Mastozoología Neotropical ISSN: 0327-9383 [email protected] Sociedad Argentina para el Estudio de los Mamíferos Argentina
Tarquino-Carbonell, Andrea del Pilar; Gutiérrez-Díaz, Karina A.; Galindo-Espinosa, Emma Y.; Reinoso-Flórez, Gladys; Solari, Sergio; Guerrero, Ricardo ECTOPARASITES ASSOCIATED WITH BATS IN NORTHEASTERN TOLIMA, COLOMBIA Mastozoología Neotropical, vol. 22, núm. 2, 2015, pp. 349-358 Sociedad Argentina para el Estudio de los Mamíferos Tucumán, Argentina
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Artículo
ECTOPARASITES ASSOCIATED WITH BATS IN NORTHEASTERN TOLIMA, COLOMBIA
Andrea del Pilar Tarquino-Carbonell1, Karina A. Gutiérrez-Díaz1, Emma Y. Galindo-Espinosa1, Gladys Reinoso-Flórez1, Sergio Solari2, and Ricardo Guerrero3
1 Grupo de Investigación en Zoología, Universidad del Tolima, Barrio Santa Helena, 730006 Ibagué, Tolima, Colombia [Correspondencia: Andrea del Pilar Tarquino-Carbonell
ABSTRACT. This study reports data on the prevalence and mean intensity of ectoparasites associated with bats in northeastern Tolima, Colombia. We captured 140 bats representing 21 species and 5 families. Most individuals represented the Phyllostomidae (84%), and Carollia perspicillata was the most frequently captured species (35%). Parasites were found in 14 of these species (66%), 8 of which (29.28%) were parasitized by Streblidae, 6 (14.28%) by Spinturnicidae, 5 (9.28%) by Macronyssidae, and 5 (7.85%) by Argasidae. Ectoparasites represented 5 families and 24 species; the most abundant was Trichobius joblingi (16.85%), followed by Radffordiella desmodi (11.04%). This research represents the first report on ectoparasites of bats in northern Tolima (Colombia).
RESUMEN. Ectoparásitos asociados con murciélagos en el noreste de Tolima, Colombia. El presente es- tudio registra los ectoparásitos asociados a murciélagos en el noreste del Tolima, Colombia, con datos sobre su prevalencia e intensidad promedio. Se capturaron 140 murciélagos distribuidos en 5 familias y 21 especies, siendo la familia Phyllostomidae la más abundante (84%), y la especie de mayor frecuencia Carollia perspicillata (35%). De las especies de murciélagos colectadas, 14 (66%) se hallaron parasitadas; 8 de estas (29.28%) fueron parasitadas por la familia Streblidae, 6 (14.28%) por Spinturnicidae, 5 (9.28%) por Macronyssidae y 5 especies (7.85%) parasitadas por Argasidae. Cinco familias y 24 especies de ectoparásitos fueron encontradas, de las cuales Trichobius joblingi fue la más abundante (16.85%) seguida por Radffordiella desmodi (11.04%). Esta investigación representa el primer reporte sobre las especies de ectoparásitos de murciélagos del norte del Tolima (Colombia).
Key words: Argasidae. Chiroptera. Host-Parasite relationships. Mesostigmata. Streblidae.
Palabras clave: Argasidae. Chiroptera. Mesostigmata. Relaciones parásito-hospedero. Streblidae.
