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Seasons influence acarine infestation in bats from tropical dry forests of Western Mexico

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Abstract

Bats are parasitized by a wide variety of ectoparasite groups, including mites and ticks (Acari). In temperate regions, infestation patterns are regulated by the host reproductive cycle, which results in parasite reproduction peaking during bat pregnancy and lactation, and declines in winter, when bats are hibernating. The host-parasite dynamics in tropical bat assemblages are less known, and might show more complexity due to the importance of biotic factors over abiotic ones in influencing community dynamics. In this study, we test the hypothesis that parasite fluctuations across the year will peak in the wet season in a tropical dry forest area, when food resources for bats are more abundant and parasites would be favoured accordingly. To test this hypothesis, we assessed the presence and abundance of mites and ticks in one nectarivorous - Leptonycteris yerbabuenae (Martínez and Villa-R) - and three insectivorous - Pteronotus davyi (Gray), P. parnellii (Gray) and P. personatus (Wagner) - bat species. We collected 3005 acarine specimens belonging to 18 species and 12 genera from 412 bats. We did not find significant seasonal variation in most cases. However, the prevalence, mean abundance and intensity of eight acarine species were significantly higher during one of the seasons. In P. parnellii, percentage of infested bats, mean number of acarines per examined individual host, and mean number of acarines per infested individual host were significantly higher during the wet season. However, the percentage of infested individuals of L. yerbabuenae was higher during the dry season, while for P. davyi and P. personatus it was almost the same in both seasons. The actual number of acarine species was also significantly higher during the wet season in the three Pteronotus species whereas in L. yerbabuenae this was higher in the dry season. Our study contributes to shed light on little known host-parasite relationships in tropical forests, highlights the relevance of biotic and abiotic factors on parasitic interactions and provides information on acarine ecology in relation to seasonality in a tropical dry forest.

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References

  • Altizer, S., Harvell, D., Friedle, E., 2003. Rapid evolutionary dynamics and disease threats to biodiversity. Trends Ecol. Evol. 18, 589–596.

    Article  Google Scholar 

  • Anderson, R.M., May, R.M., 1978. Regulation and stability of host-parasite population interactions I. Regulatory processes. J. Anim. Ecol. 47, 219–247.

    Article  Google Scholar 

  • Anderson, R.M., May, R.M., 1991. Infectious Diseases of Humans. Oxford Science Publications, Great Britain.

    Google Scholar 

  • Andresen, E., 2005. Effects of season and vegetation type on community organization of dung beetles in a tropical dry forest. Biotropica. 37, 291–300.

    Article  Google Scholar 

  • Arneberg, P., Skorping, A., Grenfell, B., Read, A.F., 1998. Host densities as determinants of abundance in parasite communities. Proc. R. Soc. Lond. B Biol. Sci. 265, 1283–1289.

    Article  Google Scholar 

  • Brennan, J.M., 1962. Four new chiggers from Mexico. J. Parasitol. 48, 618–620.

    Article  CAS  PubMed  Google Scholar 

  • Brennan, J.M., 1967. New Record of Chigger From The West Indies. Studies on The Fauna Of Curaçao And Other Caribbean Islands, 24., pp. 146–156.

    Google Scholar 

  • Brennan, J.M., Goff, M.L., 1977. Keys to the genera of chiggers of the Western Hemisphere (Acarina: Trombiculidae). J. Parasitol. 63, 554–566.

    Article  CAS  PubMed  Google Scholar 

  • Bullock, S.H., 1995. Plant reproduction in neotropical dry forest. In: Bullock, S.H., Mooney, H.A., Medina, E. (Eds.), Seasonally Dry Tropical Forests. Cambridge University Press, Cambridge, United Kingdom, pp. 277–303.

    Chapter  Google Scholar 

  • Burtt, E.H., Chow, W., Babbit, G.A., 1991. Occurrence and demography of mites of tree swallow, house wren and eastern bluebird nests. In: Loye, J.E., Zuk, M. (Eds.), Bird-Parasite Interactions: Ecology, Evolution and Behavior. Oxford University Press, Oxford, United Kingdom, pp. 104–122.

    Google Scholar 

  • Castano-Meneses, G., 2014. Trophic guild structure of a canopy ants community in a Mexican tropical deciduous forest. Sociobiology 61, 35–42.

    Article  Google Scholar 

  • Ceballos, G., Fleming, T.H., Chavez, C., Nassar, J., 1997. Population dynamics of Leptonyctens curasoae (Chiroptera: Phyllostonidae) in Jalisco, Mexico. J. Mammal. 78, 1220–1230.

