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Bat flies aggregation on Artibeus planirostris hosts in the Pantanal floodplain and surrounding plateaus

Published online by Cambridge University Press:  13 June 2019

Esther Gonçalves Morimatsu Vieira
Affiliation:
Licenciatura em Ciências Biológicas, Instituto de Biociências, Universidade Federal de Mato Grosso do Sul, 79070-900 Campo Grande, Brasil
Erich Fischer
Affiliation:
Instituto de Biociências, Universidade Federal de Mato Grosso do Sul, 79070-900 Campo Grande, Brasil
Gustavo Graciolli
Affiliation:
Instituto de Biociências, Universidade Federal de Mato Grosso do Sul, 79070-900 Campo Grande, Brasil
Carolina Ferreira Santos
Affiliation:
Instituto de Biociências, Universidade Federal de Mato Grosso do Sul, 79070-900 Campo Grande, Brasil
George Camargo
Affiliation:
Programa de Pós-graduação em Ecologia e Conservação, Instituto de Biociências, Universidade Federal de Mato Grosso do Sul, 79070-900 Campo Grande, Brasil
Maurício Silveira
Affiliation:
Programa de Pós-graduação em Ecologia e Conservação, Instituto de Biociências, Universidade Federal de Mato Grosso do Sul, 79070-900 Campo Grande, Brasil Programa de Pós-Graduação em Zoologia, Universidade de Brasília, Campus Darcy Ribeiro s/n, Asa Norte, 70910-900 Brasília, Brasil
Alan Eriksson*
Affiliation:
Programa de Pós-graduação em Ecologia e Conservação, Instituto de Biociências, Universidade Federal de Mato Grosso do Sul, 79070-900 Campo Grande, Brasil Department of Zoology, University of Otago, 340 Great King St, 9016 Dunedin, New Zealand
*
Author for correspondence: Alan Eriksson, E-mail: aferiksson@hotmail.com

Abstract

For parasites in natural systems, the most common pattern of spatial distribution is aggregation among hosts. The main causes of such aggregation are variable exposure of hosts to parasites and heterogeneity in host susceptibility. The objective of this study was to determine if there are differences in the aggregation pattern of two species of ectoparasitic flies between the Pantanal and Cerrado regions of Brazil on the bat Artibeus planirostris. We collected the ectoparasites from bats captured between 2002 and 2017 with mist nets in 21 sites in the Pantanal and 15 sites in the surrounding plateaus. The results showed that the aggregation of ectoparasitic flies in Pantanal was more pronounced than in Cerrado. The discrepancy aggregation index (D) of the bat fly Megistopoda aranea was 0.877 in Pantanal and 0.724 in Cerrado. The D values of Aspidoptera phyllostomatis was even higher, with 0.916 and 0.848 in the Pantanal and Cerrado, respectively. Differences in the shelters used may be the main factor shaping variation in aggregation, since the Pantanal does not have rock formations, with only foliage, crowns and hollow tree trunks. These differences likely affect host exposure to the parasites, leading to an increase in parasite aggregation.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2019 