Recibido 24 abril 2015. Aceptado 17 junio 2015. Editor asociado: M Lareschi 350 Mastozoología Neotropical, 22(2):349-358, Mendoza, 2015 AP Tarquino-Carbonell http://www.sarem.org.ar
INTRODUCTION conditions correspond to tropical dry forests (Holdridge, 1967). Because they cover a wide trophic spectrum and often exhibit high habitat specificity, bats Field Methods (Chiroptera) represent a good model for analyz- The material was collected between August and ing the consequences of habitat fragmentation November 2012, 3 nights per month, every night and environmental changes (Pérez-Torres and from 18:00 to 00:00 h. Five mist nets of 12 x 3 m Ahumada, 2004; Jones et al., 2009). Bats also were used at the understory and checked every represent a key group for understanding the 30 min. Bats were extracted from the mist net us- evolution and ecology of parasitism, because ing a red flashlight and separated into individual their ectoparasites are often specialized, with bags to prevent contamination between hosts. The many taxa closely associated with particular handling and collection of the organisms were made species of ectoparasites (Dick and Patterson, following the guidelines of the American Society of Mammalogists (Gannon et al., 2007; Sikes et al., 2006). 2011). Morphometric data were taken using a digital There have been relatively few studies of caliper with 0.1 mm precision. Ectoparasites were bat ectoparasites in Colombia. Early studies of collected with fine forceps and placed in Eppendorf obligate ectoparasitic Diptera in Colombia and tubes containing 70% ethanol, each one labeled with Panama highlighted the presence of the fami- the capture number from each bat. lies Streblidae (16 species) and Nycteriibidae (2 species) (Bequaert, 1940). Machado-Allison Laboratory methods and Antequera (1969) reported the distribution Bats were prepared as standard museum specimens and hosts of spinturnicid mites, including the and identified using keys and descriptions from presence of the genus Spinturnix. Subsequently, Gardner (2008). Mites were mounted in Hoyer’s Marinkelle and Grose (1981) published a list of and Lactophenol medium (Faraji and Bakker, 2008), ectoparasites in Colombian bats of the orders and examined using a Nikon Labophot microscope Diptera, Hemiptera and Siphonaptera, as well as YF21-E with phase contrast and Nikon DS-Fi1 5 families of mites, reporting a total of 88 spe- camera, and a Leica MS-5 stereomicroscope. Insects cies. Recently, Dick et al. (in press) developed a were examined in ethanol. We identified Macronys- sidae mites using Radovsky (1967), Spinturnicidae catalogue of Streblidae of Colombia, reporting with Herrin and Tipton (1975). We used Kohls et 73 species recorded in Colombia. Despite these al. (1965) to identify the species of Ornithodoros. efforts, information on Colombian bat ectopara- Diptera were identified with the keys of Wenzel sites is still scarce (Tarquino-Carbonell, 2014). (1976) and pictorial keys from Graciolli and Car- We studied associations between ectoparasites valho (2001). The specimens collected as samples and their chiropteran hosts in a fragment of are preserved in the Zoological Collection of the tropical dry forest in the northern department University of Tolima (CZUT). of Tolima, presenting data on prevalence and Data analysis intensity of infestation, and determining inter- dependence between ectoparasites and hosts. To evaluate the association of ectoparasites among different hosts, we used the following indices (Bush, MATERIALS AND METHODS 1997): Prevalence: the number of hosts infected with 1 or Study area more individuals of a particular parasite species (or taxonomic group) divided by the number of hosts The study was carried out in Chorrillo, a site of examined for that parasite species. approximately 50 ha of fragmented forest, in the Mean intensity: the average intensity of a particu- Ambalema municipality in northeastern Tolima, lar species of parasite among the infected members Colombia (4° 26’ N, 74°4 8’ W) approximately of a particular host species 273 m above sea level. The average annual tem- To determine if there are associations between the perature is 25.7 °C, and relative humidity is 80%. parasite and the bat taxa, a contingency table was Rainfall averages 3116 mm annually (Hijmans realized to each of the families of parasites found et al., 2005). The vegetation cover and climatic and a Fisher’s test was applied like in another studies ECTOPARASITES ASSOCIATED WITH BATS IN TOLIMA 351
(Almeida et al., 2011). Variables such as number of subfamily Phyllostominae, as well as in the parasitic hosts and presence of two or more parasite families Emballonuridae and Vespertilionidae, families at the same time are taken into account in were less common in general. this contingency table, testing for significant differ- ences between each parasite family with respect to Associations between ectoparasites the other families and bats
RESULTS Eight bat species (29.28%) were parasitized by streblid flies, 6 species (14.28%) by spinturni- We recorded 140 bats belonging to 21 species cids, 5 species (9.28%) by the macronyssids and and 5 families. Phyllostomidae was the most 5 species (7.85%) by argasid ticks (Table 2). A abundant family with the highest number of total of 69 hosts representing 14 bat species species registered (Table 1). The most fre- were found to be parasitized. Some species of quently captured bat species were Carollia ectoparasites collected were found in coexis- perspicillata (35%), Artibeus planirostris (14%) tence on the same host; in particular ~64% of and Desmodus rotundus (11%). Species in the these associations were found on D. rotundus.
