez-Pulido, J., González-Ruiz, N., Gardner, A.L., & Arroyo-Cabrales, J. (2014). List of recent land mammals of Mexico, 2014. Special Publications of the Museum of Texas Tech University, 63, 1-69.
Reyna-Hurtado, R., O’Farrill, G., Sima, D., Andrade, M., Padilla, A., & Sosa, L. (2010). Las aguadas de Calakmul, reservorios de fauna silvestre y de la riqueza natural de México. Biodiversitas, 93, 1-6.
Santiago-Alarcón, D. (2003). Avifauna de dos comunidades de selva baja espinosa de tinto (Haematoxylum campechianum) de la Reserva de la Biosfera Pantanos de Centla. Ornitología Neotropical, 14, 515-530.
Santos, T., & Tellería, J.L. (2006). Pérdida y fragmentación del hábitat: efecto sobre la conservación de las especies. Ecosistemas, 15(2), 3-12.
Santos-Moreno, A., Ruiz Velásquez, E., & Sánchez Martínez, A. (2010). Efecto de la intensidad de la luz lunar y de la velocidad del viento en la actividad de murciélagos filostómidos de Mena Nizanda, Oaxaca, México. Revista Mexicana de Biodiversidad, 81(3), 839-845.
Schulze, M.D., Seavy, N.E., & Whitacre, D.F. (2000). A comparison of the phyllostomid bat assemblages in undisturbed neotropical forest and in forest fragments of a slash-and-burn farming mosaic in Petén, Guatemala. Biotropica, 32(1), 174-184.
Simmons, N.B., & Voss, R.S. (1998). The mammals of Paracou, French Guiana: A Neotropical lowland rainforest fauna. Part 1. Bats. Bulletin of the American Museum of Natural History, 237, 1-219.
Tun-Dzul, F.J., Vester, H., Durán-García, R., & Schmook, B. (2008). Estructura arbórea y variabilidad temporal del NDVI en los "bajos inundables" de la Península de Yucatán, México. Polibotánica, 25, 69-90.
Turgeon, G., Vander Wal, E., Massé, A., & Pelletiera, F. (2015). Born to be wild? Response of an urban exploiter to human-modified environment and fluctuating weather conditions. Canadian Journal of Zoology, 93(4), 315-322.
Vargas-Contreras, J.A., Escalona-Segura, G., Arroyo-Cabrales, J., Rendón-von Osten, J., & Navarro, L. (2012). Conservación de Murciélagos en Campeche. Therya, 3(1), 53-66.
Wickramasinghe, L.P., Harris, S., Jones, G., & Vaughan, N. (2003). Bat activity and species richness on organic and conventional farms: impact of agricultural intensification. Journal of Applied Ecology, 40(6), 984-993.
Willig, M., Patterson, B., & Stevens, R. (2003). Patterns of range size, richness, and body size. In T.H. Kunz & M. Brock Fenton (Eds.), Bat Ecology (pp. 580-621). Chicago, US: University of Chicago Press.
Zamora-Crescencio, P., Gutiérrez-Báez, C., Folan, W.J., Domínguez-Carrasco, M.R., Villegas, P., Cabrera-Mis, G., Castro-Angulo, C.M., & Carballo, J.C. (2012). La vegetación leñosa del sitio arqueológico de Oxpemul, municipio de Calakmul, Campeche, México. Polibotánica, 33, 131-150.
Zimmerman, J.K., & Olmsted, I.C. (1992). Host tree utilization by vascular epiphytes in a seasonally inundated forest (Tintal) in Mexico. Biotropica, 24(3), 402-407.
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