Parasitic relationships between Neotropical bats and their ectoparasites are not well known, even though parasitism is one of the factors that can affect the fitness of a host population. This study characterized parasite-host relationships in relation to sex, age, body size and reproductive status in a population of Anoura geoffroyi using the indices of Prevalence, Mean Intensity and Mean Abundance. Total prevalence for 93 sampled bats was 94.6%. Two species of streblid flies that are considered primary parasites of A. geoffroyi, Exastinion clovisi (n = 203) and Anastrebla modestini (n = 152), were the most abundant ectoparasites, followed by Trichobius sp. (n = 7). Two mite species, Periglischrus vargasi (Spinturnicidae) (n = 98) and Spelaeorhynchus praecursor (Spelaeorhynchidae) (n = 11), were also found. We recorded higher mean abundance and intensity of parasitism in pregnant females compared to reproductive males and reproductively inactive females, for different specific associations of ectoparasites. Host age and body condition had no effect on the parasitological indices. Even with high rates of parasitism, parasitic load did not influence host body condition, but infestation rates by mites were higher in reproductive males and higher by flies in reproductive females, showing that ectoparasites can have variable influences between the different stages of the life history of these host bats. Thus, the reproductive activity of the hosts could be an adverse factor for resistance to parasite infestations.

Body Condition Index, Ectoparasitic relationships, Parasitological indexes

Ectoparasitism can have a strong influence on host populations (Brown and Brown 2004; Møller and Saino 2004). Its diversity is directly influenced by several factors such as geographic distribution, roost environment and by host biology, morphology and behavior (Rui and Graciolli 2005; Postawa and Nagy 2016). Pressures resulting from parasitism can increase the rate of predation on hosts, weaken host physical condition, and increase disease incidence, which can result in decreases in survival and reproduction (Neuhaus 2003; Brown and Brown 2004; Ter Hofstede and Fenton 2005). Ectoparasites may have more significant influence on bat populations, as most bats are gregarious, that can form colonies of thousands of individuals and often roost in places with limited space, such as caves (Bredt et al. 1999; Lourenço and Palmeirim 2007, 2008; Guimaraes and Ferreira 2014), which is the case for Anoura geoffroyi Gray, 1838 (Guimaraes and Ferreira 2014; Farias et al. 2018; Reis 2018).

Anoura geoffroyi (Chiroptera: Phyllostomidae) is a nectarivorous bat (13–18 g) (Koopman 1994; Reid 1997) with a wide geographic distribution in the Neotropical region, from Mexico to Peru, Bolivia, and Brazil (Simmons 2005). The species has a strong association with natural cavities and preferably uses caves as diurnal roosts (Arita 1993; Guimaraes and Ferreira 2014), where colonies of hundreds of individuals can form (Bredt et al. 1999; Farias et al. 2018; Reis 2018). The species presents seasonal population dynamics with a monoestrous reproductive pattern and reproductive activity occurring during the rainy season (Zortéa 2003; Farias et al. 2018).

Among the species of ectoparasites found on bats dipterans and mites are the most common. Dipterans of the family Streblidae are obligatory blood-sucking ectoparasites of bats, they are viviparous and have three larval stages that develop in the female’s uterus, the pupa that develops in the host’s roost and the adult, which is the hematophagous ectoparasite (Dick and Patterson 2006). Likewise, mites of the family Spinturnicidae are exclusive parasites of bats and complete their entire life cycle on the host’s body. The dispersion of these mites requires direct contact between hosts, which is facilitated by the social behaviors of bats, such as copulation, birthing of young, parental care and the habit of living in groups. They are commonly found on the patagium of the host (Rudnick 1960; Lourenço and Palmeirim 2007; Almeida et al. 2015). In temperate region, it was observed that sex, age, and reproductive status of the host strongly influences the reproductive activity of parasites, and, according to the authors, reproduction of ectoparasites of many temperate cave-dwelling bats is mostly regulated by the reproductive cycle of their bat hosts (Lourenço and Palmeirim 2008).

Studies related to different aspects of the association between ectoparasites and bats in the Neotropical region are still scarce. Thus, there is a knowledge gap about parasitological relationships resulting from the numerous factors that influence ectoparasitism in bats such as sex, age and reproductive status of the host, among others (Rui and Graciolli 2005; Patterson et al. 2007; Patterson et al. 2008; Postawa and Nagy 2016). The present study aimed to understand the ecological aspects involved in the interaction between ectoparasites and the phyllostomid bat A. geoffroyi in a colony that uses a ferruginous cave as a diurnal roost and has been present at the site for many years. The effects of bat sex, age, reproductive status, and body condition on the rate of ectoparasite infestation were investigated. Considering that the species exhibits seasonal monoestric reproductive activity during the rainy season, we hypothesize here that ectoparasites may have variable influences between the different stages of the hosts’ life history, as well as in relation to their body condition.