    Article  Google Scholar 

  • Christe, P., Arlettaz, R., Vogel, P., 2000. Variation in intensity of a parasitic mite (Spinturnix myotis) in relation to the reproductive cycle and immunocompetence of its bat host (Myotis myotis). Ecol. Lett. 3, 207–212.

    Article  Google Scholar 

  • Colín-Martínez, H., Morales-Malacara, J.B., García-Estrada, C., 2018. Epizoic fauna survey on phyllostomid bats (Chiroptera: Phyllostomidae) in a shaded coffee plantation of southeastern Chiapas, Mexico. J. Med. Entomol. 55, 172–182.

    Article  PubMed  Google Scholar 

  • Daniel, M., Stekolnikov, A.A., 2003. Chigger mites (Acari: Trombiculidae) new to the fauna of Cuba, with the description of two new species. Folia Parasitol. 50, 143–150.

    Article  Google Scholar 

  • Dietsch, T.V., 2005. Seasonal variation of infestation by ectoparasitic chigger mite larvae (Acarina: Trombiculidae) on resident and migratory birds in coffee agroecosystems of Chiapas. Mexico. J. Parasitol. 91, 1294–1303.

    Article  PubMed  Google Scholar 

  • Dusbábek, F., Lukoschus, F.S., 1975. Parasitic mites of Surinam XXXIV. Mites of the genus Eudusbabekia(Myobudae: Trombidiformes) of phyllostomid and desmodontid bats, with a key to know species. Acarologia 17, 306–319.

    PubMed  Google Scholar 

  • Esser, H.J., Foley, J.E., Bongers, F., Herre, E.A., Miller, M.J., Prins, H.H.T., Jansen, P.A., 2016. Host body size and the diversity of tick assemblages on Neotropical vertebrates. Int. J. Parasitol. Parasites Wildl. 5, 295–304.

    Article  PubMed  PubMed Central  Google Scholar 

  • Fagir, D.M., Horak, I.G., Ueckermann, E.A., Bennett, N.C., Lutermann, H., 2015. Ectoparasite diversity in the eastern rock sengis (Elephantulus myurus): the effect of seasonality and host sex. Afr. Zool. 50, 109–117.

    Article  Google Scholar 

  • Fain, A., 1973. Les Listrophorides dámerique neotropicale (Acarina: Sarcoptiformes). I. Familles Listrophoridae et Chirodiscidae. Bull. Inst. R. Sci. Nat. Belg. 49, 1–149.

    Google Scholar 

  • Goldberg, S.R., Bursey, C.R., 1993. Duration of attachment of the chigger, Eutrombicula lipovskyana (Trombiculidae) in mite pockets of Yarrow’s Spiny Lizard, Sceloporus jarrovi (Phyrnosomatidae) from Arizona. J. Wildl. Dis. 29, 142–144.

    Article  CAS  PubMed  Google Scholar 

  • Gray, J.S., Dautel, H., Estrada-Pena, A., Kahl, O., Lindgren, E., 2009. Effects of climate change in ticks and tick-borne diseases in Europe. Interdiscip. Perspect. Infect. Dis., 1–12.

    Google Scholar 

  • Guerrero, R., 1992. Catálogo de los Labidocarpidae (Acarina, Listrophoroidea) parasitos de los murciélagos (Mammalia, Chiroptera) neotropicales. Stud. Neotrop. Fauna Environ. 27, 19–41.

    Article  Google Scholar 

  • Gúizado, R.M.A., Casas-Andreu, G., 2011. Facultative specialization in the diet of the twelve-lined whiptail, Aspidoscelis lineatissima. J. Herpetol. 3, 287–290.

    Article  Google Scholar 

  • Hill, M., 1973. Diversity and evenness: a unifying notation and its consequences. Ecology 54, 427–432.

    Article  Google Scholar 

  • Hoffmann, A., 1990. Los Trombicú Tidos De Mexico (Acarida: Trombiculidae). Publicaciones Especiales. Instituto de Biología, Universidad Nacional Autónoma de Mexico, Mexico.

    Google Scholar 

  • Inclán, E.N., 2015. Artrópodofauna Ectoparásita De Los Murciélagos Leptonyctens yerbanuenae Y Glossophaga soncina De Las Grutas De Juxtlahuaca, Guerrero, Mexico. Undergraduate Thesis. Universidad Nacional Autónoma de Mexico, Mexico.

    Google Scholar 

  • Jost, L., 2006. Entropy and diversity. Oikos 113, 363–375.

    Article  Google Scholar 

  • Klukowski, M., 2004. Seasonal changes in abundance of host-seeking chiggers (Acari: Trombiculidae) and infestation on fence lizards, Sceloporus undulates. J. Herpetol. 38, 141–144.

