STREBLID BAT FLIES ON PHYLLOSTOMID BATS FROM AN ISLAND OFF THE COAST OF SÃO PAULO, BRAZIL

ABSTRACT

Streblidae is the family of bloodsucking flies, mostly tropical and subtropical, that are obligate ectoparasites of bats. A high number of these fly species are found in the Atlantic Forest, but there is little information about their quantitative descriptors. In this paper, we describe the prevalence, mean intensity, and infracommunities of streblid bat flies on phyllostomid bats from the Parque Estadual da Ilha do Cardoso, São Paulo state, Brazil. Surveys were conducted from July 1990 to July 1991 in distinct places of the island, with a total of 454 flies of 30 species collected from 132 bats of 15 species. From those, we found 44 host-parasite associations and 31 infracommunities that suffered variations due to accidental associations or contaminations. With our results, the number of Streblidae species increased from 31 to 36 in São Paulo State.

KEY-WORDS:
Infracommunity; Hippoboscoidea; Atlantic Forest

RESUMO

Streblidae é uma família de moscas hematófagas, encontradas em maior riqueza em regiões tropicais e subtropicais, ectoparasitas obrigatórias de morcegos. Um grande número de espécies é encontrado na Mata Atlântica, no entanto, não há muita informação a respeito de seus descritores quantitativos. Neste trabalho nós descrevemos a prevalência, intensidade média e as infracomunidades de moscas estréblidas em morcegos filostomídeos do Parque Estadual da Ilha do Cardoso, estado de São Paulo, Brasil. Capturas foram realizadas de julho de 1990 até julho de 1991 em diferentes localidades da ilha, de forma que 454 moscas de 30 espécies foram coletadas de 132 morcegos de 15 espécies. Com isso, encontramos 44 associações parasito-hospedeiro e 31 infracomunidades que sofreram variação em virtude de associações acidentais ou contaminações. Com os nossos resultados o número de espécies de Streblidae para o estado de São Paulo aumentou de 31 para 36.

PALAVRAS-CHAVE:
Infracomunidade; Hippoboscoidea; Mata Atlântica

INTRODUCTION

Streblidae is composed of blood-feeding flies, that are obligate ectoparasites of bats. This family is more specious in the New World, with a mostly tropical and subtropical range, and are most commonly associated with bats of the family Phyllostomidae (Dick & Miller, 2010). Streblidae comprises 237 valid species (Soares et al., 2013), of which, nearly 81 have been recorded in Brazil. In Brazil, phyllostomid bats, the main host of streblid bat flies, are represented by 43 genera and 92 species (Nogueira et al., 2014).

In the Brazilian Atlantic Forest, systematic surveys of streblid bat flies have been done in Pernambuco (Soares et al., 2013), Minas Gerais (Azevedo & Linardi, 2002), Rio de Janeiro (Almeida et al., 2011; França et al., 2013; Lourenço et al., 2014), Paraná (Graciolli & Bianconi, 2007; Silva & Ortêncio-Filho, 2011), and Rio Grande do Sul (Graciolli & Rui, 2001; Rui & Graciolli, 2005; Camilotti et al., 2010). For São Paulo state, only (Bertola et al., 2005) and (Graciolli et al., 2006) described the streblid bat fly community in two kinds of forest, Altitudinal Atlantic and semideciduos.

The objective of this paper was to study the host-parasite relationship, describing streblid bat flies infracommunities, as well as record prevalence and mean intensity of infestation from the Parque Estadual da Ilha do Cardoso.

MATERIAL & METHODS

Parque Estadual da Ilha do Cardoso (25°11’S, 47°74’W) is located on the southern coast of São Paulo State, municipality of Cananéia, Brazil. The island is made up of approximately 22,500 ha of Atlantic Forest sensu stricto. The climate is superhumid megathermal, in Thornthwaite’s classification, with no water deficit (Funari et al., 1986).

The bats were sampled monthly by (Fazzolari-Corrêa, 1995) during her Ph. D. research from July 1990 to July 1991. Five mist-nets (6 × 2.6 m) were opened for 12 hours/night during two or three days of each field excursion, being reviewed each hour until 00:00 h, and then reviewed again at 06:00 h, totaling 58,032 h.m² of sampling effort (Straube & Bianconi, 2002). The captured bats were identified in the field and most of them were killed by hanging, individualized in paper bags, and taken to the field laboratory where ectoparasites were collected and stored in 70% ethanol. Bat flies were identified using generic and specific keys for Streblidae (Guerrero, 1993, 1994a, b, 1995a, b, 1996). The bats and bat flies were deposited at the MZUSP.

