MEM INST OSWALDO CRUZ, RIO DE JANEIRO, 106(8) December 2011
PAGES: 917-925 DOI: 10.1590/S0074-02762011000800004 Full paper
Ectoparasitic insects (Diptera: Streblidae and Siphonaptera: Ischnopsyllidae) of bats from Iquitos and surrounding areas (Loreto, Peru)

Analía Gladys AutinoI; Guillermo Luis ClapsII; Rubén Marcos BarquezI, III; María Mónica DíazI, III, +

IPrograma de Investigaciones de Biodiversidad Argentina, Programa de Conservación de los Murciélagos de Argentina, Facultad de Ciencias Naturales e Instituto Miguel Lillo, Universidad Nacional de Tucumán, Tucumán, Argentina
IIInstituto Superior de Entomología Dr. Abraham Willink, Tucumán, Argentina
IIIConsejo Nacional de Investigaciones Científicas y Técnicas, Tucumán, Argentina

Abstract

Based on specimens collected from bats of different families, we add new species and extend the known ecological distribution and host associations of insect ectoparasites of bats in Peru. New information is provided for the distribution of 26 species of parasites (25 Diptera and 1 Siphonaptera: Ischnopsyllidae). Four species (Neotrichobius ectophyllae, Strebla galindoi, Strebla paramirabilis and Myodopsylla wolffsohni wolffsohni) are new for Peru and 16 represent new records for the department of Loreto. Also, we found 17 new host-ectoparasite relationships. Of note, we found remarkable new association between Neotrichobius delicatus and bat species from the families Molossidae and Noctilionidae and a novel association between Paradyschiria parvula and a species of Vespertilionidae. Host-ectoparasite specificity was recorded with 14 species as monoxenous, three oligoxenous, seven pleioxenous and two polyxenous.

The climatic and biotic diversity of Peru makes it an ideal region for the development of mammalian species (Pacheco 2002). With more than 150 species of bats, Peru is considered one of the areas with the highest diversity and abundance of bats in the Neotropical Region.

Although a number of important studies on bats have originated in Peru, little is known about the ecology and natural history of most Peruvian species and much less is known about the interactions between bats and ectoparasites. This report presents the results from an extensive survey of small mammals and their ectoparasites in the region of Iquitos (department of Loreto) in the northeast portion of the Peruvian Amazon. The survey revealed several new bat ectoparasitic insects.

We found bat flies of the family Streblidae (Diptera), that are primarily associated with bats of the family Phyllostomidae (Dick & Patterson 2007a), and the siphonapterans (family Ischnopsyllidae), that are associated with bats of the family Vespertilionidae (Whiting et al. 2008). We report 25 species of Streblidae, three of them new to Peru and one flea (Ischnopsyllidae), also new to the country. Several new host-parasite associations are reported and the known ecological ranges of many species of ectoparasites are extended.

Currently, 230 species, 33 genera and five subfamilies are recognised in the family Streblidae (Dick & Graciolli 2007). Three of these five subfamilies (Nycterophiliinae, Streblinae and Trichobiinae) are distributed in the New World, including South America (Dick & Graciolli 2007). Streblinae is an abundant and diverse subfamily of neotropical distribution (Guerrero 1996a) that contains 33 species in South America (Guerrero 1997, Graciolli 2003, Graciolli & Dick 2004). These parasites occur with bats from the families Mormoopidae, Emballonuridae, Phyllostomidae, Natalidae, Vespertilionidae and Molossidae (Autino & Claps 2008). Trichobiinae includes 17 genera and 113 species (Guerrero 1996b, 1997, Graciolli 2003) that parasitize bats of the families Noctilionidae, Phyllostomidae, Molossidae, Mormoopidae, Natalidae, Vespertilionidae and Furipteridae (Autino & Claps 2008). The genus Trichobius Gervais is the most diverse within this subfamily (68 species), but it is not analysed in the present paper because a future report is in preparation.

A species (Synthesiostrebla amorphochili) of bat fly from the family Streblidae that is endemic to Peru was first described by Townsend in 1913 and was later re-described by Jobling (1947). Koepcke (1987) also mentioned species of this family in reference to bat parasites studied at Estación Panguana, Huanuco. Guerrero (1996a) did an ecological analysis of the species parasitising bats in Pakitza, Manu National Park; the next year, he published a catalog of New World species, including 59 species from Peru (Guerrero 1997). Recently, Claps et al. (2005) added two species [Anastrebla modestini Wenzel and Exastinion clovisi (Pessôa & Guimarães)], raising the number of currently known Peruvian species to 61.

