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The effects of seasonality on host–bat fly ecological networks in a temperate mountain cave

Published online by Cambridge University Press:  12 December 2016

KARINA D. RIVERA-GARCÍA
Affiliation:
Laboratorio de Artropodología y Salud, Escuela de Biología, Benemérita Universidad Autónoma de Puebla. Blvd. Valsequillo y Av. San Claudio. Edificio 112-A, Ciudad Universitaria, Col. Jardines de San Manuel, C. P. 72570, Puebla, México
CÉSAR A. SANDOVAL-RUIZ
Affiliation:
Laboratorio de Artropodología y Salud, Escuela de Biología, Benemérita Universidad Autónoma de Puebla. Blvd. Valsequillo y Av. San Claudio. Edificio 112-A, Ciudad Universitaria, Col. Jardines de San Manuel, C. P. 72570, Puebla, México
ROMEO A. SALDAÑA-VÁZQUEZ*
Affiliation:
Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, Antigua Carretera a Pátzcuaro No. 8701, Col. Ex-Hacienda de San José de La Huerta, C.P. 58190, Morelia Michoacán, México
JORGE E. SCHONDUBE*
Affiliation:
Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, Antigua Carretera a Pátzcuaro No. 8701, Col. Ex-Hacienda de San José de La Huerta, C.P. 58190, Morelia Michoacán, México
*
*Corresponding author: Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, Antigua Carretera a Pátzcuaro No. 8701, Col. Ex-Hacienda de San José de La Huerta, C.P. 58190, Morelia Michoacán, México. Email: romeo.saldana@gmail.com; chon@iies.unam.mx
*Corresponding author: Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, Antigua Carretera a Pátzcuaro No. 8701, Col. Ex-Hacienda de San José de La Huerta, C.P. 58190, Morelia Michoacán, México. Email: romeo.saldana@gmail.com; chon@iies.unam.mx

Summary

Changes in the specialization of parasite–host interactions will be influenced by variations in host species composition. We evaluated this hypothesis by comparing the composition of bats and bat flies within a roost cave over one annual. Five bat and five bat fly species occupied the cave over the course of the study. Bat species composition was 40% different in the rainy season compared with the dry–cold and dry–warm seasons. Despite the incorporation of three new bat species into the cave during the rainy season, bat fly species composition was not affected by seasonality, since the bats that arrived in the rainy season only contributed one new bat fly species at a low prevalence. Bat–bat fly ecological networks were less specialized in the rainy season compared with the dry–cold and dry–warm seasons because of the increase of host overlap among bat fly species during this season. This study suggests that seasonality promote: (1) differences in host species composition, and (2) a reduction in the specialization of host–parasite ecological networks.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Barclay, R. M. R. (1991). Population structure of temperate zone insectivorous bats in relation to foraging behaviour and energy demand. Journal of Animal Ecology 60, 165178.CrossRefGoogle Scholar
Bauer, S. and Hoye, B. J. (2014). Migratory animals couple biodiversity and ecosystem functioning worldwide. Science 344, 12425521242552.Google Scholar
Blüthgen, N. (2010). Why network analysis is often disconnected from community ecology: a critique and an ecologist's guide. Basic and Applied Ecology 11, 185195.Google Scholar
Blüthgen, N. and Klein, A.-M. (2011). Functional complementarity and specialisation: the role of biodiversity in plant–pollinator interactions. Basic and Applied Ecology 12, 282291.Google Scholar
Brito, S. V., Corso, G., Almeida, A. M., Ferreira, F. S., Almeida, W. O., Anjos, L. A., Mesquita, D. O. and Vasconcellos, A. (2014). Phylogeny and micro-habitats utilized by lizards determine the composition of their endoparasites in the semiarid Caatinga of Northeast Brazil. Parasitology Research 113, 39633972.Google Scholar
Carranza, E. (2007). Familia Convolvulaceae. Flora del Bajío y Regiones Adyacentes 151, 1131.Google Scholar
