Bat flies from the deciduous Atlantic Forest in southern Brazil: Host-parasite relationships and parasitism rates

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1 DOI: /s W. Stefański Institute of Parasitology, PAS Acta Parasitologica, 2010, 55(2), ; ISSN 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 , Brazil Abstract This study describes the assemblage of ectoparasitic bat flies, their hosts, and parasitism rates in an Atlantic Forest area in southern Brazil. Bats were captured monthly for one year at two sites. We captured 95 bats belonging to nine species, but only Artibeus lituratus, Artibeus 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). Artibeus fimbriatus and S. lilium showed the highest values of parasite prevalence (60 and 35.7%, respectively) and mean intensities (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 biogeographical regions, but mainly in the tropics, where they parasitize species of several bat families, especially Phyllostomidae and Vespertilionidae (Prevedello et al. 2005). The geographical range of their hosts is a main factor explaining the diversity of bat flies (Marshall 1982, Gannon and Willig 1995, Dick and Gettinger 2005). The host-parasite relationships observed in the families Streblidae and Nycteribiidae may be related to the biogeographical history of the region, to the lack of specificity of some bat fly species, and to the wide geographical ranges of their hosts, impelling oligoxenous 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 southern 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 importance for studies focusing on the distributions and relationships between these groups. The few studies on bat ectoparasites 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, intensity 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 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. *Corresponding author: vagner.camilotti@gmail.com

2 Bat flies from southern Brazil 195 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 important, 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, 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 Eucalyptus sp. and Pinus sp. at the southern boundary. This vegetation 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 temperature 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 Phytotechnology, 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 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 between 0.5 and 2 m above the ground (along trails and in the forest 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 Bianconi (2002), was 15,120 m 2.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, col- Fig.1. Study area located at the boundary of the Atlantic Forest in an area of deciduous vegetation

3 196 Vagner L. Camilotti et al. lected the ectoparasites with forceps, and placed them in individual glass vials of 70% ethanol. After the ectoparasite collection, the bats were released where they were captured. The bat flies were identified and deposited in the Coleção de Referência 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 examined hosts 100) and the mean intensity of parasitism (MI) (number of parasites/number of parasitized hosts) were calculated according to Bush et al. (1997), using Quantitative Parasitology 3.0 (Rózsa et al. 2000) statistical software. We assessed 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 families (Phyllostomidae and Vespertilionidae) (Table I). The phyllostomid 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 similar 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 individuals. 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), Komeno and Linhares (1999, Brazil, 12), Graciolli and Rui (2001, Brazil, 11), Bertola et al. (2005, Brazil, 19), Dick and Gettinger (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 individuals 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 m 2.h.) was similar to other studies performed in regions with higher number of bats species (Komeno and Linhares 1999, Dias et al. 2009). Rios et al. (2008), with a larger capture effort (45,360 m 2.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 N a Np b Bat flies N P(%) MI VC Phyllostomidae Artibeus lituratus 38 1 Paratricobius longicrus (S) c Megistopoda aranea (S) Artibeus fimbriatus 15 9 Megistopoda aranea (S) ( ) 1.9 ( ) 84.4 Sturnira lilium Megistopoda proxima (S) ( ) 2.1 ( ) 89.9 Glossophaga soricina Pygoderma bilabiatum Vespertilionidae Myotis nigricans 4 2 Basilia andersoni (N) d 3 Myotis levis Eptesicus diminutus Histiotus montanus Total a Number of individuals; b number of parasitized individuals; c Streblidae; d Nycteribiidae.

4 Bat flies from southern Brazil 197 average annual minimum temperature of 9.3 C, and is located 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. According 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 parasitized (~ 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 observed in this study seems to occur throughout the geographical 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 parasite of the genus Sturnira, and record of its occurrence on another bat species may result from contamination during handling 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 definitive 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 Carvalho (2001) commented that, in areas where both A. fimbriatus and A. lituratus occur, it is more likely to find M. aranea on the former than on the latter, which was also observed in our study. Paratrichobius longicrus is a primary parasite of A. lituratus (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 velatus 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 coefficient of variation for these indexes. In contrast with the only two quantitative studies performed in Rio Grande do Sul (Graciolli and Rui 2001, Rui and Graciolli 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 studies (Table II). This result may corroborate the hypothesis of Graciolli and Bianconi (2007), who suggested that the variation of the values of prevalence may indicate that the distribution 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 Graciolli and Rui (2001) Brazil: Rio Grande do Sul Rui and Graciolli (2005) Brazil: Rio Grande do Sul Graciolli and Bianconi (2007) Brazil: Paraná Bertola et al. (2005) Brazil: São Paulo Graciolli et al. (2006b) Brazil: São Paulo Komeno and Linhares (1999) Brazil: Minas Gerais Patterson et al. (2008) Venezuela Guerrero (1996) Peru

5 198 Vagner L. Camilotti et al. 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 suggests 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 because of climatic conditions (Graciolli 2004). The finding in this study of only bat flies that are host-specific, 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 intensity 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 individuals (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 association between bats and bat flies, increase with the resistance 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. lituratus, A. fimbriatus, 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 using 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 richness 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 unfavorable to infestation by P. longicrus on A. lituratus, and also corroborate the low bat-fly richness in the area. Last, we emphasize 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. 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