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Ectoparasite richness and abundance on three species of Neotropical bats

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Title:
Ectoparasite richness and abundance on three species of Neotropical bats
Translated Title:
La riqueza y abundancia de ectoparásitos en tres especies de murciélagos neotropicales ( )
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English
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Reiter, Roxanne
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Bats   ( lcsh )
Ectoparasitic infestations   ( lcsh )
Species diversity   ( lcsh )
Costa Rica--Puntarenas--Monteverde Zone   ( lcsh )
Murciélagos
Infestaciones ectoparasitarias
Diversidad de especies
Costa Rica--Puntarenas--Zona de Monteverde
Tropical Ecology Spring 2011
Ectoparasitism on bats
Ecología Tropical Primavera 2011
Ectoparasitismo en los murciélagos
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Reports   ( lcsh )
Reports

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Abstract:
Ectoparasitic arthropods can decrease the fitness or survival of their hosts by increasing host energy expenditure. Bats harbor many species of ectoparasites; host biology, grooming, and roosting habits can affect intensity of parasite infestation. This study assessed ectoparasitism on three species of Neotropical bats by Streblid batflies (Streblidae) and bat mites (Order: Acari). Bats were netted and ectoparasites identified to the lowest taxonomic level possible. Host species had a significant impact on ectoparasite richness and abundance (Two Way ANOVA, F = 41.25, df = 2, p < 0.0001). Anoura geoffroyi suffered the most intense overall parasitism and parasitism by Streblids, but Hylonycteris underwoodi hosted more mites and had a greater richness of mites per bat (Tukey’s HSD tests, p < 0.05). Carollia perspicillata suffered very low parasitism rates by all measures. Host sex did not appear to impact ectoparasitism across species or between males and females of the same species. Ectoparasitism is likely impacted by roosting dynamics, grooming habits, and density of individuals in the colony.
Abstract:
Los artrópodos ectoparásitos pueden disminuir el éxito reproductivo o la sobrevivencia del hospedero aumentando el gasto energético. Los murciélagos hospedan varias especies de parásitos, la biología del hospedero, acicalamiento y hábitos de descanso pueden afectar la intensidad de infección por parásitos. Este estudio evalúa el ectoparasitismo en tres especies de murciélagos neotropicales por moscas de la familia Streblidae y ácaros. Los murciélagos fueron atrapados con redes y los ectoparásitos identificados al menor nivel taxonómico posible. La especie de hospedero tiene un impacto significativo en la riqueza y abundancia (Two Way ANOVA, F = 41.25, df = 2, p < 0.0001). Anoura geoffroyi sufre la mayor intensidad en general de parasitismo y también parasitismo por las moscas streblidas, pero Hyloniceteris underwoodi hospeda más acaros y tiene una mayor riqueza de los mismos por el murciélago (Tukey’s HSD tests, p < 0.05). Carollia perspicllata sufre una tasa muy baja de parasitismo en todas las medidas. El sexo del hospedero parece no tener impacto alguno en el parasitismo entre las especies o entre sexos de la misma especie. El ectoparasitismo está altamente influenciado por la dinámica de los sitios de descanso, los hábitos de acicalamiento y la densidad de individuos de la colonia.
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Text in English.
