ECTOPARASITIC FLIES (DIPTERA, STREBLIDAE) ON BATS (MAMMALIA, CHIROPTERA) IN A DRY TROPICAL FOREST IN THE NORTHERN COLOMBIA

ADRIÁN ALONSO DURÁN DEIVYS M. ÁLVAREZ GARCÍA GUSTAVO GRACIOLLI About the authors

ABSTRACT

This work represents the first report of host-parasite associations between flies of the family Streblidae and their host bats in the Colombian Caribbean region. Specimens were collected in a dry tropical forest in the Sucre department. A total of 17 species (eight genera) of Streblidae, as well as 19 species from five bat families were recorded. Strebla mirabilis, Trichobius costalimai, Trichobius parasiticus and Paradyschiria parvuloides were the most abundant ectoparasites. Prevalence of ectoparasites on bat assemblage was 48.57%. In nine bat species, more than one Streblidae species were recorded. Trichobius costalimai had the greatest number of host species. We have found remarkable new associations between Artibeus planirostris and Trichobius costalimai, Lophostoma silvicolum and Strebla mirabilis, as well as Lophostoma silvicolum and Trichobius parasiticus.

KEY-WORDS:
Colombia; Host; Parasitism; Phyllostomidae

RESUMEN

Este trabajo constituye el primer registro de las relaciones de parasitismo entre moscas Streblidae y murciélagos en la región Caribe colombiana. Los especímenes se capturaron en un bosque seco tropical del departamento de Sucre. Se registraron 17 especies de ocho géneros de Streblidae y 19 especies pertenecientes a cinco familias de murciélagos. Strebla mirabilis, Trichobius costalimai, Trichobius parasiticus y Paradyschiria parvuloides fueron los ectoparásitos más abundantes. La prevalencia de ectoparásitos sobre el ensamblaje de murciélagos fue del 48,57%. En nueve especies de murciélagos se encontró más de una especie de Streblidae. Trichobius costalimai fue la que presentó el mayor número de especies huéspedes. Resaltan por ser novedosas las asociaciones entre Artibeus planirostris-Trichobius costalimai, Lophostoma silvicolum-Strebla mirabilis y Lophostoma silvicolum-Trichobius parasiticus.

PALABRAS CLAVE:
Colombia; Huésped; Parasitismo; Phyllostomidae

INTRODUCTION

Streblidae Kolenati, 1863 is a family of bloodsucking flies specialized in ectoparasitism of bats. Like all Hippoboscoidea, fertilization and embryonic period occur inside females, and three instars larvae develop through nourishment by intrauterine glands. Gravid female flies leave the host, looking for a suitable substrate at the refuge sites and deposit a single 3rd instar larva that is ready to pupate, a phenomenon known as adenotrophic viviparity (Dick & Dittmar, 2014DICK, C.W. & DITTMAR, K. 2014. Parasitic bat flies (Diptera: Streblidae and Nycteribiidae): host specificity and potential as vectors. In: Klimpel, S. & Mehlhorn, H. (Eds.). Bats (Chiroptera) as vectors of diseases and parasites. Springer. p. 131-155. (Parasitology Research Monographs, 5)).

Streblid flies are distributed in all biogeographic regions, with a greater diversity in the Americas (Guerrero, 1993GUERRERO, R. 1993. Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) deI Nuevo Mundo. I. Clave para los géneros y Nycterophilinae. Acta Biológica Venezuélica, 14:61-75.). Currently it is divided into five subfamilies: Nycteriboscinae, Ascodipterinae, Trichobiinae, Streblinae, and Nycterophiliinae, the last three being found in the New World and are comprised of 26 genera and 158 species (Dick et al., 2016DICK, C.W.; GRACIOLLI, G. & GUERRERO, R. 2016. Family Streblidae. Zootaxa, 4122:784-802.). Nineteen genera and 73 species are currently known from Colombia, whose hosts are member of the following bat families: Emballonuridae, Furipteridae, Molossidae, Mormoopidae, Natalidae, Noctilionidae, Phyllostomidae, and Vespertilionidae (Dick et al., 2016DICK, C.W.; GRACIOLLI, G. & GUERRERO, R. 2016. Family Streblidae. Zootaxa, 4122:784-802.); however, knowledge about the host-parasite relationship among ectoparasitic flies and bats is still incipient in this country. Due to this, the present study aimed at studying the association of Streblidae with bat species in a dry tropical forest relict in northern Colombia.

