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Importance of riparian habitat for frugivorous bats in a tropical dry forest in western Mexico

Published online by Cambridge University Press:  20 December 2016

Mariana Zarazúa-Carbajal
Affiliation:
Instituto de Investigaciones en Ecosistemas y Sustentabilidad UNAM. Antigua Carretera a Pátzcuaro No. 8701 Col. Ex Hacienda de San José de La Huerta C.P. 58190 Morelia Michoacán, México
Julieta Benítez-Malvido
Affiliation:
Instituto de Investigaciones en Ecosistemas y Sustentabilidad UNAM. Antigua Carretera a Pátzcuaro No. 8701 Col. Ex Hacienda de San José de La Huerta C.P. 58190 Morelia Michoacán, México
Kathryn E. Stoner
Affiliation:
Instituto de Investigaciones en Ecosistemas y Sustentabilidad UNAM. Antigua Carretera a Pátzcuaro No. 8701 Col. Ex Hacienda de San José de La Huerta C.P. 58190 Morelia Michoacán, México

Abstract:

Riparian forests (RF) provide shelter, feeding resources and commuting areas and are fundamental for local fauna during long drought periods in tropical dry forests. Nevertheless, information regarding vertebrate ecology in tropical RF is scarce. The studies of bats in riparian habitats have been mostly focused on insectivorous assemblages in non-tropical regions. We contrasted the occurrence of frugivorous bats between RF and upland dry forest (UDF) in a Neotropical dry forest region and evaluated how vegetation structure modulates frugivorous bat presence and abundance. We sampled bat ensembles and vegetation structure in three UDF and three RF sites in Jalisco, Mexico. Bat ensembles and populations were analysed with generalized linear models, including as independent factors: (1) habitat and (2) vegetation attributes. In 72 nights we captured 840 bats belonging to seven species. No effect of habitat type or vegetation structure on species richness was found, but habitat type did affect bat species composition and abundance. Moreover, vegetation structural traits affected frugivorous bat abundance. Frugivore abundance was higher in RF than in UDF probably because RF provides greater resources and more roosting sites. Riparian forests also present more canopy cover and accessible flight spaces. Our results support the importance of RF for frugivorous bats in terms of abundance and composition. Additionally, the lack of differences in species richness between UDF and RF highlights the importance of both habitats for maintaining frugivorous bats, as well as the related ecosystem processes and services in tropical dry forest landscapes.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

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References

LITERATURE CITED

AUGUST, P. V. 1983. The role of habitat complexity and heterogeneity in structuring tropical mammal communities. Ecology 64:14951507.CrossRefGoogle Scholar
AVILA-CABADILLA, L. D., STONER, K. E., HENRY, M. & ALVAREZ-AÑORVE, M. Y. 2009. Composition, structure and diversity of phyllostomid bat assemblages in different successional stages of a tropical dry forest. Forest Ecology and Management 258:986996.CrossRefGoogle Scholar
AVILA-CABADILLA, L. D., SÁNCHEZ-AZOFEIFA, G. A., STONER, K. E., ALVAREZ-AÑORVE, M. Y., QUESADA, M. & PORTILLO-QUINTERO, C. A. 2012. Local and landscape factors determining occurrence of phyllostomid bats in tropical secondary forests. PLoS ONE 7: e35228.CrossRefGoogle ScholarPubMed
