Bat fly (Diptera: Streblidae) and common vampire bat (Chiroptera: Phyllostomidae) association in Honduras: prevalence, mean intensity, infracommunities and influence of the biological characteristics of the host

Wilson Gómez-Corea Farlem G. España David Mejía-Quintanilla Martín R. del Valle Alvarez About the authors

ABSTRACT

Bat species present a series of attributes that makes them prone to being parasitized. Bat flies (Streblidae) are hematophagous ectoparasites exclusive to bats. Our study aimed to investigate the association of bat flies with the Common vampire bat, Desmodus rotundus (É. Geoffroy, 1810), in Honduras. We analyzed the effect of sex and age of the host on parasitism. Eight localities belonging to six departments were sampled in an altitudinal range between 50 and 995 m. Field data were obtained between May 2018 to November 2019 and 80 individuals were captured, from which 395 bat flies were extracted. Four species of bat flies were registered: Strebla wiedemanni Kolenati, 1856, Trichobius parasiticus Gervais, 1844, T. joblingi Wenzel, 1966 and T. caecus Edwards, 1948. Trichobius parasiticus presented the highest prevalence and mean intensity, followed by S. wiedemanni. Trichobius joblingi and T. caecus are new records of parasitism on D. rotundus for Honduras, although we consider as an accidental association. We recorded six types of infracommunities that parasitized 85% of the hosts. The prevalence and mean intensity was not affected by age and sex of the host for any bat fly species.

KEY WORDS:
Bats; Central America; Desmodus rotundus; Phyllostomidae; Strebla; Streblidae; Trichobius

INTRODUCTION

In the Neotropical region, bat flies (Nycteribiidae and Streblidae) are the most conspicuous and well studied ectoparasites of bats (Haelewaters et al. 2018Haelewaters D, Hiller T, Dick CW (2018) Bats, Bat Flies, and Fungi: A Case of Hyperparasitism. Trends in Parasitology 9: 784-799. https://doi.org/10.1016/j.pt.2018.06.006
https://doi.org/10.1016/j.pt.2018.06.006...
). They are obligate ectoparasites exclusively associated with bats that live in the fur and on the membranes of their hosts, where they feed on blood (Dick et al. 2016Dick CW, Graciolli G, Guerrero R (2016) Family streblidae. Zootaxa 4122: 784-802. https://doi.org/10.11646/zootaxa.4122.1.67
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). They only leave their bat host to deposit a 3rd instar larvae, which develops within its mother’s oviduct and pupates directly on a surface in the bat’s roost (Hagan 1951Hagan HR (1951) Embryology of the Viviparous Insects. Ronald Press, New York, 472 pp. https://doi.org/10.1093/aibsbulletin/2.1.9-g
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, Hart 1992Hart BL (1992) Behavioral adaptations to parasites: an ethological approach. The Journal of Parasitology 78: 256-265.). Streblidae is cosmopolitan, occurring mainly in tropical areas and comprising 33 genera and about 239 species. Five subfamilies have been recognized, three of them exclusive to America: Trichobiinae, Strebliinae and Nycterophiliinae (Dick and Miller 2010Dick CW, Miller JA (2010) Streblidae (Bat Flies). In: Brown BV, Borkent A, Cumming JM, Wood DM, Woodley NE, Zumbado M (Eds) Manual of Central American Diptera. NRC Research Press, Ottawa, vol. 2, 1249-1260., Dick and Graciolli 2013Dick CW, Graciolli G (2013) Checklist of World Streblidae (Diptera: Hippoboscoidea). Available online at: https://www.researchgate.net/publication/322578987_Checklist_of_World_Streblidae_Diptera Hippoboscoidea
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). In Honduras, 48 species, 17 genera of Streblidae are known (Dick 2013Dick CW, Miller JA (2010) Streblidae (Bat Flies). In: Brown BV, Borkent A, Cumming JM, Wood DM, Woodley NE, Zumbado M (Eds) Manual of Central American Diptera. NRC Research Press, Ottawa, vol. 2, 1249-1260., Miller 2014Miller C (2014) Host specificity and ectoparasite load of bat flies in Utila, Honduras. Senior Honors Thesis, University of New Orleans, New Orleans, 21 pp. Available online at: https://scholarworks.uno.edu/honors_theses/63/?utm_source=scholarworks.uno.edu%2Fhonors_theses%2F63&utm_medium=PDF&utm_campaign=PDFCoverPages
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Many bat fly species are strictly associated to a single bat species, while their bat hosts in turn can be associated with a small number of different bat flies (Wenzel et al. 1966Wenzel RL, Tipton VJ, Kiewlicz A (1966) The Streblid bat flies of Panama (Diptera: Calyptera: Streblidae). In: Wenzel RL, Tipton VJ (Eds) Ectoparasites of Panama. Field Museum of Natural History, Chicago, 405-675., Wenzel 1976Wenzel RL (1976) The streblid bat flies of Venezuela (Diptera: Striblidae). Bringham Young University Science Bulletin 20: 1-175., Dick and Gettinger 2005Dick CW, Gettinger D (2005) A faunal survey of streblid flies (Diptera: Streblidae) associated with bats in Paraguay. Journal of Parasitology 91: 1015-1024. https://doi.org/10.1645/GE-536R.1
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). While host body condition in part limits parasite burden, competition for nutrients as well as resistance from host’s immune response have led to the evolution of highly diverse parasite communities (Haelewaters et al. 2018Haelewaters D, Hiller T, Dick CW (2018) Bats, Bat Flies, and Fungi: A Case of Hyperparasitism. Trends in Parasitology 9: 784-799. https://doi.org/10.1016/j.pt.2018.06.006
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). Morphological adaptations of ectoparasites have often led to the division of resources, allowing the coexistence of several species of parasites in a single host; each host individual forms the living environment for its associated parasites (Marshall 1982Marshall AG (1982) Ecology of insects ectoparasitic on bats. In: Kunz T (Ed.) Ecology of bats. Plenum Press, New York, 369-401. https://doi.org/10.1007/978-1-4613-3421-7_10
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, Mouillot et al. 2003Mouillot D, George-Nascimento M, Poulin R (2003) How parasites divide resources: a test of the niche apportionment hypothesis. Journal of Animal Ecology 72: 757-764. https://doi.org/10.1046/j.1365-2656.2003.00749.x
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, Haelewaters et al. 2018Haelewaters D, Hiller T, Dick CW (2018) Bats, Bat Flies, and Fungi: A Case of Hyperparasitism. Trends in Parasitology 9: 784-799. https://doi.org/10.1016/j.pt.2018.06.006
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). Bat fly species prefer particular areas on the host’s body (Roos 1961Ross A (1961) Biological studies on bat ectoparasites of the genus Trichobius (Diptera: Streblidae) in North America, North of Mexico. The Wasmann Journal of Biology 19: 229-246., Wenzel et al. 1966Wenzel RL, Tipton VJ, Kiewlicz A (1966) The Streblid bat flies of Panama (Diptera: Calyptera: Streblidae). In: Wenzel RL, Tipton VJ (Eds) Ectoparasites of Panama. Field Museum of Natural History, Chicago, 405-675., Linhares and Komeno 2000Linhares AX, Komeno CA (2000) Trichobius joblingi, Aspidoptera falcata, and Megistopoda proxima (Diptera: Streblidae) parasitic on Carollia perspicillata and Sturnira lillium (Chiroptera: Phyllostomidae) in southeastern Brazil: sex ratios seasonality, host site preference, and effect of parasitism on the host. Journal of Parasitology 86: 167-170. https://doi.org/10.1645/0022-3395(2000)086[0167:TJAFAM]2.0.CO;2, ter Hofstede et al. 2004ter Hofstede HM, Fenton MB, Whitaker JO (2004) Host and host-site specificity of bat flies (Díptera: Streblidae and Nycteribiidae) on Neotropical bats (Chiroptera). Canadian Journal of Zoology 82: 616-626. https://doi.org/10.1139/Z04-031
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).