We followed (Bush et al., 1997) for definitions of prevalence (P), mean intensity of infestation (MI) and infracommunity. Confidence intervals (CI) were calculated using Quantitative Parasitology 3.0 (Rózsa et al., 2000). Bat species with less than 10 captured specimens were excluded in all analysis we made, in infracommunity description were removed the bats that all infracommunities were made by flies with mean intensity equating to one, without sufficient information for CI calculating.

Bat flies known to be associated with specific bat species, that were found on another bat species were considered to be accidental infestations when both bats were captured, principally if the main host was abundant.

RESULTS

We identified 454 streblid bat flies of 30 species, collected from 15 species of phyllostomid bats (Table 1). The most abundant flies were Megistopoda proxima (Séguy, 1926) (n = 75), Trichobius dugesioides dugesioidesWenzel, 1966 (n = 66) and Strebla miriabilis (Waterhouse, 1879) (n = 38)

TABLE 1
Streblidae fly species collected from bats in Parque Estadual da Ilha do Cardoso, municipality of Cananéia, São Paulo. ^a Accidental infestation; ^b new record of bat fly species for São Paulo state; ^c Insuficient data to calcule coinfidence intervals.

Host	n	Bat fly	n	P (95% CI)	MI (95% CI)
Anoura caudifer (É. Geoffroy, 1818)	4	Paratrichobius longicrus (Ribeiro, 1907)a	1	-	-
		Trichobius tiptoni Wenzel, 1976	6	-	-
Anoura geoffroyi Gray, 1838	1	Anastrebla modestini Wenzel, 1966	1	-	-
		Exastinion clovisi (Pessôa & Guimaraes, 1937)	3	-	-
Artibeus fimbriatus Gray, 1838	32	Aspidoptera phyllostomatis (Perty, 1833)	13	25 (11.4-43.4)	1.63 (1-3)
		Megistopoda aranea (Coquillett, 1899)	15	21.9 (9.2-40)	2.14 (1.29-2.86)
		Metelasmus pseudopterus Coquillett, 1907	9	21.9 (9.2-40)	1.29 (1-1.57)
		Trichobius tiptoniWenzel, 1976a	1	3.1 (0.07-16,2)	1c
Artibeus lituratus (Olfers, 1818)	58	Aspidoptera falcataWenzel, 1976a	1	1.7 (0.04-9.2)	1c
		Megistopoda aranea (Coquillett, 1899)a	1	1.7 (0.04-9.2)	1c
		Megistopoda proxima (Séguy, 1926)a	2	3.4 (0.04-11.9)	1c
		Paratrichobius longicrus (Ribeiro, 1907)	35	32.8 (21.0-46.3)	1.84 (1.47-2.21)
		Trichobius sp. dugesii groupa	2	1.7 (0.04-9.2)	2c
Artibeus obscurus (Schinz, 1821)	93	Paratrichobius longicrus (Ribeiro, 1907)a	1	1.1 (0.02-5.9)	1c
		Trichobius dugesii Townsend, 1891	1	1.1 (0.02-5.9)	1c
Carollia perspicillata (Linnaeus, 1758)	17	Strebla guajiro (Garcia & Casal, 1965)	4	17.6 (3.7-43.4)	1.33 (1.00-1.67)
		Strebla sp.1	1	5.9 (0.14-28.7)	1c
		Trichobius anducei Guerreiro, 1998	1	5.9 (0.14-28.7)	1c
		Trichobius joblingi Wenzel, 1966	18	47.1 (22.9-72.1)	2.25 (1.50-2.88)
Chiroderma doriae (Thomas, 1891)	1
Dermanura cinerea Gervais, 1856	20	Neotrichobius delicatus (Machado-Allison, 1966)b	1	5 (0.1-24.8)	1c
		Strebla sp.2	1	5 (0.1-24.8)	1c
Desmodus rotundus (É. Geoffroy, 1810)	7	Strebla hertigiWenzel, 1966a	3	-	-
		Strebla wiedemanni Kolenati, 1856	30	-	-
		Trichobius dugesioides dugesioides Wenzel, 1966	10	-	-
		Trichobius furmani Wenzel, 1966	14	-	-
Diphylla ecaudata Spix, 1823	1	Strebla diphyllaeWenzel, 1966b	5	-	-
		Trichobius diphyllaeWenzel, 1966b	6	-	-
Glossophaga soricina (Pallas, 1776)	1
Lampronycteris brachyotis (Dobson, 1879)	1
Platyrrhinus lineatus (É. Geoffroy, 1810)	19	Paratrichobius longicrus (Ribeiro, 1907)	2	5.3 (0.26-22.6)	2c
		Paratrichobius salviniWenzel, 1966b	4	21.1 (6.05-45.7)	1c
Pygoderma bilabiatum (Wagner, 1834)	2
Sturnira lilium (É. Geoffroy, 1810)	89	Aspidoptera falcata Wenzel, 1976	15	11.2 (5.5-19.7)	1.50 (1.10-1.90)
		Aspidoptera phyllostomatis (Perty, 1833)a	1	1.1 (0.02-5.2)	1c
		Megistopoda aranea (Coquillett, 1899)a	1	1.1 (0.02-5.2)	1c
		Megistopoda proxima (Séguy, 1926)	75	42.7 (32.2-53.6)	1.97 (1.61-2.37)
		Trichobius phyllostomae Kessel, 1925	2	2.2 (0.2-7.9)	1c
		Trichobius sp. parasiticus complexa	3	3.4 (0.7-9.5)	1c
Sturnira tildae de la Torre, 1959	16	Megistopoda proxima (Séguy, 1926)	17	56.3 (29.9-80.2)	1.89 (1.11-3.78)
		Trichobius sp. parasiticus complex	1	6.3 (0.15-30.24)	1c
Tonatia bidens (Spix, 1823)	11	Strebla miriabilis (Waterhouse, 1879)b	38	72.7 (39.0-94.0)	4.75 (2.75-7.38)
		Trichobius dugesioides dugesioides Wenzel, 1966	66	90.9 (58.7-99.7)	6.60 (3.90-10.60)
		Trichobius sp.	2	9.1 (0.47-40.4)	2c
Trachops cirrhosus (Spix, 1823)	5	Strebla miriabilis (Waterhouse, 1879)b	17	-	-
		Trichobius dugesioides dugesioides Wenzel, 1966	22	-	-
Vampyressa pusilla (Wagner, 1843)	2	Neotrichobius sp.	1	-	-
		Trichobius sp. dugesii complex	1	-	-

