Twenty-seven specimens of the common vampire D. rotundus were captured from the district of San Bartolomé, Huarochirí Province, Lima, Peru. Of this population, 19 individuals (70.4%) were parasitized by at least one ectoparasitic species. The taxa and ectoparasitic species registered on the D. rotundus sample are shown in Table 1.

The community of parasites on D. rotundus consisted of adult specimens of two species of bat flies in the family Streblidae, nymphs and larvae of a tick species belonging to the family Argasidae and three species of lice (considered accidental) of the families Menoponidae and Philopteridae (Figure 1). Among the collected species, Ornithodoros peruvianus Kohls, Clifford & Jones 1969 was the ectoparasite with the highest prevalence (P% = 51.85), Mean intensity (IM = 13.7) and abundance (s = 183).

In our review, we found 104 species of ectoparasites in bats from Peru in two major groups: Hexapoda (Diptera, Hemiptera, Siphonaptera) and Arachnida (Mesostigmata and Ixodida). Of these 104 species, 99 were identified at the species level, and the rest at genus level only. The groups with the highest number of species were the families Streblidae (Diptera) (s = 59) and Spinturnicidae (Mesostigmata) (s = 20) (Table 2). Among the species with the higher number of hosts, Aspidoptera falcata Wenzel, 1976 and Megistopoda aranea (Coquillett, 1899) were recorded on eight host species each (Table 2).

We found at least one record of some species of ectoparasite in seventy-five species of bats in Peru. These bat species are distributed in seven families, with Phyllostomidae being the one with the most reports of parasitized bats (s = 58). The bat species with the highest number of reported ectoparasitic species were Lophostoma silvicolum d’Orbigny, 1836, Phyllostomus elongatus (Geoffroy, 1810) and Phyllostomus hastatus (Pallas, 1767) with ten species each, followed by Carollia perspicillata (Linnaeus, 1758) and Lophostoma silvicolum d’Orbigny, 1836. Accidental ectoparasites were not considered in this count.

According to the level of specificity of the ectoparasites for their hosts, species with monoxenic associations (s = 47) were the most common, followed by oligoxenic ones (s = 21). Species of Diptera were observed to present the four types of association (Table 3).

In regards to the geographical distribution of ectoparasites and their hosts in Peru, 19 of the 24 departments in the Peruvian territory present at least some reports of an association of ectoparasites and bats. The departments of Madre de Dios and Loreto have the highest number of records, 40 and 37 species of ectoparasites, respectively, and 40 species of hosts in Loreto, followed by Madre de Dios with 30 species of hosts. Cajamarca, Huancavelica, La Libertad, Moquegua, and Tacna are the only five departments with no reports of ectoparasites on bats (Figure 2).

It has been reported that the typical vampire bat D. rotundus hosts seven species of ectoparasites in Peru: Aspidoptera falcata (Claps et al., 2005), Megistopoda aranea (Claps et al., 2005), Ornithodorus peruvianus (Kohls et al., 1969), Periglischrus herrerai Machado-Allison, 1965 (Mendoza-Uribe & Chavez-Chorocco, 2003; Gettinger, 2018), Strebla wiedemanni Kolenati, 1856 (Wenzel, 1970; Claps et al., 2005; Autino et al., 2011), Trichobius furmani Wenzel, 1966 (Wenzel et al., 1966; Guerrero, 1995a), and Trichobius parasiticus Gervais, 1844 (Wenzel, 1970; Elliot et al., 1985; Guerrero, 1995a). Of these species, O. peruvianus, S. wiedemanni, and T. parasiticus were also found in our study.