    Article  Google Scholar 

  • Kohls, G.M., Sonenshine, D.E., Clifford, CM., 1965. The systematics of Subfamily Ornithodorinae (Acarina: Argasidae). II. Identification of the larvae of the Western hemisphere and descriptions of three new species. Ann. Entomol. Soc. Am. 58, 331–364.

    Article  CAS  PubMed  Google Scholar 

  • Kohls, G.M., Clifford, C.M., Jones, E.K., 1968. The systematics of Subfamily Ornithodorinae (Acarina: Argasidae). IV. Eight new species ofOrnithodoros from the Western hemisphere. Ann. Entomol. Soc. Am. 62, 1035–1043.

    Article  Google Scholar 

  • Krantz, G.W., Walter, D.E., 2009. A Manual of Acarology, third ed. Texas Tech University Press, Lubbock, Texas.

    Google Scholar 

  • Lafferty, K.D., 1997. Environmental parasitology: What can parasites tell us about human impacts on the environment. Parasitol. Today 13, 251–255.

    Article  CAS  PubMed  Google Scholar 

  • Lareschi, M., Krasnov, B.R., 2010. Determinants of ectoparasite assemblage structure on rodent hosts from South American marshlands: the effect of host species, locality and season. Med. Vet. Entomol. 24, 284–292.

    CAS  PubMed  Google Scholar 

  • Lehmann, T., 1993. Ectoparasites: Direct impact on host fitness. Parasitol. Today 9, 8–13.

    Article  CAS  PubMed  Google Scholar 

  • Levings, S.C., Windsor, D.M., 1984. Seasonal and annual variation in litter arthropod populations. In: Leigh, E.G., Rand, A.S., Windsor, D.M. (Eds.), The Ecology of a Tropical Forest. Smithsonian Institution Press, Washington, D. C., pp. 355–387.

    Google Scholar 

  • Lourenço, S.I., Palmeirim, J.M., 2008. Which factors regulate the reproduction of ectoparasites of temperate-zone cave-dwelling bats? J. Parasitol. Res. 104, 127–134.

    Article  Google Scholar 

  • Luguterah, A., Lawer, E.A., 2015. Effect of dietary guild (frugivory and insectivory) and other host characteristics on ectoparasites abundance (mite and nycteribiid) of chiropterans. Folia Parasitol. 62, 1–21.

    Article  CAS  Google Scholar 

  • Lumbad, A.S., Vredevoe, L.K., 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. Southwestern. Nat. 56, 369–377.

    Article  Google Scholar 

  • Marshall, A.G., 1981. The Ecology of Ectoparasitic Insects. Academic Press, London.

    Google Scholar 

  • Maurer, V., Baumgártner, J., 1992. Temperature influence on life table statistics of the chicken mite Dennanyssus gaiiinae (Acari: Dermanyssidae). Exp. Appl. Acarol. 15, 27–40.

    Article  CAS  PubMed  Google Scholar 

  • May, R.M., Anderson, R.M., 1978. Regulation and stability of host-parasite population interactions II. Destabilizing processes. J. Animal. Ecol. 47, 249–267.

    Article  Google Scholar 

  • McLean, J.A., Speakman, J.R., 1997. Non-nutritional maternal support in the brown long-eared bat. Anim. Behav. 54, 1193–1204.

    Article  CAS  PubMed  Google Scholar 

  • Méndez-Alonzo, R., Pineda-Garria, F., Paz, H., Resell, J. A., Olson, M.E., 2013. Leaf phenology is associated with soil water availability and xylem traits in tropical dry forest. Trees 27, 745–754.

    Article  Google Scholar 

  • Merino, S., Potti, J., 1996. Weather dependent effects of nest ectoparasites on their bird hosts. Ecography. 19, 107–113.

    Article  Google Scholar 

  • Morales-Malacara, J.B., 1998. Ácaros Mesostigmata parásitos de murciélagos de Mexico. Ph.D. dissertation. Universidad Nacional Autónoma de Mexico, Mexico.

    Google Scholar 

  • Mouritsen, K.N., Poulin, J., 2002. Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology. 124, 101–117.

    Article  Google Scholar 

  • Mysterud, A., Qyiller, L., Meisingset, E.L., Viljugrein, H., 2016. Parasite load and seasonal migration in red deer. Oecologia. 180, 401–407.

    Article  PubMed  Google Scholar 

  • Oliver, J.H., 1989. Biology and systematics of ticks (Acari: Ixodida). Annu. Rev. Ecol. Syst. 20, 397–430.