The prevalence varied from 1.1 (0.02-5.2), Aspidoptera phyllostomatis (Perty, 1833) and Megistopoda aranea (Coquillett, 1899) on Sturnira lilium (É. Geoffroy, 1810), to 90.9 (58.7-99.7), T. dugesioides dugesioidesWenzel, 1966 on Tonatia bidens (Spix, 1823), while the mean intensity varied from 1, all the single occurrences, to 6.60 (3.90-10.60), T. dugesioides dugesioides on T. bidens (Table 1).

We found 31 infracommunities on nine species of phylostomids (Table 3). Excluding accidental associations or contaminations, the richness of infracommunities was 1 to 4. On S. lilium, the bat species with the most infested individuals, we mainly found a single bat fly species infracommunity, M. aranea, the same was noticed for A. lituratus (Olfers, 1818) infested by Paratrichobius longicrus (Miranda-Ribeiro, 1907).

DISCUSSION

The most associations between flies and bats found were previously recorded in the Atlantic Forest and the state of São Paulo (Bertola et al., 2005; Graciolli et al., 2008). The richness of streblid flies from Parque Estadual da Ilha do Cardoso was higher than in other works from the Atlantic Forest sensu stricto (Graciolli & Rui, 2001; Bertola et al., 2005; Rui & Graciolli, 2005; Soares et al., 2013; Lourenço et al., 2014).

Five species of streblid bat flies are recorded for the first time in São Paulo state, they are Neotrichobius delicatus (Machado-Allison, 1966), Trichobius diphyllaeWenzel, 1966, Paratrichobius salviniWenzel, 1966Strebla diphyllaeWenzel, 1966 and S. miriabilis, increasing the number of registered Streblidae species for the state to 36.