BULLOCK, S. H. & SOLIS-MAGALLANES, A. S. 1990. Phenology of canopy trees of a tropical deciduous forest in Mexico. Biotropica 22:2235.Google Scholar
CARAS, T. & KORINE, C. 2009. Effect of vegetation density on the use of trails by bats in a secondary tropical rain forest. Journal of Tropical Ecology 25:97101.Google Scholar
CASTRO-LUNA, A. A., SOSA, V. J. & CASTILLO-CAMPOS, G. 2007. Bat diversity and abundance associated with the degree of secondary succession in a tropical forest mosaic in south-eastern Mexico. Animal Conservation 10:219228.Google Scholar
CHÁVEZ, C. & CEBALLOS, G. 2001. Diversidad y abundancia de murciélagos en selvas secas de estacionalidad contrastante en el oeste de México. Revista Mexicana de Mastozoología 5:2744.CrossRefGoogle Scholar
CRAWLEY, M. J. 2007. The R book. Wiley, Chichester. 942 pp.Google Scholar
DE LA PEÑA-CUÉLLAR, E., BENÍTEZ-MALVIDO, J., AVILA-CABADILLA, L. D., MARTÍNEZ-RAMOS, M. & ESTRADA, A. 2015. Structure and diversity of phyllostomid bat assemblages on riparian corridors in a human-dominated tropical landscape. Ecology and Evolution 5:903913.Google Scholar
DURÁN, E., BALVANERA, P., LOTT, E. J., SEGURA, G., ROSAS, E., ISLAS, A. & FRANCO, M. 2002. Composición, estructura y dinámica de la vegetación. Pp. 443472 in Noguera, F. A., Vega, J. & Quesada, M. (eds.). Historia natural de Chamela. Instituto de Biología Universidad Nacional Autónoma de México, Distrito Federal.Google Scholar
ESTRADA, A. & COATES-ESTRADA, R. 2001. Bat species richness in live fences and in corridors of residual rain forest vegetation at Los Tuxtlas, Mexico. Ecography 24:94102.CrossRefGoogle Scholar
ESTRADA, A., COATES-ESTRADA, R. & MERITT, D. 1993. Bats species richness and abundance in tropical rain forest fragments and in agricultural habitats at Los Tuxtlas, Mexico. Ecography 16:309318.Google Scholar
EVELYN, M. J. & STYLES, D. A. 2003. Roosting requirements of two frugivorous bats (Sturnira lilium and Artibeus intermedius) in fragmented Neotropical forest. Biotropica 35:405418.Google Scholar
FAUTH, J. E., BERNARDO, J., CAMARA, M., RESETARITS, W. J., VAN BUSKIRK, J. & MCCOLLUM, S. A. 1996. Simplifying the jargon of community ecology: a conceptual approach. American Naturalist 147:282286.Google Scholar
FEINSINGER, P. 2001. Designing field studies for biodiversity conservation. Island Press, Washington, DC. 212 pp.Google Scholar
FENTON, M. B. & KUNZ, T. H. 1977. Movements and behavior. Pp. 351364 in Baker, R. J., Jones, K. & Carter, D. C. (eds.). Biology of bats of the New World family Phyllostomidae, part 2. Texas Tech. University Press, Lubbock.Google Scholar
FENTON, M. B., ACHARYA, L. D., AUDET, D., HICKEY, M. B. C., MERRIMAN, C., OBRIST, M. K., SYME, D. M. & ADKINS, B. 1992. Phyllostomid bats (Chiroptera: Phyllostomidae) as indicators of habitat disruptions in the Neotropics. Biotropica 24:440446.CrossRefGoogle Scholar
FRANKLIN, J. F. 1992. Scientific basis for new perspectives in forests and streams. Pp. 2572 in Naiman, R.J. (ed.). Watershed management: balancing sustainability and environmental change. Springer Verlag, New York.CrossRefGoogle Scholar