MATERIAL AND METHODS

Study area

The study was carried out at the Reserva Forestal Protectora Serranía de Coraza, in the department of Sucre, Colombia (09°31’58.02”N; 75°20’59.85”W) (Figure 1). This zone corresponds to a dry tropical forest relict (Holdridge, 1979HOLDRIDGE, L. 1979. Ecología basada en zonas de vida. San José, Costa Rica.Instituto Interamericano de Ciencias Agrícolas.), the climate is warm, with average temperatures of 26.8°C and relative humidity of 77%. The average annual rainfall is between 1,000 and 1,200 mm (Aguilera, 2005AGUILERA, M. 2005. La economía del departamento de Sucre: ganadería y sector público. Cartagena, Colombia, Banco de la República. (Serie Documentos de Trabajo sobre Economia Regional, n. 63)). A detailed description of the vegetation may be consulted in Cuervo et al. (1986CUERVO, A.; BARBOSA, C. & DE LA OSSA, J. 1986. Aspectos ecológicos y etológicos de primates con énfasis en Alouatta seniculus (Cebidae), de la región de Colosó, Serranía de San Jacinto (Sucre), Costa Norte de Colombia. Caldasia, 14:68-70.).

FIGURE 1:
Study sites of host-ectoparasite relationship between Streblidae and bats in Colombia. Darker areas correspond to higher altitudes.

Captures of hosts and bat flies

Sampling was carried out between June 2013 and March 2014. Four mist nets (6 × 2.5 m each) were set up, at ground level, from 6 to 12 pm. Bats were sexed and identified based on Linares (2000LINARES, O. 2000. Murciélagos. In: Linares, O. (Ed.). Mamíferos de Venezuela. Venezuela, Sociedad Conservacionista Audubon de Venezuela. p. 349-591.) and Muñoz (2001MUÑOZ, J. 2001. Los murciélagos de Colombia. Sistemática, distribución, descripción, historia natural y ecología. Medellín, Editorial Universidad de Antioquia.). Bat flies were removed with entomological tweezers and conserved in 70% ethanol. All samples were labeled with host information, collection site, and date. Streblidae specimens collected were identified following taxonomic keys published by Guerrero (1993GUERRERO, R. 1993. Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) deI Nuevo Mundo. I. Clave para los géneros y Nycterophilinae. Acta Biológica Venezuélica, 14:61-75.), Guerrero (1994aGUERRERO, R. 1994a. Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) del Nuevo Mundo. II. Los grupos: Pallidus, Caecus, Major, Uniformis y Longipes del género Trichobius Gervais, 1844. Acta Biológica Venezuélica, 15(1):1-18., bGUERRERO, R. 1994b. Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) del Nuevo Mundo. IV. Trichobiinae con alas desarrolladas. Boletín Entomológico Venezolano (n.s.), 9(2):161-192.), Guerrero (1995aGUERRERO, R. 1995a. Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) del Nuevo Mundo. V. Trichobiinae con alas reducidas o ausentes y misceláneos. Boletín Entomológico Venezolano (n.s.), 10(2):135-160., bGUERRERO, R. 1995b. 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 Venezuélica (n.s.), 15(3-4):1-27.) and Guerrero (1996GUERRERO, R. 1996. Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) del Nuevo Mundo. VI. Streblinae. Acta Biológica Venezuélica, 16(2):1-25.). Diptera material was deposited at the Coleção Zoológica de Referência da Universidade Federal de Mato Grosso do Sul (ZUFMS), Campo Grande (Brasil) and at the Entomology Laboratory of the Sucre University (LEUS), in Sincelejo (Colombia).