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References

Barbier, E and Graciolli, G (2016) Community of bat flies (Streblidae and Nycteribiidae) on bats in the Cerrado of Central-West Brazil: hosts, aggregation, prevalence, infestation intensity, and infracommunities. Studies on Neotropical Fauna and Environment 51, 176187.Google Scholar
Bertola, PB, Aires, CC, Favorito, SE, Graciolli, G, Amaku, M and Pinto-Da-Rocha, R (2005) Bat flies (Diptera: Streblidae, Nycteribiidae) parasitic on bats (Mammalia: Chiroptera) at Parque Estadual da Cantareira, São Paulo, Brazil: parasitism rates and host-parasite associations. Memorias do Instituto Oswaldo Cruz 100, 2532.Google Scholar
Bezerra, RHS and Bocchiglieri, A (2018) Association of ectoparasites (Diptera and Acari) on bats (Mammalia) in a restinga habitat in northeastern Brazil. Parasitology Research 117, 34133420.Google Scholar
Boag, B, Lello, J, Fenton, A, Tompkins, DM and Hudson, PJ (2001) Patterns of parasite aggregation in the wild European rabbit (Oryctolagus cuniculus). International Journal for Parasitology 31, 14211428.Google Scholar
Bolívar-Cimé, B, Cuxim-Koyoc, A, Reyes-Novelo, E, Morales-Malacara, JB, Laborde, J and Flores-Peredo, R (2018) Habitat fragmentation and the prevalence of parasites (Diptera, Streblidae) on three phyllostomid bat species. Biotropica 50, 9097.Google Scholar
Breviglieri, CPB and Uieda, W (2014) Tree cavities used as diurnal roosts by Neotropical bats. Folia Zoologica 63, 206215.Google Scholar
Cordero-Schmidt, E, Medeiros-Guimarães, M, Vargas-Mena, JC, Carvalho, B, Ferreira, RL, Rodriguez-Herrera, B and Venticinque, EM (2016) Are leaves a good option in Caatinga's menu? First record of folivory in Artibeus planirostris (Phyllostomidae) in the Semiarid Forest, Brazil. Acta Chiropterologica 18, 489497.Google Scholar
Díaz, MM and Linares García, VH (2012) Refugios naturales y artificiales de murciélagos (Mammalia:Chiroptera) en la selva baja en el Noroeste de Perú. Gayana (Concepción) 76, 117130.Google Scholar
Dick, CW and Patterson, BD (2006) Bat flies: obligate ectoparasites of bats. In Morand, S, Krasnov, BR and Poulin, R (eds), Micromammals and Macroparasites From Evolutionary Ecology to Management. Tokyo: Springer-Verlag, pp. 179194.Google Scholar
Dick, CW and Dittmar, K (2014) Parasitic Bat flies (Diptera: Streblidae and Nycteribiidae): host specificity and potential as vectors. In Klimpel, S and Mehlhorn, H (eds), Bats (Chiroptera) as Vectors of Diseases and Parasites: Facts and Myths. Berlin: Springer, pp. 131155.Google Scholar
Dick, CW and Graciolli, G (2018) Checklist of world Streblidae (Diptera: Hippoboscoidea). Available at https://www.researchgate.net/publication/322578987_CHECKLIST_OF_WORLD_STREBLIDAE_DIPTERA_HIPPOBOSCOIDEA (Accessed 20 November 2018).Google Scholar
Dittmar, K, Dick, CW, Patterson, BD, Whiting, MF and Gruwell, ME (2009) Pupal deposition and ecology of bat flies (Diptera: Streblidae): Trichobius sp. (caecus group) in a Mexican cave habitat. The Journal of Parasitology 95, 308314.Google Scholar
Dornelles, GDP, Graciolli, G, Odon, A and Bordignon, MO (2017) Infracommunities of Streblidae and Nycteribiidae (Diptera) on bats in an ecotone area between Cerrado and Atlantic Forest in the state of Mato Grosso do Sul. Iheringia. Série Zoologia 107, 15.Google Scholar
Eriksson, A, Graciolli, G and Fischer, E (2011) Bat flies on phyllostomid hosts in the Cerrado region: component community, prevalence and intensity of parasitism. Memórias do Instituto Oswaldo Cruz 106, 274278.Google Scholar
Esbérard, C, Astúa, D, Geise, L, Costa, L and Pereira, L (2012) Do young Carollia perspicillata (Chiroptera: Phyllostomidae) present higher infestation rates of Streblidae (Diptera)? Brazilian Journal of Biology 72, 617621.Google Scholar
Fischer, E, Silveira, M, Munin, RL, Camargo, G, Santos, CF, Pereira, MJR, Fischer, W and Eriksson, A (2018) Bats in the dry and wet Pantanal. Hystrix 29, 1117.Google Scholar
Fritz, GN (1983) Biology and ecology of bat flies (Diptera: Streblidae) on bats in the genus Carollia. Journal of Medical Entomology 20, 110.Google Scholar
Garbino, GST and Tavares, VC (2018) Roosting ecology of Stenodermatinae bats (Phyllostomidae): evolution of foliage roosting and correlated phenotypes. Mammal Review 48, 7589.Google Scholar
Graciolli, G, Zortéa, M and Carvalho, LFADC (2010) Bat flies (Diptera, Streblidae and Nycteribiidae) in a Cerrado area of Goiás State, Brazil. Revista Brasileira de Entomologia 54, 511514.Google Scholar
Guerrero, R (1995) Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) del Nuevo Mundo. V. Trichobiinae com alas reducidas o ausentes y miscelaneos. Boletin de Entomologia Venezolana 10, 135160.Google Scholar
Hansen, F, Jeltsch, F, Tackmann, K, Staubach, C and Thulke, H-H (2004) Processes leading to a spatial aggregation of Echinococcus multilocularis in its natural intermediate host Microtus arvalis. International Journal for Parasitology 34, 3744.Google Scholar