Bats have several attributes that make them prone to being parasitized: gregarious behavior, grooming, body size, age, sex, individual genetic aspects, nutritional status, areas of activity (see Poulin and Morand 2004Poulin R, Morand S (2004) Parasite biodiversity. Smithsonian Institution Press, Washington, D.C., 216 pp.). Compared to mammals of similar size, their life expectancy is very high (Seim et al. 2013Seim I, Fang X, Xiong Z, Lobanov AV, Huang Z, Ma S, Feng Y, Turanov AA, Zhu Y, Lenz TL, Gerashchenko MV, Fan D, Hee-Yim S, Yao X, Jordan D, Xiong Y, Ma Y, Lyapunov AN, Chen G, Kulakova OI, Sun Y, Lee SG, Bronson RT, Moskalev AA, Sunyaev SR, Zhang G, Krogh A, Wang J, Gladyshev VN (2013) Genome analysis reveals insights into physiology and longevity of the Brandt’s bat Myotis brandtii. Nature Communications 4: 2212. https://doi.org/10.1038/ncomms3212
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, Garbino et al. 2021Garbino GST, Feijó A, Beltrão-Mendes R, Rocha PA da (2021) Evolution of litter size in bats and its influence on longevity and roosting ecology. Biological Journal of the Linnean Society 132: 676-684. https://doi.org/10.1093/biolinnean/blaa203
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). Bats use a variety of roost structures, including foliage, tree cavities, abandoned buildings, and large cave systems (Patterson et al. 2007Patterson B, Dick C, Dittmar K (2007) Roosting habits of bats affect their parasitism by bat flies (Diptera: Streblidae). Journal of Tropical Ecology 23: 177-189. https://doi.org/10.1017/S0266467406003816
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). Male and female bats often behave differently and exhibit sexual segregation, particularly pronounced during the maternity season when females congregate to give birth and raise offspring (Fleming 1988Fleming TH (1988) The short-tailed fruit bat: a study in plant-animal interactions. University of Chicago Press, Chicago, 365 pp., McCracken and Wilkinson 2000McCracken GF, Wilkinson GS (2000) Bat mating systems. In: Crichton EG, Krutzsch PH (Eds) Reproductive biology of bats. Academic Press, New York, 321-362., Kunz and Lumsden 2003Kunz TH, Lumsden LF (2003) Ecology of cavity and foliage roosting bats. In: Kunz TH, Fenton MB (Eds) Bat ecology. University of Chicago Press, Chicago, 3-89., Chaverri et al. 2007Chaverri G, Quiros OE, Gamba-Rios M, Kunz TH (2007) Ecological correlates of roost fidelity in the tentmaking bat Artibeus watsoni. Ethology 113: 598-605. https://doi.org/10.1111/j.1439-0310.2007.01365.x
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). In contrast, many males frequently roost singly or in low numbers away from females, especially during the nursing season (McCracken and Wilkinson 2000McCracken GF, Wilkinson GS (2000) Bat mating systems. In: Crichton EG, Krutzsch PH (Eds) Reproductive biology of bats. Academic Press, New York, 321-362., Altringham 2011Altringham JD (2011) Bats: from evolution to conservation. Oxford University Press, Oxford, 2nd ed., 324 pp. https://doi.org/10.1093/acprof:osobl/9780199207114.001.0001
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) and can display lower roost fidelity than females (e.g., Morrison 1979Morrison DW (1979) Apparent Male Defense of Tree Hollows in the Fruit Bat, Artibeus jamaicensis. Journal of Mammalogy 60: 11-15. https://doi.org/10.2307/1379753
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). Some males, however, roost with groups of females in harems year round (McCracken and Wilkinson 2000McCracken GF, Wilkinson GS (2000) Bat mating systems. In: Crichton EG, Krutzsch PH (Eds) Reproductive biology of bats. Academic Press, New York, 321-362.). Grooming is one of the major causes of parasite mortality (Marshall 1982Marshall AG (1982) Ecology of insects ectoparasitic on bats. In: Kunz T (Ed.) Ecology of bats. Plenum Press, New York, 369-401. https://doi.org/10.1007/978-1-4613-3421-7_10
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), during breeding, females can reduce the intensity of this behavior and in juvenile individuals it is not very marked (Berlota et al. 2005Bertola PB, Aires CC, Favorito SE, Graciolli G, Amaku M, Pinto-Da-Rocha R (2005) Bat flies (Diptera: Streblidae, Nycteribiidae) parasitic on bats (Mammalia: Chiroptera) at Parque Estadual da Cantareira, Sáo Paulo, Brazil: Parasitism rates and host-parasite associations. Memórias do Instituto Oswaldo Cruz 100: 25-32. https://doi.org/10.1590/S0074-02762005000100005
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, Bezerra and Bocchiglieri 2018Bezerra RHS, Bocchiglieri A (2018) Association of ectoparasites (Diptera and Acari) on bats (Mammalia) in a restinga habitat in northeastern Brazil. Parasitology Research 117: 3413-3420. https://doi.org/10.1007/s00436-018-6034-0
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). Such ecological variation may cause bat species to differ in their susceptibility to the prevalence and intensity of parasitism, parameters directly related to the degree of exposure of hosts to parasites (Bush et al. 1997Bush AO, Lafferty K, Lotz J, Shosta JA (1997) Parasitology meets ecology on its own terms: Margolis et al. revisi ted. The Journal of Parasitology 83: 575-583. https://doi.org/10.2307/3284227
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).

The Common vampire bat Desmodus rotundus (É. Geoffroy, 1810) (Chiroptera: Phyllostomidae) has a wide geographical distribution in America, occurring from México to Argentina (Greenhall et al. 1983Greenhall AM, Joermann G, Schmidt U (1983) Desmodus rotundus. Mammalian Species 202: 1-6. https://doi.org/doi.org/10.2307/3503895
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, Koopman 1988Koopman KF (1988). Systematic and distribution. In: Greenhall AM, Schmidt U (Eds) Natural history of vampire bats. CRC Press, Florida, 7-1.). For this reason, the species has been relatively well-studied regarding its ectoparasitic fauna. Studies have recorded the presence of different bat fly species, the most frequent being those of Trichobius and Strebla (Wenzel et al. 1966Wenzel RL, Tipton VJ, Kiewlicz A (1966) The Streblid bat flies of Panama (Diptera: Calyptera: Streblidae). In: Wenzel RL, Tipton VJ (Eds) Ectoparasites of Panama. Field Museum of Natural History, Chicago, 405-675., Guerrero 1997Guerrero R (1997) Catálogo de los Streblidae (Diptera: Pupipara) parasitos de murcielagos (Mammalia: Chiroptera) del nuevo mundo. VII. Lista de especies, hospedadores y paises. Acta Biologica Venezuelica 17: 9-24.). In this context, our aim was to describe and analyse the association of bat flies with D. rotundus in Honduras, through different parasitic indices. We also identified infracommunities and tested the influence of the sex and age of the host on parasitism of bat flies.

MATERIAL AND METHODS

This study was conducted in Honduras, a Central America country with an area of 112,492 km2 that is divided into 18 departments. Characterized by elevations ranging from 0 to 2870 m.a.s.l. Honduras has a diverse topography and wide variety of tropical habitats. Some portions of the country have a dry climate with little rain, whereas other areas receive regular heavy rainfall; the annual average rainfall is 1000 to 2500 mm (Zúñiga 1990). The average annual temperature is 16 °C in the mountainous areas of the central and western region, and up to 24 °C in the inland valleys and the Atlantic coast (Zúñiga 1990Zúniga E (1990) Las Modalidades de la Lluvia en Honduras. Editorial Guaymuras, Tegucigalpa, 141 pp., Navarro-Racines et al. 2018Navarro-Racines CE, Monserrate F, Llanos L, Obando D, Córdoba Sánchez J (2018) Desarrollo de los Escenarios Climáticos de Honduras y Módulo Académico de Capacitación. CIAT, PNUD, Dirección Nacional de Cambio Climático de MiAmbiente, Honduras, 140 pp.). Field samplings were carried out in eight localities, in an altitudinal range between 50 and 995 m (Table 1). We used a Garmin eTrex 10 Global Positioning System, we obtained geographical coordinates (WGS 84) and elevation, and mapped them using QGIS version 3.14 (Fig. 1).

Figure 1
Geographic location of the study sites in Honduras: 1) Joya Grande, 2) Río Arcagual, 3) Los Ochales, 4) Lainez, 5) El Hizopo, 6) Cuevas de Talgua, 7) UNAG, 8 Kurpha. See Table 1 for details.

Table 1
Sampling locations in Honduras between May 2018 to November 2019 with their respective geographic information and distribution by department of bat flies. Code in map (CM), Altitude (A).