Data analysis

To evaluate the associations of ectoparasites among different hosts, we used the following indices (Bush et al., 1997BUSH, A.; LAFFERTY, K.; LOTZ, J. & SHOSTAK, A. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology, 83:575-583.): Prevalence (P = number of infested hosts divided by number of examined hosts, multiplied by 100), and Mean Intensity (MI = number of ectoparasites of a particular parasite species divided by the infected members of a particular host species). The indices were calculated using Quantitative Parasitology 3.0 software (Rózsa et al., 2000RÓZSA, L.; REICZIGEL, J. & MAJOROS, G. 2000. Quantifying parasites in samples of hosts. Journal of Parasitology, 86(2):228-232.). We also calculated the Specificity Index (SI = percentage of all individuals of an ectoparasite species found on a host) (Dick & Gettinger, 2005DICK, C.W. & GETTINGER, D. 2005. A faunal survey of streblid bat flies (Diptera: Streblidae) associated with bats in Paraguay. Journal of Parasitology, 91:1015-1024.). The difference in the sex ratio in Streblidae species was evaluated by Exact Binomial Test (McDonald, 2008MCDONALD, J.H. 2008. Handbook of biological statistics. Baltimore, Sparky House Publishing.).

Primary associations were determined when a host species had 5% or more of the individuals of a given parasite species (Dick, 2007DICK, C.W. 2007. High host specificity of obligate ectoparasites. Ecological Entomology, 32:446-450.), as well as considering high prevalence and mean intensity, and the literature data; while accidental or transitory associations in which a host was associated with less than 5% of the total individuals of a parasite species, in rare cases, and/or low prevalence and mean intensity (Dick, 2007DICK, C.W. 2007. High host specificity of obligate ectoparasites. Ecological Entomology, 32:446-450.; Santos et al., 2009SANTOS, C.; DIAS, P.; RODRIGUES, F.; LOBATO, K.; ROSA, L.; OLIVEIRA, T. & REBÊLO, J. 2009. Moscas ectoparasitas (Diptera: Streblidae) de morcegos (Mammalia: Chiroptera) do município de São Luís, MA: taxas de infestação e associações parasito-hospedeiro. Neotropical Entomology, 38(5):595-601.).

RESULTS

A total of 300 bat flies belonging to 17 species and eight genera of Streblidae were collected. The most abundant species was Strebla mirabilis (Waterhouse, 1879) (24.33%), followed by Trichobius costalimai Guimarães, 1938 (18.33%), Trichobius parasiticus Gervais, 1844 (15.67%) and Paradyschiria parvuloides Wenzel, 1966 (13%), while the other species had relative abundances below 8% (Table 1). Male number (n = 168; 56%) was higher than female (n = 132; 44%), with a male-biased sex ratio in 11 species, although with a significant difference only in T. parasiticus (Table 1).

TABLE 1:
List of species, abundance and sex ratio of Streblidae on bats in a dry tropical forest in the Colombian Caribbean region.

Nineteen species were represented in 105 bats captured, of the following families: Phyllostomidae (15 spp.), Noctilionidae (1 sp.), Molossidae (1 sp.), Emballunuridae (1 sp.) and Mormoopidae (1 sp.). The 80% of specimens were collected from the first family, while the remaining 20% belonged to the other four. The most abundant host species was Glyphonycteris daviesi (Hill, 1964) (14.29%), followed by Desmodus rotundus (E. Geoffroy, 1810) (10.48%), Lonchophylla concava Goldman (1914) (10.48%), Noctilio albiventris Desmarest, 1818 (10.48%), Artibeus lituratus (Olfers, 1818) (9.52%), Artibeus planirostris (Spix, 1823) (8.57%), Molossus molossus (Pallas, 1766) (7.62%) and Phyllostomus discolor Wagner, 1843 (6.67%), the remaining represented 21.89% of the total (Table 2).

TABLE 2:
Associations between bats and Streblidae in a dry tropical forest in the Colombian Caribbean region.

Ectoparasites prevalence in bat assemblage was 48.57%, while that in the species ranged of 0% to 100%. Four species of bats were not parasitized: Pteronotus parnellii (Gray, 1843), Saccopteryx bilineata (Temminck, 1838), Micronycteris megalotis (Gray, 1843) and M. molossus. Nine bat species were found with more than one Streblidae, D. rotundus and A. planirostris had the greatest ectoparasites richness (seven species each), followed by Lophostoma silvicolum d’Orbigny, 1836 (6 spp.), Platyrrhinus helleri (Peters, 1866) and G. daviesi (5 spp.), A. lituratus (4 spp.), P. discolor (3 spp.), and Trinycteris nicefori Sanborn, 1949 and N. albiventris (2 spp.) (Table 2).

