Mastozoología Neotropical ISSN: 0327-9383 ISSN: 1666-0536 [email protected] Sociedad Argentina para el Estudio de los Mamíferos Argentina
Ramalho, Daniel F.; Graciolli, Gustavo; Aguiar, Ludmilla M. S. BAT FLY (DIPTERA: STREBLIDAE) PARASITISM IN DEGRADED AND PRESERVED AREAS IN A NEOTROPICAL SAVANNA Mastozoología Neotropical, vol. 25, no. 1, 2018, January-June, pp. 245-250 Sociedad Argentina para el Estudio de los Mamíferos Argentina
Available in: https://www.redalyc.org/articulo.oa?id=45758865021
How to cite Complete issue Scientific Information System Redalyc More information about this article Network of Scientific Journals from Latin America and the Caribbean, Spain and Journal's webpage in redalyc.org Portugal Project academic non-profit, developed under the open access initiative Mastozoología Neotropical, 25(1):245-250, Mendoza, 2018 Copyright ©SAREM, 2018 http://www.sarem.org.ar Versión on-line ISSN 1666-0536 http://www.sbmz.com.br
Nota
BAT FLY (DIPTERA: STREBLIDAE) PARASITISM IN DEGRADED AND PRESERVED AREAS IN A NEOTROPICAL SAVANNA
Daniel F. Ramalho1, 2, Gustavo Graciolli3, and Ludmilla M. S. Aguiar1, 2, 4
1 Programa de Pós-Graduação em Ecologia (PGECL), Universidade de Brasília (UnB), Brasília, Brazil. [Correspondence:
ABSTRACT. We assessed the relationship between bat fly parasitism and habitat degradation. We used mist nets to capture 522 individuals of Carollia perspicillata and 429 individuals from eight fly species in the Brazil- ian Cerrado. Specimens were captured in degraded areas surrounding protected areas and within the protected areas. Trichobius joblingi was the most frequent parasite of Carollia perspicillata; consequently, it was analyzed in greater detail. Sex and age were not critical factors for parasitism. A robust anthropogenic influence was observed; unexpectedly, a higher prevalence and abundance of bat flies were observed in preserved areas.
RESUMO. Parasitismo por moscas ectoparasitas (Diptera: Streblidae) de morcegos em áreas degradadas e preservadas de uma savanna Neotropical. Avaliamos a relação entre parasitismo de moscas ectoparasitas de morcegos e degradação do habitat. Com redes de neblina instaladas no Cerrado, capturamos 522 indivíduos de C. perspicillata e 429 indivíduos de oito espécies de Streblidae. As capturas foram realizadas em áreas prote- gidas e em áreas degradadas nos seus arredores. Trichobius joblingi era altamente representativa em Carollia perspicillata; consequentemente, esta espécie foi analisada com mais detalhe. Apesar de sexo e idade não serem fatores críticos para prevalência e intensidade de infestação, há uma forte influência antropogênica; inespera- damente, a maior prevalência e abundância de moscas está nas áreas preservadas.
Key words: Carollia perspicillata. Cerrado. Ectoparasite. Hippoboscoidea. Trichobius joblingi.
Palavras-chave: Carollia perspicillata. Cerrado. Ectoparasita. Hippoboscoidea. Trichobius joblingi.