The field data were obtained between May 2018 and November 2019. We used mist nets with the lengths of 12 m and 9 m long x 3 m high (38 mm mesh) set at ground-level (~0.5-4.0 m height). We surveyed three nights at each site with an ope rating time of 05:00 pm to 10:00 pm, with nets checked for captured bats at 15 minutes intervals. The mist nets were placed, considering the characteristics of the sampled locations, trails, glades, near streams, caves, and shelters (Kunz et al. 2009Kunz TH, Hodgkison R, Weise C (2009) Methods of capturing and handling bats. In: Kunz TH, Parsons S (Eds) Ecological and behavioral methods for the study of bats. Johns Hopkins University Press, Baltimore, 2nd ed., 3-35.) and avoiding the days close to the full moon (Saldaña-Vázquez and Munguía-Rosas 2013Saldaña-Vázquez RA, Munguía-Rosas MA (2013) Lunar phobia in bats and its ecological correlates: A meta-analysis. Mammalian Biology 78: 216-219. https://doi.org/10.1016/j.mambio.2012.08.004
https://doi.org/10.1016/j.mambio.2012.08...
). For taxonomic identification of the bats, we used the publications of Timm et al. (1999Timm RM, Laval RK, Rodrigues B (1999) Clave de campo para los Murciélagos de Costa Rica. Brenesia 52: 1-32.), Medellín et al. (2008Medellín RA, Arita TH, Sánchez HO (2008) Identificación de los murciélagos de México, clave de campo. Instituto de Ecología, Universidad Nacional Autónoma de México, D.F, México, 2nd ed., 83 pp.) and Medina-Fitoria (2014Medina-Fitoria A (2014) Murciélagos de Nicaragua, guía de campo. MARENA/PCMN, Managua, 280 pp.). Each individual bat captured was classified according to the sex class (males and females), age (adults and juveniles), determined by the degree of ossification of the epiphysis of the phalanges (Brunet-Rossini and Wilkinson 2009Brunet-Rossini AK, Wilkinson GS (2009) Methods for age estimation and the study of senescence in bats. In: Kunz TH, Parsons S (Eds) Ecological and behavioral methods for the study of bats. The Johns Hopkins University Press, Baltimore, 315-325.). Bats were captured and handled in the field following guidelines approved by the American Society of Mammalogists (Sikes and the Animal Care and Use Committee of the American Society of Mammalogists 2016Sikes RS, The Animal Care and Use Committee of the American Society of Mammalogists (2016) Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. Journal of Mammalogy 97: 663-688. https://doi.org/10.1093/jmammal/gyw078
https://doi.org/10.1093/jmammal/gyw078...
). The research and collection of the specimens were carried out with the permission granted by ICF (Instituto Nacional de Desarrollo y Conservación Forestal, Áreas Protegidas y Vida Silvestre), resolution DE-MP-067-2018.

Bats captured in the mist nets were individually placed in cloth bags to prevent contamination of ectoparasite samples. The entire body of each bat was systematically examined with entomological forceps until no additional bat flies were found. The bat flies extracted were placed in Eppendorf tubes (assigning an individual registration code, for each bat), with 70% ethanol, 5% glycerin and 25% distilled water (Whitaker et al. 2009Whitaker JO Jr, Ritzi CM, Dick CW (2009) Collecting and preserving bat ectoparsites for ecological study. In: Kunz TH, Parsons S (Eds) Ecological and behavioral methods for the study of bats . Johns Hopkins University Press, Baltimore , 2nd ed., 806-827.). All the collected individuals were counted and identified using stereoscopic microscope, in the installations of the Entomology Museum of the Universidad Nacional Autonoma de Honduras (UNAH). We used the reference literature for taxonomic identification, Wenzel et al. (1966Wenzel RL, Tipton VJ, Kiewlicz A (1966) The Streblid bat flies of Panama (Diptera: Calyptera: Streblidae). In: Wenzel RL, Tipton VJ (Eds) Ectoparasites of Panama. Field Museum of Natural History, Chicago, 405-675.), Wenzel (1976Wenzel RL (1976) The streblid bat flies of Venezuela (Diptera: Striblidae). Bringham Young University Science Bulletin 20: 1-175.), Guerrero (1994Guerrero R (1994) Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) del Nuevo Mundo. II. Los grupos: pallidus, caecus, major, uniformis y longipes del genero Trichobius Gervais, 1844. Acta Biologica Venezuelica 15: 1-1., 1995Guerrero R (1995) Catalogo de los Streblidos (Diptera: Pupipara) parasitos de murcielagos (Mammalia: Chiroptera) del Nuevo mendo. III. Los Grupos: Dugessi, Dunii y Phyllostomae del genero Trichobius Gervais, 1844. Acta Biologica Venezuelica 14: 1-27.). Voucher specimens were deposited in the entomology collection of the Natural History Museum of the Universidad Nacional Autonoma de Honduras in the Valle de Sula: UNAH-VS: UVS-I-1189, UVS-I-1190, UVS-I-1191, UVS-I-1192.

To analyse the parasite-host association, we consider three parasitological parameters: prevalence, mean abundance, mean intensity (Bush et al. 1997Bush AO, Lafferty K, Lotz J, Shosta JA (1997) Parasitology meets ecology on its own terms: Margolis et al. revisi ted. The Journal of Parasitology 83: 575-583. https://doi.org/10.2307/3284227
https://doi.org/10.2307/3284227...
). The prevalence (P) is the proportion of hosts infested with a particular ectoparasite species divided by the total number of hosts examined (Bush et al. 1997Bush AO, Lafferty K, Lotz J, Shosta JA (1997) Parasitology meets ecology on its own terms: Margolis et al. revisi ted. The Journal of Parasitology 83: 575-583. https://doi.org/10.2307/3284227
https://doi.org/10.2307/3284227...
). Mean abundance (MA) is the total number of individuals of an ectoparasite species in a sample of a host species divided by the total number of hosts examined (Bush et al. 1997). Mean intensity (MI) represents the total number of individuals of an ectoparasite species in a sample of a host species divided by the total number of hosts infested (Bush et al. 1997Bush AO, Lafferty K, Lotz J, Shosta JA (1997) Parasitology meets ecology on its own terms: Margolis et al. revisi ted. The Journal of Parasitology 83: 575-583. https://doi.org/10.2307/3284227
https://doi.org/10.2307/3284227...
). We estimated the confidence intervals (at 95%) for these parameters and were calculated using Quantitative Parasitology software 3.0 (Reiczigel et al. 2019Reiczigel J, Marozzi M, Fábián I and Rózsa L (2019) Biostatistics for parasitologists - a primer to Quantitative Parasitology. Trends in Parasitology 35: 277-281. https://doi.org/10.1016/j.pt.2019.01.003
https://doi.org/10.1016/j.pt.2019.01.003...
).

To determine if the intrinsic attributes (sex: male-female, age: juvenile-adult) of the Common vampire bat are conditioning factors of the different bat fly species, we performed analysis for three species of bat flies. We used Fisher’s exact Test to compare prevalence and a Bootstrap two-sample t test to compare both mean intensity (Reiczigel et al. 2019Reiczigel J, Marozzi M, Fábián I and Rózsa L (2019) Biostatistics for parasitologists - a primer to Quantitative Parasitology. Trends in Parasitology 35: 277-281. https://doi.org/10.1016/j.pt.2019.01.003
https://doi.org/10.1016/j.pt.2019.01.003...
). Trichobius caecus was excluded from statistical analysis, due to their low abundance in our sample size. Infracommunities (community of parasite infrapopulations in a single host, sensu Bush et al. 1997Bush AO, Lafferty K, Lotz J, Shosta JA (1997) Parasitology meets ecology on its own terms: Margolis et al. revisi ted. The Journal of Parasitology 83: 575-583. https://doi.org/10.2307/3284227
https://doi.org/10.2307/3284227...
) are represented through their relative frequency in percentage. A Spearman rank correlation test (rs) was performed between the associations of primary and accidental bat flies in the same host. The complementary analysis were carried out using the PAST version 4.03 (Hammer et al. 2001Hammer O, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electronica 4: 1-9.), with the significant level at p < 0.05. The capture effort was calculated according to Straube and Bianconi (2002Straube FC, Bianconi GV (2002) Sobre a grandeza e a unidade utilizada para estimar esforço de captura com utilização de redes-de-neblina. Chiroptera Neotropical 8: 150-152.).

RESULTS

With a sampling effort of 19.017 m2/h, a total of 80 bats were captured and reviewed, of which 68 were infected with at least one bat fly species (Fig. 2). A total of 395 bat flies were collected, belonging to four species, two genera in two subfamilies. The most abundant was Trichobiinae (n = 315; 79.75%) with three species and Streblinae (n = 80; 20.25%) only with one species. Trichobius parasiticus Gervais, 1844 and Strebla wiedemanni Kolenati, 1856 have a primary association with this host, whereas Trichobius joblingiWenzel, 1966Wenzel RL, Tipton VJ, Kiewlicz A (1966) The Streblid bat flies of Panama (Diptera: Calyptera: Streblidae). In: Wenzel RL, Tipton VJ (Eds) Ectoparasites of Panama. Field Museum of Natural History, Chicago, 405-675. and Trichobius caecus Edwards, 1948 are considered non-primary species.

Figure 2
Infestation intensity of Strebla wiedemanni, Trichobius joblingi, T. parasiticus and T. caecus, collected on Desmodus rotundus between May 2018 to November 2019 in Honduras.