Streblidae with greatest number of host species were: T. costalimai associated with 6 spp. of bats, followed by S. mirabilis, T. perspicillatus and T. joblingi (associated with 5 spp.), T. parasiticus and Strebla wiedemannii Kolenati, 1856 (associated with 4 spp.). While, Megistopoda aranea (Coquillet, 1899) and Aspidoptera phyllostomatis (Perty, 1833) were associated with 3 spp., Strebla hertigi Wenzel, 1966, Mastoptera minuta (Costa-Lima, 1921) and P. parvuloides were found on 2 spp. Only one specimen was collected of Strebla alvarezi, Wenzel, 1966, Strebla kohlsi Wenzel, 1966, Trichobius dugesii Townsend 1891, Trichobius longipes (Rudow, 1767), Megistopoda proxima (Séguy, 1926) and Speiseria ambigua Kessel, 1925, only these bat flies were found on just a single host species (Table 2). Also, three new host-parasite associations were found: Artibeus planirostris-Trichobius costalimai, Lophostoma silvicolum-Strebla mirabilis and Lophostoma silvicolum-Trichobius parasiticus.

DISCUSSION

Streblidae species found in this study (17 spp.) correspond to 23.28% of the total species recorded in Colombia (73 spp.) (Dick et al., 2016DICK, C.W.; GRACIOLLI, G. & GUERRERO, R. 2016. Family Streblidae. Zootaxa, 4122:784-802.). The department of Sucre has previously reported nine species, five of which were not found in this work: Nycterophilia parnelli Wenzel, 1966, Strebla altmani Wenzel, 1966, Mastoptera guimaraesi Wenzel, 1966, Trichobius galei Wenzel, 1966 and Trichobius caecus Edwards, 1918 (Dick et al., 2016DICK, C.W.; GRACIOLLI, G. & GUERRERO, R. 2016. Family Streblidae. Zootaxa, 4122:784-802.). The richness of Streblidae in the department of Sucre is extended to 22, with 13 new records. The species M. aranea, M. proxima, S. alvarezi, S. hertigi, S. kohlsi and T. dugesii are new records for the Colombian Caribbean, with current total of 33 species for this region (Dick et al., 2016DICK, C.W.; GRACIOLLI, G. & GUERRERO, R. 2016. Family Streblidae. Zootaxa, 4122:784-802.).

The higher male abundance of Streblidae found in this study is consistent with that reported by other authors (Fritz, 1983FRITZ, G. 1983. Biology and ecology of bat flies (Diptera: Streblidae) on bats in the genus Carollia. Journal of Medical Entomology, 20:1-10.; Dick & Patterson, 2008DICK, C.W. & PATTERSON, B. 2008. An excess of males: skewed sex ratios in bat flies (Diptera: Streblidae). Evolutionary Ecology, 22:757-769.; Autino et al., 2011AUTINO, A.G.; CLAPS, G.L.; BARQUEZ, R.M. & DÍAZ, M.M. 2011. Ectoparasitic insects (Diptera: Streblidae and Siphonaptera: Ischnopsyllidae) of bats from Iquitos and surrounding areas (Loreto, Peru). Memórias do Instituto Oswaldo Cruz, 106(8):917-925.). According to Wenzel (1976WENZEL, R. 1976. The Streblidae bat flies of Venezuela (Diptera: Streblidae). Brigham Young of University Sciences Bulletin, Biological Series, 20:1-177.), this difference can be caused by the collecting method, since male flies are more active and more easily detected on host bodies than females. On the other hand, Fritz (1983) suggested that females leave the host during the first hours of the night for larviposition, so bats may have more males than females during times in which they are foraging outside the refuges. While, Dick & Patterson (2008DICK, C.W. & PATTERSON, B. 2008. An excess of males: skewed sex ratios in bat flies (Diptera: Streblidae). Evolutionary Ecology, 22:757-769.) and Dittmar et al. (2011DITTMAR, K.; MORSE, S.; GRUWELL, M.; MAYBERRY, J. & DIBLASI, E. 2011. Spatial and temporal complexities of reproductive behavior and sex ratios: a case from parasitic insects. Plos One, 6(5):1-9.) indicated that the bias is due to selective grooming by the hosts, because females are larger than males, host-grooming activity removes or kills more females than males. However, sex ratio can vary seasonally (Marshall, 1981MARSHALL, A. 1981. The sex ratio in ectoparasitic insects. Ecological Entomology, 6:155-174.) and evaluations based on short-term or limited surveys may provide an incomplete picture (Autino et al., 2011AUTINO, A.G.; CLAPS, G.L.; BARQUEZ, R.M. & DÍAZ, M.M. 2011. Ectoparasitic insects (Diptera: Streblidae and Siphonaptera: Ischnopsyllidae) of bats from Iquitos and surrounding areas (Loreto, Peru). Memórias do Instituto Oswaldo Cruz, 106(8):917-925.).