Table 1 Bat species reported in this study.
Family Species N %
Emballonuridae Rhynchonycteris naso (Wied-Neuwied, 1820) 1 0.7 Saccopteryx bilineata (Temminck, 1838) 1 0.7
Noctilionidae Noctilio albiventris (Desmarest, 1818) 1 0.7
Phyllostomidae Trachops cirrhosus (Spix, 1823) 6 4.3 Tonatia saurophila (Koopman and Williams, 1951) 1 0.7 Phyllostomus hastatus (Pallas, 1767) 1 0.7 Lophostoma silvicola (d’Orbigny, 1836) 1 0.7 Lonchophylla robusta (Miller, 1912) 1 0.7 Glossophaga soricina (Pallas, 1976) 3 2.1 Carollia perspicillata (Linnaeus, 1758) 49 35 Carollia brevicauda (Schinz, 1821) 4 2.9 Sturnira lilium (E. Geoffroy, 1810) 7 5 Dermanura anderseni (Miller, 1902) 1 0.7 Artibeus planirostris (Spix, 1823) 20 14 Artibeus lituratus (Olfers, 1818) 7 5 Uroderma bilobatum (Peters, 1866) 1 0.7 Desmodus rotundus (E. Geoffroy, 1810) 16 11
Vestertilionidae Eptesicus brasiliensis(D’Orbigny and Gervais, 1847) 1 0.7 Myotis albescens (E. Geoffroy, 1806) 1 0.7 Myotis riparius (Handley, 1960) 2 1.4
Molossidae Molossus rufus (Geoffroy, 1805) 15 11 352 Mastozoología Neotropical, 22(2):349-358, Mendoza, 2015 AP Tarquino-Carbonell http://www.sarem.org.ar
Table 2 Parasitic associations found in this study.
Hosts N A B C D A+D A+B+C A+B+D B+C B+D B+C+D C+D A. planirostris 20 2 2 7 2 0 0 0 1 0 0 1 A. lituratus 7 0 0 5 4 0 0 0 0 0 0 1 C. brevicauda 4 0 0 0 5 0 0 0 0 0 0 0 C. perspicillata 49 0 0 0 25 0 0 0 0 0 0 0 D. rotundus 16 3 7 5 9 1 1 1 1 3 2 0 E. brasliensis 1 0 1 0 0 0 0 0 0 0 0 0 G. soricina 1 0 0 0 1 0 0 0 0 0 0 0 L. silvicolum 1 0 1 0 0 0 0 0 0 0 0 0 M. rufus 15 3 1 0 0 0 0 0 0 0 0 0 M. albescens 1 0 0 1 0 0 0 0 0 0 0 0 N. albivetris 1 1 0 0 0 0 0 0 0 0 0 0 P. hastatus 1 0 0 1 1 0 0 0 0 0 0 1 S. lilium 7 0 0 2 2 0 0 0 0 0 0 0 Total 124 9 12 21 49 1 1 1 2 3 2 3 n = total number of hosts. A. Argasidae - A. B. Macronyssidae - C. Spinturnicidae - D. Streblidae - A + D. Argasidae + Streblidae (if found at the same time).