Infestation by mites and bat flies is very common in bats. Flea parasitism is not often observed, although members of the family Ischnopsyllidae are exclusive to bats (Marshall 1981a). Fleas primarily parasitize insectivorous bats. This preference may be because the bats live in caves and tree holes, which provide optimal conditions for the development of flea larvae and pupae (Johnson 1957). The family Ischnopsyllidae contains two subfamilies, 20 genera and 122 species distributed worldwide (Lewis 1998). The subfamily Ischnopsyllinae includes five South American genera. From Peru, two species of Hormopsylla (Hormopsylla egena Jordan and Hormopsylla trux Jordan), one of Myodopsylla (Myodopsylla setosa Johnson) and one of Sternopsylla (Sternopsylla distincta speciosa Johnson) (Del Ponte 1977) have been reported.

 

MATERIALS AND METHODS

Field research was conducted between December 2003-December 2006. Collecting sites were along the Iquitos-Nauta Highway, in several districts of the provinces of Maynas and Requena, in Loreto (Supplementary data). These points included primary and secondary forest, as well as rural, suburban and urban areas. Bats were captured with mist nets placed at different heights, from 0.2 m above the ground up to the sub-canopy (2-4 m) and canopy levels (6-18 m). The nets were active from 06:00 pm-01:00 am and checked every hour. Some specimens were found while searching diurnal roosts in tree cavities, foliage, culverts, buildings and so on. Each bat was placed individually in a fabric bag in order to collect only the parasites belonging to that particular specimen.

For the bats, we followed the nomenclature introduced by Simmons (2005) and Gardner (2008) for most taxa and that of Solari et al. (2009) for Dermanura. External measurements, body mass, sex and reproductive condition were all recorded in the field for each bat specimen, following Díaz et al. (1998). Voucher specimens of bats were prepared as skins and skeletons or preserved in alcohol. Most of the specimens are still being catalogued for deposit in the Museo de Historia Natural de San Marcos, Lima, Peru and the Colección Mamíferos Lillo, Tucumán, Argentina. Meanwhile, host voucher specimens are identified with the acronyms of the field catalogue of María Mónica Díaz (MMD) and, for specimens already catalogued there, with the acronyms of the Colección Mamíferos Lillo (CML).

Ectoparasites were taken in the field from the pelage of 129 specimens of bats and preserved in 70% ethyl alcohol. In the lab, the parasites were placed in a solution of 70% ethylic alcohol, 5% glycerin and 25% distilled water (Whitaker Jr. 1988, Autino 1996). The parasites were identified at the laboratory with a stereoscopic microscope and some individuals were mounted in Canada balsam to be observed with a compound microscope. All parasite specimens mentioned in this report were deposited at the Annexes section of the CML with the same number of the host voucher specimen.

For the systematic arrangement of Diptera, we followed Wenzel et al. (1966), Wenzel (1976) and Graciolli and Carvalho (2001), for Siphonaptera, we followed Hopkins and Rothschild (1953, 1956) and Johnson (1957). Host-ectoparasite specificity (Marshall 1981b) and a comparison for each specimen with previous information available from Peru are shown in Table I.

Ectoparasites were classified according to the number and diversity of host species on which they were found: monoxenous, found only on one host species; oligoxenous, found on more than one host species of the same genus; pleioxenous, found on hosts from a single family and polyxenous, found on host species of two or more families (Marshall 1981b, Jameson 1985, ter Hofstede et al. 2004).

All cited localities have been alphabetically arranged and listed in the Supplementary data; geographical coordinates were obtained with a Global Positioning System. The specimens examined are included in Table II.

 

RESULTS AND DISCUSSION

Our intensive four-year study of the Peruvian Amazon has increased knowledge about the ectoparasitic insect fauna of bats. We studied parasitic species from the families Diptera (Streblidae) and Siphonaptera (Ischnopsyllidae) found on 35 species of bats (approximately 40% of the total of species from Iquitos): 30 Phyllostomidae (112 specimens), two Noctilionidae (5 specimens), one Molossidae (1 specimen) and two Vespertilionidae (2 specimens) (Tables I, II). We studied 246 ectoparasitic dipterous belonging to 26 bat fly species (Streblidae) and one species of flea (Ischnopsyllidae) represented by one specimen (Table II).

Four new species of parasitic insects are added to the fauna of Peru: Neotrochobius ectophyllae Wenzel, Strebla galindoi Wenzel, Strebla paramirabilis Wenzel (Diptera, Streblidae) and Myodopsylla wolffsohni wolffsohni (Rothschild) (Siphonaptera, Ischnopsyllidae).