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Ectoparasite richness and abundance on three species of Neotropical bats Roxanne Reiter Department of Biology, University of Puget Sound ABSTRACT Ectoparasite arthropods can decrease the fitness or survival of their hosts by increasing host energy expenditure Bats harbor many species of ectoparasites ; host biology, grooming, and roosting habits can affect intensity of parasite infestation This study assessed ectoparasitism on three species of Neotropical bat s by Streblid batflies (Streblidae) and bat mites (Order: Acari). Bats were netted and ectoparasites identified to the lowest taxonomic level possible Host s pecies had a significant impact on ectoparasite richness and abundance (Two Way ANOVA, F = 41.25, df = 2, p < 0.0001 ) Anoura geoffroyi suffered the most intense overall p arasitism and parasitism by Streblids, but Hylonycteris underwoodi hosted more mites and had a greater richness of mites per bat tests, p < 0 .05) Carollia perspicillata suffered very low p a rasitism rates by all measures. Host sex did not appear to impact ectoparasitism across species or between males and females of the same species. Ectoparasitism is likely impacted by roosting dynamics, grooming habits, and density of individuals in the colony RESUMEN Artropodos ectoparsitos pueden disminuir el exito reproductivo o la sobrevivencia del hospedero aumentando el gasto energtico. Los murcilagos hospedan varias especies de parsitos, la biologa del hospedero, acicalamiento y hbitos de descanso pueden afectar la intensidad de infeccin por parsitos. Este estudio evala ectoparasitismo en tres especies de murcilagos neotropicales por moscas de la familia Streblidae y acaros. Los murcilagos fueron atrapados con redes y los ectoparsitos identificados al menor nivel taxonmico posible. La especie de hospedero tiene un impacto significativo en la riqueza y abundancia (Two Way ANOVA, F = 41.25, df = 2, p < 0.0001). An oura geoffroyi sufre la mayor intensidad en general de parasitismo y tambin parasitismo por moscas streblidas, pero Hyloniceteris underwoodi hospeda ms acaro y tiene una mayor riqueza de los mismos por murcilago Carollia p erspicllata sufre una tasa muy baja de parasitismo en todas las medidas. El sexo del hospedero parece no tener impacto alguno en el parasitismo entre las especies o entre sexos de la misma especie. Ectoparasitismo esta altamente influenciado por la din mica de los sitios de descanso, los habitos de acicala miento y la densidad de individuos de la colonia. INTRODUCTION Ectoparasites are organisms that live and feed on the external surfaces of other animals. In some cases, ectoparasites can reduce long term survival, reduce clutch size, alter breeding behavior, or inc rease the cost of reproduction ( Lucan 2006 Presley and Willig 2008 ). B at s (Chiroptera) host a higher diversity of order s pecific arthropod ectoparasites than any other mammal order (P atterson et al. 2008) and the greatest diversity of ectoparasites occurs on the family Phyllostomidae in the New World tropics (Wenzel et al. 1966). Some common parasites of tropical bats include several clades of mites (Order: Acari; Lucan 2006, Christe et al. 2007) and the Streblid batflies (Diptera: Streblidae; Wenzel et al. 1966, Bertola et al. 2005, Dick and Patterson 2006, Christe et al. 2007, Presley and Willig 2008) Although the fitness costs of bat ectoparasitism are not well understood, mite in festations cause d heightened grooming rates, decreased resting time, and elevated metabolism in bat hosts (Giorgi et al. 2001). Ectoparasite load may be affected by behavioral and biological characters between host species and sex es

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Differences in b at ec toparasitism between species can be influenced by roosting habits and host grooming behavior ( Lucan 2006, Patterson et al. 2007). Firstly, s ome ectoparasites deposit eggs or larv a e on the walls of the roost; for this reason, ephemeral roost sites are less conducive to parasite transmission (Hofstede and Fenton 2005, Patterson et al. 2007 Stuckey 2009 ). S econdly, s pecies that roost in large colonies have been observed supporting l arge populations of parasites (Wenzel et al. 1966 Dick et al. 2003 ) Thirdly, h igh host density in a roost also likely favors contact between individuals and thus increases the chance of parasite transmission between individuals (Lucan 2006). The reverse trend has also been observed for low density roosts; even for some large colonies, bats that space themselves further from their neighbors decrease the chance of transmitting parasites (Dick et al. 2003). For these three reasons, large dens ely packed colonies roost ing in more permanent structures are expected to support the heaviest parasite