Bat flies from the deciduous Atlantic Forest in southern Brazil:
Host-parasite relationships and parasitism rates
Vagner Luis Camilotti*, Gustavo Graciolli, Marcelo M. Weber, Jeferson L. S. Arruda and Nilton C. Cáceres
Laboratório de Ecologia de Aves e Mamíferos, Departamento de Biologia, CCNE, Universidade Federal de Santa Maria, Camobi,Santa Maria, RS, CEP 97.110-970, Brazil
Abstract
T
his study describes the assemblage of ectoparasitic bat flies, their hosts, and parasitism rates in an Atlantic Forest area in south-ern Brazil. Bats were captured monthly for one year at two sites. We captured 95 bats belonging to nine species, but onlyArti-beus lituratus, ArtiArti-beus fimbriatus, Sturnira lilium (Phyllostomidae) and Myotis nigricans (Vespertilionidae) were found to be
parasitized. The bat flies collected were: Streblidae – Paratrichobius longicrus (on A. lituratus) and Megistopoda aranea (on
A. lituratus and A. fimbriatus), Megistopoda proxima (on S. lilium); Nycteribiidae – Basilia andersoni (on M. nigricans). Arti-beus fimbriatus and S. lilium showed the highest values of parasite prevalence (60 and 35.7%, respectively) and mean
intensi-ties (1.9 and 2.1, respectively). Only two parasitized individuals of A. lituratus were found, resulting in the lowest local rate of parasite prevalence (2.6%) and mean intensity (1.0). This low rate may result from the use of ephemeral roosts in the area. The high values of frequency and number of flies per host on A. fimbriatus and S. lilium in relation to other studies could be explained by the low richness of bat flies here, and in turn, by low competition among fly species per host.
Keywords
Ectoparasitic bat flies, Streblidae, Nycteribiidae, epidemiology, deciduous Atlantic Forest, host-parasite relationship
Introduction
Streblidae and Nycteribiidae (Hippoboscoidea) are obligate hematophagous bat parasites and are restricted to one genus or species of host (Wenzel et al. 1966, Marshall 1982, Dick and Patterson 2006). These two families are distributed in all bio-geographical regions, but mainly in the tropics, where they par-asitize species of several bat families, especially Phyllosto-midae and Vespertilionidae (Prevedello et al. 2005).
The geographical range of their hosts is a main factor ex-plaining the diversity of bat flies (Marshall 1982, Gannon and Willig 1995, Dick and Gettinger 2005). The host-parasite re-lationships observed in the families Streblidae and Nycteribi-idae may be related to the biogeographical history of the re-gion, to the lack of specificity of some bat fly species, and to the wide geographical ranges of their hosts, impelling oligoxe-nous bat flies (Megistopoda aranea, for example) to adapt to the regional host fauna (Rui and Graciolli 2005). The state of Rio Grande do Sul in southern Brazil includes parts of the Paranaense and Pampean provinces (Cabrera and Willink 1980), and also the southern range limits of many bat species of the family Phyllostomidae, which coincide with the south-ern limit of the Atlantic Forest (Fabián et al. 1999). In addition
to these biogeographical particularities, the region contains a mosaic of vegetation types (Rambo 2005), increasing its im-portance for studies focusing on the distributions and rela-tionships between these groups. The few studies on bat ec-toparasites in southern Brazil include those of Graciolli and Rui (2001), Graciolli (2004) and Rui and Graciolli (2005) in dense Atlantic Forest, and some commentaries in the studies of Guimarães (1941) and Guimarães and D’Andretta (1956).
The number of quantitative studies aiming to describe an epidemiological pattern of host-parasite relationships between bats and flies has increased during the last 10 years. Recent studies have revealed the rates of parasitism (prevalence, in-tensity or mean abundance of infestation) of some bat fly species on their hosts in different parts of Brazil (Komeno and Linhares 1999, Graciolli and Rui 2001, Bertola et al. 2005, Rui and Graciolli 2005, Rios et al. 2008) and countries in the Americas (Gannon and Willig 1995 in Puerto Rico; Guerrero 1996 in Peru; ter Hofstede and Fenton 2004 in Belize; Dick et
al. 2003 in the USA). Only two of these studies (Graciolli and
Rui 2001, Rui and Graciolli 2005) were carried out in Rio Grande do Sul. In spite of this increased effort, the need for more studies on this question still remains, in order better to understand the ecology of bat fly parasitism.