Urbanization and habitat degradation may is observed, whereas the abundance of more have detrimental effects and can alter species specialized species tends to decrease (Willig diversity and abundance patterns (Kurta & et al. 2007). Neotropical bat species, such Teramino 1992). In urban areas, an increased as Carollia perspicillata, Sturnira lilium and abundance of generalist bat species that are well Artibeus lituratus are abundant in urban areas adapted to anthropogenic habitat alterations because of the high resource availability pres-
Recibido: 13 septiembre 2017. Aceptado: 14 marzo 2018. Editor asociado: R Robles 246 Mastozoología Neotropical, 25(1):245-250, Mendoza, 2018 D. F. Ramalho et al. http://www.sarem.org.ar - http://www.sbmz.com.br ent in human-modified environments (Flem- variation in parasitism in relation to the sex ing 1988; Willig et al. 2007). Environmental and age of the bat. We focus on Seba’s short- characteristics may also influence parasitism tailed bat Carollia perspicillata in the city of (Krasnov et al. 2007; Pilosof et al. 2012) for Brasília, Federal District of Brazil. Brasília is in species that rely on roosts for pupae deposi- the central region of the country at an altitude tion, such as bat flies (Dick & Patterson 2007). of 1160 m, and it is located in the core area Bat flies belong to the families Streblidae and of the Cerrado biome (Fig. 1). The Cerrado Nycteribiidae and are exclusive ectoparasites of is considered one of the world’s hotspots of bats (Marshall 1981). Each of these species of biodiversity. Sixty percent of the original Cer- flies usually parasitizes a single bat species or rado area has been deforested at a rate that has genus (Wenzel et al. 1966; Dick 2007). reached 30 000 km² per year (Machado et al. Studies have suggested that habitat degra- 2004). The study area is in a tropical savanna dation increase rates of parasitism because (Aw) according to Köppen–Geiger classification. habitat loss promotes higher concentration of We collected bats and flies in a typical cerrado hosts, which can increase stress and facilitate sensu strictu phytophysiognomy within three parasite transmission (Mbora & McPeek 2009). protected areas (PAs) in the city of Brasília: Conversely, other studies have shown that rates the National Park of Brasília - PNB (42 389 ha, of parasitism are higher in preserved areas 15°41′42″ S/48°08′10″ W), the Environmental (Pilosof et al. 2012; Frank et al. 2016). To date, Protection Area Gama-Cabeça de Veado - APA few studies have assessed the influence of ur- GCV (25 000 ha, 15°52′29″ S/47°50′48″ W), and banization and environmental quality in bat fly the Ecological Station of Águas Emendadas - parasitism. Furthermore, these limited studies ESECAE (10,547 ha, 15°36′32″ S/47°33′03″ W) have presented contrasting results (Pilosof et (Fig. 1). Brasília is the fourth most populated al. 2012; Saldaña-Vázquez et al. 2012; Frank et city in Brazil and has approximately three al. 2016; Bolívar-Cimé et al. 2017). million inhabitants; thus, the three sampling Therefore, we aim to evaluate the relation- locations are within a highly urbanized land- ship between parasitism in degraded versus scape. Bats and bat flies were collected at 24 preserved habitats and explore intraspecific capture sites in continuous fragments of cerrado
Fig. 1. Study areas and sampling sites in Brasília, Federal District, Brazil. 1. PNB, National Park of Brasília; 2. APA GCV, Environmental Protection Area Gama-Cabeça-de-Veado; and 3. ESECAE, Ecological Station of Águas Emendadas. Closed squares represent preserved areas, and open squares represent degraded areas. BAT FLY PARASITISM IN A NEOTROPICAL SAVANNA BAT 247 located inside the protected areas (preserved age, habitat, as well as with the interactions habitats) and in small fragments surrounding between these variables, we used a Multi- the protected areas within the urban matrix variate Analysis of Variance (MANOVA). We (degraded habitats). conducted all tests on the R 3.2.2 platform (R From April 2012 to August 2013, we sampled Core Team 2015), and the significance level during 96 trap nights using ten mist nets (12 was set at p<0.05. × 2.5 m), which were opened from 18:00 to We examined 522 Carollia perspicillata indi- 24:00 h. The total sampling effort was 5760 viduals, of which 187 were parasitized with a net/hours, equally distributed among sampling total of 429 