Trichobius parasticus was the most abundant bat fly parasitizing D. rotundus in this study. Of the 395 bat flies collected, a total of 295 were T. parasiticus individuals, found on a total 58 bats. The highest prevalence value of the hosts was 72.50% provided by T. parasiticus, followed by S. wiedemanni with 25%. A total of 80 were S. wiedemanni individuals, parasitizing a total 20 bats. The mean abundance was 0.01 to 3.69 and the mean intensity of parasitic infestation ranges from 1.66 to 5.17, with an average 3.22 bat flies per host (Table 2). The greatest number of parasites collected from a single host was 18 individuals of T. parasiticus.

Table 2
Bat fly species collected on Desmodus rotundus between May 2018 to November 2019 in Honduras. Number of bat flies collected (N), number of infested hosts (IH), mean abundance (MA), mean intensity of infestation (MI), prevalence (P%), and maximum and minimum value (M/M), (95% CI in brackets).

We recorded six types of infracommunities that parasiti zed 85% of the hosts (Fig. 3). We found higher frequencies of infracommunities with one species (frequency of occurrence = 35, n = 201) than of infracommunities with two or more species (frequency of occurrence = 20, n = 194). Strebla wiedemanni presented a frequency of occurrence of five, while T. parasiticus with 30 was the most frequent, providing the highest prevalence among the hosts, 54.55%. Among the associations of the species of the genus Trichobius + Strebla, which share the same host, one association has three species and another three have two species. Trichobius parasiticus + S. wiedemanni was the most frequent coexistence, with a frequency of occurrence of 12 (21.82%), followed by four occurrences by T. parasiticus + T. joblingi. The rest of the associations presented a frequency of occurrence the two times. Trichobius parasiticus and T. joblingi had a statistically non-significant negative correlation (rs = -0.30, p = 0.49). The same non-significant association was found for T. parasiticus and T. caecus (rs = -0.86, p = 0.66).

Figure 3
Infracommunities of bat flies and relative frequency, collected on D. rotundus between May 2018 to November 2019 in Honduras.

The prevalence and mean intensity of infestation of T. parasiticus presented similar values in each of these parameters between males and females. While in the age class, the juvenile individuals present a higher prevalence of T. parasiticus (94. 74) and S wiedemanni (36.84) (Tables 3, 4). According to the results obtained for T. parasiticus, S. wiedemanni and T. joblingi, the prevalence test indicates no significant difference in the classes studied. Bootstrap two-sample t test suggests that the mean intensity of infestation was not affected by age and sex of the host for any of the species analyzed.

Table 3
Comparison of the prevalence by sex and age on Desmodus rotundus, considering the three bat fly species analysed. Number of infested hosts (IH), number of uninfested hosts (UH).

Table 4
Comparison of the mean intensity by sex and age on Desmodus rotundus, considering the three bat fly species analyzed. Number of infested hosts (IH), number of uninfested hosts (UH).

DISCUSSION

Bat fly association on D. rotundus

We found four species of bat flies on D. rotundus from different regions of Honduras. The highest values of the parasitic indices were for the two species of primary bat flies. Our data failed to support the hypothesis based, sex and age of the host, none of the bat flies studied showed preference. We found that the bat flies present different patterns of distribution and association in the hosts.

Among the bat flies S. wiedemanni and T. parasiticus repre senting the most common primary parasites in almost the entire distribution of D. rotundus (Wenzel et al. 1966Wenzel RL, Tipton VJ, Kiewlicz A (1966) The Streblid bat flies of Panama (Diptera: Calyptera: Streblidae). In: Wenzel RL, Tipton VJ (Eds) Ectoparasites of Panama. Field Museum of Natural History, Chicago, 405-675., Wenzel 1976Wenzel RL (1976) The streblid bat flies of Venezuela (Diptera: Striblidae). Bringham Young University Science Bulletin 20: 1-175., ter Hofstede et al. 2004ter Hofstede HM, Fenton MB, Whitaker JO (2004) Host and host-site specificity of bat flies (Díptera: Streblidae and Nycteribiidae) on Neotropical bats (Chiroptera). Canadian Journal of Zoology 82: 616-626. https://doi.org/10.1139/Z04-031
https://doi.org/10.1139/Z04-031...
, Dick 2013Dick CW, Graciolli G (2013) Checklist of World Streblidae (Diptera: Hippoboscoidea). Available online at: https://www.researchgate.net/publication/322578987_Checklist_of_World_Streblidae_Diptera Hippoboscoidea
https://www.researchgate.net/publication...
). Strebla wiedemanni is a primary and characteristic parasite of D. rotundus, occurs in Argentina, Brazil, Bolivia, Colombia, Ecuador, El Salvador, Guatemala, Honduras, Mexico, Panama, Peru, Suriname, Trinidad and Venezuela (Wenzel et al. 1966Wenzel RL, Tipton VJ, Kiewlicz A (1966) The Streblid bat flies of Panama (Diptera: Calyptera: Streblidae). In: Wenzel RL, Tipton VJ (Eds) Ectoparasites of Panama. Field Museum of Natural History, Chicago, 405-675., Guerrero 1996Guerrero R (1996) Catalogo de los Streblidos (Diptera: Pupipara) parasitos de murcielagos (Mammalia: Chiroptera) del Nuevo mundo. VI. Streblinae. Acta Biologica Venezuelica 16: 1-25., 1997Guerrero R (1997) Catálogo de los Streblidae (Diptera: Pupipara) parasitos de murcielagos (Mammalia: Chiroptera) del nuevo mundo. VII. Lista de especies, hospedadores y paises. Acta Biologica Venezuelica 17: 9-24., Dick 2013Dick CW (2013) Review of the Bat Flies of Honduras, Central América (Díptera: Streblidae). Journal of Parasitoly Research 2013: 437696. https://doi.org/10.1155/2013/437696
https://doi.org/10.1155/2013/437696...
). Of the genus Trichobius, only T. parasiticus is a characteristic parasite associated on D. rotundus, throughout its geographic distribution (Dick 2013Dick CW (2013) Review of the Bat Flies of Honduras, Central América (Díptera: Streblidae). Journal of Parasitoly Research 2013: 437696. https://doi.org/10.1155/2013/437696
https://doi.org/10.1155/2013/437696...
), however Trichobius furmani Wenzel, 1966, seems to replace in some areas of South America (Guerrero 1995Guerrero R (1995) Catalogo de los Streblidos (Diptera: Pupipara) parasitos de murcielagos (Mammalia: Chiroptera) del Nuevo mendo. III. Los Grupos: Dugessi, Dunii y Phyllostomae del genero Trichobius Gervais, 1844. Acta Biologica Venezuelica 14: 1-27.). Although T. joblingi and T. caecus are new records of parasitism for the Common vampire bat in Honduras, they are an accidental association, given the high specificity of ectoparasites (Dick 2007Dick CW (2007) High host specifificity of obligate ectoparasites. Ecological Entomology 32: 446-450. https://doi.org/10.1111/j.1365-2311.2007.00836.x
https://doi.org/10.1111/j.1365-2311.2007...
). Trichobius caecus occurs on momoorpid bats of Pteronotus (Wenzel 1976Wenzel RL (1976) The streblid bat flies of Venezuela (Diptera: Striblidae). Bringham Young University Science Bulletin 20: 1-175.).