loads Additionally, g rooming is implied as the leading cause of adult parasite mortality ( Bertola et al. 2005, Dick and Patterson 2006 ) and fr equency a nd intensity of grooming effort is likely to differ between bat species A number of studies on both tropical and temperate bat species have also shown that female bats generally stuffer greater rates of ectoparasitism than males (Dick et al. 2003, Lucan 2006, Christe et al. 2007, Patterson et al. 2008, Presley and Willig 2008). This difference has predominantly been attributed to sex specific roosting behaviors. Maternity colonies, typically dense aggregations of females and their pups, can s upport large parasite populations and bias parasitism rates towards females (Dick et al. 2003 Christe et al. 2007 ) This trend reflects the increased opportunity for mother to mother and mother to pup parasite transmission (Lucan 2006, Christe et al. 200 7, Patterson et al. 2008, Presley and Willig 2008). The potential for maternity colonies to support large parasite populations, compounded with the observation that reproductive females spend less time grooming (presumably because grooming is an energetic ally costly activity; McLean and Speakman 1997) are probable explanations for the sex bias in parasitism rates. Another p otential contributing factor is the immunosuppressive effects of sex hormones during reproductive periods (Lucan 2006, Patterson et al 2008), although both female and male sex hormones can compromise immune function and thus the ir effect on sex bias is unclear (Christe et al. 2000). In this study I examine d variation in ectoparasite load on thr ee species of Neotropical bats (Phyllosto midae) with variable colony sizes; one lives in small groups (10 20 bats) another in larger groups (20+), and one with a known colony size of 100 150 individuals. The species occur in overlapping ranges in the Monteverde area in Puntarenas, Costa Rica and all live in permanent roosts (none are foliage roosters; Laval and Rodriguez H, 2002 ). METHODS Study Sites Bats were mist netted during April 2011 near Monteverde Costa Rica in the hummingbird gar dens at Bosque Nuboso and SelvaT ura and mist and butterfly netted at an abandoned house on the University of Georgia p roperty in San Luis, Costa Rica (Figure 1). All captures occurred between dusk and 9:30pm.

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Figure 1. Study sites where three species of Phyllostomid bats were captured to assess ectoparasite loads. Nectarivorous bats Anoura geoffroyi and Hylonycteris underwoodi were mistnetted in t he hummingbird garden in Selva T ura approximately 1500 m elevation which is surrounded by Pa cific slope Lower Montane Wet Forest (left). Carollia perspicillata a frugivore, roosted in an abandoned house at 1200 m elevation on the University of Georgia station in San Luis (right). The house is surrounded by Atlantic slope secondary Premontane Moist Forest Study Species Three species of bats from the family Phyllostomidae were studied in this experiment: Carollia perspicillata This primarily frugivorous bat ranges from Southern Mexico to Paraguay and is common i n Costa Rican lowlands up to ~15 00 m It is found in almost all habitats in its range. Colony sizes range from harems of 20 to groups of thousands, although the colony studied here was comprised of about 100 150 individuals of mixed sexes living in the abandoned house on the Univers ity of Georgia property (Figure 1 ) The density of bats in the house was low, and individuals were spread out with relation to one another C. perspicillata is the most extensively studied of any bat species (Laval and Rodriguez H, 2002 ) Anoura geoffroyi This species ranges from Northern Mexico to Southeastern Brazil from mid elevations up to ~2050 m. A. geoffroyi is not abundant throughout its range but can be locally abundant. A large number of these nectarivorous bats frequent the hummingbi rd feeders in the Bosque Nuboso and at Selvatura ( Figure 1; LaVal and Rodriguez H, 2002 ). Colonies of 20+ individuals roost in a variety of shelters, but this colony is suspected to roost in hollow trees. Hylonycteris underwoodi Mainy nectarivorous H. underwoodi is found from Mexico to Panama at elevations up to 3000 m (Jones and Homan 1974). S mall groups of 10 20 individuals roost in many permanent structures but this colony likely roosts in hollow trees ( Richard LaVal, personal communication ). Ect oparasite Diversity Streblid batflies (Diptera: Streblidae) are obligate blood sucking ectoparasites of bats that live in fur and wing membranes (Wenzel et al. 1996, Patterson et al. 2007). These ectoparasites are only found living on Neotropical bats. The bats exhibit no apparent response to the nearly