A total of 93 bats were captured, 88 of which were infested, resulting in a prevalence rate of 94.6% (0.8–1.0, CI 95%). The total of 471 ectoparasites collected included flies of three species of the family Streblidae – Anastrebla modestini Wenzel, 1966 (n = 152, Fig. 1), Exastinion clovisi (Pessoa & Guimarães, 1936) (n = 203, Fig. 2) and Trichobius sp. (n = 7, Fig. 3). Specimens of two species of mites were also collected – Periglischrus vargasi Hoffmann, 1944 (Spinturnicidae, n = 98, Fig. 4) and S. praecursor (n = 11, Fig. 5). Mean Intensity (MI) was 5.35 (± 3.47) ectoparasites per host while Mean Abundance (MA) was 5.06 (± 3.58) ectoparasites per host.

Figure 1. 

A ventral view of Anastrebla modestini, 40× magnification B detail of head, 100× C detail of wing and leg, 100× D detail of femur and setae, 100×. Leica DM500 optical microscope. Scale bars: 0.5 mm (A–D).

Figure 2. 

A dorsal view of Exastinion clovisi, 40× magnification B detail of thorax, 100× C distal detail of the leg, 100× D detail of abdomen, 100×. Leica DM500 optical microscope. Scale bars: 0.5 mm (A, B, D); 0.1 mm (C).

Figure 3. 

A dorsal view of Trichobius sp., 40× magnification B detail of wing, 100×. Leica DM500 optical microscope. Scale bars: 0.5 mm (A, B).

Figure 4. 

A specimen of Periglischrus vargasi, 40× magnification B detail of gnatossome, 400× C detail of setae insertion in the leg, 400× D distal detail of the leg, 400×. Leica DM500 optical microscope. Scale bars: 0.5 mm (A); 0.1 mm (B–D).

Figure 5. 

A specimen of Spelaeorhynchus praecursor, 40× magnification B detail of gnatossome, 100× C detail of legs, 100× D detail of leg and setae, 100×. Leica DM500 optical microscope. Scale bars: 0.5 mm (A–D).

Infestation analysis for all ectoparasites (Table 1) revealed that host sex did not affect P (p = 1.00), MA (t = 1.14; p = 0.24) or MI (t = 1.31; p = 0.18). Reproductively active and inactive males showed no differences in the indexes (P: p = 1.0; MI: t = -1.31, p = 0.21; MA: t = -1.52, p = 0.16), as was also the case for pregnant and inactive females (P: p = 0.55; MI: t = 0.30, p = 0.75; MA: t = 0.83, p = 0.39). On the other hand, pregnant females had higher MA than reproductively active males (t = 2.12, p = 0.03) (Table 1).

For the specific association between A. geoffroyi and E. clovisi (Table 2), female hosts had higher MA (t = 2.31, p = 0.02) than did male hosts, while for the association between A. geoffroyi and A. modestini (Table 2), pregnant females had higher P (p = 0.02) and higher MA (t = 2.87, p = 0.006) than did inactive females. Pregnant females were also more parasitized than reproductive active males, with significant differences in P (p = 0.005), MA (t = 3.32, p = 0.006) and MI (t = 1.99, p = 0.04). For the association between A. geoffroyi and the mite P. vargasi (Table 2), MA and MI were higher for pregnant females compared to inactive females (MA: t = -2.79, p = 0.009; MI t = – 2.93, p = 0.01), while reproductively active males were more parasitized than pregnant females with respect to MA and MI (MA: t = -2.34, p = 0.02; MI: t = -3.17, p = 0.01) (Table 2).

Analyses found no correlation between host BCI and parasitic load for males in general (r_s = -0.05; n = 43; p = 0.70); for reproductively active males (r_s = -0.05; n = 32; p = 0.75); for inactive males (r_s = 0.19; n = 11; p = 0.75); for females in general (r_s = 0.002; n = 50; p = 0.98); for pregnant females (r_s = 0.17; n = 18; p = 0.740); for inactive females (r_s = -0.26; n = 32; p = 0.14); for adults (r_s = 0.13; n = 52; p = 0.33) and for non-adults (r_s = -0.21; n = 41; p = 0.17).

The present study registered two common species of parasitic flies belonging to the family Streblidae, A. modestini and E. clovisi, both having already been registered as primary parasites of A. geoffroyi (Wenzel et al. 1976). Both species are widely distributed in the Neotropical region, as are their hosts (Komeno and Linhares 1999; Graciolli and Rui 2001; Bertola et al. 2005; Simmons 2005; Moras et al. 2013; Dornelles and Graciolli 2017; Trujillo-Pahua and Ibáñez-Bernal 2018). Trichobius spp. was not abundant in the present study, although some species of the genus have been previously registered on A. geoffroyi, such as Trichobius tiptoni (Graciolli and Rui 2001) and T. propinquus (De Vasconcelos et al. 2015), or Trichobius sp. (dugesii complex) (Reis 2018).