Hijmans, RJ, Cameron, SE, Parra, JL, Jones, PG and Jarvis, A (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25, 19651978.Google Scholar
Hiller, T, Honner, B, Page, RA and Tschapka, M (2018) Leg structure explains host site preference in bat flies (Diptera: Streblidae) parasitizing Neotropical bats (Chiroptera: Phyllostomidae). Parasitology 145, 14751482.Google Scholar
Kottek, M, Grieser, J, Beck, C, Rudolf, B and Rubel, F (2006) World map of the Köppen-Geiger climate classification updated. Meteorologische Zeitschrift 15, 259263.Google Scholar
Lewis, SE (1995) Roost fidelity of bats: a review. Journal of Mammalogy 76, 481496.Google Scholar
Lourenço, EC, Patrício, PMP, Pinheiro, MC, Dias, RM and Famadas, KM (2014) Streblidae (Diptera) on bats (Chiroptera) in an area of Atlantic Forest, state of Rio de Janeiro. Revista Brasileira de Parasitologia Veterinária 23, 164170.Google Scholar
Mercante, MA, Rodrigues, SC and Ross, JLS (2011) Geomorphology and habitat diversity in the Pantanal. Brazilian Journal of Biology 71, 233240.Google Scholar
Morrill, A and Forbes, MR (2012) Random parasite encounters coupled with condition-linked immunity of hosts generate parasite aggregation. International Journal for Parasitology 42, 701706.Google Scholar
Nunes da Cunha, C and Junk, WJ (2010) A preliminary classification of habitats of the Pantanal of Mato Grosso and Mato Grosso do Sul, and its relation to national and international wetland classification systems. In Junk, WJ, Nunes da Cunha, C and Wantzen, KM (eds), The Pantanal: Ecology, Biodiversity and Sustainable Management of A Large Neotropical Seasonal Wetland. Sofia: Pensoft, pp. 127141.Google Scholar
Overal, WL (1980) Host-relations of the batfly Megistopoda aranea (Diptera: Streblidae) in Panama. The University of Kansas Science Bulletin 52, 120.Google Scholar
Patrício, PMP, Lourenço, EC, de Freitas, AQ and Famadas, KM (2016) Host morphophysiological conditions and environment abiotic factors correlate with bat flies (Streblidae) prevalence and intensity in Artibeus leach, 1821 (Phyllostomidae). Ciência Rural 46, 648653.Google Scholar
Patterson, BD, Dick, CW and Dittmar, K (2007) Roosting habits of bats affect their parasitism by bat flies (Diptera: Streblidae). Journal of Tropical Ecology 23, 177189.Google Scholar
Pilosof, S, Dick, CW, Korine, C, Patterson, BD and Krasnov, BR (2012) Effects of anthropogenic disturbance and climate on patterns of bat fly parasitism. PLoS ONE 7, e41487.Google Scholar
Pott, A, Oliveira, A, Damasceno-Junior, G and Silva, J (2011) Plant diversity of the Pantanal wetland. Brazilian Journal of Biology 71, 265273.Google Scholar
Poulin, R (1993) The disparity between observed and uniform distributions: a new look at parasite aggregation. International Journal for Parasitology 23, 937944.Google Scholar
Poulin, R (2007) Parasite aggregation: causes and consequences. In Poulin, R (ed.), Evolutionary Ecology of Parasites. New Jersey: Princeton University Press, pp. 2378.Google Scholar
Poulin, R (2013) Explaining variability in parasite aggregation levels among host samples. Parasitology 140, 541546.Google Scholar
Presley, SJ (2011) Interspecific aggregation of ectoparasites on bats: importance of hosts as habitats supersedes interspecific interactions. Oikos 120, 832841.Google Scholar
Reiczigel, J, Marozzi, M, Fábián, I and Rózsa, L (2019) Biostatistics for parasitologists – a primer to Quantitative Parasitology. Trends in Parasitology 35, 277281.Google Scholar
Rui, AM and Graciolli, G (2005) Moscas ectoparasitas (Diptera, Streblidae) de morcegos (Chiroptera, Phyllostomidae) no sul do Brasil: associações hospedeiros-parasitos e taxas de infestação. Revista Brasileira de Zoologia 22, 438445.Google Scholar
Sallun-Filho, W, Karmann, I and Lobo, HAS (2010) Cavernas na Serra da Bodoquena. O Carste 22, 2733.Google Scholar
Shaw, DJ and Dobson, AP (1995) Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111, S111S113.Google Scholar
Silva, JSV and Carlini, FJ (2015) Vegetation cover of the Upper Paraguai Basin in Mato Grosso do Sul State: comparison between Pantanal wetland and the plateau. Geografia 40, 211226.Google Scholar
Silveira, M, Tomas, WM, Fischer, E and Bordignon, MO (2018) Habitat occupancy by Artibeus planirostris bats in the Pantanal wetland, Brazil. Mammalian Biology 91, 16.Google Scholar
ter Hofstede, HM and Fenton, MB (2005) Relationships between roost preferences, ectoparasite density, and grooming behaviour of Neotropical bats. Journal of Zoology 266, 333340.Google Scholar
Warburton, EM and Vonhof, MJ (2018) From individual heterogeneity to population-level overdispersion: quantifying the relative roles of host exposure and parasite establishment in driving aggregated helminth distributions. International Journal for Parasitology 48, 309318.Google Scholar
Wenzel, RL (1976) The streblid batflies of Venezuela (Diptera: Streblidae). Young University Science Bulletin, Biological Series 20, 1177.Google Scholar