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constant feeding of the Streblids, whose bites can be painful to humans (Dick and Patterson 2006). Male Streblid batflies live their entire lives on the host and females leave only to et al. 1966, Dick and Gettinger 2005). For this reason, ephemeral roost sites are less conducive to transmission of Streblid batflies (Hofstede and Fenton 2005, Patterson et al. 2007). Bat mites (Acari) are another group of obligate blood sucking parasites that live mainly on the wing membranes of bat hosts (Lucan 2006). They complete their entire life cycle on the host and depend on close host contact between hosts for transmission (Christe et al. 2007). M ites observed on these bats likely belong to the Spinturnicidae family, which are exclusive ectoparasites of bats ( Christe et al. 2000). Data collection Once captured, bats wer e held in cloth bags for no longer than 45 minutes until parasites could be removed Species and sex were recorded for each bat. If present, e ctoparasites were clearly visible or found by blowing on the fur and removed with forceps (Figure 2) Both mites and Stre blid batflies were collected from the bats. The parasites from each bat were stored in an ethanol filled vial for later identification Bats were marked to avoid recapture my clipping a small patch of fur from the back. In the lab, mites were classified to morphospecies and Streblid batflies were identified to genus and, if possible, species Figure 2. Locating ectoparasites on the bat hosts. In addition to blowing on the fur, the w ing membrane s of the bats were examined for parasites ( H underwoodi pictured; left ) Streblid batfly Exastinion clovisi was found on the wing membranes of A geoffroyi and on one H underwoodi individual It was common to find groups of E. clovisi on bats (right) R ESULTS Four genera of Streblid batflies and two morphospecies of mites were identified on the three bat species (Table 1, Appendix A). Four other species of mite were observed on the hosts but could not be consistently collected because they were either too numerous, too small or fragile, or on delicate tissues of the host bat. These mites were excluded from statistical analysis.

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Table 1. E ctoparasite richness and abundance differed for the three species of bat. The most abundant parasite, Streblid batfly Exastinion clovisi was found almost exclusively on A. geoffroyi The second most abundant parasite was White mite 2, found most often on H. underwoodi Even considering sample sizes differed, H. underwoodi had the most mites and A. geoffroyi had the most Streblid batflies of the three species Numbers in cells indicate the total number of each parasite identified for all individuals of that species. Parasite species Exastinion clovisi Strebla sp. Trichobius sp. Anastrebla sp. White mite 1 White mite 2 A. geoffroyi (n = 52) 202 25 1 0 20 1 H. underwoodi (n = 37) 1 13 0 1 17 43 C. perspicillata (n = 39) 0 2 14 0 1 0 Ectoparasite Richness Ectoparasite richness differ ed significantly between the three species of bat ( Figure 3; Two Way ANOVA, F = 41.25, df = 2, p < 0.0001). A. geoffroyi hosted an average of 1.59 0.09 (SE) species of parasite per bat just over double the parasite richness of 0.78 0.13 (SE) found on H. underwoodi C. perspicillata had the lowest parasite richness with an average of only 0.31 0.12 (SE) parasites per bat. Parasite richness differed s ignificantly between all three bat species (Figure 3 ; < 0.05). Male bats had slightly hi gher ectoparasite richness (n = 73 mean = 1.06 0.081 SE) than females (n= 55, mean = 0.98 0.104 SE ), but h ost sex did not significantly impact parasite richness across all species (Two Way ANOVA, F = 0.355, df = 1, p = 0.5521). Likewise, w ithin a given species, sex did not significantly affect ectoparasite richness (Two Way ANOVA, F = 0.037, df = 2, p = 0.96). The impact of mites and Streblid batflies on overall richness was examined in separate analyses. Host species also had a significant impact on mite richness ( Figure 3; Two Way ANOVA, F = 6.34, df = 2, p = 0.002). Average mite richness on C. perspicillata was 0 .026 0.082 (SE) was more than ten times lower than the other two species ( < 0.05). Although they did not differ significantly, H. underwoodi with a mean of 0.46 0.095 (SE) had more mites per bat than A. geoffroyi mean 0 .30 0.064 (SE) by about 0.15. Similarly, Streblid batfly richness was significantly affected by host species ( Figure 3; Two Way ANOVA, F = 56.17, df = 2, p < 0.001). A. geoffroyi had about four times the Streblid batfly richness and was significantly different from the other two species ( < 0.05). A. geoffroyi hosted an average of 1.28 0.067 (SE) species of Streblid batflies compared to 0.32 0.099 (SE) for H. underwoodi and 0.28 0.086 (SE) for C. perspicillata.