The mites P. vargasi and S. praecursor have reduced host specificity, commonly occurring on several Neotropical bat species (Herrin and Tipton 1975; Moras et al. 2013; Almeida et al. 2015). The present study found S. praecursor specimens to strongly attach to the tragus of the host, a behavior that has been regularly recorded for this species (Fain et al. 1967; Peracchi 1990).

Our data showed a high prevalence rate of most parasites. A study with Artibeus lituratus and Sturnira lilium, frugivorous phyllostomid bats that commonly roost in treetops and/or human buildings, found much lower prevalence rates, with 3.4% and 9.1% prevalences, respectively (Dornelles and Graciolli 2017). Environmental factors and host behavior can influence prevalence rates, while type of diurnal roost occupied by the host is one of the factors that indirectly influences prevalence rates (Kunz 1982; Ter Hofstede and Fenton 2005). A host habit of changing roosts can disrupt the life cycle of ectoparasitic flies, which spend part of their life cycle inside the roosts, while such movements would not affect mites, because they spend their entire life cycle on the host’s body (Kunz 1982; Lewis 1995).

The studied bat population has used Piedade cave as a diurnal roost for at least a decade and the species is known to prefer caves (Guimaraes and Ferreira 2014). Caves represent favorable diurnal roosts for many bats, as they provide a stable microclimate and protection against predators and adverse weather (Kunz 1982; Lewis 1995). Because such roosts are confined spaces, the very habit of living in a group facilitates body contact and the host-switching activity of ectoparasites. Therefore, it is plausible to hypothesize the existence of an association between the high prevalence rate recorded in the present study (94.6%) and the type of shelter (cave) used, although further investigation is needed.

The present study registered an influence of host sex on the Mean Abundance in the association between E. clovisi and female hosts. Higher infestation levels for females have been frequently reported in the literature (Christe et al. 2007; Patterson et al. 2008; Presley and Willig 2008). By adding the reproductive status of females to the analysis, the results were able to reveal that pregnant females were more parasitized by flies than were non-pregnant females and males. Similar results were found by Reis (2018) in a study conducted in another cave inhabited by A. geoffroyi. The greater fly parasitism of pregnant females is consistent with observations for other bat species such as A. lituratus (Bertola et al. 2005), Megaderma lyra (Sundari et al. 2005), Miniopterus schreibersii (Lourenço and Palmeirim 2008), and Cynopterus brachyotis (Lee et al. 2018).

The Lourenço and Palmeirim (2008) study in temperate zone showed that four parasite species had a similar reproductive pattern, reproducing more intensively during the pregnancy and nursing seasons of M. schreibersii, mainly on pregnant and juvenile bats. The authors concluded that this may be an adaptative trait in which the reproductive cycles of the parasite species are adjusted to the cycles of their hosts in a seasonal environment. This hypothesis could explain our results and those of other studies with similar results. Further studies focusing on the synchrony of the reproductive cycles of ectoparasites and their hosts, in other regions with marked seasonality, may bring new clarifications about this relationship.

Thus, especially for pregnant female, a lower immunological defense during the reproductive phase, due to endocrine changes inherent to reproduction (Grossman 1985; Christie et al. 2000) can facilitate their greater infestation during a period of greater reproductive activity of their ectoparasites (Lourenço and Palmeirim 2008). Reproductively active males, on the other hand, were more parasitized by P. vargasi, than were pregnant females. Anoura geoffroyi males exhibit polygyny and the mating season is relatively short (3 months) (Farias et al. 2018). The energy expenditure directed by these animals for mating in a short period may lead to a more debilitated health condition, facilitating the infestation by mites. Thus, the reproductive activity of the hosts could be an adverse factor for resistance to parasite infestations (Christie et al. 2000), even though it does not affect their body condition. However, other factors acting together can contribute to this result (Lourenço and Palmeirim 2008), needing to be tested.

Even with high parasitism rates, the data of the present study demonstrated that parasite load did not influence host BCI. Although BCI is commonly used in studies involving parasites, it has also presented contradictory results in different studies about it being correlated or not with parasite load (Marshall 1982; Christe et al. 2000; Lučan 2006; Lourenço and Palmeirim 2007; Pearce and O´Shea 2007; Lee et al. 2018). According to Postawa and Nagy (2016), even if ectoparasite density varies, the health of the host is unlikely to be affected, as ectoparasites feed mainly on host lymph and blood and do not directly consume other resources such as fatty acids, so there is no direct impact on BCI.

We thank Fundo de Incentivo à Pesquisa (FIP PUC Minas) and Fundação de Amparo à Pesquisa de Minas Gerais (FAPEMIG) for funding the project, and MEC/SESu (Tutorial Education Program) for scholarships granted to LLLV. We also thank the Brazilian Chico Mendes Institute for Biodiversity Conservation (ICMBIO) for providing the license (#45686-2) to capture the animals and the staff of the Santuário Nossa Senhora da Piedade for allowing us to collect the bats. LFOB thanks Coordination for the Improvement of Higher Education Personnel for providing a post-doctoral scholarship from the National Postdoctoral Programme (CAPES-PNPD/Brazil). We thank Erik Wild for English revision.