bat flies from the deciduous atlantic forest in southern brazil: host-parasite relationships and...

DOI: 10.2478/s11686-010-0026-2© W. Stefanski Institute of Parasitology, PASActa Parasitologica, 2010, 55(2), 194–200; ISSN 1230-2821

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. CáceresLaboratório de Ecologia de Aves e Mamíferos, Departamento de Biologia, CCNE, Universidade Federal de Santa Maria, Camobi,

Santa Maria, RS, CEP 97.110-970, Brazil

AbstractThis 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 only Arti-beus lituratus, Artibeus fimbriatus, Sturnira lilium (Phyllostomidae) and Myotis nigricans (Vespertilionidae) were found to beparasitized. The bat flies collected were: Streblidae – Paratrichobius longicrus (on A. lituratus) and Megistopoda aranea (onA. 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 ofparasite prevalence (2.6%) and mean intensity (1.0). This low rate may result from the use of ephemeral roosts in the area. Thehigh values of frequency and number of flies per host on A. fimbriatus and S. lilium in relation to other studies could be explainedby the low richness of bat flies here, and in turn, by low competition among fly species per host.

KeywordsEctoparasitic bat flies, Streblidae, Nycteribiidae, epidemiology, deciduous Atlantic Forest, host-parasite relationship

Introduction

Streblidae and Nycteribiidae (Hippoboscoidea) are obligatehematophagous bat parasites and are restricted to one genus orspecies of host (Wenzel et al. 1966, Marshall 1982, Dick andPatterson 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 andWillig 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 tothe wide geographical ranges of their hosts, impelling oligoxe-nous bat flies (Megistopoda aranea, for example) to adapt tothe regional host fauna (Rui and Graciolli 2005). The state ofRio Grande do Sul in southern Brazil includes parts of theParanaense and Pampean provinces (Cabrera and Willink1980), and also the southern range limits of many bat speciesof 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 amosaic 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 denseAtlantic Forest, and some commentaries in the studies ofGuimarães (1941) and Guimarães and D’Andretta (1956).

The number of quantitative studies aiming to describe anepidemiological pattern of host-parasite relationships betweenbats and flies has increased during the last 10 years. Recentstudies have revealed the rates of parasitism (prevalence, in-tensity or mean abundance of infestation) of some bat flyspecies on their hosts in different parts of Brazil (Komeno andLinhares 1999, Graciolli and Rui 2001, Bertola et al. 2005, Ruiand Graciolli 2005, Rios et al. 2008) and countries in theAmericas (Gannon and Willig 1995 in Puerto Rico; Guerrero1996 in Peru; ter Hofstede and Fenton 2004 in Belize; Dick etal. 2003 in the USA). Only two of these studies (Graciolli andRui 2001, Rui and Graciolli 2005) were carried out in RioGrande do Sul. In spite of this increased effort, the need formore studies on this question still remains, in order better tounderstand the ecology of bat fly parasitism.

*Corresponding author: [email protected]

Bat flies from southern Brazil 195

Herein we describe an ectoparasitic assemblage and theparasitism rates on their hosts in an area of deciduous AtlanticForest in Rio Grande do Sul, southern Brazil. The goal of thisstudy was to increase the understanding of the distribution andhost-parasite relationships of the bat fly species in an impor-tant, scarcely studied region. In Brazil, this is the southernmoststudy focusing on these subjects to date.

Materials and methods

The study was undertaken at the Morro do Elefante, locatedin the city of Santa Maria (29°40΄S, 53°43΄W), Rio Grandedo 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. Thelocal arboreal vegetation is very heterogeneous, composed of67 species belonging to 57 genera and 30 families (Machadoand 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 atype Cfa warm humid temperate climate. Rainfall is regularlydistributed through the year, and annual rainfall ranges from

1500 mm to 1750 mm (Pereira et al. 1989). The mean monthlyrainfall during the year averages 127 mm, and the mean tem-perature averages 19.8°C, with a mean minimum of 9.3°C inJune and a mean maximum of 24.7°C in January (data obtainedfrom 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 wasplaced at 100 m from the forest edge, and the second was at thetop of the hill. Bats were captured monthly from Januarythrough December 2005. Bat collections were carried out onfour 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. Onemist net was placed above the canopy (± 13 m above theground). The nets were opened at sunset and checked every 15minutes 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 withcolored necklaces to avoid counting the same individual morethan 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

Vagner L. Camilotti et al.196

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. Thebat flies were identified and deposited in the Coleção de Re-ferência Zoológica da Universidade Federal do Mato Grossodo Sul (ZUFMS).