The most studied families of ectoparasites on bats are the Streblidae and Nycteribiidae due to their specificity to their hosts (Aguiar & Antonini, 2016; Reeves & Lloyd, 2019). The family Streblidae has been reported typically associated with bats of the family Phyllostomidae (Aguiar & Antonini, 2016); S. wiedemanni and T. parasiticus have been reported in the present study with relatively low P% and MI (P% = 22.2, MI = 1.17 and P% = 11, MI = 1.33, respectively) on D. rotundus. Different studies have reported a broad range of values of these variables for these two ectoparasites on D. rotundus. Aguiar & Antonini (2011), in studies on the same host in Brazil, found intermediate values in S. wiedemanni (P% = 43.6, IM = 3.57), and in T. parasiticus (P% = 29.5, IM = 2.09); Rojas et al. (2008), in Costa Rica, observed low values in S. wiedemanni (P% = 11.9, IM = 2.12) and high values in T. parasiticus (P% = 91.4, IM = 5.65); González-Ávalos et al. (2014), in Mexico, found low values for S. wiedemanni (P% = 3.2) and high for T. parasiticus (P% = 94.3); Aguiar & Antonini (2016), in Brazil, found intermediate values for S. wiedemanni (P% = 44, IM = 3.6) and T. parasiticus (P% = 30, IM = 2.1); Guerrero (2019), in Venezuela, found intermediate values for S. wiedemanni (P% = 53.04, IM = 4.27) and low values for T. parasiticus (P% = 16.4, IM = 30.2). These differences may indicate that the two species present a fluctuating behavior, acting as the nucleus, secondary or satellite species of the parasitic community of D. rotundus, which may be influenced by different factors: environmental (specific to each ecosystem), or degree of disturbance (Lafferty & Kuris, 2005).

Early reports noted that one of the groups that are not usually found in bats is chewing lice (Phthiraptera). However, there are few reports of this significant association being considered incidental. In one of the first reports of mallophagans on bats, Gerberg & Goble (1941) noted two cases: a species of the genus Physconelloides Ewing, 1927, probably Physconelloides galapagensis (Kellogg & Kuwana, 1902), on Carollia perspicillata (reported as Hemiderma perspicilliatum) and another species, Geomydoecus (Geomydoecus) geomydis (Osborn, 1891), collected from Leptonycteris nivalis (Saussure, 1860) in Nuevo León, México. In this study, only presence was reported, but no plausible explanation for accidental parasitism was provided; still, Gerberg & Goble (1941) speculated that mallophagans can occur naturally in bats.

Another finding was by Cerny & Scholz (1983), who reported Brueelia straminea (Denny, 1842) (Philopteridae) in a single specimen of Pipistrellus kuhlii (Kuhl, 1817) in the town of Beyugdash, near Gobustan, Republic of Azerbaijan. Cerny & Scholz (1983) hypothesized that the transmission of B. straminea to P. kuhlii must have occurred in a place where the accidental host and the specific host, Dendrocopos major (Linnaeus, 1758), shared the same refuge for a particular time.

In our study, three species of lice, Columbicola columbae (Linnaeus, 1758), Campanulotes compar (Burmeister, 1838), and Colpocephalum sp. were collected from the coat of D. rotundus. These ectoparasite species are considered typical of columbiform birds, specifically the common pigeon Columba livia Gmelin, 1789 (González & Roldán, 2010; Castro et al., 2017; Abdullah et al., 2018). It is also known that these species often parasitize domestic birds such as the common chicken Gallus gallus domesticus (Linnaeus, 1758) (de Chirinos et al., 2001; Ferreira et al., 2013; Jassim & Hadi, 2019). Thus, we can consider two possibilities to explain the infestation of these lice in the vampire bat; the first is that D. rotundus has become parasitized when coming into contact with the common pigeon, perhaps when feeding on it; and the second possibility, when feeding on the domestic chicken. Of the two, we consider the latter most likely, based on reports of the selectivity and preference of D. rotundus for the blood of the domestic hen over other domestic and wild animals, probably because they are more predictable and easily available for D. rotundus (Bobrowiec et al., 2015).

Based on the above and the results presented in this study, we consider that lice parasitosis in bats is an accidental interaction, and that it is rare, with very few reports. We do not share the idea that it is a natural interaction, as implied by Gerberg & Goble (1941).