A previous study in Honduras recorded T. caecus on Phyllostomus discolor Wagner, 1843 and P. mesoamericanus Smith, 1972 (cited as P. parnellii, see Pavan and Marroig 2016Pavan AC, Marroig G (2016) Integrating multiple evidences in taxonomy: species diversity and phylogeny of mustached bats (Mormoopidae: Pteronotus). Molecular Phylogenetics and Evolution 103: 184-198. https://doi.org/10.1016/j.ympev.2016.07.011
https://doi.org/10.1016/j.ympev.2016.07....
) (Dick 2013Dick CW, Graciolli G (2013) Checklist of World Streblidae (Diptera: Hippoboscoidea). Available online at: https://www.researchgate.net/publication/322578987_Checklist_of_World_Streblidae_Diptera Hippoboscoidea
https://www.researchgate.net/publication...
). We captured D. rotundus and P. mesoamericanus, on the same sampling night, and both species of bats were parasitized. It is possible that horizontal transfer from P. mesoamericanus occurred; considering the only previous registration of this association is mentioned by Wenzel et al. (1966Wenzel RL, Tipton VJ, Kiewlicz A (1966) The Streblid bat flies of Panama (Diptera: Calyptera: Streblidae). In: Wenzel RL, Tipton VJ (Eds) Ectoparasites of Panama. Field Museum of Natural History, Chicago, 405-675.) in Venezuela. Trichobius joblingi is a characteristic parasite of Carollia species throughout the extent of its range (Wenzel et al. 1966Wenzel RL, Tipton VJ, Kiewlicz A (1966) The Streblid bat flies of Panama (Diptera: Calyptera: Streblidae). In: Wenzel RL, Tipton VJ (Eds) Ectoparasites of Panama. Field Museum of Natural History, Chicago, 405-675., Wenzel 1976Wenzel RL (1976) The streblid bat flies of Venezuela (Diptera: Striblidae). Bringham Young University Science Bulletin 20: 1-175., Guerrero 1994Guerrero R (1994) Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) del Nuevo Mundo. II. Los grupos: pallidus, caecus, major, uniformis y longipes del genero Trichobius Gervais, 1844. Acta Biologica Venezuelica 15: 1-1.). In this study in the different sampling sites (Cortés, Lempira, El Paraiso, Gracias a Dios, Olancho and Valle); species of Carollia were sympatric with D. rotundus, mainly C. perspicillata (Linnaeus, 1758) and probably shared roost. Apparently, T. joblingi has low host specificity, since it has been registered as a parasite on D. rotundus in Brazil, Colombia, Mexico, Panama, Trinidad and Tobago and Venezuela (Wenzel et al. 1966Wenzel RL, Tipton VJ, Kiewlicz A (1966) The Streblid bat flies of Panama (Diptera: Calyptera: Streblidae). In: Wenzel RL, Tipton VJ (Eds) Ectoparasites of Panama. Field Museum of Natural History, Chicago, 405-675., Wenzel 1976Wenzel RL (1976) The streblid bat flies of Venezuela (Diptera: Striblidae). Bringham Young University Science Bulletin 20: 1-175., Bertola et al. 2005Bertola PB, Aires CC, Favorito SE, Graciolli G, Amaku M, Pinto-Da-Rocha R (2005) Bat flies (Diptera: Streblidae, Nycteribiidae) parasitic on bats (Mammalia: Chiroptera) at Parque Estadual da Cantareira, Sáo Paulo, Brazil: Parasitism rates and host-parasite associations. Memórias do Instituto Oswaldo Cruz 100: 25-32. https://doi.org/10.1590/S0074-02762005000100005
https://doi.org/10.1590/S0074-0276200500...
, 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. https://doi.org/10.1016/j.rmb.2015.04.012
https://doi.org/10.1016/j.rmb.2015.04.01...
, Durán et al. 2017Durán AA, García DMA, Graciolli G (2017) Ectoparasitic flies (Diptera, Streblidae) on bats (Mammalia, Chiroptera) in a dry tropical forest in the northern Colombia. Papeis Avulsos de Zoologia 57: 105-111. https://doi.org/10.11606/0031-1049.2017.57.08
https://doi.org/10.11606/0031-1049.2017....
), is possibly the most common ectopara sitic fly in the Neotropical region (Guerrero 1995Guerrero R (1995) Catalogo de los Streblidos (Diptera: Pupipara) parasitos de murcielagos (Mammalia: Chiroptera) del Nuevo mendo. III. Los Grupos: Dugessi, Dunii y Phyllostomae del genero Trichobius Gervais, 1844. Acta Biologica Venezuelica 14: 1-27.). The social structure of the Common vampire bat is complex and developed, they are generally spatially separated from other bat species that use the same shelter (Wilkinson 1985Wilkinson GS (1985) The social organization of the common vampire bat. Behavioral Ecology and Sociobiology 17: 123-134. https://doi.org/10.1007/BF00299244
https://doi.org/10.1007/BF00299244...
, Kunz and Lumsden 2003Kunz TH, Lumsden LF (2003) Ecology of cavity and foliage roosting bats. In: Kunz TH, Fenton MB (Eds) Bat ecology. University of Chicago Press, Chicago, 3-89., Aguiar and Antonini 2011Aguiar LM, Antonini Y (2011) Descriptive ecology of bat flies (Diptera: Hippoboscoidea) associated with vampire bats (Chiroptera: Phyllostomidae) in the cerrado of Central Brazil. Memórias do Instituto Oswaldo Cruz 106: 170-176. https://doi.org/10.1590/S0074-02762011000200009
https://doi.org/10.1590/S0074-0276201100...
); some ectoparasitic species are more likely to show strong host preferences when alternative bat host species roost together, while less specificity has been observed when host species roost alone (e.g., the streblid Raymondia pagodarum Speiser, 1900 prefers Hipposideros speoris (Schneider, 1800) over Rhinolophus rouxii Temminck, 1835, when these two bat species roost together - Seneviratne et al. 2009Seneviratne SS, Fernando HC, Udagama-Randeniya PV (2009) Host specificity in bat ectoparasites: a natural experiment. International Journal for Parasitology 39: 995-1002. https://doi.org/10.1016/j.ijpara.2008.12.009
https://doi.org/10.1016/j.ijpara.2008.12...
).

We were more successful in registering D. rotundus parasitized by bat flies in environments close to caves, which in fact are considered favorable for parasitism, as cave-roosting bats usually carry heavier parasite loads, and host a greater diversity of ectoparasites (Kunz 1982Kunz TH (1982) Roosting Ecology of Bats. In: Kunz TH (Ed.) Ecology of Bats. Springer, Boston, 1-55. https://doi.org/10.1007/978-1-4613-3421-7_1
https://doi.org/10.1007/978-1-4613-3421-...
, Patterson et al. 2007Patterson B, Dick C, Dittmar K (2007) Roosting habits of bats affect their parasitism by bat flies (Diptera: Streblidae). Journal of Tropical Ecology 23: 177-189. https://doi.org/10.1017/S0266467406003816
https://doi.org/10.1017/S026646740600381...
). Therefore, we would expect greater prevalence of infestation in species of bats with high roost fidelity than those with low roost fidelity (Fenton et al. 2001Fenton MB, Bernard E, Bouchard S, Hollis L, Johnston DS, Lausen CL, Ratcliffe JM, Riskin DK, Taylor JR, Zigouris J (2001) The bat fauna of Lamanai, Belize: roosts and trophic roles. Journal of Tropical Ecology 17: 511-524. https://doi.org/10.1017/S0266467401001389
https://doi.org/10.1017/S026646740100138...
, Kunz and Lumsden 2003Kunz TH, Lumsden LF (2003) Ecology of cavity and foliage roosting bats. In: Kunz TH, Fenton MB (Eds) Bat ecology. University of Chicago Press, Chicago, 3-89.). Trajano (1996Trajano E (1996) Movements of cave bats in southeastern Brazil, with emphasis on the population ecology of the common vampire bat, Desmodus rotundus (Chiroptera). Biotropica 28: 121-129. https://doi.org/10.2307/2388777
https://doi.org/10.2307/2388777...
) reported that, in a karst area of Brazil, D. rotundus moves between caves located in a relatively small area (2-3 km radius) and shows some degree of roost fidelity for some months.