Herein we describe an ectoparasitic assemblage and the parasitism rates on their hosts in an area of deciduous Atlantic Forest in Rio Grande do Sul, southern Brazil. The goal of this study was to increase the understanding of the distribution and host-parasite relationships of the bat fly species in an impor-tant, scarcely studied region. In Brazil, this is the southernmost study focusing on these subjects to date.
Materials and methods
The study was undertaken at the Morro do Elefante, located in the city of Santa Maria (29°40΄S, 53°43΄W), Rio Grande do Sul (Fig. 1), at the boundary of the Meridional Plateau. This hill rises from its base at 199 m a.s.l. to 462 m a.s.l. The local arboreal vegetation is very heterogeneous, composed of 67 species belonging to 57 genera and 30 families (Machado and Longhi 1990), and also contains small patches of
Euca-lyptus sp. and Pinus sp. at the southern boundary. This
veg-etation has been classified as deciduous Atlantic Forest (Rizzini 1997).
According to the Köppen classification, the region has a type Cfa warm humid temperate climate. Rainfall is regularly distributed through the year, and annual rainfall ranges from
1500 mm to 1750 mm (Pereira et al. 1989). The mean monthly rainfall during the year averages 127 mm, and the mean tem-perature averages 19.8°C, with a mean minimum of 9.3°C in June and a mean maximum of 24.7°C in January (data obtained from the Climate Station of the Department of Phytotechnol-ogy, Universidade Federal de Santa Maria).
We sampled at two locations in the study area. The first was placed at 100 m from the forest edge, and the second was at the top of the hill. Bats were captured monthly from January through December 2005. Bat collections were carried out on four consecutive nights per month, two nights in each location, using six mist nets (7 × 2 m). Five of the nets were placed be-tween 0.5 and 2 m above the ground (along trails and in the for-est interior), a minimum of 10 m apart from one another. One mist net was placed above the canopy (± 13 m above the ground). The nets were opened at sunset and checked every 15 minutes for three hours (two alternating nights per location) and for 1.5 h before dawn during one night at each location. The capture effort, calculated according to Straube and Bian-coni (2002), was 15,120 m2.h.
Bat species identification followed Vizotto and Taddei (1973) and Barquez et al. (1993). The bats were marked with colored necklaces to avoid counting the same individual more than once. We visually checked the bats’ pelage and wings,
lected the ectoparasites with forceps, and placed them in in-dividual glass vials of 70% ethanol. After the ectoparasite col-lection, the bats were released where they were captured. The bat flies were identified and deposited in the Coleção de Re-ferência Zoológica da Universidade Federal do Mato Grosso do Sul (ZUFMS).
Parasitism rates were used to assess the infestation by bat flies on Artibeus lituratus (Olfers, 1818), A. fimbriatus Gray, 1838 and Sturnira lilium (E. Geoffroy, 1810) because they were the most common bat species found in this study. The prevalence (P) (number of parasitized hosts/number of exam-ined hosts × 100) and the mean intensity of parasitism (MI) (number of parasites/number of parasitized hosts) were cal-culated according to Bush et al. (1997), using Quantitative Par-asitology 3.0 (Rózsa et al. 2000) statistical software. We as-sessed the limits of confidence for the P and MI values at 95%, and the coefficient of variation of parasitism for species with higher parasitism rates (A. fimbriatus and S. lilium).
Results
We captured 95 bats belonging to nine species and two fami-lies (Phyllostomidae and Vespertilionidae) (Table I). The phyl-lostomid species comprised 90.4% of the captures, and the most abundant species were Artibeus lituratus (40%), Sturnira
lilium (29.4%) and Artibeus fimbriatus (15.8%). Overall, only
23 individuals of A. lituratus, A. fimbriatus, S. lilium (Phyllostomidae) and Myotis nigricans (Schinz, 1821) (Vesperti -lionidae) were parasitized by flies (Table I).
We recovered 43 bat flies belonging to four species:
Megistopoda proxima (Séguy, 1926), Megistopoda aranea
(Coquillett, 1899), Paratrichobius longicrus (Miranda Ribeiro, 1907) (Streblidae) and Basilia andersoni Peterson et Maa, 1970 (Nycteribiidae). The relationships of the bat flies and their hosts, and the prevalence rates and mean intensity of parasitism are shown in Table I. Comparing the variation coefficient, the
most parasitized species, A. fimbriatus and S. lilium, had sim-ilar rates of parasitism (Table I).