The most common association between ecto- only found in D. rotundus, followed by parasites families was between Streblidae and Macronyssoides conciliatus in A. planirostris. Spinturnicidae. Argasidae. This family was represented by Streblidae. Eleven bat fly species were only two species (Table 6); however, they were recorded for this family. The most abundant found in large numbers and on five different bat fly is Trichobius parasiticus, present in host species, including diverse subfamilies D. rotundus, and Trichobius joblingi, found on with different trophic guilds (i. e. fisher bat C. perspicillata. The bat flies reported in this and vampire bat). study (Table 3) represent 18% of all species We also found Trombiculidae larvae on a registered in Colombia (Guerrero, 1997). Saccopteryx bilineata male, although they could The most abundant bat fly was T. joblingi, not be identified to species due to deterioration found on both species of Carollia. Four spe- of the proboscis. cies of Trichobius were found on five species The frequency data of Streblidae was sig- of bats. nificantly associated (Fisher’s p = 0.003) with Spinturnicidae. Six spinturnicid species the frequency values of each of the other were found in association with six host spe- three families of parasites found in this study. cies (Table 4). The most abundant species was No other significant associations were found Periglischrus iheringi, followed by Periglischrus between families. ojasti. We found adult males, females and, in smaller numbers, male protonymphs of DISCUSSION P. iheringi on two host species (Table 4). Macronyssidae. Four macronyssid species Phyllostomidae was the family with greatest were present on 12 individuals of five bat species richness and abundance (Table 1). This species (Table 5). The most frequently en- is consistent with results of studies of bat rich- countered species was Raddfordiella desmodi, ness in other Colombian tropical dry forests ECTOPARASITES ASSOCIATED WITH BATS IN TOLIMA 353
Table 3 Bat fly associations found in this study.
Sex ratio Total Hosts N nP Parasites P(%) MI ♂/♀ N %
Artibeus planirostris 20 2 Megistopoda aranea 0.50 3 100 10 1.5
Artibeus lituratus 7 2 Aspidoptera phyllostomatis 1.00 2 33.3 29 1 2 Megistopoda aranea 3.00 4 66.7 29 2
Carollia brevicauda 4 1 Mastoptera minuta 0.00 1 10 25 1 1 Strebla guajiro 0.00 1 10 25 1 2 Trichobius joblingi 0.60 8 80 50 4
Carollia perspicillata 49 3 Speiseria ambigua 0.33 4 6.9 6 1.3 1 Strebla guajiro 0.00 1 1.7 2 22 Trichobius joblingi 0.77 53 91.4 45 2.4
Desmodus rotundus 16 9 Trichobius parasiticus 1.21 53 100 56 5.8
Glossophaga soricina 3 1 Trichobius uniformis 0.00 1 100 33 1
Phyllostomus hastatus 1 1 Trichobius longipes 0.50 3 7.9 100 3 1 Mastoptera guimaraesi 1.69 35 92.1 100 35
Sturnira lilium 7 3 Megistopoda próxima 2.00 3 100 43 1
nP = number of parasitized hosts, N= number of collected parasites, P (%) = Prevalence, MI= mean intensity
(Ballesteros et al., 2007; Sánchez et al., 2007; areas, eating a wide variety of fruits, allowing Mantilla-Meluk, 2009). These results might be seed dispersion within forests (Cadena et al. attributed to the variety of trophic guilds that 1988). The evidence indicates that D. rotundus this family presents and their wide geographic is especially abundant in areas with a high den- distribution in the country (Ballesteros et al., sity of domestic animals (Sánchez et al., 2010). 2007; Sánchez et al., 2007; Mantilla-Meluk, This factor could explain their high abundance 2009). In terms of species richness and lo- in the study site during the sampling period. cal areas of importance for bat conservation, The low number of species from the families Chorrillo has almost a third of the bat spe- Emballonuridae and Vespertilionidae could be cies reported for the Department of Tolima related to limitations of sampling methods and (Galindo-Espinosa et al., 2010; Gutierrez et the flight behavior of the species, because these al., 2010; Solari et al., 2013). families are characterized by high flight between Species of Carollia are characterized by their and above the forest canopy (Bergallo et al., adaptation to changes in habitat conditions, a 2003; Simmons and Voss, 1998). Moreover, pattern applicable to various Neotropical areas relative to phyllostomids, their echolocation (Kalko, 1998; Simmons and Voss, 1998; Soriano, allows them to better detect and avoid mist nets 2000; Willig et al., 2007). Artibeus planirostris (Ortegón-Martínez and Pérez-Torres, 2007). can move easily between open and fragmented Specifically, members of Phyllostominae usually 354 Mastozoología Neotropical, 22(2):349-358, Mendoza, 2015 AP Tarquino-Carbonell http://www.sarem.org.ar