ectoparasites, resulting in a total sites (240 net/hours in each site). Captured bats prevalence of 35.82% and a mean intensity were identified following Diaz et al. (2016). of 2.29 (±1.7) flies/host. We identified eight We removed ectoparasites from each bat with species of ectoparasites: Aspidoptera falcata, tweezers and brushes and fixed them in 70% Megistopoda proxima, Paratrichobius longicrus, alcohol. Bat flies were identified to the spe- Speiseria ambigua, Stebla guajiro, Trichobius cies level following Guerrero (1993, 1994a; b, lonchophyllae, Trichobius tiptoni and Trichobius 1995a; b, 1996). We deposited two individuals joblingi. Because the latter species was present (one male and one female) of each bat species in 90.91% of host individuals, we analyzed the and all Diptera into the Collection of Chirop- relationship between parasitism rates and the tera at the University of Brasilia (CCUnB) as habitat type, sex, and age for this species. voucher material (Carollia perspicillata: CCUnB Carollia perspicillata was more abundant in 0722 ♂ and CCUnB 0629 ♀; Trichobius joblingi: degraded habitats (343 individuals) than in CCUnBd 0634 – CCUnBd 0821). We used two preserved habitats (179 specimens). Prevalence indicators of parasitism (Bush et al. 1997) to was only related to the habitat type, and it describe bat fly infestation: prevalence (number was higher in preserved areas (χ² = 14.174, of parasitized hosts/number of hosts examined p = 0.0002). Sex and age were not related to × 10) and mean intensity of infestation (number prevalence (χ² = 1.926, p = 0.1652 and χ² = 0.144, of ectoparasites/number of parasitized host ± p = 0.7048, respectively) (Table 1). The intensity standard deviation). Because data were not of infestation was also significantly higher in independent, we used Pearson’s Chi-squared preserved areas (p = 0.000526). Sex and age as tests with Yates’ continuity correction to evalu- well as all interactions among the three fac- ate possible differences in prevalence between tors were not related to the mean intensity of sexes, age classes, and habitat types. To describe infestation (Table 2). the relationship of the intensity of infestation Our results show that populations of (number of parasites per individual) with sex, C. perspicillata found in preserved areas are
Table 1 Prevalence and mean intensity of Trichobius joblingi on Carollia perspicillata in sampling points in the city of Brasília, Federal District, Brazil (p = Pearson’s Chi-squared and Multivariate Analysis of Variance [MANOVA]).
Mean intensity Prevalence (%) p p (Mean±SD) Sex Female 39.38 0.1652 2.33±1.60 0.639927 Male 30.20 2.23±1.93 Age Adult 36.67 0.7048 2.36±1.69 0.254658 Young 33.33 2.07±1.79 Habitat Protected 52.51 0.0002 2.77±2.06 0.000526 Degraded 27.11 1.82±1.08 248 Mastozoología Neotropical, 25(1):245-250, Mendoza, 2018 D. F. Ramalho et al. http://www.sarem.org.ar - http://www.sbmz.com.br
Table 2 Values derived from the Multivariate Analysis of Variance (MANOVA) between the mean intensity and predictable variables (sex, age, habitat type, and all interactions) of Trichobius joblingi isolated from Carollia perspicillata at sampling points in the city of Brasília, Federal District, Brazil. Mean square, Mean Sq.; F values, F; and significant values, p.
Variable Mean Sq. F p
Habitat 34.17 12.501 0.000526 Sex 0.60 0.220 0.639927 Age 3.57 1.307 0.254658 Habitat × Sex 1.57 0.574 0.449811 Habitat × Age 0.79 0.290 0.591147 Sex × Age 0.54 0.198 0.656976 Habitat × Sex × Age 1.18 0.433 0.511317
more frequently parasitized by Trichobius observed by Frank et al. (2016) for female joblingi than populations found in degraded bats in Costa Rica, where a higher number of areas. This result is similar to the one observed parasites was observed in poorer areas than in for Sturnira ludovici in Mexico, where popula- preserved areas. tions found in natural forest fragments had a In our study area, degraded sites had a higher higher prevalence than those found in coffee diversity and abundance of hosts, which sug- plantations (Saldaña-Vázquez et al. 2012). A gests that a dilution effect could be causing high incidence of parasitism has also been the observed difference in parasitism. Frank observed in Artibeus jamaicensis in preserved et al. (2016) observed that areas with higher areas in Mexico, where prevalence was posi- bat species richness had lower parasite loads, tively