FUKUI, D., MURAKAMI, M., NAKANO, S. & AOI, T. 2006. Effect of emergent aquatic insects on bat foraging in a riparian forest. Journal of Animal Ecology 75:12521258.CrossRefGoogle Scholar
GALINDO-GONZÁLEZ, J. & SOSA, V. J. 2003. Frugivorous bats in isolated trees and riparian vegetation associated with human-made pastures in a fragmented tropical landscape. The Southern Naturalist 48:579589.2.0.CO;2>CrossRefGoogle Scholar
GENTRY, A. H. 1982. Patterns of Neotropical plant species diversity. Evolutionary Biology 15:184.Google Scholar
GRINDAL, S. D., MORISSETTE, J. L. & BRIGHAM, R. M. 1999. Concentration of bat activity in riparian habitats over an elevational gradient. Canadian Journal of Zoology 77:972977.Google Scholar
GRISCOM, H. P., KALKO, E. K. V. & ASHTON, M. S. 2007. Frugivory by small vertebrates within a deforested, dry tropical region of Central America. Biotropica 39:278282.Google Scholar
HOFSTEDE, H. M. & FENTON, M. B. 2005. Relationships between roost preferences, ectoparasite density, and grooming behavior of Neotropical bats. Journal of Zoology (London) 266:333340.Google Scholar
HOLDRIDGE, L. R. 1967. Life zone ecology. Tropical Science Center, San Jose. 206 pp.Google Scholar
HOLLOWAY, G. L. & BARCLAY, R. M. 2000. Importance of prairie riparian zones to bats in southeastern Alberta. Ecoscience 7:115122.Google Scholar
JANZEN, D. H. & WILSON, D. E. 1983. Mammals. Pp. 426442 in Janzen, D. H. (ed.). Costa Rican natural history. University of Chicago Press, Chicago.CrossRefGoogle Scholar
KALKO, E. K. & HANDLEY, C. O. 2001. Neotropical bats in the canopy: diversity, community structure, and implications for conservation. Plant Ecology 153:319333.Google Scholar
KEUROGHLIAN, A. & EATON, D. P. 2008. Importance of rare habitats and riparian zones in a tropical forest fragment: preferential use by Tayassu pecari, a wide-ranging frugivore. Journal of Zoology 275:283293.Google Scholar
KINDT, R. & COE, R. 2005. Tree diversity analysis. World Agroforestry Center, Nairobi. 196 pp.Google Scholar
KLINBEIL, B. T. & WILLIG, M. R. 2010. Seasonal differences in population-, ensemble- and community-level responses of bats to landscape structure in Amazonia. Oikos 119:16541664.Google Scholar
LEHMKUHL, J. F., PEFFER, R. D. & O'CONNELL, M. A. 2008. Riparian and upland small mammals on the East slope of the Cascade Range, Washington. Northwest Science 82:94107.CrossRefGoogle Scholar
LLOYD, A., LAW, B. & GOLDINGAY, R. 2006. Bat activity on riparian zones and upper slopes in Australian timber production forests and the effectiveness of riparian buffers. Biological Conservation 129:207220.Google Scholar
LOBOVA, T. A., GEISELMAN, C. K. & MORI, S. A. 2009. Seed dispersal by bats in the Neotropics. The New York Botanical Garden Press, New York. 471 pp.Google Scholar
LOTT, E. J. & ATKINSON, T. H. 2002. Biodiversidad y fitogeografía de Chamela-Cuixmala, Jalisco. Pp. 83136 in Noguera, F. A., Vega, J. & Quesada, M. (eds.). Historia natural de Chamela. Instituto de Biología, Universidad Nacional Autónoma de México, Distrito Federal.Google Scholar
LOTT, E. J., BULLOCK, S. H. & SOLIS-MAGALLANES, J. A. 1987. Floristic diversity and structure of Upland and Arroyo Forests of Coastal Jalisco. Biotropica 19:228235.Google Scholar