hunt their prey at higher open spaces or forest edges (Montenegro and Romero-Ruiz, 1999), thus explaining their low catch. Associations between ectoparasites 4 11 10 7.5 1.8 7.5 MI 6.33 and bats 30 30 30 20 Streblid flies are typical and widespread in the 100 100 100 P(%) Neotropics (Carrrejo and González-Obando, 4 9 1992). This family lives mainly on bats of the 15 11 10 15 19 Total family Phyllostomidae, which are also widely 0 0 0 distributed and abundant throughout the Neo- % 100 100 100 100 tropics (Guerrero, 1996). On the other hand, ♀ the most species-rich genus was Trichobius. 7 2 0 0 0 4 3 N Species in this genus are generally quite mo- bile with greater ability to fly relative to other 0 0 0 % 100 100 100 100 bat flies. For example,T. joblingi, a winged fly ♂ that lives in roost sites often shared by two 8 9 0 4 9 9 N 14 or more host species, actively moves outside the body of the host (Guerrero, 1996; Dick 0 0 0 0 0 0 %
100 and Patterson, 2006). In fact, this genus is ♂
P usually quite abundant in studies of this type 0 0 0 0 0 2 0 N (Guerrero, 1996; Dick and Patterson, 2006; Almeida et al., 2011). 0 0 0 0 0 % Aspidoptera phyllostomatis has been reported 100 100
P on Artibeus jamaicensis (Guerrero, 1997), but = protonymph female, P (%) = Prevalence, MI = mean intensity mean = MI Prevalence, = (%) P female, protonymph = Table4 ♂ 0 0 0 0 0 2
N there is no record of its occurrence on Artibeus 10 planirostris. However, changes in Artibeus tax- onomy for northern South America (Larsen et al., 2007, 2010) and recent reviews show that A. jamaicensis is restricted to the Colombian Caribbean region (Solari et al., 2013). For the Parasites Spinturnicid mite associations found in thein study. found associations mite Spinturnicid Magdalena valley of Department of Tolima, these bats must be recognized as A. planirostris Periglischrus ojasti Periglischrus Periglischrustorrealbai Periglischrus acutisternus Periglischrus Spinturnix americanus Spinturnix Periglischrus herrerai Periglischrus Periglischrus iheringi Periglischrus Periglischrus iheringi Periglischrus (Solari et al., 2013). Therefore, in this study we note that the species of Artibeus recorded in 2 1 1 1 5 2 3 nP northern Tolima is A. planirostris, which was parasitized by Aspidoptera phyllostomatis. 7 1 1 1 7 N 16 20 The incidence of Streblidae was very high for some bat species such as C. perspicillata and D. rotundus (Table 3), although the prevalence
nP = number of parasitized hosts, P = protonymph, P protonymph, = P hosts, parasitized of number = nP in this study is lower than that previously reported in Colombia (Marinkelle and Grose, 1981) for the same species. Low host specific- ity has been proposed for these bat flies, as Sturniralilium Phyllostomus hastatus Myotis albescens Myotis Desmodusrotundus Artibeuslituratus Artibeusplanirostris Hosts many species of bats that share the same roost sites are exposed to similar parasites (Theodor, 1957). On the other hand, Streblidae are very common among phyllostomid species, which could explain this finding compared to groups ECTOPARASITES ASSOCIATED WITH BATS IN TOLIMA 355
Table 5 Macronyssid mite associations found in the study
P ♀ Hosts N nP Parasites Total P(%) MI N % N % Artibeus planirostris 20 2 Macronyssoides conciliatus 0 0 4 100 4 10 2 Desmodus rotundus 16 8 Radffordiella desmodi 34 100 6 100 40 50 5.71 Eptesicus brasiliensis 1 1 Steatonyssus occidentalis 8 100 1 100 9 100 9 Lophostoma silvicolum 1 1 Parichoronyssus bakeri 0 0 2 100 2 100 2 Molossus rufus 15 1 Macronyssoides conciliatus 0 0 3 100 3 6.7 3
nP = number of parasitized hosts, P = protonymph, P (%) = Prevalence, MI = mean intensity
Table 6 Argasid tick associations found in the study
L Hosts N nP Parasites Total P(%) MI N %
Artibeus planirostris 20 2 Ornithodoros hasei 8 0 8 10 4
Desmodus rotundus 16 1 Ornithodoros hasei 5 0 5 10 5 16 2 O. pavloskiella natalinus 14 0 14 10 7
Molossus rufus 15 3 Ornithodoros hasei 5 0 5 20 1.7
Myotis albescens 1 1 Ornithodoros hasei 1 0 1 100 1