Phyllostomidae was the family with greatest species richness and abundance, which agrees with results found by other studies in the department of Sucre (Sampedro et al., 2007SAMPEDRO, A.; MARTÍNES, C.; DE LA OSSA, K.; OTERO, Y.; SANTOS, L.; OSORIO, S. & MERCADO, A. 2007. Nuevos registros de especies de murciélagos para el Departamento de Sucre y algunos datos sobre su ecología en esta región colombiana. Caldasia, 29:355-362.; Galván-Guevara et al., 2009GALVÁN-GUEVARA, S.; SIERRA, M.; GÓMEZ, F.; DE LA OSSA, J. & FAJARDO-PATIÑO, A. 2009. Biodiversidad en el área de influencia de la estación Primates de Colosó, Sucre, Colombia. Revista Colombiana de Ciencia Animal, 1:98-121.; Montes et al., 2012MONTES, A.; DURÁN, A.; OVIEDO, N.; LÓPEZ, Y. & DÍAZ, J. 2012. Nuevos datos sobre la distribución de Pteronotus personatus (Wagner, 1843) (Chiroptera: Mormoopidae) en Colombia. Revista Colombiana de Ciencia Animal, 4(2):435-440.; Durán & Canchila, 2015DURÁN, A. & CANCHILA, S. 2015. Ensamblaje de murciélagos (Mammalia: Chiroptera) en dos zonas del departamento de Sucre, Colombia. Acta Zoológica Mexicana (n.s.), 31(3):358-366.). This area has a dry tropical forest relict with abundant food and refuge availability, moreover, this family has the highest diversity in the Neotropical region, with a wide range of trophic guilds and foraging habits in all forest strata (Bonaccorso, 1979BONACCORSO, F. 1979. Foraging and reproductive ecology in a Panamanian bat community. Bulletin of the Florida State Museum Biological Science, 24(4):360-406.; Fleming, 1986FLEMING, T. 1986. The structure of neotropical bat communities: a preliminary analysis. Revista Chilena de Historia Natural, 59:135-150.; Gardner, 2008GARDNER, A. 2008. Mammals of South America: Marsupials, xenarthrans, shrews, and bats. Chicago, University of Chicago Press.). On the other hand, the low number of individuals caught from other families, such as Mormoopidae and Emballonuridae, is due to sampling limitations (mist nets being installed only at ground level) and flight behavior, because these families are characterized as species with high flight between and above the forest canopy (Bonaccorso, 1979BONACCORSO, F. 1979. Foraging and reproductive ecology in a Panamanian bat community. Bulletin of the Florida State Museum Biological Science, 24(4):360-406.; Muñoz, 2001MUÑOZ, J. 2001. Los murciélagos de Colombia. Sistemática, distribución, descripción, historia natural y ecología. Medellín, Editorial Universidad de Antioquia.; Gardner, 2008GARDNER, A. 2008. Mammals of South America: Marsupials, xenarthrans, shrews, and bats. Chicago, University of Chicago Press.; Tarquino-Carbonell et al., 2015TARQUINO-CARBONELL, A.; GUITIERREZ-DÍAZ, K.; GALINDO-ESPINOZA, E.; REINOSO-FLÓREZ, G.; SOLARI, S. & GUERRERO, R. 2015. Ectoparasites associated with bats in Northastern Tolima, Colombia. Mastozoología Neotropical, 22(2):349-358.).