For the first time in the Atlantic Forest P. salvini was registered on P. lineatus. Paratrichobius Costa Lima, 1921 is a genus usually associated with Stenodermatinae, a subfamily of Phyllostomidae (Dick & Miller, 2010), which includes bats of the genus Platyrrhinus Saussure, 1860. Platyrrhinus aurarius (Handley & Ferris, 1972), P. brachycephalus (Rouk & Carter, 1972), P. dorsalis (Thomas, 1900), P. lineatus and P. vittatus (Peters, 1860) have all been found infested by Paratrichobius longicrus, while P. salvini has only been found on Platyrrhinus brachycepalus and P. helleri (Peters, 1866) (Guerrero, 1994a).

According to (Dick, 2007), one-third of all batfly-bat associations were not considered primary (prevalence less than 5%). Of all the parasite-host relationships found (n = 44), we considered a quarter (n = 12) of those accidental infestations. Indeed, ten of the records we considered as contamination are also non-primary associations (P < 5%), and there is one association that was not considered contamination, Trichobius phyllostomae Kessel, 1925 on S. lilium, because all species of the Trichobius phyllostomae group tend to show high specificity and occur with low prevalence (less than 8%) (Wenzel et al. 1966, Wenzel 1976, Bertola et al., 2005, Rui & Graciolli, 2005).

TABLE 2
Infracommunity description of streblid bat flies found parasitizing phyllostomid bats from Parque Estadual da Ilha do Cardoso, São Paulo. ^a Infracommunity with accidental fly.

Host (n)	Infracommunity	Frequency
Artibeus fimbriatus (15)	Megistopoda aranea	4
	Aspidoptera phyllostomatis	3
	Metelasmus pseudopterus	3
	A. phyllostomatis + M. aranea	1
	A. phyllostomatis + M. pseudopterus	1
	A. phyllostomatis + M. aranea + M. pseudopterus	2
	A. phyllostomatis + M. pseudopterus + Trichobius tiptonia	1
Artibeus lituratus (22)	Paratrichobius longicrus	18
	Megistopoda proximaa	1
	Trichobius sp. (dugesii group)a	1
	P. longicrus + Megistopoda araneaa	1
	Aspidoptera falcata + M. proximaa	1
Carollia perspicillata (8)	Trichobius joblingi	5
	T. joblingi + Strebla guajiro	2
	T. joblingi + Trichobius anducei + S. guajiro + Strebla sp.1	1
Platyrrhinus lineatus (5)	Paratrichobius salvini	4
	Paratrichobius longicrus	1
Sturnira lilium (46)	Megistopoda próxima	31
	Aspidoptera falcata	4
	Trichobius sp. (parasiticus complex)a	1
	A. falcata + M. proxima	3
	A. falcata + Trichobius phyllostomae	2
	A. falcata + Trichobius sp. (parasiticus complex)a	1
	M. proxima + Trichobius sp. (parasiticus complex)a	2
	M. proxima + P. longicrusa	1
	A. falcata + A. phyllostomatis + M. aranea + M. proximaa	1
Sturnira tildae (9)	Megistopoda próxima	8
	M. proxima + Trichobius sp. (parasiticus complex)a	1
Tonatia bidens (10)	Trichobius dugesioides dugesioides	1
	T. dugesioides dugesioides + Strebla miriabilis	8
	T. dugesioides dugesioides + Trichobius sp.	1

Considering primary associations, the prevalence and mean intensity of bat flies found on S. lilium, Artibeus lituratus (Olfers, 1818) and Artibeus fimbriatus Gray, 1838 were like those found by (Lourenço et al., 2014), except for Aspidoptera falcataWenzel, 1976 on S. lilium, whose prevalence was higher than our results. Prevalence of Trichobius joblingiWenzel, 1966 infesting Carollia perspicillata (Linnaeus, 1758) was higher than in works by (França et al., 2013) and similar to other works (Bertola et al., 2005; Lourenço et al., 2014). Trichobius dugesioides dugesioides and S. miriabilis on T. bidens had the highest prevalence and mean intensity.