Artibeus lituratus was the only bat species that hosted two
fly species, P. longicrus and M. aranea, each on different in-dividuals. We did not find more than one species of bat fly on the same bat.
Discussion
In this study we found a low richness of bat flies (four species) when compared with other studies of bat fly assemblages in South America: Autino et al. (1999, Argentina, 11 species), Ko-meno and Linhares (1999, Brazil, 12), Graciolli and Rui (2001, Brazil, 11), Bertola et al. (2005, Brazil, 19), Dick and Gettin-ger (2005, Paraguay, 31), Rui and Graciolli (2005, Brazil, 9), Graciolli and Bianconi (2007, Brazil, 9), Graciolli et al. (2006b, Brazil, 9) and Dias et al. (2009, Brazil, 24). This result can be explained by four principal reasons: (1) intrinsic factors of bat flies, where many species are sensitive to factors external to the host, such as climate, vegetation (Prevedello et
al. 2005) and the kind of roost used by the bat (Wenzel et al.
1966, Marshall 1981, Lewis 1995, ter Hofstede and Fenton 2005, Patterson et al. 2007); (2) the location of the study area outside the ranges of many hosts (Fabián et al. 1999) found in the other studies; (3) the low number of bat species and indi-viduals captured, as well as by (4) differences in capture effort among the studies.
Our capture effort (four consecutive capture nights during one year, resulting in 15,120 m2.h.) was similar to other
stud-ies performed in regions with higher number of bats specstud-ies (Komeno and Linhares 1999, Dias et al. 2009). Rios et al. (2008), with a larger capture effort (45,360 m2.h.), found a low
richness in the Caatinga (three bat flies species), an ecosystem with high climate stress (Prado 2003) and low diversity of many taxa (Oliveira et al. 2003, Rosa et al. 2003), including bats (Marinho-Filho and Sazima 1998). Our study area has an
Table I. Prevalence (P), mean intensity (MI) and confidence interval at 95% (between parentheses) and variation coefficient (VC) of bat flies
at the Morro do Elefante, Santa Maria, RS, southern Brazil
Bat species Na Npb Bat flies N P(%) MI VC
Phyllostomidae
Artibeus lituratus 38 1 Paratricobius longicrus (S)c 1 2.6 1.0
1 Megistopoda aranea (S) 1 2.6 1.0
Artibeus fimbriatus 15 9 Megistopoda aranea (S) 17 60.0 (32.28–83.67) 1.9 (1.33–2.56) 84.4
Sturnira lilium 28 10 Megistopoda proxima (S) 21 35.7 (18.64–55.94) 2.1 (1.50–2.80) 89.9
Glossophaga soricina 3 0 – 0 – –
Pygoderma bilabiatum 2 0 – 0 – –
Vespertilionidae
Myotis nigricans 4 2 Basilia andersoni (N)d 3 – –
Myotis levis 1 0 – 0 – –
Eptesicus diminutus 3 0 – 0 – –
Histiotus montanus 1 0 – 0 – –
Total 95 23 43
average annual minimum temperature of 9.3°C, and is lo-cated in a vegetation type that has low bat richness compared with the Atlantic Rain Forest in southern Brazil (Weber 2009). In the latter, Graciolli and Rui (2001) and Rui and Graciolli (2005) found just 11 and seven Streblidae, respectively. Ac-cording to Prevedello et al. (2005), the lowest bat-fly richness occurs in the deciduous Atlantic Forest (17 species), followed by, in increasing order, Atlantic Rain Forest (18) and Araucaria Forest (25). These factors of vegetation type and climate stress may explain the low bat-fly richness in the study area, in the deciduous Atlantic Forest. In spite of the low capture effort, we almost captured 100 bat individuals and only 23 were para-sitized (~ 20%). We do not believe that this proportion could change with an increase in number of bats captured. Thus, we suppose that the local environmental complexity (biotic and abiotic factors) may be strongly limiting the distribution of many bat flies species, as suggested by Prevedello et al. (2005). The relationship between M. proxima and S. lilium ob-served in this study seems to occur throughout the geographi-cal distribution of the host (Graciolli and Rui 2001), and has been observed in Pará and Santa Catarina (Wenzel et al. 1966), Minas Gerais (Komeno and Linhares 1999), Rio Grande do Sul (Graciolli and Rui 2001, Rui and Graciolli 2005), São Paulo (Bertola et al. 2005) and Mato Grosso do Sul (Graciolli et al. 2006a). Megistopoda proxima is considered the primary para-site of the genus Sturnira, and record of its occurrence on an-other bat species may result from contamination during han-dling of the captures (Graciolli and Carvalho 2001, Dick 2007) and also from sharing roosts with other bat species (Dick 2007).