MARQUES, J. T., RAMOS PEREIRA, M. J., MARQUES, T. A., SANTOS, C. D., SANTANA, J., BEJA, P. & PALMEIRIM, J. M. 2013. Optimizing sampling design to deal with mist-net avoidance in Amazonian birds and bats. PLoS ONE 8: e74505.Google Scholar
MCCUNE, B. & GRACE, J. B. 2002. Analysis of ecological communities. MjM Software Design, Gleneden Beach. 300 pp.Google Scholar
MEDELLÍN, R. A., EQUIHUA, M. & AMIN, M. A. 2000. Bat diversity and abundance as indicators of disturbance in Neotropical rainforests. Conservation Biology 14:16661675.Google Scholar
MEDELLÍN, R. A., ARITA, H. T. & SÁNCHEZ, O. 2008. Identificación de los murciélagos de México, clave de campo. Instituto de Ecología, Universidad Nacional Autónoma de México, México. 78 pp.Google Scholar
MEDINA, A., HARVEY, C. A., SÁNCHEZ-MERLO, D., VÍLCHEZ, S. & HERNÁNDEZ, B. 2007. Bat diversity and movement in an agricultural landscape in Matiguás, Nicaragua. Biotropica 39:120128.Google Scholar
MILAKOVIC, B., PARKER, K. L., GUSTINE, D. D., LAY, R. J., WALKER, A. B. D. & GILLINGHAM, M. P. 2011. Habitat selection by a focal predator Canis lupus in a multiprey ecosystem of the northern Rockies. Journal of Mammalogy 92:568582.CrossRefGoogle Scholar
MONADJEM, A. & RESIDE, A. 2008. The influence of riparian vegetation on the distribution and abundance of bats in African savanna. Acta Chiropterologica 10:339348.CrossRefGoogle Scholar
MORENO, C. & HALFFTER, G. 2000. Assessing the completeness of bat biodiversity inventories using species accumulation curves. Journal of Applied Ecology 37:149158.Google Scholar
MORRISON, D. W. & HANDLEY, C. O. 1991. Roosting behavior. Pp. 131135 in Handley, C. O., Wilson, D. E. & Gardner, A. L. (eds). Demography and natural history of the Common Fruit Bat, Artibeus jamaicensis, on Barro Colorado Island, Panama. Smithsonian Institution Press Washington, DC.Google Scholar
NAIMAN, R. J., DÉCAMPS, H. & MCCLAIN, M. E. 2005. Riparia: ecology, conservation and management of streamside communities. Elsevier Academic Press, San Diego. 448 pp.Google Scholar
NATIONAL RESEARCH COUNCIL. 2002. Riparian areas: functions and strategies for management. The National Academies Press, Washington, DC. 444 pp.Google Scholar
NÚÑEZ-PEREZ, R. 2006. Área de actividad, patrones de actividad y movimiento del jaguar (Panthera onca) y del puma (Puma concolor) en la Reserva de la Biosfera Chamela-Cuixmala, Jalisco. Master's thesis, Universidad Nacional Autónoma de México. 121 pp.Google Scholar
OBER, H. K. & HAYES, J. P. 2008. Influence of vegetation on bat use of riparian areas at multiple spatial scales. Journal of Wildlife Management 72:396404.CrossRefGoogle Scholar
ORTIZ-RAMÍREZ, D., LORENZO, C., NARAJO, N. & LEÓN-PANIAGUA, L. 2006. Roost selection by three frugivorous bats Chiroptera: Phyllostomidae in the Lacandon Forest, Chiapas, Mexico. Revista Mexicana de Biodiversidad 77:261270.Google Scholar
RAUTENBACH, I. L., FENTON, M. B. & WHITING, M. J. 1996. Bats in riverine forests and woodlands: a latitudinal transect in southern Africa. Canadian Journal of Zoology 74:312322.Google Scholar
SABO, J. L., SPONSELLER, R., DIXON, M., GADE, K., HARMS, T., HEFFERNAN, J., JANI, A., KATZ, G., WOYKAN, C., WATTS, J. & WELTER, J. 2005. Riparian zones increase regional species richness by harboring different, not more, species. Ecology 86:5662.Google Scholar