A high number of infracommunities (n = 31) were described, but almost one third were due to accidental infestation, which emphasizes the importance of reducing contamination by using careful collection methods when working with these mobile ectoparasites. Apart from T. bidens, all others infracommunities found on bat species were made predominantly by a single species of fly, this may be a pattern, but there are not many works that we can compare our finding with. (Moras et al., 2013) described the infracommunities on bats in Minas Gerais state, counting the bat flies and mites, but the number of bats infested was not high enough to see a pattern.

CONCLUSION

The present paper studied the host-parasite associations between streblid bat flies and bats from an island of Atlantic Forest in São Paulo state, with the goal of contributing to progress of quantitative descriptors (P and MI) and infracommunity knowledge of these parasites for the region. The species of bat flies for São Paulo state has increased to 36 with this study. For a better understanding of interactions among bat flies on the same bat hosts, more papers quantitatively describing the infracommunities are necessary.

ACKNOWLEDGMENTS

We are very grateful to Silvia Fazzolari-Côrrea who collected and deposited bat flies at the Museu de Zoologia da Universidade de São Paulo for others researchers to use; and for being a generous person. We thank Prof. Dra. Eliana Marques Cancello, that was the head of the Entomology collection of MZUSP, for allow us to examine the bat flies. We thank Hannah Doerrier for the English review. GG and GD are also grateful to CNPq (process # 302328/2012-2) and CAPES (# 1567829/2015-2), and FUNDECT for the support provided.