Megistopoda aranea parasitized both species of Artibeus
captured. This bat fly is considered a primary parasite of
A. fimbritatus, A. jamaicensis Leach, 1821 and A. planirostris
(Spix, 1823) (Gannon and Willig 1995, Dick and Gettinger 2005). Its occurrence on other bat species (see Graciolli and Rui 2001) could be a contamination or a transition to the de-finitive host (Graciolli and Rui 2001, Dick and Gettinger 2005, Dick 2007). We found nine parasitized individuals of
A. fimbriatus but only one of A. lituratus. Graciolli and
Car-valho (2001) commented that, in areas where both A.
fim-briatus and A. lituratus occur, it is more likely to find
M. aranea on the former than on the latter, which was also
ob-served in our study.
Paratrichobius longicrus is a primary parasite of A. litu-ratus (Wenzel and Tipton 1966, Graciolli and Rui 2001). We
found it parasitizing only one individual of A. lituratus. This association was also observed in the states of Minas Gerais (Whitaker and Mumford 1977), Rio Grande do Sul (Graciolli and Rui 2001), São Paulo (Bertola et al. 2005) and the Distrito Federal (Coimbra et al. 1984), and also in Paraguay (Dick and Gettinger 2005). Paratrichobius longicrus was also recorded on other bat species belonging to different families (see Komeno and Linhares 1999, Graciolli and Carvalho 2001, Bertola et al. 2005), on which this bat fly could be facultative or a case of contamination (Dick 2007).
Basilia andersoni was found in our study only on Myotis nigricans. Peterson and Maa (1970) recorded it on Histiotus ve-latus in Brazil and on Eptesicus furinalis and Myotis riparius
in Uruguay, where these two bat species were later reclassified by E.M. Gonzales (Autino et al. 2004). Recently, B. andersoni was recorded on Myotis nigricans in Brazil (Graciolli and Carvalho 2001, Graciolli 2004, Bertola et al. 2005, Graciolli and Bianconi 2007) and on Myotis levis, M. riparius and
M. albescens in Uruguay (Autino et al. 2004). These results
found in Brazil as well as in Uruguay evidence the preference of this bat fly for bats of the genus Myotis.
Our values of prevalence and mean intensity of parasitism differed from other studies (Table II). This contrast could be better observed if those studies had also calculated the coeffi-cient of variation for these indexes. In contrast with the only two quantitative studies performed in Rio Grande do Sul (Gra-ciolli and Rui 2001, Rui and Gra(Gra-ciolli 2005), the values for prevalence that we obtained were higher (considering only the bats A. fimbriatus and S. lilium). However, the values for mean intensity are not much different from the available stud-ies (Table II). This result may corroborate the hypothesis of Graciolli and Bianconi (2007), who suggested that the varia-tion of the values of prevalence may indicate that the distri-bution of Streblidae on different host populations is variable. With the exception of Guerrero (1996), who found high values of prevalence in Peru, those studies that obtained the
Table II. Prevalence and mean intensity of parasitism for the host-parasite relationships between Artibeus lituratus/Paratrichobius longicrus, A. fimbriatus/Megistopoda aranea and Sturnira lilium/M. proxima recorded in this and other studies
Study Locale Prevalence Mean intensity
A. lit. A. fim. S. lil. A. lit. A. fim. S. lil.
Present study Brazil: Rio Grande do Sul 2.63 60.0 35.7 1.0 1.9 2.1
Graciolli and Rui (2001) Brazil: Rio Grande do Sul 35.1 21.7 – – – –
Rui and Graciolli (2005) Brazil: Rio Grande do Sul 20.9 6.5 19.4 1.7 1.5 2.2
Graciolli and Bianconi (2007) Brazil: Paraná 32.0 – 65.4 1.5 – 2.0
Bertola et al. (2005) Brazil: São Paulo 33.3 – 27.1 1.8 – 1.0
Graciolli et al. (2006b) Brazil: São Paulo 12.6 – 20.0 1.3 – 2.5
Komeno and Linhares (1999) Brazil: Minas Gerais – – 34.0 – – 1.8
Patterson et al. (2008) Venezuela 15.0 39.1 1.3 1.8
highest values for both prevalence and mean intensity indexes were performed in southern Brazil (Graciolli and Rui 2001, Rui and Graciolli 2005, Graciolli and Bianconi 2007). This sug-gests that there is a tendency for a high frequency of parasitism and a high number of individual bat flies of the same species on the host. This could be explained by a low host (Fabián et
al. 1999, Weber 2009) and bat fly richness in this region
be-cause of climatic conditions (Graciolli 2004).