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Figure 3. A. geoffroyi had the highest overall ectoparasite richness (mites and Streblid batflies), which was double that of H. underwoodi and five times greater than C. perspicillata Mite richnesses were similar for A. geoffroyi and H, underwoodi C. perspicillata had the significantly fewest mite species per bat and suffered low parasitism by all three measures The most S treblid batfly species were found on A. geoffr oy which greatly contributed to it exhibiting the highest overall ectoparasite richness. Different symbols above bars within each group indicate significant differences and error bars represent +/ one SE. Ectoparasite Abundance Abundance of ectoparasites differed between species ( Figure 4; Two Way ANOVA, F = 27.89, df = 2, p < 0.0001). Individuals of A. geoffroyi had the highest parasite abundance with an average of 4.58 0.36 (SE) parasites per bat. This was significantly higher and more than twice the parasitism on H. underwoodi which averaged 2.03 0.53 (SE) parasites per host ( Figure 4; < 0.05). C. perspicillata had the fewest parasite s per bat, averaging 0.46 0.46 (SE) with nearly ten times less than A. geoffroyi and a quarter that of H. underwoodi Although females (n = 55, mean = 3.28 0.413 SE) had slightly higher parasite abundance than males (n = 73, mean = 2.45 0.320 SE), host sex did not significantly influence parasite abundance across all sp ecies (Two Way ANOVA, F = 2.00, df = 1, p = 0.16). Likewise, w ithin a given species, sex did not significantly affect ectoparasite abundance (Two Way ANOVA, F = 0.8975, df = 2, p = 0.41). Mite abundance differed between bat host species ( Figure 4; Two Way ANOVA, F = 6.34, df = 2, p = 0.002). C. perspicillata had an extremely low mite abundance of 0.03 0.334 (SE) mites per bat but was not significantly different from A. geoffroyi with 0.394 0.259 (SE) mites per bat. H. underwoodi with a mean of 1.62 0.386 (SE) mites per bat had significantly more mites than the other two species ( Figure 4; C. perspicillata 0 0.2 0.4 0.6 0.8 1 1.2 1.4 1.6 1.8 Overall Mites Streblid batflies Ectoparasite richness A. geoffroyi H. underwoodi C. perspicillata N = 52 N = 37 N = 39 * ** *

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had remarkably low mite abundance, with only one mite observed on all 39 individuals (Table 1). Streblid batf ly ab undance was also significantly impacted by host species ( Figure 4; Two Way ANOVA, F = 56.17, df = 2, p < 0.001). A. geoffroyi hosted an average of 4.18 0.261 (SE) batflies per bat, about ten times more than either of the other two species (Figure 4 ). H. underwoodi hosted an average of 0.405 0.387 (SE) and C. perspicillata 0.436 0.335 (SE) species of Streblid batflies. Streblid batfly abundance contributes greatly to overall parasite abundance, as A. geoffroyi had fewer mites than H. underwoodi yet had significantly more parasites overall. C. perspicillata had the least number of mites, Streblid batflies and overall parasites per host. Figure 4. Similar to trends obs erved for ectoparasite richness, A. geoffroyi hosted the greatest overall number of parasites and the most Streblid batflies of all three species. H. underwoodi had the second higheset overall parasite abundance per bat, influenced mainly by its high mite abundance. C. perspicillata had lo w parasite abundance by all three measures. Different symbols above bars within each group indicate significant differences and error bars represent +/ one SE. C. perspicillata = 0.578) hosted only three species of parasite compared to five species for each H. underwoodi = 1.074) and A. geoffroyi Table 1). Although their richnesses differed, parasite diversity was not significantly different between C. perspicil lata and A. geoffroyi (Shannon Weiner, df = 245, modified t = 0.37, p = 0.71; modified t test from Zar, 1984). Parasite diversity on H. underwoodi however, was significantly higher than both A. geoffroyi (df = 379, modified t = 4.19, p < 0.001) and C. pe rspicillata (df = 264, modified t = 2.56, p = 0.011). Based on the total number of captured bats with parasites, parasitism for the three species differed from expected values considering sample sizes for each species (Chi square, df = 2, p < 0.05). A re markably high proportion of A. geoffroyi individuals were parasitized, with 49 of 52 0 1 2 3 4 5 6 Overall Mites Streblid batflies Ectoparasite abundance A. geoffroyi H. underwoodi C. perspicillata ** *** * N = 52 N = 37 N = 39