SALVADOR, S., CLAVERO, M. & PITMAN, R. L. 2011. Large mammal species richness and habitat use in an upper Amazonian forest used for ecotourism. Mammalian Biology 76:115123.Google Scholar
SÁNCHEZ-AZOFEIFA, G. A., QUESADA, M., RODRÍGUEZ, J. P., NASSAR, J. M., STONER, K. E., CASTILLO, A., GARVIN, T., ZENT, E. L., CALVO-ALVARADO, J. C., KALACSKA, M., FAJARDO, L., GAMMON, J. A. & CUEVAS-REYES, P. 2005. Research priorities for Neotropical dry forests. Biotropica 37:477485.Google Scholar
SÁNCHEZ-AZOFEIFA, G. A., QUESADA, M., CUEVAS-REYES, P., CASTILLO, A. & SÁNCHEZ-MONTOYA, G. 2009. Land cover and conservation in the area of influence of the Chamela-Cuixmala Biosphere Reserve, Mexico. Forest Ecology and Management 258:907912.Google Scholar
SEGURA, G., BALVANERA, P., DURÁN, E. & PEREZ, A. 2003. Tree community structure and stem mortality along a water availability gradient in a Mexican tropical dry forest. Plant Ecology 169:259271.Google Scholar
SILKES, R. S. & GANNON, W. L., ANIMAL CARE AND USE COMMITTEE OF THE AMERICAN SOCIETY OF MAMMALOGISTS. 2011. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. Journal of Mammalogy 92:235253.Google Scholar
SIMMONS, N. B. 2005. Order Chiroptera. Pp. 312529 in Wilson, D. E. & Reeder, D. M. (eds). Mammal species of the world: a taxonomic and geographic reference. Johns Hopkins University Press, Baltimore.Google Scholar
SOYKAN, C. U., BRAND, L. A., RIES, L., STROMBERG, J. C., HASS, C., SIMMONS, D. A. JR., PATTERSON, W. J. D. & SABO, J. L. 2012. Multitaxonomic diversity patterns along a desert riparian – upland gradient. PLoS ONE 7: e28235.Google Scholar
STONER, K. E. 2002. Murciélagos nectarívoros y frugívoros del bosque caducifolio de la Reserva de la Biósfera Chamela-Cuixmala. Pp. 379395 in Noguera, F.A., Vega, J. & Quesada, M. (eds). Historia natural de Chamela. Instituto de Biología, Universidad Nacional Autónoma de México, Distrito Federal.Google Scholar
STONER, K. E. & TIMM, R. M. 2011. Seasonally dry tropical forest mammals: adaptations and seasonal patterns. Pp. 85106 in Dirzo, R., Young, H. S., Mooney, H. A. & Ceballos, G. (eds). Seasonally dry tropical forests: conservation and ecology. Island Press, Washington, DC.CrossRefGoogle Scholar
STONER, K. E., O-SALAZAR, K. A., FERNÁNDEZ, R. C. & QUESADA, M. 2003. Population dynamics, reproduction, and diet of the lesser long-nosed bat Leptonycteris curasoae in Jalisco, México: implications for conservation. Biodiversity and Conservation 12:357373.Google Scholar
TIMM, R. M. & LAVAL, R. K. 1998. A field key to the bats of Costa Rica. Occasional Publication Series, University of Kansas Center of Latin American Studies 22:130.Google Scholar
VALENZUELA, D. & CEBALLOS, G. 2000. Habitat selection, home range, and activity of the White-nosed coati Nasua narica in a Mexican tropical dry forest. Journal of Mammalogy 81:810819.Google Scholar
VARGAS-CONTRERAS, J., MEDELLÍN, R. A., ESCALONA-SEGURA, G. & INTERIÁN-SOSA, L. 2009. Vegetation complexity and bat-plant dispersal in Calakmul, Mexico. Journal of Natural History 43:219243.Google Scholar
WILLIAMS, J. A., O'FARRELL, M. J. & RIDDLE, B. R. 2006. Habitat use by bats in a riparian corridor of the Mojave Desert in Southern Nevada. Journal of Mammalogy 87:11451153.Google Scholar