The finding in this study of only bat flies that are host-spe-cific, as well as a low richness of these parasites, may mean that competition for hosts is low. This could enable a larger number of individual bat flies of the same species to occur on a host individual, which could explain the values of mean in-tensity found (Table II). However, the absence of large-scale distributional studies on bat flies does not enable us to confirm this supposition.
The low prevalence and mean intensity that we found on
A. lituratus, the species with the most individuals captured,
could be due to the solitary habit, to the small number of in-dividuals (5–16) in the colonies (Peracchi et al. 2006), or to the use of tree foliage for roosting (ter Hofstede and Fenton 2005). Prevalence, mean intensity, and the evolutionary parasitic as-sociation between bats and bat flies, increase with the resis-tance and durability of bat roosts (Wenzel et al. 1966, Marshall 1981, Lewis 1995, ter Hofstede and Fenton 2005, Patterson et
al. 2007). Bats roosting in foliage tend to change their roosts
more frequently and to form smaller colonies (due to roost ephemerality and wide availability) than bats roosting in caves and crevices (Kunz 1982, Timm 1987, Lewis 1995, Patterson
et al. 2007). This behavior is unfavorable to bat fly pupae,
which develop on the roost surface (Wenzel and Peterson 1987, Dick and Patterson 2006, Patterson et al. 2007). Komeno and Linhares (1999) did not find parasitism on A. lituratus, and suggested that the absence of caves in their study area was the cause. In this way, the kind of roost utilized by A. lituratus could be the explanation for the low number of P. longicrus recorded. The differences in parasitism rates among A.
litura-tus, A. fimbrialitura-tus, and S. lilium, as well as the similarity in the
values between the last two species, may indicate an effect of behavioral characteristics in relation to the use of roosts in our study area. Therefore, A. fimbriatus and S. lilium could be us-ing less-ephemeral roosts than A. lituratus.
Our results from this southernmost study performed in Brazil indicate that the deciduous Atlantic Forest has a low richness of bat flies, corroborating the results of Prevedello et
al. (2005). This could result from the low richness of hosts and
the low winter temperatures in the region. The low bat-fly rich-ness could be an explanation for the largest number of bat-fly individuals on the hosts (mean intensity), possibly due to low competition for the hosts, as we observed on A. fimbriatus and
S. lilium. The small number of durable roosts could be
unfa-vorable to infestation by P. longicrus on A. lituratus, and also corroborate the low bat-fly richness in the area. Last, we em-phasize the need for more studies in regional vegetation types, in order to establish a biogeographical pattern for the bat-fly
species, as well as for the host-parasite relationships observed to the present.
Acknowledgments. We thank the Fundação de Apoio à Pesquisa do
Rio Grande do Sul (FAPERGS) and the Pro-reitoria de Pesquisa e Pós-graduação da Universidade Federal de Santa Maria – Fundo de Incentivo a Pesquisa (FIPE), for grants to V.L. Camilotti and M.M. Weber, respectively. We also thank Daniela O. de Lima and Bethânia Azambuja for helping in the fieldwork. NC Cáceres is a CNPq re-search fellow.
References
Autino A.G., Claps G.L., Barquez R.M. 1999. Insectos ectoparási-tos de murciélagos de las yungas de la Argentina. Acta
Zoo-logica Mexicana, 78, 119–169.
Autino A.G., Claps G.L., González E.M. 2004. Nuevos registros de insectos (Diptera y Siphonaptera) ectoparasitos de murciéla-gos (Vespertilionidae) del norte de Uruguay. Journal of
Neo-tropical Mammalogy, 11, 81–83.