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individuals or 9 4. 2 3 % hosting ecto parasit es The same trend was not observed for the other species; 57% of H. underwoodi had parasites close to the 62.5% weighted overall parasitism rate for the three species combined Only 26% of C. perspicillata had parasites which was significantly fewer than expected by chance if the three species had equal chances of being parasitized. Of the 55 total females captured, 62% wer e parasitized. Females of C. perspicillata were least frequently found with parasites (n = 19, 21% parasitized) followed by H. underwoodi (n = 10, 60% parasitized) and then A. geoffroyi (n = 26, 92% parasitized). Similar trends were observed for the 73 ma les, of whom 63% had parasites; C. perspicillata males had the lowest parasitism rates (n = 20, 30% parasitized) followed again by H. underwoodi (n = 27, 56% parasitized) and then A. geoffroyi (n = 26, 96% parasitized). The difference in parasitism between male and female bats does not differ from expected values based on sample size (Chi square, df= 1, p > 0.05). Likewise, comparisons of parasitism by sex within each species do not differ from expected values based on number of males and females captured for each species (Chi square tests, df=1, p > 0.05). DISCUSSION Species Effects R oost size did not appear to be the determining factor in ectoparasite load for these three species of bats. The species with the smallest roosting colonies, H. underwoodi was more heavily infested by mites and harbored more total parasites than C. perspicillata with a known colony size of more than 100 individuals. Although I could not quantify colony size for A. geoffroyi t hose individuals harbored more parasites than the C. perspicillata colony by every measure. I conclude that the variation in observed parasitism rates on these species may be more an effect of host density in the roost than roost size itself. In the aban doned house, C. perspicillata were spread out and able to distance themselves from conspecifics. If the other two species are indeed roosting in hollow trees, individuals are more likely to be roosting in closer quarters, which could have caused their obs erved higher parasite loads (Lucan 2006). A second factor potentially contributing to the observed variation in parasite load could be innate differences in grooming proficiency between species. Variation in grooming habits between the species is unknown and was not assessed in this study, but if one species was more efficient or devoted more energy to grooming behaviors their parasite loads would be disproportionately lower. Thirdly, host age may have impacted parasitism rates. Age was also not assessed in this study, but it is possible that juveniles have compromised immune resistance to parasitism or are less efficient at grooming. Sex Effects In contrast to records from previous literature, host sex did no t appear to influence observed ectoparasitism rates ( Lucan 2006, Christe et al. 2007, Patterson et al. 2008). The lack of sex bias in parasitism rates for these three species may be related to several factors; firstly, reproductive status may not have pla yed a significant role in influencing parasitism in this study Although I collected data for several pregnant females of each species, the seemingly high proportion of inactive females did not suggest I was netting from maternity colonies at any site. The C. perspicillata study group was not living in a materni ty colony in the abandoned house,

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and perhaps a lack of maternity colonies for all three sp ecies diminished the sex bias in parasitism observed in other studies. Secondly, grooming habits were not assessed and may have differed between sexes. It is possible that males and females within a given sex invest comparable energy in grooming behavio r, or that pregnant and lactating females of these three species do not groom le ss than males as was observed in another species of bat (McLean and Speakman 1997). Continuations of Research Future studies of ectoparasitism on these three bats could incor porat e host reproductive status and age. More research is needed on the roosting biology and dynamics for all three species, but particularly for A. geoffroyi and H. underwoodi which are extremely data deficient. In future studies for which limited time plays a role in collecting and analyzing data, I would recommend focusing on one study species and obtaining a larger sample size to make trends due to