Noctilio albiventris 1 1 Ornithodoros hasei 11 0 11 100 11
nP = number of parasitized hosts, larvae L = P (%) = Prevalence, MI = mean intensity
of mites already reported in other studies 3 families of ectoparasites and their equal (Guerrero, 1996). Bat flies are often dependent proportions suggest that the remaining families on the presence of the other groups; i.e., bat were associated uniformly for this study. Taxa flies will be associated with particular species exhibiting the lowest ectoparasite prevalence depending on which bat species are present in and mean intensity were those species that particular roosts. shelter in open areas. Also, caves allow greater The high interdependence found for streblids horizontal transfer of ectoparasites relative to in the contingency table reflects by abundance open habitats (Guerrero, 1993; Guerrero, 1996; of Streblidae on C. perspicillata and D. rotundus, Dick and Paterson, 2006) revealing their strongest association in rela- It has been proposed that the presence or tion to other groups of ectoparasites. Thus, absence of one parasitic fly species may facilitate bat flies on C. perspicillata were significantly the presence or absence of another fly species, more likely to be the only parasites on their by representing the persistence of two species host to be found in association with other of parasites in a host over time (Dick and Get- parasites. The significant results for the other tinger, 2005). In some cases, these associations 356 Mastozoología Neotropical, 22(2):349-358, Mendoza, 2015 AP Tarquino-Carbonell http://www.sarem.org.ar occur even when the parasites are in different americanus has been described parasitizing genera (Dick and Gettinger, 2005). The degree Brazilian Myotis spp. (Silva et al., 2013). Ours of specificity in bat flies as obligate ectoparasites is the first report of this association for the has been debated and some studies suggest a region of Tolima. high specificity (Dick and Gettinger, 2005), The proportion of Macronyssidae was low although higher host densities could provide a relative to other groups, such as streblids. Their substrate rich for bat flies and might be affect- range of movement is much lower than other ing associations of these flies (Guerrero, 1993; groups, gives them greater specificity in rela- Dick y Paterson, 2006). However, certain factors tion to other groups of ectoparasites (Radovsky, that influence the specificity such as physical 1967). We found no males of this family on any isolation, climate, competition, predation and hosts, likely because Macronyssidae males do physiological and morphological adaptation are not consume blood (Radosky, 1967). The low recognized (Marshall, 1976, 1982). number of macronyssid mites collected in this The dynamics of mites as obligate ecto- study makes it difficult to compare their preva- parasites of bats, unlike other groups such as lence with other studies, which reported higher Streblidae, have not been studied in recent numbers of mites. For example, Radffordiella decades and little is known about the regional desmodi species has been found in associa- distribution of species in the case of Colombia tion with Desmodus in Costa Rica (Rojas et (Bequaert, 1940; Machado-Allison and Ante- al., 2008). Steatonyssus occidentalis has been quera, 1969; Marinkelle and Grose, 1981). These found in some genus of Vespertilionidae (Ra- studies only include new species descriptions, dovsky, 1967). Macronyssoides conciliatus can reflecting the paucity of recent studies on be found in Molossus genus (Radovsky, 1967), taxonomy of ectoparasites and parasite-host and the recently described P. bakeri (Morales- relationship. Malacara and Guerrero, 2007) can be found The Spinturnicidae family, found only on the in some Phyllostomidae. The low number of wings and tail membranes of the host, exhibit a specimens collected in this study may indicate life cycle morphologically adapted and modified contamination, so it is necessary to obtain more relative to other Mesostigmata (Rudnick, 1960). samples to gain an accurate understanding of In general, this family can be easily found in any their prevalence. given bats group of the New World due to their Argasid ticks can be found in well-estab- morphological, ecological and behavioral con- lished colonies of bats, where high transfer ditions (Dowling, 2006). Periglischrus