Barquez R.M., Giannini N.P., Mares M.A. 1993. Guide to the Bats of Argentina/Guia de los Murcielagos de Argentina. Oklahoma Museum of Natural History, Oklahoma, USA, 119 pp. Bertola P.B., Aires C.C., Favorito S.E., Graciolli G., Amaku M.,
Pinto-da-Rocha R. 2005. Bat flies (Diptera: Streblidae, Nycteribii-dae) parasitic on bats (Mammalia: Chiroptera) at Parque Esta-dual da Cantareira, São Paulo, Brasil: parasitism rates and host-parasite associations. Memórias do Instituto Oswaldo Cruz, 100, 25–32. DOI: 10.1590/S0074-02762005000100005. Bush A.O., Lafferty J.M., Lotz J.M., Shostak A.W. 1997.
Parasitol-ogy meets ecolParasitol-ogy on its own terms: Margolis et al. revisited.
Journal of Parasitology, 83, 575–583. DOI: 10.2307/328
4227.
Cabrera A.L., Willink A. 1980. Biogeografia de America Latina. 2nd ed., OAS, Washington DC, USA, 117 pp.
Coimbra C.E.A., Guimarães L.R., Mello D.A. 1984. Ocorrência de Streblidae (Diptera: Pupipara) em morcegos capturados em regiões de cerrado do Brasil central. Revista Brasileira de
En-tomologia, 28, 547–550.
Dias P.A., Santos C.L.C., Rodrigues F.S., Rosa L.C., Lobato K.S., Rebêlo J.M.M. 2009. Espécies de moscas ectoparasitas (Dip-tera, Hippoboscoidea) de morcegos (Mammalia, Chiroptera) no estado do Maranhão. Revista Brasileira de Entomologia, 53, 128–133.
Dick C.W. 2007. High host specificity of obligate ectoparasites.
Eco-logical Entomology, 32, 446–450. DOI: 10.1111/j.1365-2311.
2006.00836.x.
Dick C.W., Gannon M.R., Little W.E., Patrick M.J. 2003. Ectopara-site associations of bats from central Pennsylvania. Journal
of Medical Entomology, 40, 813–819. DOI:
10.1603/0022-2585-40.6.813.
Dick C.W., Gettinger D. 2005. A faunal survey of streblid flies (Diptera: Streblidae) associated with bats in Paraguay.
Jour-nal of Parasitology, 91, 1015–1024. DOI: 10.1645/GE-536R.1.
Dick C.W., Patterson B.D. 2006. Bat flies: obligate ectoparasites of bats. In: (Eds. S. Morand, B. Krasnov and R. Poulin)
Micro-mammals and Macroparasites: From Evolutionary Ecology to Management. Springer-Verlag Publishing, Tokyo, 179–194.
Fabián M.E., Rui A.M., Oliveira K.P. 1999. Distribuição geográfica de morcegos Phyllostomidae (Mammalia: Chiroptera) no Rio Grande do Sul, Brasil. Iheringia, 87, 143–156.
Gannon M.R., Willig M.R. 1995. Ecology of ectoparasites from trop-ical bats. Environmental Entomology, 24, 1495–1503.
Graciolli G. 2004. Nycteribiidae (Diptera, Hippoboscoidea) no sul do Brasil. Revista Brasileira de Zoologia, 21, 971–985. Graciolli G., Bianconi G.V. 2007. Moscas ectoparasitas (Diptera,
Streblidae e Nycteribiidae) em morcegos (Mammalia, Chi-roptera) em área de Floresta com Araucária no Estado do Pa-raná, sul do Brasil. Revista Brasileira de Zoologia, 24, 246–249.
Graciolli G., Cáceres N.C., Bornschein M.R. 2006a. Novos registros de moscas ectoparasitas (Diptera, Streblidae e Nycteribiidae) de morcegos (Mammalia, Chiroptera) em áreas de transição cerrado-floresta estacional no Mato Grosso do Sul, Brasil.
Biota Neotropica, 6, 1–4.
Graciolli G., Carvalho C.J.B. 2001. Moscas ectoparasitas (Diptera, Streblidae e Nycteribiidae) de morcegos (Mammalia, Chi-roptera) do Estado do Paraná, Brasil. I. Basilia, taxonomia e chave pictórica para as espécies. Revista Brasileira de
Zoolo-gia, 18, 33–49.