Sixteen species of Streblidae (including 8 Streblinae and 8 Trichobiinae) are here cited for the first time for Loreto. With respect to the species of Streblinae, Metelasmus pseudopterus Coquillett and Strebla guajiro (García and Casal) were previously known from the departments of Madre de Dios and Pasco (Guerrero 1996a, b), Strebla curvata Wenzel, Strebla kohlsi Wenzel and Strebla machadoi Wenzel were known from Madre de Dios (Guerrero 1996a), Strebla hertigi Wenzel from Huanuco and Piura (Wenzel 1970) and Strebla tonatie (Kessel) from Cusco. On the other hand, Strebla obtusa Wenzel, a rare species according to Guerrero (1996b), was only known from three localities in Venezuela and from one undetermined locality in Peru. With respect to the species of Trichobiinae, Aspidoptera falcata Wenzel was known from Cusco, Lima, Madre de Dios and Pasco (Guerrero 1995, 1996a, Claps et al. 2005), Aspidoptera phyllostomatis (Perty) from Madre de Dios and Pasco (Guerrero 1996a), Megistopoda aranea (Coquillet) has been cited in five departments of Peru (Lima, Huanuco, Lambayeque, Madre de Dios and Pasco), but exact localities were known only in two of them, Lima and Madre de Dios (Wenzel 1970, Guerrero 1994, 1996a, Claps et al. 2005). Megistopoda proxima (Séguy) was cited in only one precise locality within Madre de Dios and from Pasco, but without a specific locality (Wenzel 1970, Guerrero 1994, 1996a), Neotrochobius delicatus (Machado Allison) and Paradyschiria fusca Speiser were previously known from Pasco (Guerrero 1994, 1995), Paradyschiria parvula Falcoz from Cusco and Madre de Dios (Guerrero 1995, 1996a) and Paratrichobius dunni (Curran) from Madre de Dios (Guerrero 1994, 1996a).

Paratrichobius longicrus (Miranda Ribeiro) and Pseudostrebla ribeiroi Costa Lima were already cited for Loreto, but without precise collecting sites (Wenzel 1970); thus, our data define localities for the distribution of these species in Loreto.

The finding of N. delicatus on bats of the families Molossidae (Molossus rufus É. Geoffroy St.-Hilaire) and Noctilionidae (Noctilio albiventris Desmarest), as well as the finding of P. parvula on a species of Vespertilionidae (Myotis simus O. Thomas), are remarkable. For Neotrichobius delicatus, we recorded a new association with the Phyllostomid bat Rhinophylla fischerae D.C. Carter and the association with species of bats belonging to families where this parasite was not previously recorded as are N. albiventris (family Noctilionidae) and M. rufus (family Molossidae). As these are very rare and previously unknown associations, it is necessary to add that the specimens of Noctilio and Molossus were the first collected each respective netting night and that their parasites were removed and fixed in alcohol prior to collecting other species of bats. This makes it unlikely that there was accidental infection by manipulation.

P. parvula, known primarily as a parasite of bats of the family Noctilionidae and only occasionally of Phyllostomidae, Molossidae and Emballonuridae (Marinkelle & Grose 1981, Guerrero 1995, Graciolli & Carvalho 2001), was not previously observed on vespertilionid bats. However, we collected a specimen P. parvula on a specimen of the bat M. simus, representing the first report of this parasite with the family Vespertilionidae.

Wenzel (1976) suggested that the presence of P. parvula on bats others than members of the family Noctilionidae could be considered accidental or transitory infections. However, we found P. parvula on a specimen of M. simus, a member of the family Vespertilinidae, which was not collected simultaneously with any specimens of Noctilio, suggesting that it was not an accidental infection. Also, we captured a specimen of N. albiventris (MMD 1718) that was parasitised by three species of Streblidae (P. parvula, P. fusca and N. delicatus).

We have found the following new host-parasite associations: S. galindoi-Tonatia saurophila, Strebla kolshi-Glossophaga soricina Pallas, A. falcata-Sturnira magna de la Torre, A. falcata-Rhinophylla pumilio W. Peters, M. aranea-Platyrrhinus brachycephalus (Rouk and Carter), P. dunni-P. brachycephalus and P. dunni-Vampyriscus bidens (Dobson).

Although Strebla consocia Wenzel is considered typical for Phyllostomus hastatus (Pallas) and Phyllostomus elongatus (É. Geoffroy St.-Hilaire), we report here its association with P. brachycephalus, Lophostoma brasiliense W. Peters and L. silvicolum. None of these bats was collected along with any Phyllostomus. Therefore, we dismiss the possibility of accidental infection posited by other authors (Dick 2006, Dick & Patterson 2007a).

S. machadoi was known only as a parasite of bats of the genus Micronycteris, but we add here another genus and species of bat, Mimon crenulatum (É. Geoffroy St.-Hilaire), as a host of this species. S. hertigi is reported herein for P. elongatus; this species was known as a typical parasite of the bats P. hastatus and Phyllostomus discolor (J.A. Wagner) (Guerrero 1996b). With respect to S. tonatie, it was previously known as a common parasite of the genus Tonatia (that now includes genus Lophostoma) but also cited for Sturnira lilium (Guerrero 1996b). Here, we add the bat Micronycteris megalotis (Gray), which represents a new genus and species of host for this parasite.