    Article  Google Scholar 

  • Ortega, S., 2009. Riqueza Y Carga Parasitaria, Y Su Reflejo En El Sistema De Defensa De Los Murciélagos Macrotus californiens Y Macrotus waterhousii En Zonas Neárticas Y Neotropicales De Mexico. Undergraduate Thesis. Universidad Nacional Autónoma de Mexico, Mexico.

    Google Scholar 

  • Palacios-Vargas, J.C., Vazquez, I., Morales-Malacara, J.B., 1985. Aspectos faunísticos yecológicos de laGrutadeJuxtlahuaca, Guerrero. Mexico. Mém. Biospeol. 12, 135–142.

    Google Scholar 

  • Palacios-Vargas, J.G., Castano-Meneses, G., Gómez-Anaya, J.A., Martínez-Yrizar, A., Mejía-Recamier, B.E., Martínez-Sánchez, J., 2007. Litter and soil arthropods diversity and density in a tropical dry forest ecosystem in Western Mexico. Biodivers. Conserv. 16, 3703–3717.

    Article  Google Scholar 

  • Pescador-Rubio, A., Rodriguez-Palafox, A., Noguera, F.A., 2002. Diversidad y estacionalidad de arthropoda. In: Noguera, F.A., Vega, R.J.H., Garcia, A.A.N., Ouesada, A.M. (Eds.), Historia Natural de Chamela. Instituto de Biología, Universidad Nacional Autónoma de Mexico, Mexico, pp. 183–201.

    Google Scholar 

  • Poulin, R., 1999. The functional importance of parasites in animal communities: many roles at many levels? Int. J. Parasitol. 29, 903–914.

    Article  CAS  PubMed  Google Scholar 

  • Poulin, R., 2011. Evolutionary Ecology of Parasites. Princeton University Press.

    Google Scholar 

  • Presley, S.J., 2004. Ectoparasitic Assemblages of Paraguayan Bats: Ecological and Evolutionary Perspectives. Ph. D. Dissertation. Texas Tech University.

    Google Scholar 

  • Pringle, E.G., Dirzo, R., Gordon, D.M., 2012. Plant defence, herbivory, and the growth of Cordia alliodoa trees and their symbiotic Azteca ant colonies. Oecologia 170, 677–685.

    Article  PubMed  Google Scholar 

  • Radovsky, F.J., 1967. The Macronyssidae and Laelapidae (Acarina: Mesostigmata) parasitic on bats. Univ. Calif. Publ. Entomol. 46, 1–288.

    Google Scholar 

  • Reiczigel, J., Rózsa, L., 2005. Quantitative Parasitology 3.0. Budapest. Distributed by the Authors.

    Google Scholar 

  • Reisen, W.K., Kennedy, M.L., Reisen, N.T., 1976. Winter ecology of ectoparasites collected from hibernatingMyofis velifer (Allen) in southwestern Oklahoma (Chiroptera: Vespertilionidae). J. Parasitol. 62, 628–635.

    Article  CAS  PubMed  Google Scholar 

  • Rivera-Garria, K.D., Sandoval-Ruiz, C.A., Saldana-Vazquez, R.A., Schondube, J.E., 2017. The effect of seasonality on host-bat fly ecological networks in a temperate mountain cave. Parasitology 144, 692–697.

    Article  Google Scholar 

  • Rudnick, A., 1960. A revision of the mites of the family Spinturnicidae (Acarina). Univ. Calif. Publ. Entomol. 17, 157–284.

    Google Scholar 

  • Rzedowski, J., 1981. Vegetación De Mexico. Editorial Limusa, Mexico City.

    Google Scholar 

  • Salinas-Ramos, V., Zaldfvar-Riverón, A., Rebollo-Hernández, A., Herrera-Montalvo, L.G., 2017. Seasonal variation of bat-flies (Diptera: Streblidae) in four bat species from a tropical dry forest. Mammalia. 82, 113–143.

    Google Scholar 

  • Sasa, M., 1961. Biology of chiggers. Annu. Rev. Entomol. 61, 221–244.

    Article  Google Scholar 

  • Sheeler-Gordon, L.L., Owen, R.D., 1999. Host tracking or resource tracking? The case of Periglischrus Wing Mites (Acarina: Spinturnicidae) of Leaf-Nosed Bats (Chiroptera: Phyllostomidae) from Michoacán, Mexico. Acta Zool. Mex. 76, 85–102.

    Google Scholar 

  • Stanko, M., Krasnov, B.R., Morand, S., 2006. Relationship between host abundance and parasite distribution: inferring regulating mechanisms from census data. J. Animal. Ecol. 75, 575–583.