Graciolli G., Passos F.C., Pedro W.A., Lim B.K. 2006b. Moscas ecto-parasitas (Diptera, Streblidae) de morcegos filostomídeos (Mammalia, Chiroptera) na Estação Ecológica dos Caetetus, São Paulo, Brasil. Revista Brasileira de Zoologia, 23, 298–299. Graciolli G., Rui A.M. 2001. Streblidae (Diptera, Hippoboscoidea) em morcegos (Chiroptera, Phyllostomidae) no nordeste do Rio Grande do Sul, Brasil. Iheringia, 90, 85–92.
Guerrero R. 1996. Streblidae (Diptera: Pupipara) parásitos de los murciélagos de Pakitza, Parque Nacional Manu (Perú). In: (Eds. D.E. Wilson and A. Sandoval) Manu: La Biodiversidad
del Sureste del Perú. Smithsonian Institution Press,
Washing-ton DC, USA, 627–641.
Guimarães L.R. 1941. Notas sobre Streblidae. Papéis Avulsos do
De-partamento de Zoologia, 1, 213–222.
Guimarães L.R., D’Andretta M.A.V. 1956. Sinopse dos Nycteribiidae (Diptera) do Novo Mundo. Arquivos de Zoologia do Estado
de São Paulo, 10, 1–184.
Komeno C.A., Linhares A.X. 1999. Bat flies parasitic on some Phyl-lostomidae bats in southeastern Brazil: Parasitism rates and host-parasite relationships. Memórias do Instituto Oswaldo
Cruz, 94, 151–156.
Lewis S.E. 1995. Roost fidelity of bats: a review. Journal of
Mam-malogy, 76, 481–496. DOI: 10.2307/1382357.
Kunz T.H. 1982. Roosting ecology of bats. In: (Eds. T.H. Kunz)
Ecol-ogy of Bats. Plenum Press, New York, USA, 1–55.
Machado P.F.S., Longhi S.J. 1990. Aspectos florísticos e fitossocio-lógicos do ‘Morro do Elefante’, Santa Maria, RS. Revista do
Centro de Ciências Rurais, 20, 261–280.
Marinho-Filho J., Sazima I. 1998. Brazilian bats and conservation biology: a first survey. In: (Eds. T.H. Kunz and P.A. Racey)
Bat Biology and Conservation. Smithsonian Institution Press,
Washington DC, USA, 282–294.
Marshall A.G. 1981. The ecology of ectoparasitic insects. Academic Press, London, UK, 459 pp.
Marshall A.G. 1982. Ecology of insects ectoparasitic on bats. In: (Ed. T.H. Kunz) Ecology of Bats. Plenum Press, New York, USA, 369–401.
Miranda Ribeiro A. 1907. Alguns dípteros interessantes. Archivos do
Museu Nacional do Rio de Janeiro, 14, 231–239.
Oliveira J.A., Gonçalves P.R., Bonvicino C.R. 2003. Mamíferos da Caatinga. In: (Eds. I.R. Leal, M. Tabarelli and J.M.C. Silva)
Ecologia e Conservação da Caatinga. Editora Universitária
da UFPE, Recife, BR, 275–302.
Patterson B.D., Dick K.W., Dittmar K. 2007. Roosting habits of bats affect their parasitism by bat flies (Diptera: Streblidae).
Jour-nal of Tropical Ecology, 23, 177–189. DOI: 10.1017/S026646
7406003816.
Patterson B.D., Dick C.W., Dittmar K. 2008. Parasitism by bat flies (Diptera: Streblidae) on neotropical bats: effects of host body
size, distribution, and abundance. Parasitology Research, 103, 1091–1100. DOI: 10.1007/s00436-008-1097-y.
Peracchi A.L., Lima I.P., Reis N.R., Nogueira M.R., Ortêncio-Filho H. 2006. Ordem Chiroptera. In: (Eds. N.R. Reis, A.L. Perac-chi, W.A. Pedro and I.P. Lima) Mamíferos do Brasil. Nélio dos Reis, Londrina, BR, 153–164.
Pereira P.R.B., Netto L.R.G., Borin C.J.A., Sartori M.G.B. 1989. Con-tribuição à geografia física do município de Santa Maria: uni-dades de paisagem. Geografia, Ensino e Pesquisa, 3, 37–68. Peterson B.V., Maa T.C. 1970. One new and one previously un-recorded species of Basilia (Diptera: Nycteribiidae) from Uruguay. Canadian Entomology, 102, 1480–1487.
Prado D.E. 2003. As Caatingas da América do Sul. In: (Eds. I.R. Leal, M. Tabarelli and J.M.C. Silva) Ecologia e Conservação da
Caatinga. Editora Universitária da UFPE, Recife, BR, 3–74.