Parasitism rates were used to assess the infestation by batflies on Artibeus lituratus (Olfers, 1818), A. fimbriatus Gray,1838 and Sturnira lilium (E. Geoffroy, 1810) because theywere the most common bat species found in this study. Theprevalence (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 withhigher 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 themost abundant species were Artibeus lituratus (40%), Sturniralilium (29.4%) and Artibeus fimbriatus (15.8%). Overall, only23 individuals of A. lituratus, A. fimbriatus, S. lilium (Phyl-lostomidae) 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 theirhosts, and the prevalence rates and mean intensity of parasitismare 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 twofly species, P. longicrus and M. aranea, each on different in-dividuals. We did not find more than one species of bat fly onthe 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 inSouth 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) intrinsicfactors of bat flies, where many species are sensitive to factorsexternal to the host, such as climate, vegetation (Prevedello etal. 2005) and the kind of roost used by the bat (Wenzel et al.1966, Marshall 1981, Lewis 1995, ter Hofstede and Fenton2005, Patterson et al. 2007); (2) the location of the study areaoutside the ranges of many hosts (Fabián et al. 1999) found inthe other studies; (3) the low number of bat species and indi-viduals captured, as well as by (4) differences in capture effortamong the studies.

Our capture effort (four consecutive capture nights duringone year, resulting in 15,120 m2.h.) was similar to other stud-ies 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 m2.h.), found a lowrichness in the Caatinga (three bat flies species), an ecosystemwith high climate stress (Prado 2003) and low diversity ofmany taxa (Oliveira et al. 2003, Rosa et al. 2003), includingbats (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

PhyllostomidaeArtibeus lituratus 38 1 Paratricobius longicrus (S)c 1 2.6 1.0

1 Megistopoda aranea (S) 1 2.6 1.0Artibeus fimbriatus 15 9 Megistopoda aranea (S) 17 60.0 (32.28–83.67) 1.9 (1.33–2.56) 84.4Sturnira lilium 28 10 Megistopoda proxima (S) 21 35.7 (18.64–55.94) 2.1 (1.50–2.80) 89.9Glossophaga soricina 3 0 – 0 – –Pygoderma bilabiatum 2 0 – 0 – –VespertilionidaeMyotis 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

aNumber of individuals; bnumber of parasitized individuals; cStreblidae; dNycteribiidae.


average annual minimum temperature of 9.3°C, and is lo-cated in a vegetation type that has low bat richness comparedwith 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 richnessoccurs in the deciduous Atlantic Forest (17 species), followedby, in increasing order, Atlantic Rain Forest (18) and AraucariaForest (25). These factors of vegetation type and climate stressmay explain the low bat-fly richness in the study area, in thedeciduous Atlantic Forest. In spite of the low capture effort, wealmost captured 100 bat individuals and only 23 were para-sitized (~ 20%). We do not believe that this proportion couldchange with an increase in number of bats captured. Thus, wesuppose that the local environmental complexity (biotic andabiotic factors) may be strongly limiting the distribution ofmany 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 hasbeen 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 Artibeuscaptured. This bat fly is considered a primary parasite ofA. fimbritatus, A. jamaicensis Leach, 1821 and A. planirostris(Spix, 1823) (Gannon and Willig 1995, Dick and Gettinger2005). Its occurrence on other bat species (see Graciolli andRui 2001) could be a contamination or a transition to the de-finitive host (Graciolli and Rui 2001, Dick and Gettinger2005, Dick 2007). We found nine parasitized individuals ofA. 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). Wefound it parasitizing only one individual of A. lituratus. Thisassociation was also observed in the states of Minas Gerais(Whitaker and Mumford 1977), Rio Grande do Sul (Graciolliand Rui 2001), São Paulo (Bertola et al. 2005) and the DistritoFederal (Coimbra et al. 1984), and also in Paraguay (Dick andGettinger 2005). Paratrichobius longicrus was also recordedon other bat species belonging to different families (seeKomeno and Linhares 1999, Graciolli and Carvalho 2001,Bertola et al. 2005), on which this bat fly could be facultativeor a case of contamination (Dick 2007).