Ornithodoros peruvianus was described by Kohls et al. (1969) from three hosts, with D. rotundus as a typical host collected from the department of Lima. Venzal et al. (2012) studied the same ectoparasite on the same host raised in Chile and provided new morphological data and a tentative diagnosis of O. peruvianus; however, the material considered by the latter authors showed severe damage to the hypostome, an organ of taxonomic importance. Finally, Muñoz-Leal et al. (2020) contributed with a complete redescription of the larva, nymph, and adult stages of female and male O. peruvianus collected from the same host in northern Chile, which helped identify the specimens in this study.

In Peru, the diversity of mammals has been estimated at 559 species (Pacheco et al., 2018), of which 189 are species that belong to the order Chiroptera (Velazco, 2020). In this study, we present a summary of the reports of ectoparasites of bats in Peru, in which we found information for 75 species of bats, that is, there is no such information for 60.31% (s = 114) of bat species in Peru, which calls for further studies.

Previous checklists have summarized the fauna of endoparasites (Santos & Gibson, 2015; Minaya et al., 2020) and ectoparasites (Guerrero, 1997; Frank et al., 2014) on bats from South America including Peru. Frank et al. (2014) listed 38 species of ectoparasites, including 36 bat fly species (Streblidae 30, Nycteribiidae 6) and two Siphonaptera species. However, compared to our checklist, 59 species are registered in the Streblidae family (96.67% more) and four in Siphonaptera (100% more).

According to the specificity of the ectoparasites for their bat host, a greater variety of types of association was seen in the flies, presenting the four types of established associations. Even so, the monoxenous species were the most numerous. This high host specificity was also observed in other studies (Dick, 2007; Dick & Patterson, 2007). According to these authors, the behavior of the hosts, which live in large groups in close physical contact with other species of bats is not sufficient to increase the occurrence of oligoxenous or polyxenous species. The higher prevalence of monoxenous species could be explained by: (1) a mutual adaptation between host and its parasite that results in an immunological reaction that reduces the physical defense of the host (Dick & Patterson, 2007; Frank et al., 2014); and (2) the co-evolution of both groups playing a vital role in the specificity of the host, which is supported by the correlation between the phylogenies of the Streblidae and Nycteribiidae with their respective hosts (Patterson et al., 1998; Dick & Patterson, 2007). However, the latter is questioned by Graciolli & Carvalho (2012), who used phylogenic comparisons to show that some species, like Trichobius phyllostomae group (Streblidae), do not seem to have co-speciated with their bat hosts (Subfamily Stenodermatinae), with colonization of a new host providing a more likely explanation for this association.

The other group with higher specificity for their hosts is Acarina Mesostigmata, where only monoxenous, stenoxenous and oligoxenous species have been found. Within this group, the Spinturnicidae presented the highest number of species. According to Gettinger (2018), the family Spinturnicidae is one of the most specific in bats of the family Phyllostomidae compared to other host families, and polygenic species are not known.

Regarding the reported geographic distribution of ectoparasites and their hosts, some regions like Loreto and Madre de Dios have the highest number records because they have been comparatively more studied, probably because of the high diversity of bats that can be found in these regions, where the ecoregions of high-altitude rain forests (high jungle) and Amazonian tropical forest (low jungle) predominate. Most reports of bat ectoparasites in Peru result from the efforts of Autino et al. (2011) in Loreto, and Guerrero (1994b; 1995b) in Madre de Dios, which added significantly to this checklist.

It is worth mentioning that the species Artibeus jamaicensis Leach, 1821, Pteronotus parnellii rubiginosus Gray, 1843, and Molossus currentium Thomas, 1901 are not distributed in Peru according to Miller et al. (2016), Solari (2016) and Barquez & Diaz (2016), respectively. However, they have been considered in this checklist because they were cited in the works of Guerrero (1994b, 1995b, 1996a), Need et al. (1991), Kohls et al. (1969), and Autino et al. (1999). A review of the material deposited in the respective collections mentioned in these works is necessary to confirm species assignments.