    Article  Google Scholar 

  • Stoner, K.E., Salazar, K.A.O., Fernandez, R.C.R., Quesada, M., 2003. Population dynamics, reproduction, and diet of the lesser long- nosed bat (Leptonycteris curasoae) in Jalisco, Mexico: implications for conservation. Biodivers. Conserv. 12, 357–373.

    Article  Google Scholar 

  • Ter Hofstede, H.M., Fenton, M.B., 2005. Relationships between roost References, ectoparasite density, and grooming behavior of Neotropical bats. J. Zool. 266, 333–340.

    Article  Google Scholar 

  • Tlapaya-Romero, L., Horváth, A., Gallina-Tessaro, S., Naranjo, E.J., Gómez, B., 2015. Prevalencia y abundancia de moscas parasitas asociadas a una comunidad de murciélagos caverncolas en latrinitaria, Chiapas, Mexico. Rev. Mex. Biodivers. 86, 377–385.

    Article  Google Scholar 

  • Traub, R., 1949. Observations on Tsutsugamushi disease (scrub typhus) in Assam and Burma: The mite, Trombicula deliensis Walch, and its relation to scrub typhus in Assam. Am. J. Hyg. 50, 361–374.

    Google Scholar 

  • Tuegel, M.A., Wrenn, W.J., 1998. Sexual dimorphism in morphology and development of the pest chigger, Eutrombicula rinnabaris (Acari: Trombiculidae). Int. J. Acarol. 24, 199–211.

    Article  Google Scholar 

  • Vega, O.M.E., 2013. Riqueza Y Carga Parasitaria, Y Su Reflejo En El Sistema De Defensa De Los Murciélagos Pteronotus parnellii Y Pteronotus personatus En Zonas Neárticas Y Neotropicales De Mexico. Undergraduate Thesis. Universidad Nacional Autónoma de Mexico, Mexico.

    Google Scholar 

  • Vercammen-Grandjean, P.H., 1967. Revision of the genus Tecomaúana Hoffman., 194. (Acarina, Trombiculidae). Acarologia 9, 848–864.

    Google Scholar 

  • Vercammen-Grandjean, P.H., Watkins, S.G., Beck, A.J., 1965. Revision of Warthonia glenni Brenna., 1962. and American bat parasite (Acarina: Leeuwenhoekiidae). Acarologia 7, 492–509.

    CAS  PubMed  Google Scholar 

  • Villegas-Guzman, G.A., López-González, C., Vargas, M., 2005. Ectoparasites associated to two species ofCorynorhinus (Chiroptera: Vespertilionidae) from the Guanaceví Mining Region, Durango, Mexico. J. Med. Entomol. 43, 125–127.

    Google Scholar 

  • Warburton, E.M., Pearl, C.A., Vonhof, M.J., 2016. Relationships between host body condition and immunocompetence, not host sex, best predict parasite burden in a bat-helminth system. J. Parasitol. Res. 115, 2155–2164.

    Article  Google Scholar 

  • Whitaker Jr., J.O., Morales-Malacara, J.B., 2005. Ectoparasites and other associates (ectodytes) of mammals of Mexico. In: Sánchez-Cordero, V., Medellín, R.A. (Eds.), Contribuciones Mastozoológicas En Homenaje a Bernardo Villa. Biology and Ecology Institutes, Mexico, p. 500.

    Google Scholar 

  • Whitakerjr., J.O., Ritzi, C.M., Dick, C.W., 2009. Collecting and preserving bat ectoparsites for ecological study. In: Kunz, T.H., Parsons, S. (Eds.), Ecological and Behavioral Methods for the Study of Bats., second ed. Johns Hopkins University Press, Baltimore, MD, pp. 806–827.

    Google Scholar 

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  1. Instituto de Biología, Universidad Nacional Autónoma de México, A. P. 70-153, Ciudad de México, 04510, Mexico

    Valeria B. Salinas-Ramos

  2. Estación de Biología Chamela, Instituto de Biología, Universidad Nacional Autónoma de México, A.P. 21, San Patricio, Jalisco, 48980, Mexico

    L. Gerardo Herrera M

  3. UMDI, Facultad de Ciencias, Universidad Nacional Autónoma de México, Campus Juriquilla, Boulevard Juriquilla 3001, Querétaro, 76230, Mexico

    Juan B. Morales-Mlalacara

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Salinas-Ramos, V.B., Herrera M, L.G. & Morales-Mlalacara, J.B. Seasons influence acarine infestation in bats from tropical dry forests of Western Mexico. Mamm Biol 96, 37–44 (2019). https://doi.org/10.1016/j.mambio.2019.03.011

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