sex, reproductive status, and age. The large population of A. geoffroyi in Montever de that frequents the hummingbird gardens at SelvaTura and Bosque Nuboso would be a relatively easy group to study. ACKNOWLEDGEMENTS First, I extend a special thanks to Emily Hollenbeck for her assistance in the field, for accompanying me even on the rain y nights and being my second set of hands when I truly needed the help. Secondly, an equally special thank you to Moncho Calderon for his skill in identifying the bats, teaching me how to mist net and all around gettin g me on track with my project. Their h elp was indispensible in the field and they both made this project possible for me. Another big thank you goes to Arturo Cruz Obando for his expert guidance in San Luis and help capturing bats, and also for my first moto ride. Gisella Fernandez deserves a thank you for assistance with statistics and helping me keep my cool when the diversity template nearly made me crazy. I would also like to sincerely thank Alan Masters for his advice, patience, guidance and help with statistic al analysis. Lastly, thanks very much to Bosque Nuboso, Selvatura La Estacion Biologica and the University of Georgia field station for allowing me to net on their properties. LITERATURE CITED Bertola, P.B., C. C. Aires, S. E. Favorito, G. Gracioli, M. Amaku, and R. Pinto de Rocha. 2005. Bat flies (Diptera: Streblidae, Nycteribiidae) parasitic on bats (Mammalia: Chiroptera) at Parque Estadual de Cantareira, Sao Paulo, Brazil: parasitism rates and host parasite associations. Memoirs of the Institute of Oswaldo Cruz 100: 25 32. Christe, P., R. Arlettaz, and P. Vogel. 2000. Variation in intensity of a parasitic mite ( Spinturnix myoti ) in relation to the reproductive cycle and immunocompetence of its bat host ( Myotis myotis ). Ecology Letters 3: 207 212. Christe, P., O. Glaizot, G. Evanno, N. Brunydonckx, G. Devevy, G. Yannic, P. Patthey, A. Maeder, P. Vogel, and R. Arlettaz. 2007. Host sex and ectoparasites choice: preference for, and higher sur vival on female hosts. Journal of Animal Ecol ogy 76: 703 710. Dick, C. W., M. R. Gannon, W. E. Little, and M. J. Patrick. 2003. Ectoparasite associations of bats from central Pennsylvania. Journal of Medical Entomology 40: 813 819. Dick, C. W., and D. Gettinger. 2005. A faunal survey of Streblid flies (Diptera: Streblidae) associated with bats in Paraguay. Journal of Parasitology 91: 1015 1024.

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Dick, C. W. and B. D. Patterson. 2006. Bat flies: obligate ectoparasites of bats In: Micromammals and macroparasites from evolutionary ecology to mamagement Springer Verlag, Tokyo, Japan, pp. 179 194. Giorgi, M. S., R. Arlettaz, P. Christe and P. Vogel. 2001. The energetic grooming costs imposed by a parasitic mite ( Spinturnix myoti ) upon its bat host ( Myotis myotis ). Proceedings of the Royal Society 268: 2071 2075. Jones Jr., J. K., and J. A. Homan. 1974. Hylonycteris underwoodi Mammalian Species 32: 1 2. Laval, R. and B. Rodriguez H. 2002. Bats of Costa Rica R. K. Laval ed. INBio, Costa Rica. Lucan, R. K. 2006. Relationships between the parasitic mite Spinturnix andegavinus (Acari: Spinturnicidae) and its bat host, Myotis daubentonii (Chiroptera: Verpertilionidae): seasonal, sex and age related variation in infestation and possible impact of the parasite on the host condition and roosting behavior. Folia Parasitology 53: 147 152. McLean, J. A., and J. R. Speakman. 1997 Non nutritional maternal support in the brown long eared bat. Animal Behavior 54: 1193 1204. Patterson, B. D., C. W. Dick, and K. Dittmar. 2007. Roosting habits of bats affect their parasitism by bat flies (Diptera: Streblidae). Journal of Tropical Ecology 23: 177 189. Patterson, B. D., C. W. Dick, and K. Dittmar. 2008. Sex biases in parasitism of neotropical bats by bat flies (Diptera: Streblidae). Journal of Tropical Ecology 24: 387 396. As citing: Zahn, A. and D. Rupp. 2004. Ectoparasite load in European verspertilionid bats. Journal of Zoology 262: 383 391. Presley, S. J., and M. R. Willig. 2008. Intraspecific patterns of ectoparasite abundances on Paraguayan bats: effects of host sex and body size. Journal of Tropical Ecology 24: 75 83. Stuckey, M. 2009. Ectoparasite presence, density and unit load in re lation to tent roosting behavior of Neotropical bats. Berkeley Scientific Journal 13: 62 72. Wenzel, R. L., V. J. Tipton, and A. Kiewlicz. 1966. The Streblid batflies of Panama (Diptera Calypterae: Streblidae). Ectoparasites of Panama: 405 675.