iheringi of ectoparasites occurs (Guerrero, 1996). is commonly found in species of Artibeus and Ornithodoros hasei has been found in as- Uroderma, and other species as S. lilium (Her- sociation with species of the genus Artibeus, rin and Tipton, 1975). This species has been Phyllostomus, Noctilio, Rhogeeesa and Molossus reported in Colombia in several leaf-nosed bat for Colombia (Marinkelle and Grose, 1981). species including some species of Glossophaga Ornithodoros (Pavloskyella) natalinus has only (Marinkelle and Grose, 1981) without refer- been reported previously on bats of the genus ences to A. planirostris, which might indicate Natalus (Capinera, 2008). We present the first contamination or misidentification of the host. report of Ornithodoros (Pavloskyella) natalinus However, the association between these two on individuals of D. rotundus for this region. species has already been extensively described Results from our study suggest this local- from previous works in Brazil (Almeida et al., ity can provide important information about 2008; Silva et al., 2013). bat-ectoparasites relationships in dry forests, Periglischrus ojasti has been reported in an ecosystem that has previously been only Colombia parasitizing S. lilium and S. ludovici, rarely studied. In particular, we found that while P. acutisternus has primarily been report- bat species most frequently parasitized (C. per- ed in association with species of Phyllostomus, spicillata, D. rotundus and A. planirostris) are as we found in this study (Marinkelle and those which inhabit transformed spaces and Grose, 1981). In the Neotropics, Spinturnix secondary vegetation, exhibiting habitat flex- ECTOPARASITES ASSOCIATED WITH BATS IN TOLIMA 357 ibility. This habitat preference, in addition to Valle: Colección de Edición Previa. Universidad del ectoparasite ecology, roosting site, bat biology Valle. Serie Investigaciones. DICK CW and D GETTINGER. 2005. A faunal survey of and host behavior, influence the association streblid bat flies (Diptera: Streblidae) associated with and competition between different ectoparasites bats in Paraguay. Journal of Parasitology 91:1015-1024. families and the parasite load of the hosts. Our DICK CW and B PATTERSON. 2006. Bat flies as obligate data relating to prevalence of major groups and ectoparasites of bats. Pp. 54-66, in: Micromammals and macroparasites: How are they and how interact? species of ectoparasites present in bat popula- (S Morand, ed.). Editorial Springer. Museum tions of northern Tolima could help inform Smitsonian, New York. and provide direction for further research on DICK CW, G GRACIOLLI, and R GUERRERO. (In press). these topics. 30. Family Streblidae. In: Catalogue of Streblidae of Colombia. Special volume of Zootaxa. 25 pp. DOWLING AP. 2006. Mesostigmatid mites as parasites ACKNOWLEDGEMENTS of small mammals. Pp. 103-117 in: Micromammals and macroparasites: From evolutionary ecology to To Viviana García, Azucena Ramirez, Fabian Santos, Kevin management (S Morand, B Krasnov, and R Poulin, Gonzalez, Daniel Duran, Enryque Torres, Steven Liévano, eds.). Springer-Verlag, Tokyo. Luisa Beltran, Daniela Ortiz, and Angela Navarro for their FARAJI F and FA BAKKER. 2008. Modified method for field supportment. To the Instituto de Zoología y Ecología clearing, staining and mounting plant-inhabiting mites. Tropical from the Universidad Central de Venezuela and European Journal Entomology 105:793-795. the people who made it possible to stay in this country GALINDO-ESPINOSA EY, KA GUTIÉRREZ, and to review the material. To Luz Stella Sierra, Jenny Sierra, G REINOSO. 2010. Lista de quirópteros del Jennifer Sierra, Paola Mojica for their help in Caracas. To departamento del Tolima, Colombia. Biota Colombiana the people from Chorrillo for receiving us very generously 11:107-116. in the location. We are very grateful to Carl Dick and an GANNON WL, RS SIKES, and THE ANIMAL CARE anonymous reviewer for their suggestions. Special thanks AND USE COMMITTEE OF THE AMERICAN to Erin Kane for their comments. The lead author is es- SOCIETY OF MAMMALOGISTS. 2007. Guidelines pecially grateful to Fredy Quintero for his support in this of the American Society of Mammalogists for the use work. This research was funded by the Comité Central de of wild mammals in research. 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