Ectoparasites prevalence in the bat assemblage (P: 48.57%) was greater than reported in other dry tropical forest of Colombia (P: 36.42%) (Figure 1), which present approximately twice of average annual rainfall (Tarquino-Carbonell et al., 2015TARQUINO-CARBONELL, A.; GUITIERREZ-DÍAZ, K.; GALINDO-ESPINOZA, E.; REINOSO-FLÓREZ, G.; SOLARI, S. & GUERRERO, R. 2015. Ectoparasites associated with bats in Northastern Tolima, Colombia. Mastozoología Neotropical, 22(2):349-358.). On the other hand, studies in Brazil show a prevalence of 36.88% in São Paulo (Bertola et al., 2005BERTOLA, P.B.; AIRES, C.C.; FAVORITO, S.E.; GRACIOLLI, G.; AMAKU, M. & 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. Memórias do Instituto Oswaldo Cruz, 100:25-32.), 29.90% in Pernambuco (Soares et al., 2013SOARES, F.A.M.; GRACIOLLI, G.; ALCÂNTARA, D.M.C.; RIBEIRO, C.E.B.P.; VALENÇA, G.C. & FERRARI, S.F. 2013. Bat flies (Diptera: Streblidae) ectoparasites of bats at an Atlantic Rainforest site in northeastern Brazil. Biota Neotropical, 13(2):242-246.), 28.9% in Maranhão (Santos et al., 2009SANTOS, C.; DIAS, P.; RODRIGUES, F.; LOBATO, K.; ROSA, L.; OLIVEIRA, T. & REBÊLO, J. 2009. Moscas ectoparasitas (Diptera: Streblidae) de morcegos (Mammalia: Chiroptera) do município de São Luís, MA: taxas de infestação e associações parasito-hospedeiro. Neotropical Entomology, 38(5):595-601.), 23% in Rio de Janeiro (França et al., 2013FRANÇA, D.S.; PEREIRA, S.N.; MAAS, A.C.S.; MARTINS, M.A.; BOLZAN, D.P.; LIMA, I.P.; DIAS, D. & PERACCHI, A.L. 2013. Ectoparasitic flies (Diptera, Streblidae) of bats (Chiroptera, Phyllostomidae) in an Atlantic Forest area, southeastern Brazil. Brazilian Journal of Biology, 73(4):847-854.), and 20.12% in Rio Grande do Sul (Rui & Graciolli, 2005RUI, A. & GRACIOLLI, G. 2005. Moscas ectoparasitas (Diptera, Streblidae) de morcegos (Chiroptera, Phyllostomidae) no sul do Brasil: associações hospedeiro-parasitos e taxas de infestação. Revista Brasileira de Zoologia, 22(2):438-445.); while Cuxim-Koyoc et al. (2015CUXIM-KOYOC, A.; REYES-NOVELO, E.; MORALES-MALACARA, J.; BOLÍVAR-CIMÉ, B. & LABORDE, J. 2015. Streblidae (Diptera: Hippoboscoidea) from Yucatán and updates species list for México. Journal of Medical Entomology, 52(5):947-961.) found a prevalence of 74.06% in Yucatán-México. These differences may be related to the conditions in which the studies were conducted, variations in host and ectoparasites communities, and to different biogeographic history (Rui & Graciolli, 2005RUI, A. & GRACIOLLI, G. 2005. Moscas ectoparasitas (Diptera, Streblidae) de morcegos (Chiroptera, Phyllostomidae) no sul do Brasil: associações hospedeiro-parasitos e taxas de infestação. Revista Brasileira de Zoologia, 22(2):438-445.; Lourenço et al., 2016LOURENÇO, E.C.; ALMEIDA, J.C. & FAMADAS, K.M. 2016. Richness of ectoparasitic flies (Diptera: Streblidae) of bats (Chiroptera): a systematic review and meta-analysis of studies in Brazil. Parasitology Research, 115(11):4379-4388.).

The new host-ectoparasites associations (Artibeus planirostris-Trichobius costalimai, Lophostoma silvicolum-Strebla mirabilis, and Lophostoma silvicolum-Trichobius parasiticus) can be considered primary according to the established definition of Dick (2007DICK, C.W. 2007. High host specificity of obligate ectoparasites. Ecological Entomology, 32:446-450.). On the other hand, several associations found in this study may be classified as accidental or transitory because they have not previously registered and had low SI (Table 2). Graciolli & Carvalho (2001GRACIOLLI, G. & CARVALHO, C. 2001. Moscas ectoparasitas (Diptera: Hippoboscoidea) de morcegos (Mammalia: Chiroptera) do estado do Paraná. II. Streblidae. Chave pictórica para gêneros e espécies. Revista Brasileira de Zoologia, 18:907-960.) suggested that this type of association may be related to failures in the collection methodology or due to the proximity of refuges used by different bats species, and will require additional studies in order to validate these parasitic relationships.