Prevalence, Mean abundance and Mean intensity

There are few studies of bat flies on D. rotundus in Honduras and the Central American region that calculate prevalence, mean intensity of the infestation or other parasitic indices; this lack of information makes it difficult to establish comparisons. The prevalence can be highly variable in this host (P% = 0-100%), depending on the ectoparasite species, generally T. parasiticus and S. wiedemanni show the highest values, with some exceptions for accidental bat fly species (e.g., T. joblingi P% = 70, 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. https://doi.org/10.1016/j.rmb.2015.04.012
https://doi.org/10.1016/j.rmb.2015.04.01...
). In this study, the highest prevalence was for T. parasiticus (P% = 72.50), followed by S. wiedemanni (P% = 25). Rojas et al. (2008Rojas A, Jiménez A, Vargas M, Zumbado M, Herrero MV (2008) Ectoparasites of the common vampire bat (Desmodus rotundus) in Costa Rica: parasitism rates and biogeographic trends. Mastozoología Neotropical 15: 181-187.) in Costa Rica, recorded a high prevalence of T. parasiticus (P% = 91.4) while that for S. wiedemanni was lower (P% = 11. 4). In Brazil, Aguiar and Antonini (2011Aguiar LM, Antonini Y (2011) Descriptive ecology of bat flies (Diptera: Hippoboscoidea) associated with vampire bats (Chiroptera: Phyllostomidae) in the cerrado of Central Brazil. Memórias do Instituto Oswaldo Cruz 106: 170-176. https://doi.org/10.1590/S0074-02762011000200009
https://doi.org/10.1590/S0074-0276201100...
, 2016Aguiar LMS, Antonini Y (2016) Prevalence and intensity of Streblidae in bats from a Neotropical savanna region in Brazil. Folia Parasitologica 63: 024. https://doi.org/10.14411/fp.2016.024
https://doi.org/10.14411/fp.2016.024...
), found intermediate values and the highest prevalence in S. wiedemanni (P% = 43.6, P% = 44) and in T. parasiticus was (P% = 29.5, P% = 30) values of both studies respectively. Minaya et al. (2021Minaya D, Mendoza J, Iannacone J (2021) Ectoparasitic fauna on the common vampire bat Desmodus rotundus (Geoffroy, 1810) (Chiroptera: Phyllostomidae) from Huarochiri, Lima, and a checklist of ectoparasites in bats of Peru. Graellsia 77: e135. https://doi.org/10.3989/graellsia.2021.v77.293
https://doi.org/10.3989/graellsia.2021.v...
) report low values in Peru, S. wiedemanni (P% = 22.22) and T. parasiticus (P% = 11.11). In our study, the mean abundance and the mean intensity was higher for T. parasiticus (MA = 3.69, MI = 5.17), followed by S. wiedemanni (MA = 1, MI = 4), similar results were found by Rojas et al. (2008) for mean intensity in T. parasiticus (MI = 5.65) while for S. wiedemanni (MI = 2.12). Aguiar and Antonini (2011Aguiar LM, Antonini Y (2011) Descriptive ecology of bat flies (Diptera: Hippoboscoidea) associated with vampire bats (Chiroptera: Phyllostomidae) in the cerrado of Central Brazil. Memórias do Instituto Oswaldo Cruz 106: 170-176. https://doi.org/10.1590/S0074-02762011000200009
https://doi.org/10.1590/S0074-0276201100...
) found in S. wiedemanni (MA = 1.56, MI = 3.57) and in T. parasiticus (MA = 0.62, MI = 2.09). These variations in the parasitological indices may be due to climatic differences, different biogeographic regions, environmental heterogeneity, variations of the hosts between localities, as well as differences in the sampling effort (Rui and Graciolli 2005Rui A, 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: 438-445. https://doi.org/10.1590/S0101-81752005000200021
https://doi.org/10.1590/S0101-8175200500...
, Vinarski et al. 2007Vinarski MV, Korallo NP, Krasnov BR, Shenbrot GI, Poulin R (2007) Decay of similarity of gamasid mite assemblages parasitic on Paleartic small mammals: geographic distance, host-species composition or environment. Journal of Biogeography 34: 1691-1700. https://doi.org/10.1111/j.1365-2699.2007.01735.x
https://doi.org/10.1111/j.1365-2699.2007...
, Lourenço et al. 2016Lourenço EC, Almeida JC, Famadas KM (2016) Richness of ectoparasitic flies (Diptera: Streblidae) of bats (Chiroptera) - a systematic review and meta-analysis of studies in Brazil. Parasitology Research 115: 4379-4388. https://doi.org/10.1007/s00436-016-5223-y
https://doi.org/10.1007/s00436-016-5223-...
). Variations may also indicate that parasites are often unevenly distributed among hosts (Shaw and Dobson 1995Shaw DJ, Dobson AP (1995) Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111: S111-S113. https://doi.org/10.1017/S0031182000075855
https://doi.org/10.1017/S003118200007585...
, Poulin 2007Poulin R (2007) Evolutionary ecology of parasite. Princeton University Press, Princeton, 2nd ed., 332 pp. https://doi.org/10.1515/9781400840809
https://doi.org/10.1515/9781400840809...
).

Infracommunities

In this study, the higher frequencies of infracommunities with one species than with two or more species indicate a possible pattern of association (Barbier and Graciolli 2016Barbier E, 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: 176-187. https://doi.org/10.1080/01650521.2016.1215042
https://doi.org/10.1080/01650521.2016.12...
). The maximum number of parasites per host individual was 18 bat flies, Aguiar and Antonini (2011Aguiar LM, Antonini Y (2011) Descriptive ecology of bat flies (Diptera: Hippoboscoidea) associated with vampire bats (Chiroptera: Phyllostomidae) in the cerrado of Central Brazil. Memórias do Instituto Oswaldo Cruz 106: 170-176. https://doi.org/10.1590/S0074-02762011000200009
https://doi.org/10.1590/S0074-0276201100...
) in Brazil registered 25 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. https://doi.org/10.1016/j.rmb.2015.04.012
https://doi.org/10.1016/j.rmb.2015.04.01...
) in Mexico 26. Trichobius parasiticus + S. wiedemanni presented a higher frequency between the associations of different bat fly species; this infracommunity is widely registered in this host (e.g., Aguiar and Antonini 2011Aguiar LM, Antonini Y (2011) Descriptive ecology of bat flies (Diptera: Hippoboscoidea) associated with vampire bats (Chiroptera: Phyllostomidae) in the cerrado of Central Brazil. Memórias do Instituto Oswaldo Cruz 106: 170-176. https://doi.org/10.1590/S0074-02762011000200009
https://doi.org/10.1590/S0074-0276201100...
, 2016Aguiar LMS, Antonini Y (2016) Prevalence and intensity of Streblidae in bats from a Neotropical savanna region in Brazil. Folia Parasitologica 63: 024. https://doi.org/10.14411/fp.2016.024
https://doi.org/10.14411/fp.2016.024...
, Hiller et al. 2018Hiller T, Honner B, Page R, Tschapka M (2018). Leg structure explains host site preference in bat flies (Diptera: Streblidae) parasitizing neotropical bats (Chiroptera: Phyllostomidae). Parasitology 145: 1475-1482. https://doi.org/10.1017/S0031182018000318
https://doi.org/10.1017/S003118201800031...
, Graciolli et al. 2019Graciolli G, Guerrero R, Catzeflis F (2019) Streblid bat flies (Diptera) and other ectoparasites on bats (Mammalia: Chiroptera) from French Guiana. Biota Neotropica 19: e20180724. https://doi.org/10.1590/1676-0611-BN-2018-0724
https://doi.org/10.1590/1676-0611-BN-201...
, Barbier et al. 2021Barbier E, Falcão F, Bernard E (2021) Bat-ectoparasitic fly relationships in a seasonally dry tropical forest in Brazil. Parasitology Research 120: 3507-3517. https://doi.org/10.1007/s00436-021-07301-w
https://doi.org/10.1007/s00436-021-07301...
). Teixeira and Ferreira (2010Teixeira ALM, Ferreira RL (2010) Fauna de dipteros parasitas (Diptera: Streblidae) e taxas de infestação em morcegos presentes em cavidades artificiais em Minas Gerais. Chiroptera Neotropical 16: 748-754) record S. wiedemanni and T. furmani, considering that the second species replaces T. parasiticus in some regions of South America (Bertola et al. 2005Bertola PB, Aires CC, Favorito SE, Graciolli G, Amaku M, Pinto-Da-Rocha R (2005) Bat flies (Diptera: Streblidae, Nycteribiidae) parasitic on bats (Mammalia: Chiroptera) at Parque Estadual da Cantareira, Sáo Paulo, Brazil: Parasitism rates and host-parasite associations. Memórias do Instituto Oswaldo Cruz 100: 25-32. https://doi.org/10.1590/S0074-02762005000100005
https://doi.org/10.1590/S0074-0276200500...
, Guerrero 1995Guerrero R (1995) Catalogo de los Streblidos (Diptera: Pupipara) parasitos de murcielagos (Mammalia: Chiroptera) del Nuevo mendo. III. Los Grupos: Dugessi, Dunii y Phyllostomae del genero Trichobius Gervais, 1844. Acta Biologica Venezuelica 14: 1-27.). We also register infracommunities that include accidental species mainly T. joblingi, while (Soares et al. 2017Soares FAM, da Rocha PA, Mikalauskas JS, Graciolli G, Ferrari SF (2017) Ectoparasitic bat flies (Diptera, Streblidae) of bats (Chiroptera, Mammalia) from Mata do Junco Wildlife Refuge, Sergipe, Northeastern Brazil. Oecologia Australis 21: 385-395. https://doi.org/10.4257/oeco.2017.2104.03
https://doi.org/10.4257/oeco.2017.2104.0...
) report associations formed only by accidental species (i.e., T. joblingi + Speiseria ambigua Kessel, 1925, Aspidoptera falcataWenzel, 1976Wenzel RL (1976) The streblid bat flies of Venezuela (Diptera: Striblidae). Bringham Young University Science Bulletin 20: 1-175. + Megistopoda proxima (Séguy, 1926)). The coexistence of these infracommunities can be explained by the fact that they are made up of species of different genera, which may result in less competition between bat flies (Krasnov et al. 2014Krasnov BR, Pilosof S, Stanko M, Morand S, Korallo-Vinarskaya NP, Vinarski MV, Poulin R (2014) Co-occurrence and phylogenetic distance in communities of mammalian ectoparasites: Limiting similarity versus environmental filtering. Oikos 123: 63-70. https://doi.org/10.1111/j.1600-0706.2013.00646.x
https://doi.org/10.1111/j.1600-0706.2013...
), since they present different morphologies and exploit various body niches in the hosts (Marshall 1982Marshall AG (1982) Ecology of insects ectoparasitic on bats. In: Kunz T (Ed.) Ecology of bats. Plenum Press, New York, 369-401. https://doi.org/10.1007/978-1-4613-3421-7_10
https://doi.org/10.1007/978-1-4613-3421-...
, Presley 2011Presley SJ (2011) Interspecific aggregation of ectoparasites on bats: importance of hosts as habitats supersedes interspecific interactions. Oikos 120: 832-841. https://doi.org/10.1111/j.1600-0706.2010.19199.x
https://doi.org/10.1111/j.1600-0706.2010...
, Hiller et al. 2018Hiller T, Honner B, Page R, Tschapka M (2018). Leg structure explains host site preference in bat flies (Diptera: Streblidae) parasitizing neotropical bats (Chiroptera: Phyllostomidae). Parasitology 145: 1475-1482. https://doi.org/10.1017/S0031182018000318
https://doi.org/10.1017/S003118201800031...
). Species of the Streblinae subfamily have a preference for hair-covered body surfaces, while species of the Trichobiinae subfamily tend to be found more frequently on wing membranes (ter Hofstede et al. 2004ter Hofstede HM, Fenton MB, Whitaker JO (2004) Host and host-site specificity of bat flies (Díptera: Streblidae and Nycteribiidae) on Neotropical bats (Chiroptera). Canadian Journal of Zoology 82: 616-626. https://doi.org/10.1139/Z04-031
https://doi.org/10.1139/Z04-031...
). Associations of species of the same genus, such as the one recorded here (T. parasiticus + T. joblingi) are considered less frequent due to the existence of competition for the host body between more closely related species (Ingram and Shurin 2009Ingram T, Shurin JB (2009) Trait-based assembly and phylogenetic structure in northeast Pacific rockfish assemblages. Ecology 90: 2444-2453. https://doi.org/10.1890/08-1841.1
https://doi.org/10.1890/08-1841.1...
, Krasnov et al. 2014Krasnov BR, Pilosof S, Stanko M, Morand S, Korallo-Vinarskaya NP, Vinarski MV, Poulin R (2014) Co-occurrence and phylogenetic distance in communities of mammalian ectoparasites: Limiting similarity versus environmental filtering. Oikos 123: 63-70. https://doi.org/10.1111/j.1600-0706.2013.00646.x
https://doi.org/10.1111/j.1600-0706.2013...
, Hiller et al. 2018Hiller T, Honner B, Page R, Tschapka M (2018). Leg structure explains host site preference in bat flies (Diptera: Streblidae) parasitizing neotropical bats (Chiroptera: Phyllostomidae). Parasitology 145: 1475-1482. https://doi.org/10.1017/S0031182018000318
https://doi.org/10.1017/S003118201800031...
).