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Appendix A Bat ectoparasites and their host species Parasite Species Host Species Exastinion clovisi A. geoffroyi and H. underwoodi Strebla sp. A. geoffroyi C. perspicillata and H. underwoodi Anastrebla sp. H. underwoodi Trichobius sp. A. geoffroyi and C. perspicillata White mite 1 A. geoffroyi, C. perspicillata and H. underwoodi White mite 2 A. geoffroyi and H. underwoodi


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La riqueza y abundancia de ectoparsitos en tres especies de murcilagos neotropicales
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Ectoparasite richness and abundance on three species of Neotropical bats
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Ectoparasitic arthropods can decrease the fitness or survival of their hosts by increasing host energy expenditure. Bats harbor many species of ectoparasites; host biology, grooming, and roosting habits can affect intensity of parasite infestation. This study assessed ectoparasitism on three species of Neotropical bats by Streblid batflies (Streblidae) and bat mites (Order: Acari). Bats were netted and ectoparasites identified to the lowest taxonomic level possible. Host species had a significant impact on ectoparasite richness and abundance (Two Way ANOVA, F = 41.25, df = 2, p < 0.0001). Anoura geoffroyi suffered the most intense overall parasitism and parasitism by Streblids, but Hylonycteris underwoodi hosted more mites and had a greater richness of mites per bat (Tukeys HSD tests, p < 0.05). Carollia perspicillata suffered very low parasitism rates by all measures. Host sex did not appear to impact ectoparasitism across species or between males and females of the same species. Ectoparasitism is likely impacted by roosting dynamics, grooming habits, and density of individuals in the colony.
Los artrpodos ectoparsitos pueden disminuir el xito reproductivo o la sobrevivencia del hospedero aumentando el gasto energtico. Los murcilagos hospedan varias especies de parsitos, la biologa del hospedero, acicalamiento y hbitos de descanso pueden afectar la intensidad de infeccin por parsitos. Este estudio evala el ectoparasitismo en tres especies de murcilagos neotropicales por moscas de la familia Streblidae y caros. Los murcilagos fueron atrapados con redes y los ectoparsitos identificados al menor nivel taxonmico posible. La especie de hospedero tiene un impacto significativo en la riqueza y abundancia (Two Way ANOVA, F = 41.25, df = 2, p < 0.0001). Anoura geoffroyi sufre la mayor intensidad en general de parasitismo y tambin parasitismo por las moscas streblidas, pero Hyloniceteris underwoodi hospeda ms acaros y tiene una mayor riqueza de los mismos por el murcilago (Tukeys HSD tests, p < 0.05). Carollia perspicllata sufre una tasa muy baja de parasitismo en todas las medidas. El sexo del hospedero parece no tener impacto alguno en el parasitismo entre las especies o entre sexos de la misma especie. El ectoparasitismo est altamente influenciado por la dinmica de los sitios de descanso, los hbitos de acicalamiento y la densidad de individuos de la colonia.
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Text in English.
650
Bats
Ectoparasitic infestations
Species diversity
Costa Rica--Puntarenas--Monteverde Zone
4
Murcilagos
Infestaciones ectoparasitarias
Diversidad de especies
Costa Rica--Puntarenas--Zona de Monteverde
653
Tropical Ecology Spring 2011
Ectoparasitism on bats
Ecologa Tropical Primavera 2011
Ectoparasitismo en los murcilagos
655
Reports
720
CIEE
773
t Monteverde Institute : Tropical Ecology
856
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