The absence of Streblidae on M. megalotis, M. molossus, P. parnellii, and S. bilineata could be related to the low number of individuals captured or due to unevidenced reasons. Several studies show some unparasitized bat species (Hofstede et al., 2004HOFSTEDE, H.; FENTON, M. & WHITAKER, J. 2004. Host and host-site specificity of bat flies (Diptera: Streblidae and Nycteribiidae) on Neotropical bats (Chiroptera). Canadian Journal of Zoology, 82:616-626.; Bertola et al., 2005BERTOLA, P.B.; AIRES, C.C.; FAVORITO, S.E.; GRACIOLLI, G.; AMAKU, M. & 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. Memórias do Instituto Oswaldo Cruz, 100:25-32.), however, Guerrero (1997GUERRERO, R. 1997. Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) del Nuevo Mundo. VII. Lista de especies, hospedadores y países. Acta Biológica Venezuélica, 17:9-24.) offers a Streblidae list with host reported in America, and Saccopteryx leptura Schreber, 1774 is the only species that is not associated with any ectoparasite. Futhermore, these species of bats were also found infested in other studies, as Hofstede et al. (2004HOFSTEDE, H.; FENTON, M. & WHITAKER, J. 2004. Host and host-site specificity of bat flies (Diptera: Streblidae and Nycteribiidae) on Neotropical bats (Chiroptera). Canadian Journal of Zoology, 82:616-626.), Bertola et al. (2005BERTOLA, P.B.; AIRES, C.C.; FAVORITO, S.E.; GRACIOLLI, G.; AMAKU, M. & 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. Memórias do Instituto Oswaldo Cruz, 100:25-32.), Dick & Gettinger (2005DICK, C.W. & GETTINGER, D. 2005. A faunal survey of streblid bat flies (Diptera: Streblidae) associated with bats in Paraguay. Journal of Parasitology, 91:1015-1024.), Autino et al. (2011AUTINO, A.G.; CLAPS, G.L.; BARQUEZ, R.M. & DÍAZ, M.M. 2011. Ectoparasitic insects (Diptera: Streblidae and Siphonaptera: Ischnopsyllidae) of bats from Iquitos and surrounding areas (Loreto, Peru). Memórias do Instituto Oswaldo Cruz, 106(8):917-925.), Figueiredo et al. (2015FIGUEIREDO, D.; GRACIOLLI, G. & AGUIAR, L. 2015. New records of bat flies (Diptera, Streblidae and Nycteribiidae) in Cerrado of Central Brazil. Check List, 11(5):1761.), and Tlapaya-Romero et al. (2015TLAPAYA-ROMERO, L.; HORVÁTH, A.; GALLINA-TESSARO, S.; NARANJO, E. & 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, 86:377-385.).

It is important to highlight that this is the second study carried out in the Colombian dry tropical forests (Figure 1). Through this work, it was possible expand the knowledge of streblid flies and their host-parasitic associations in the Sucre department and the Colombian Caribbean region. However, other species are expected to be registered in this and other regions of the country, because there are still few studies related to bat flies and also by the existence of different geographical areas to explore.

ACKNOWLEDGMENTS

We are grateful to Carlos Molano and members of Grupo de Investigación en Zoología y Ecología for their help in fieldwork, also to the University of Sucre by partially financial support for this study and to the Federal University of Mato Grosso do Sul by logistics that allowed developing activities of taxonomic identification of Streblidae. The second author thanks to Rodrigo Dios, Marcelo Santis and Filipe Gudin for reviewing earlier versions of the manuscript, and Daniel Alcantara for his help with the preparation of map.

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  • 1
    Editor Responsável: Carlos José Einicker Lamas

Publication Dates

  • Publication in this collection
    2017

History

  • Received
    14 Dec 2016
  • Accepted
    16 Mar 2017
Museu de Zoologia da Universidade de São Paulo Av. Nazaré, 481, Ipiranga, 04263-000 São Paulo SP Brasil, Tel.: (55 11) 2065-8133 - São Paulo - SP - Brazil
E-mail: einicker@usp.br