Age and sex of the host

Sex and age of the host did not influence on the prevalence and intensity of infection of the bat flies. This may be due to the ecology of the species involved, the roosting behaviour, the social organization (Greenhall et al. 1983Greenhall AM, Joermann G, Schmidt U (1983) Desmodus rotundus. Mammalian Species 202: 1-6. https://doi.org/doi.org/10.2307/3503895
https://doi.org/doi.org/10.2307/3503895...
, Wilkinson 1985Wilkinson GS (1985) The social organization of the common vampire bat. Behavioral Ecology and Sociobiology 17: 123-134. https://doi.org/10.1007/BF00299244
https://doi.org/10.1007/BF00299244...
), variability of the sampled localities, and mainly because of the size of the sample of bats and bat fly species. 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. https://doi.org/10.1016/j.rmb.2015.04.012
https://doi.org/10.1016/j.rmb.2015.04.01...
) found on D. rotundus that females had a higher prevalence of T. joblingi. Other studies show that the influence of host sex does not show a significant relationship for different species of bats and bat flies (e.g., Moura et al. 2003Moura MO, Bordignon MO, Graciolli G (2003) Host characteristics do not affect community structure of ectoparasites on the fishing bat Noctilio leporinus (L., 1758) (Mammalia: Chiroptera). Memórias do Instituto Oswaldo Cruz 98: 811-815. https://doi.org/10.1590/S0074-02762003000600017
https://doi.org/10.1590/S0074-0276200300...
, Rui and Graciolli 2005Rui A, 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: 438-445. https://doi.org/10.1590/S0101-81752005000200021
https://doi.org/10.1590/S0101-8175200500...
, Graciolli and Bianconi 2007Graciolli G, Bianconi GV (2007) Moscas ectoparasitas (Diptera, Streblidae e Nycteribiidae) em morcegos (Mammalia, Chiroptera) em área de Floresta com Araucária no Estado do Paraná, sul do Brasil. Revista Brasileira de Zoologia 24: 246-249. https://doi.org/10.1590/S0101-81752007000100033
https://doi.org/10.1590/S0101-8175200700...
, Ramalho et al. 2018Ramalho DF, Graciolli G, Aguiar L (2018) Bat fly (Diptera: Streblidae) parasitism in degraded and preserved areas in a neotropical savanna. Mastozoología Neotropical 25: 245-250. https://doi.org/10.31687/saremMN.18.25.1.0.21
https://doi.org/10.31687/saremMN.18.25.1...
). However, it has been documented that female and juvenile bats should be infested with bat fly species more often and in higher intensities as they roost predominantly in year-round stable groups together with their offspring (Christe et al. 2000Christe P, Arlettaz R, Vogel P (2000) Variation in intensity of a parasitic mite (Spinturnix myoti) in relation to the reproductive cycle and immunocompetence of its bat host (Myotis myotis). Ecology Letters 3: 207-212. https://doi.org/10.1046/j.1461-0248.2000.00142.x
https://doi.org/10.1046/j.1461-0248.2000...
, Bertola et al. 2005Bertola PB, Aires CC, Favorito SE, Graciolli G, Amaku M, Pinto-Da-Rocha R (2005) Bat flies (Diptera: Streblidae, Nycteribiidae) parasitic on bats (Mammalia: Chiroptera) at Parque Estadual da Cantareira, Sáo Paulo, Brazil: Parasitism rates and host-parasite associations. Memórias do Instituto Oswaldo Cruz 100: 25-32. https://doi.org/10.1590/S0074-02762005000100005
https://doi.org/10.1590/S0074-0276200500...
, Dick and Patterson 2007Dick CW, Patterson BD (2007) Against all odds: Explaining high host specificity in dispersal-prone parasites. International Journal for Parasitology 37: 871-876. https://doi.org/10.1016/j.ijpara.2007.02.004
https://doi.org/10.1016/j.ijpara.2007.02...
, Patterson et al. 2008Patterson BD, Dick CW, Dittmar K (2008) Sex biases in parasitism of Neotropical bats by bat flies (Diptera: Streblidae). Journal of Tropical Ecology 24: 387-396. https://doi.org/10.1017/S0266467408005117
https://doi.org/10.1017/S026646740800511...
, Presley and Willig 2008Presley SJ, Willig M (2008) Intraspecific patterns of ectoparasite abundances on Paraguayan bats: Effects of host sex and body size. Journal of Tropical Ecology 24: 75-83. https://doi.org/10.1017/S0266467407004683
https://doi.org/10.1017/S026646740700468...
, Webber and Willis 2016Webber QMR, Willis CKR (2016) Sociality, Parasites, and Pathogens in Bats. In: Ortega J (Ed.) Sociality in Bats. Springer, Cham, 105-139. https://doi.org/10.1007/978-3-319-38953-0_5
https://doi.org/10.1007/978-3-319-38953-...
). Some studies have also shown that males harbor more ectoparasites than female bats (Komeno and Linhares 1999Komeno CA, Linhares AX (1999) Batflies parasitic on some phyllostomid bats in southeastern Brazil: parasitism rates and host-parasite relationships. Memórias do Instituto Oswaldo Cruz 94: 151-156. https://doi.org/10.1590/s0074-02761999000200004
https://doi.org/10.1590/s0074-0276199900...
, Zhang et al. 2010Zhang L, Parsons S, Daszak P, Wei L, Zhu G, Zhang S (2010) Variation in the abundance of ectoparasites mites of flat-headed bats. Journal of Mammalogy 91: 136-143. https://doi.org/10.1644/08-MAMM-A-306R2.1
https://doi.org/10.1644/08-MAMM-A-306R2....
).