Clark, B. K., Clark, B. S. and Leslie, D. M. (1997). Seasonal variation in use of caves by the endangered Ozark Big-eared Bat (Corynorhinus townsendii ingens) in Oklahoma. The American Midland Naturalist 137, 388392.Google Scholar
Dick, C. W. and Miller, J. A. (2010). Streblidae (Bat Flies). In Manual of Central American Diptera, Vol 2 (ed. Brown, B. V., Borkent, A., Cumming, J. M., Wood, D. M., Woodley, N. E. and Zumbado, M. A.), pp. 12491260. NCR Research Press, Ottawa, Canada.Google Scholar
Dick, C. W. and Patterson, B. D. (2006). Bat flies: obligate ectoparasites of bats. In Micromammals and Macroparasites (ed. Morand, S., Krasnov, B. R. and Poulin, R.), pp. 179194. Springer Japan, Tokyo.Google Scholar
Dick, C. W., Esbérard, C. E. L., Graciolli, G., Bergallo, H. G. and Gettinger, D. (2009). Assessing host specificity of obligate ectoparasites in the absence of dispersal barriers. Parasitology Research 105, 13451349.Google Scholar
Dittmar, K., Dick, C. W., Patterson, B. D., Whiring, M. F. and Gruwell, M. E. (2009). Pupal deposition and ecology of bat flies (Diptera: Streblidae): Trichobius sp. (caecus group) in a Mexican cave habitat. Journal of Parasitology 95, 308314.Google Scholar
Dormann, C. F., Gruber, B. and Fründ, J. (2008). Introducing the bipartite package: analysing ecological networks. R News 8, 811.Google Scholar
Fagir, D. M., Horak, I. G., Ueckermann, E. A., Bennett, N. C. and Lutermann, H. (2015). Ectoparasite diversity in the eastern rock sengis (Elephantulus myurus): the effect of seasonality and host sex. African Zoology 50, 109117.Google Scholar
Ferreyra-García, D. (2016). Efecto del microclima en la ocupación de refugios cavernícolas por murciélagos. Thesis. Universidad Michoacana de San Nicolás de Hidalgo, Morelia, Mexico, 66 p.Google Scholar
Fontaine, C., Guimarães, P. R. Jr., Kéfi, S., Loeuille, N., Memmott, J., van der Putten, W. H., van Veen, F. J. F. and Thébault, E. (2011). The ecological and evolutionary implications of merging different types of networks. Ecology Letters 14, 11701181.Google Scholar
Guerrero, R. (1995). Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) del Nuevo Mundo. III. Los grupos: Dugesii, Dunni y Phyllostomae del género Trichobius Gervais, 1844. Acta Biológica Venezuelica 15, 127.Google Scholar
Herbers, J. M. (1985). Seasonal structuring of a north temperature ant community. Insectes Sociaux 32, 224240.Google Scholar
INEGI (2009) Prontuario de Información Geográfica Municipal de los Estados Unidos Mexicanos. Michoacán de Ocampo, Morelia, Clave geoestadística 16053. http://www3.inegi.org.mx/sistemas/mexicocifras/datos-geograficos/16/16053.pdf Google Scholar
Kunz, T. H. (1982). Ecology of Bats. Plenum Publishing Corporation, New York.Google Scholar
Lareschi, M. and Krasnov, B. R. (2010). Determinants of ectoparasite assemblage structure on rodent hosts from South American marshlands: the effect of host species, locality and season. Medical and Veterinary Entomology 24, 284292.Google Scholar
Legendre, P. and Legendre, L. F. J. (2012). Numerical Ecology. 3rd English Edition. Elsevier, Amsterdam, The Netherlands.Google Scholar
Lumbad, A. S., Vredevoe, L. K. and Taylor, E. N. (2011). Season and sex of host affect intensities of ectoparasites in Western Fence Lizards (Sceloporus occidentalis) on the Central Coast of California. The Southwestern Naturalist 56, 369377.CrossRefGoogle Scholar
Lundberg, J. and McFarlane, D. A. (2015). Microclimate and niche constructionism in tropical bat caves: a case study from Mount Elgon, Kenya. In Caves and Karst Across Time (ed. Feinberg, J., Gao, Y. and Alexander, E. C. J.), pp. 119. Geological Society of America, Boulder, Colorado.Google Scholar
Medellín, R., Arita, H. and Sánchez, O. (2008). Identificación de los murciélagos de México, 2nd Edn. Instituto de Ecología-UNAM & CONABIO, México, d.f.Google Scholar
Mello, M. A. R. (2009). Temporal variation in the organization of a Neotropical assemblage of leaf-nosed bats (Chiroptera: Phyllostomidae). Acta Oecologica 35, 280286.Google Scholar