Basilia andersoni was found in our study only on Myotisnigricans. Peterson and Maa (1970) recorded it on Histiotus ve-latus in Brazil and on Eptesicus furinalis and Myotis ripariusin Uruguay, where these two bat species were later reclassifiedby E.M. Gonzales (Autino et al. 2004). Recently, B. andersoniwas recorded on Myotis nigricans in Brazil (Graciolli andCarvalho 2001, Graciolli 2004, Bertola et al. 2005, Graciolliand Bianconi 2007) and on Myotis levis, M. riparius andM. albescens in Uruguay (Autino et al. 2004). These resultsfound in Brazil as well as in Uruguay evidence the preferenceof this bat fly for bats of the genus Myotis.

Our values of prevalence and mean intensity of parasitismdiffered from other studies (Table II). This contrast could bebetter observed if those studies had also calculated the coeffi-cient of variation for these indexes. In contrast with the onlytwo quantitative studies performed in Rio Grande do Sul (Gra-ciolli and Rui 2001, Rui and Graciolli 2005), the values forprevalence that we obtained were higher (considering only thebats A. fimbriatus and S. lilium). However, the values formean intensity are not much different from the available stud-ies (Table II). This result may corroborate the hypothesis ofGraciolli 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 highvalues 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 2.1Graciolli 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 2.2Graciolli and Bianconi (2007) Brazil: Paraná 32.0 – 65.4 1.5 – 2.0Bertola et al. (2005) Brazil: São Paulo 33.3 – 27.1 1.8 – 1.0Graciolli et al. (2006b) Brazil: São Paulo 12.6 – 20.0 1.3 – 2.5Komeno and Linhares (1999) Brazil: Minas Gerais – – 34.0 – – 1.8Patterson et al. (2008) Venezuela 15.0 39.1 1.3 1.8Guerrero (1996) Peru 47.6 – 46.2 1.4 – 1.6


highest values for both prevalence and mean intensity indexeswere performed in southern Brazil (Graciolli and Rui 2001, Ruiand Graciolli 2005, Graciolli and Bianconi 2007). This sug-gests that there is a tendency for a high frequency of parasitismand a high number of individual bat flies of the same specieson the host. This could be explained by a low host (Fabián etal. 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 meanthat competition for hosts is low. This could enable a largernumber of individual bat flies of the same species to occur ona host individual, which could explain the values of mean in-tensity found (Table II). However, the absence of large-scaledistributional studies on bat flies does not enable us to confirmthis supposition.

The low prevalence and mean intensity that we found onA. 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 theuse 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, Marshall1981, Lewis 1995, ter Hofstede and Fenton 2005, Patterson etal. 2007). Bats roosting in foliage tend to change their roostsmore frequently and to form smaller colonies (due to roostephemerality and wide availability) than bats roosting in cavesand crevices (Kunz 1982, Timm 1987, Lewis 1995, Pattersonet al. 2007). This behavior is unfavorable to bat fly pupae,which develop on the roost surface (Wenzel and Peterson1987, Dick and Patterson 2006, Patterson et al. 2007). Komenoand Linhares (1999) did not find parasitism on A. lituratus, andsuggested that the absence of caves in their study area was thecause. In this way, the kind of roost utilized by A. lituratuscould be the explanation for the low number of P. longicrusrecorded. The differences in parasitism rates among A. litura-tus, A. fimbriatus, and S. lilium, as well as the similarity in thevalues between the last two species, may indicate an effect ofbehavioral characteristics in relation to the use of roosts in ourstudy area. Therefore, A. fimbriatus and S. lilium could be us-ing less-ephemeral roosts than A. lituratus.

Our results from this southernmost study performed inBrazil indicate that the deciduous Atlantic Forest has a lowrichness of bat flies, corroborating the results of Prevedello etal. (2005). This could result from the low richness of hosts andthe low winter temperatures in the region. The low bat-fly rich-ness could be an explanation for the largest number of bat-flyindividuals on the hosts (mean intensity), possibly due to lowcompetition for the hosts, as we observed on A. fimbriatus andS. lilium. The small number of durable roosts could be unfa-vorable to infestation by P. longicrus on A. lituratus, and alsocorroborate 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 observedto the present.

Acknowledgments. We thank the Fundação de Apoio à Pesquisa doRio Grande do Sul (FAPERGS) and the Pro-reitoria de Pesquisa ePós-graduação da Universidade Federal de Santa Maria – Fundo deIncentivo a Pesquisa (FIPE), for grants to V.L. Camilotti and M.M.Weber, respectively. We also thank Daniela O. de Lima and BethâniaAzambuja for helping in the fieldwork. NC Cáceres is a CNPq re-search fellow.

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