Overall, this study provides significant information of ectoparasites studied in relation to age and sex of the host, aggregate distribution of bat flies on D. rotundus, occurrence in Honduras and reveals the need for new studies in the country. Since biotic and abiotic factors play an important role in the host specificity, prevalence and parasitic intensity (Marshall 1982Marshall AG (1982) Ecology of insects ectoparasitic on bats. In: Kunz T (Ed.) Ecology of bats. Plenum Press, New York, 369-401. https://doi.org/10.1007/978-1-4613-3421-7_10
https://doi.org/10.1007/978-1-4613-3421-...
, Poulin and Morand 2004Poulin R, Morand S (2004) Parasite biodiversity. Smithsonian Institution Press, Washington, D.C., 216 pp., Haelewaters et al. 2018Haelewaters D, Hiller T, Dick CW (2018) Bats, Bat Flies, and Fungi: A Case of Hyperparasitism. Trends in Parasitology 9: 784-799. https://doi.org/10.1016/j.pt.2018.06.006
https://doi.org/10.1016/j.pt.2018.06.006...
). It is necessary to evaluate different regions, ecosystems, host species and variables (e.g., microclime, infracommunities, self-grooming, bat age, body mass, bat hormones, immune system, specialization, predators and parasites, community ecology of bat flies - Ross 1961Ross A (1961) Biological studies on bat ectoparasites of the genus Trichobius (Diptera: Streblidae) in North America, North of Mexico. The Wasmann Journal of Biology 19: 229-246., Overal 1980Overal WL (1980) Host-relations of the batfly Megistopoda aranea (Diptera: Streblidae) in Panamá. The University of Kansas Science Bulletin 52: 1-20., Christe et al. 2000Christe P, Arlettaz R, Vogel P (2000) Variation in intensity of a parasitic mite (Spinturnix myoti) in relation to the reproductive cycle and immunocompetence of its bat host (Myotis myotis). Ecology Letters 3: 207-212. https://doi.org/10.1046/j.1461-0248.2000.00142.x
https://doi.org/10.1046/j.1461-0248.2000...
, Moura et al. 2003Moura MO, Bordignon MO, Graciolli G (2003) Host characteristics do not affect community structure of ectoparasites on the fishing bat Noctilio leporinus (L., 1758) (Mammalia: Chiroptera). Memórias do Instituto Oswaldo Cruz 98: 811-815. https://doi.org/10.1590/S0074-02762003000600017
https://doi.org/10.1590/S0074-0276200300...
, 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. https://doi.org/10.1016/j.rmb.2015.04.012
https://doi.org/10.1016/j.rmb.2015.04.01...
, Warburton et al. 2016Warburton EM, Pearl CA, Vonhof MJ (2016) Relationships between host bodycondition and immunocompetence, not host sex, best predict parasite burdenin a bat-helminth system. Journal of Parasitology Research 115: 2155-2164. https://doi.org/10.1007/s00436-016-4957-x
https://doi.org/10.1007/s00436-016-4957-...
, Hiller et al. 2018Hiller T, Honner B, Page R, Tschapka M (2018). Leg structure explains host site preference in bat flies (Diptera: Streblidae) parasitizing neotropical bats (Chiroptera: Phyllostomidae). Parasitology 145: 1475-1482. https://doi.org/10.1017/S0031182018000318
https://doi.org/10.1017/S003118201800031...
, Barbier et al. 2021Barbier E, Falcão F, Bernard E (2021) Bat-ectoparasitic fly relationships in a seasonally dry tropical forest in Brazil. Parasitology Research 120: 3507-3517. https://doi.org/10.1007/s00436-021-07301-w
https://doi.org/10.1007/s00436-021-07301...
). Furthermore, D. rotundus and bat fly species can play an important role in the transmission and maintenance of different pathogenic microorganisms (Brandão et al. 2008Brandão PE, Scheffer K, Villarreal LY, Achkar S, Oliveira RDN, Fahl WDO, Castilho J, Kotait I, Richtzenhain L, Richtzenhain LJ (2008) A coronavirus detected in the vampire bat Desmodus rotundus. Brazilian Journal of Infectious Diseases 12: 466-468. https://doi.org/10.1590/S1413-86702008000600003
https://doi.org/10.1590/S1413-8670200800...
, Schneider et al. 2009Schneider MC, Romijn PC, Uieda W, Tamayo H, da Silva DF, Belotto A, da Silva JB, Leanes LF (2009) Rabies transmitted by vampire bats to humans: An emerging zoonotic disease in Latin America? Revista Panamericana de Salud Pública 25: 260-269. https://doi.org/260-269. 10.1590/s1020-49892009000300010, Bai et al. 2011Bai Y, Kosoy M, Recuenco S, Alvarez D, Moran D, Turmelle A, Ellison J, Garcia DL, Estevez A, Lindblade K, Rupprecht C (2011) Bartonella spp. in Bats, Guatemala. Emerging Infectious Diseases 17: 1269-1272. https://doi.org/10.3201/eid1707.101867
https://doi.org/10.3201/eid1707.101867...
, Morse et al. 2012Morse SF, Olival KJ, Kosoy M, Billeter S, Patterson BD, Dick CW, Dittmar K (2012) Global distribution and genetic diversity of Bartonella in bat flies (Hippoboscoidea, Streblidae, Nycteribiidae). Infection, Genetics and Evolution 12: 171-723. https://doi.org/10.1016/j.meegid.2012.06.009
https://doi.org/10.1016/j.meegid.2012.06...
, Lima et al. 2013Lima FES, Cibulsk SP, Carnielli P Jr, Elesbao F, Batista HB, Roehe PM, Franco AC (2013) First detection of adenovirus in the vampire bat (Desmodus rotundus) in Brazil. Virus Genes 47: 378-381. https://doi.org/10.1007/s11262-013-0947-6
https://doi.org/10.1007/s11262-013-0947-...
, Abundes-Gallegos et al. 2018Abundes-Gallegos J, Salas-Rojas M, Galvez-Romero G, Perea-Martínez L, Obregón-Morales CY, Morales-Malacara JB, Chomel BB, Stuckey MJ, Moreno-Sandoval H, García-Baltazar A, Nogueda-Torres B, Zuñiga G, Aguilar-Setién A (2018) Detection of dengue virus in bat flies (Diptera: Streblidae) of common vampire bats, Desmodus rotundus, in Progreso, Hidalgo, Mexico. Vector-Borne and Zoonotic Diseases 18: 70-73. https://doi.org/10.1089/vbz.2017.2163
https://doi.org/10.1089/vbz.2017.2163...
, Ballados-González et al. 2018Ballados-González GG, Sánchez-Montes S, Romero-Salas D, Colunga-Salas P, Gutiérrez-Molina R, León-Paniagua L, Becker I, Méndez-Ojeda ML, Barrientos-Salcedo C, Serna-Lagunes R, Cruz-Romero A (2018) Detection of pathogenic Leptospira species associated with phyllostomid bats (Mammalia: Chiroptera) from Veracruz, Mexico. Transboundary and Emerging Diseases 65: 773-781. https://doi.org/10.1111/tbed.12802
https://doi.org/10.1111/tbed.12802...
, Bergner et al. 2021Bergner LM, Mollentze N, Orton RJ, Tello C, Broos A, Biek R, Streicker DG (2021) Characterizing and Evaluating the Zoonotic Potential of Novel Viruses Discovered in Vampire Bats. Viruses 13: 252. https://doi.org/10.3390/v13020252
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), therefore new studies may increase the understanding of this interaction.

ACKNOWLEDGEMENTS

We thank the following institutions for the support they gave us: Programa de Conservación de Murciélagos en Honduras (PCMH), Joya Grande Zoo, Universidad Nacional de Agricultura (UNAG), Wildlife Conservation Society (WSC), Japan International Cooperation Agency (JICA), Fundación Yuscarán, MDI, INCEBIO, MAPANCE-PROCELAQUE, Comité para la defensa y desarrollo del Golfo de Fonseca (CODDEFFAGOLF) and the Entomology Museum of the Universidad Nacional Autonoma de Honduras (UNAH). To Alejandro Paz, Fausto Elvir, Jonathan Hernández, Héctor Portillo, Leonel Marineros, Hermes Vega and Juan Pablo Suazo for their collaboration in the samplings. We also thank Tom Brown for English review, Santiago Alvarez and two anonymous reviewers for helpful comments and suggestions for preliminary versions of the manuscript. To the Fundação de Amparo à Pesquisa do Estado da Bahia for fellowship (Proccess BOL0342/2020).

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ADDITIONAL NOTES

  • Zoobank register

    http://zoobank.org/34F2F6A5-8B3A-42B7-8E79-A052B94897AB
  • How to cite this article

    Gómez-Corea W, España FG, Mejía-Quintanilla D, Alvarez MRV (2022) Bat fly-common vampire bat association in Honduras: prevalence, mean intensity, infracommunities and influence of the biological characteristics of the host (Diptera: Hippoboscidae; Chiroptera: Phyllostomidae). Zoologia (Curitiba) 39: e21018. https://doi.org/10.1590/S1984-4689.v39.e21018
  • Published by

    Sociedade Brasileira de Zoologia at Scientific Electronic Library Online (https://www.scielo.br/zool)

Publication Dates

  • Publication in this collection
    07 Feb 2022
  • Date of issue
    2022

History

  • Received
    11 Aug 2021
  • Accepted
    19 Nov 2021
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