Coincident with what was observed by Guerrero (1996a), our samples showed a male-biased sex ratio (54% males, 46% females). Some authors suggest that this is most likely due to the fact that the females leave the host every ~10 days to make a prepupal deposition in the refuges of the host (Overal 1980, Marshall 1982, Fritz 1983). However Dick and Patterson (2007b) mention that traditional explanations for male-biased sex ratio, such as sampling effects, unequal longevity between sexes and differential dispersal capability are refuted in favour of an alternative hypothesis. They suggest that the bias is due to selective grooming by the hosts. Because females are larger than males, host-grooming activity removes or kills more females than males. However, sex ratio can vary seasonally (Marshall 1981b) and evaluations based on short-term or limited surveys may provide an incomplete picture. According to Dittmar et al. (2011), specific data on bat fly sex-ratios are rare and, at times, confounding.

With respect to fleas, only one specimen of the species, M. wolffsohni wolffhsoni, was recorded on the bat Myotis albescens (É. Geoffroy St.-Hilaire) (family Vespertilionidae); thus, the proportion of sexes cannot be analysed.

Host-ectoparasite specificity - Host-ectoparasite specificity can be influenced by several factors, including host isolation, climate, competition, depredation, morphological characteristics and physiological adaptation (Marshall 1976). According to Dick and Patterson (2007a), it relies on a set of intrinsic biologic proprieties of the host and ectoparasite as well as ecological and evolutionary relationships. The degree of specificity among arthropod ectoparasites and the methodology used to evaluate specificity are still disputed (Poulin 2007). Some studies conclude that the fleas do not present a high degree of specificity to the hosts, most likely because many species of bats usually roost together and share a common pool of parasites (Theodor 1957). In fact, the bat fleas of family Ischnopsyllidae are unique in that all genera are pleioxenous (Jamerson 1985).

In this study, we found 14 (54%) monoxenous, seven (27%) pleioxenous, three (11%) oligoxenous and two (8%) polyxenous species (Table I). However, when we compared our observations to previous Peruvian records, we found varied information (Table I), possibly due to accidental infections or lack of surveys. Thus, species recorded in this study as monoxenous, including S. kohlsi, Strebla wiedemanni, A. phyllostomatis and Mastoptera minuta (Costa Lima), were recorded by other authors as oligoxenous (Guerrero 1995, 1996b) or pleioxenous (Guerrero 1995, 1996b). N. delicatus, P. dunni and P. longicrus (Guerrero 1994, 1996a) were recorded as monoxenous in other studies, but we found them on different species and even different families of bats. In this study, S. consocia and S. guajiro were found to be pleioxenous and P. parvula oligoxenous, though the two first species have been recorded as oligoxenous (Guerrero 1996a) and the last one as polyxenous (Guerrero 1995) in the literature. Graciolli and Dick (2004) also considered M. pseudopterus as oligoxenous, with the primary hosts being Artibeus jamaicensis Leach, Artibeus fimbriatus Gray and Artibeus planirostris (Spix). S. curvata, recorded as monoxenous, was usually found on bats of the genus Glossophaga (Wenzel 1976, Dick & Gettinger 2005, Dick et al. 2007), but we collected this species on a specimen of Carollia brevicauda (Schinz). S. wiedemanni Kolenati was found parasitising several species of bats (Marinkelle & Grose 1981, Guerrero 1996b, Graciolli & Carvalho 2001, Rios et al. 2008, Rojas et al. 2008), but we only found it on Desmodus rotundus (É. Geoffroy St.-Hilaire) (monoxenous), which is considered its primary host (Aguiar & Antonini 2011). Noctiliostrebla aitkeni Wenzel is known mainly as a parasite of Noctilio leporinus (Linnaeus) and recorded as monoxenous, but we found this species in sympatry with P. fusca on one specimen of N. leporinus (MMD 2809), an association also observed by Graciolli and Carvalho (2001).

 

ACKNOWLEDGEMENTS

To Joseph Vinetz, principal investigator, of the grants that supported the fieldwork, to INRENA, Ministerio de Agricultura of Peru, for the permits to capture and collect the specimens, to Yesenia Doris Chillitupa Campos, Victor Linares, Sixto Mananita, Harold Portocarrero, Cesar Ahuanari, Rubi Angulo and students of the Universidad Nacional de San Marcos, for their help in lab and fieldwork, and to Nofre Sánchez and IVITA, for his help with the preparation of ectoparasites in lab.

 

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Received 14 January 2011
Accepted 9 August 2011
Financial support: NIAID-NIH, USA (R01TW005860, D43TW007120, K24AI068903), CONICET

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