Mysterud, A., Qviller, L., Meisingset, E. L. and Viljugrein, H. (2016). Parasite load and seasonal migration in red deer. Oecologia 180, 401407.Google Scholar
Obame-Nkoghe, J., Rahola, N., Bourgarel, M., Yangari, P., Prugnolle, F., Maganga, G. D., Leroy, E.-M., Fontenille, D., Ayala, D. and Paupy, C. (2016). Bat flies (Diptera: Nycteribiidae and Streblidae) infesting cave-dwelling bats in Gabon: diversity, dynamics and potential role in Polychromophilus melanipherus transmission. Parasites & Vectors 9, 1.Google Scholar
Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., OHara, R. B., Gavin, L., Simpson, P. S. M., Stevens, M. H. H. and Wagner, H. (2013). Vegan. 2nd Edn. R project.Google Scholar
Pianka, E. R. (1973). The structure of lizard communities. Annual Review of Ecology and Systematics 4, 5374.Google Scholar
Pinheiro, F., Diniz, I. R., Coelho, D. and Bandeira, M. P. S. (2002). Seasonal pattern of insect abundance in the Brazilian cerrado. Austral Ecology 27, 132136.Google Scholar
R Core Team Development (2012). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Ritzi, C. M., Ammerman, L. K., Dixon, M. T. and Richerson, J. V. (2001). Bat ectoparasites from the Trans-Pecos Region of Texas, including notes from Big Bend National Park. Journal of Medical Entomology 38, 400404.Google Scholar
Rojas, D., Vale, Á., Ferrero, V. and Navarro, L. (2011). When did plants become important to leaf-nosed bats? Diversification of feeding habits in the family Phyllostomidae. Molecular Ecology 20, 22172228.Google Scholar
Rzedowski, J. (2006). Vegetación de México. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO), Ciudad de México.Google Scholar
Segura-Trujillo, C. A. and Lidicker, W. Z. (2016). New perspectives on trophic guilds of arthropodivorous bats in North and Central America. Journal of Mammalogy 97, 644654.Google Scholar
Sosa, V. J., Hernández-Salazar, E., Hernández-Conrique, D. and Castro-Luna, A. A. (2008). Murciélagos. In Agroecosistemas cafetaleros de Veracruz: Biodiversidad, manejo y conservación (ed. Manson, R. H., Hernández-Ortiz, V., Gallina, S. and Mehltrter, K.), pp. 181192. Instituto Nacional de Ecología & Instituto de Ecología A.C., Xalapa.Google Scholar
Stoner, K. E. (2005). Phyllostomid bat community structure and abundance in two contrasting tropical dry forests. Biotropica 37, 591599.Google Scholar
Stoner, K. E., O-Salazar, K. A., R-Fernández, R. C. and Quesada, M. (2003). Population dynamics, reproduction, and diet of the lesser long-nosed bat (Leptonycteris curasoae) in Jalisco, Mexico: implications for conservation. Biodiversity and Conservation 12, 357373.Google Scholar
Tlapaya-Romero, L., Horváth, A., Gallina-Tessaro, S., Naranjo, E. and Gómez, B. (2015). Prevalencia y abundancia de moscas parásitas asociadas a una comunidad de murciélagos cavernícolas en La Trinitaria, Chiapas, México. Revista Mexicana de Biodiversidad 86, 377385.Google Scholar
Torres-Flores, J. W., López-Wilchis, R. and Soto-Castruita, A. (2012). Dinámica poblacional, selección de sitios de percha y patrones reproductivos de algunos murciélagos cavernícolas en el oeste de México. Revista de Biología Tropical 60, 13691389.Google Scholar
Wenzel, R. L. (1976). The Streblid bat flies of Venezuela (Diptera: Streblidae). Brigham Young University Science Bulletin, Provo, Utah, USA.Google Scholar
Wenzel, R. L., Tipton, V. J. and Kiewlicz, A. (1966). The Streblid Batflies of Panama (Diptera: Streblidae). In Ectoparasites of Panama (ed. Wenzel, R. L. and Tipton, V. J.), pp. 405675. Field Museum of Natural History, Chicago, Illinois.Google Scholar
Wolda, H. (1988). Insect seasonality: why? Annual Review of Ecology and Systematics 19, 118.Google Scholar
Zarazúa-Carbajal, M., Saldaña-Vázquez, R. A., Sandoval-Ruíz, C. A., Stoner, K. E. and Benítez-Malvido, J. (2016). The specificity of host–bat fly interaction networks across vegetation and seasonal variation. Parasitology Research 115, 40374044.Google Scholar