Prevedello J.A., Graciolli G., Carvalho C.J.B. 2005. A fauna de díp-teros (Streblidae e Nycteribiidae) ectoparasitas de morcegos (Chiroptera) do estado do Paraná, Brasil: Composição, distri-buição e áreas prioritárias para novos estudos. Biociências, 13, 193–209.
Rambo B. 2005. A fisionomia do Rio Grande do Sul: ensaio de mono-grafia natural. 3rd ed., UNISINOS, São Leopoldo, BR, 473 pp. Rios G.F.P., Sá-Neto R.J., Graciolli G. 2008. Fauna de dípteros pa-rasitas de morcegos em uma área de Caatinga do nordeste do Brasil. Chiroptera Neotropical, 14, 339–345.
Rizzini C.T. 1997. Tratado de fitogeografia do Brasil. 2nd ed., Âm-bito Cultural, Rio de Janeiro, BR, 747 pp.
Rosa R.S., Menezes N.A., Britski H.A., Costa W.J.E.M., Groth F. 2003. Diversidade, padrões de distribuição e conservação dos peixes da Caatinga. In: (Eds. I.R. Leal, M. Tabarelli and J.M.C. Silva) Ecologia e Conservação da Caatinga. Editora Universitária da UFPE, Recife, BR, 135–180.
Rózsa L., Reiczigel J., Majoros G. 2000. Quantifying parasites in sam-ples of hosts. Journal of Parasitology, 86, 228–232. DOI: 10.2307/3284760.
Rui A.M., Graciolli G. 2005. Moscas ectoparasitas (Diptera, Strebli-dae) de morcegos (Chiroptera, PhyllostomiStrebli-dae) no sul do Bra-sil: associações hospedeiros-parasitos e taxas de infestação.
Revista Brasileira de Zoologia, 22, 438–445.
Straube F.C., Bianconi G.V. 2002. Sobre a grandeza e a unidade uti-lizada para estimar o esforço de captura com utilização de redes-de-neblina. Chiroptera Neotropical, 8, 150–152. ter Hofstede H.M., Fenton M.B. 2005. Relationships between roost
preferences, ectoparasite density, and grooming behaviour of Neotropical bats. Journal of Zoology, 266, 333–340. DOI: 10.1017/S095283690500693X.
ter Hofstade H.M., Fenton M.B., Whitaker J.O., Jr. 2004. Host and host-site specificity of batflies (Diptera: Streblidae and Nyc-teribiidae) on Neotropical bats (Chiroptera). Canadian
Jour-nal of Zoology, 82, 616–626. DOI: 10.1139/z04-030.
Timm R.M. 1987. Tent construction by bats of the genera Artibeus and Uroderma. Fieldiana Zoologica, 39, 187–212.
Vizotto L.D., Taddei V.A. 1973. Chave para determinação de quiróp-teros brasileiros. Revista da Faculdade de Filosofia, Ciências
e Letras São José do Rio Preto – Boletim de Ciências, 1, 1–72.
Weber M.M. 2009. Biogeografia de morcegos (Chiroptera) em área de transição floresta-campo no sudeste da América do Sul. MSc. Thesis, Universidade Federal de Santa Maria, Santa Maria, Brazil.
Wenzel R.L., Peterson B.V. 1987. Streblidae. In: (Eds. J.F. McAlpine, B.V. Peterson, G.E. Shewell, H.J. Teskey, J.R. Vockeroth and D.M. Wood) Manual of Neartic Diptera. Volume 2. Mono-graph number 28. Miister of Supply and Services, Canada, 1293–1301.
Wenzel R.L., Tipton V.J. 1966. Some relationships between mammal hosts and their ectoparasites. In: (Eds. R.L. Wenzel and V.J.
Tipton) Ectoparasites of Panama. Field Museum of Natural History, Chicago, Illinois, USA, 677–723.
Wenzel R.L., Tipton V.J., Kiewlicz A. 1966. The streblid bat flies of Panama (Diptera: Calyptera: Streblidae). In: (Eds. R.L.
Wen-(Accepted January 12, 2010)
zel and V.J. Tipton) Ectoparasites of Panama. Field Museum of Natural History, Chicago, Illinois, USA, 405–675. Whitaker J.O., Mumford R.E. 1977. Records of ectoparasites from