REFERENCES

• ALMEIDA, J.C.; SILVIA, S.S.P.; SERRA-FREIRE, N.M. & VALIM, M.P. 2011. Ectoparasites (Insecta and Acari) associated with bats in Southeastern Brazil. Journal of Medical Entomology, 48:753-757.
• AZEVEDO, A.A. & LINARDI, P.M. 2002. Streblidae (Diptera) of phyllostomid bats from Minas Gerais, Brazil. Memórias do Instituto Oswaldo Cruz, 97:421-422.
• BERTOLA, 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.
• BUSH, A.O.; LAFFERTY, K.D.; LOTZ, J.M. & SHOSTAK, A.W. 1997. Parasitology meets Ecology on its own terms: Margolis et al. Revisited. Journal of Parasitology, 83:575-583.
• CAMILOTTI, V.L.; GRACIOLLI, G.; WEBER, M.M.; ARRUDA, J.L.S. & CÁRCERES, N. 2010. Bat flies from the deciduous Atlantic Forest in southern Brazil: Host-parasite relationships and parasitism rates. Acta Parasitologica, 55:194-200.
• DICK, C.W. 2007. High host specificity of obligate ectoparasites. Ecological Entomology, 32:446-450.
• DICK, C.W. & MILLER, J.A. 2010. Streblidae (Bat Flies). In: BROWN, B.V.; BORKENT, A.; CUMMING, J.M.; WOOD, D.M.; WOODLEY, N.E. & ZUMBADO, M. (Eds.). Manual of Central American Diptera. Ottawa, NRC Research Press. v. 2, p. 1249-1260.
• FAZZOLARI-CORRÊA, S. 1995. Aspectos Sistemáticos, Ecológicos e Reprodutivos de Morcegos na Mata Atlântica. (Tese de doutorado). Universidade de São Paulo, São Paulo.
• FRANÇA, 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, 73:847-854.
• FUNARI, F.L.; STRUFFALDI-DEVUONO, Y. & SALUM, S.T. 1986. Balanço hídrico de duas áreas de Mata Atlântica: reserva biológica de Paranapiacaba e Parque Estadual da Ilha do Cardoso (Estado de São Paulo). In: Congresso da Sociedade de Botânica de São Paulo, 6º. Anais. Campinas, Sociedade Brasileira de Botanica. p. 95-101.
• GRACIOLLI, G. & BIANCONI, G.V. 2007. Moscas ectoparasitas (Diptera, Streblidae e Nycteribiidae) em morcegos (Mammalia, Chiroptera) em áreas de Floresta com Araucária no Estado do Paraná, sul do Brasil. Revista Brasileira de Zoologia, 24:246-249.
• GRACIOLLI, G. & RUI, A.M. 2001. Streblidae (Diptera, Hippoboscoidea) em morcegos (Chiroptera, Phyllostomidae) no nordeste do Rio Grande do Sul, Brasil. Iheringia, Série Zoologia, 90:85-92.
• GRACIOLLI, G.; AZEVEDO, A.A.; ÁRZUA, M.; BARROS-BATTESTI, D.M. & LINARDI, P.M. 2008. Artrópodos ectoparasitos de morcegos no Brasil. In: PACHECO, S.; MARQUES, R.V. & ESBERÁRD, C.E.L. (Eds.). Morcegos do Brasil: biologia, sistemática, ecologia e conservação. Porto Alegre, Armazém Digital. p. 123-128.
• GRACIOLLI, G.; PASSOS, F.C.; PEDRO, W.A. & LIM, B.K. 2006. Moscas ectoparasitas (Diptera, Streblidae) de morcegos filostomídeos (Mammalia, Chiroptera) na Estação Ecológica dos Caeteteus, São Paulo, Brasil. Revista Brasileira de Zoologia, 26:298-299.
• GUERRERO, R. 1993. Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) del nuevo mundo. I. Clave para los géneros y Nycterophiliinae. Acta Biologica Venezuelica, 14:61-75.
• GUERRERO, R. 1994a. Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) del nuevo mundo. IV. Trichobiinae con alas desarrolladas. Boletín de Entomología Venezolana, 9:161-192.
• GUERRERO, R. 1994b. 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 Biologica Venezuelica, 15:1-18.
• GUERRERO, R. 1995a. Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) del nuevo mundo. III. Los grupos: dugesii, dunni y phyllostomae del género Trichobius Gervaos, 1844. Acta Biologica Venezuelica, 15:1-27.
• GUERRERO, R. 1995b. Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) del nuevo mundo. V. Trichobiinae con alas reducidas o ausentes y miscelaneos. Boletín de Entomología Venezolana, 10:135-160.
• GUERRERO, R. 1996. Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) del nuevo mundo. VI. Streblinae. Acta Biologica Venezuelica, 16:1-25.
• LOURENÇO, E.C.; PATRÍCIO, P.M.P.; PINHEIRO, M.C.; DIAS, R.M. & FAMADAS, K.M. 2014. Streblidae (Diptera) on bats (Chiroptera) in an area of Atlantic Forest, state of Rio de Janeiro. Revista Brasileira de Parasitologia Veterinária, 32:164-170.
• MORAS, L.M.; BERNARDI, L.F.O.; GRACIOLLI, G. & GREGORIN, R. 2013. Bat flies (Diptera: Streblidae, Nycteribiidae) and mites (Acari) associated with bats (Mammalia: Chiroptera) in a high-altitude region in southern Minas Gerais, Brazil. Acta Parasitologica, 58:556-563.
• NOGUEIRA, M.R.; LIMA, I.P.; MORATELLI, R.; TAVARES, V.C.; GREGORIN, R. & PERACCHI, A.L. 2014. Checklist of Brazilian bats, with comments on original records. Check list, 10:808-821.
• RÓZSA, L.; REICZIGEL, J. & MAJOROS, G. 2000. Quantifying parasites in samples of hosts. Journal of Parasitology, 86:228-232.
• RUI, 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, 22:438-445.
• SILVA, J.R.R. & ORTÊNCIO-FILHO, H. 2011. Dípteros ectoparasitas (Insecta, Diptera) em morcegos (Chiroptera, Mammalia) na Reserva Biológica das Perobas Paraná, Brasil. Iheringia, Série Zoologia, 101:220-224.
• SOARES, F.A.M.; GRACIOLLI, G.; ALCANTARA, 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 Brasil. Biota Neotropica, 13:242-246.
• STRAUBE, F.C. & BIANCONI, G.V. 2002. Sobre a grandeza e a unidade utilizada para estimar esforço de captura com a utilização de redes-de-neblina. Chiroptera Neotropical, 8:150-152.
• WENZEL, R.L. 1976. The streblid batflies of Venezuela (Diptera: Streblidae). Brigham Young University Science Bulletin, Biological Series, 20:1-177.
• WENZEL, R.L.; TIPTON, V.J. & KIEWLIEZ, A. 1966. The streblid bat flies of Panama (Diptera: Calypterae: Streblidae). In: WENZEL, R.L. & TIPTON, V.J. (Eds.). Ectoparasites of Panama. Chicago, Field Museum of Natural History. p. 405-675.

• 1
  Editor Responsável: Carlos José Einicker Lamas

Publication Dates

• Publication in this collection
  June 2017

History

• Received
  02 Feb 2017
• Accepted
  16 Mar 2017