correlated with the percentage of forest indicating the presence of a dilution effect in cover and landscape connectivity (Bolívar-Cimé the bat-fly relationship. et al. 2017). Moreover, habitat quality can directly influ- Regarding the intensity of infestation, our ence the reproductive rates and survival of results corroborate previous studies in which ectoparasites (Marshall 1981; Patterson et al. higher parasite abundance was observed in 2007). Fragmented areas tend to present signifi- preserved areas. For example, in Costa Rica, cant changes in environmental characteristics, male bats in preserved areas hosted more para- such as temperature and humidity (Matlack sites than bats situated in species-poor areas 1993), which could be detrimental to parasites. (Frank et al. 2016). In a study in Venezuela, In the present study, sex and age were not Pilosof et al. (2012) found that the parasitism predictors of parasitism rates; however, previ- of Artibeus planirostris and Pteronotus parnellii ous studies have shown that females carried was inversely proportional to the human popu- more parasites than males (Fritz 1983; Pat- lation density. terson et al. 2008). These studies suggest that In contrast, the relationship between habitat the formation of nursing groups during the degradation and Carollia perspicillata parasit- reproductive period may facilitate horizon- ism found in this study was inconsistent with tal transmission, thereby increasing parasite findings of a study of the same species in prevalence. However, Carollia perspicillata is Venezuela where the mean abundance of bat not known to form nursing groups (Cloutier flies was positively related to human density & Thomas 1992), which may explain why we and increased in densely occupied areas (Pi- did not observe differences in parasite loads losof et al. 2012). The same relationship was related to sex or age. BAT FLY PARASITISM IN A NEOTROPICAL SAVANNA BAT 249
Variation among studies suggests that fu- Chiroptera) del Nuevo Mundo. II. Los grupos: pallidus, ture investigations should be performed to caecus, major, uniformis y longipes del género Trichobius Gervais, 1844. Acta Biologica Venezuelica 5:1-18. determine the factors that influence parasitism Guerrero, R. 1994b. Catalogo de los Streblidae (Diptera: across habitats and species. The effect of human Pupipara) parásitos de murciélagos (Mammalia: interference on patterns of bat-fly interactions Chiroptera) del Nuevo Mundo. IV. Trichobiinae con remains unclear. However, our results indicate alas desarrolladas. Boletín de Entomología Venezolana 9:161-192. that the anthropogenic influence is robust and Guerrero, R. 1995a. Catalogo de los Streblidae (Diptera: the prevalence and abundance of bat flies is Pupipara) parásitos de murciélagos (Mammalia: high in preserved areas. Chiroptera) del Nuevo Mundo. III. Los gupos: dugesii, dunni y phyllostomae del género Trichobius Gervais, 1844. Acta Biologica Venezuelica 5:1-27. Acknowledgments. We thank SISBIOTA/ICMBIO for Guerrero, R. 1995b. Catalogo de los Streblidae (Diptera: permission (27719-28) to study in the research area and Pupipara) parásitos de murciélagos (Mammalia: CNPq for providing funding to DFR (130876/2013-5) and Chiroptera) del Nuevo Mundo. V. Trichobiinae con a fellow research grant to LMSA (309299/2016-0) and GG alas reducidas o ausentes y misceláneos. Boletín de (304616/2015-0). We also thank the anonymous reviewers Entomología Venezolana 10:135-160. and the editors for their comments and suggestions that Guerrero, R. 1996. Catalogo de los Streblidae (Diptera: helped us improve our paper. Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) del Nuevo Mundo. VI. Streblinae. Acta LITERATURE CITED Biologica Venezuelica 16:1-25. Krasnov, B. R., M. Stanko, & S. Morand. 2007. Host Bolívar-Cimé, B., A. Cuxim-Koyoc, E. Reyes-Novelo, community structure and infestation by ixodid J. B. Morales-Malacara, J. Laborde, & R. Flores- ticks: repeatability, dilution effect and ecological Peredo. 2017. Habitat fragmentation and the specialization. Oecologia 154:185-194. prevalence of parasites (Diptera, Streblidae) on three Kurta, A., & J. A. Teramino. 1992. Bat community Phyllostomid bat species. Biotropica 50:90-97. structure in an urban park. Ecography 15:257-261. Bush, A. O., K. D. Lafferty, J. M. Lotz, & A. W. Shostak. Machado, R. B. et al. 2004. Estimativas de perda da área 1997. Parasitology meets ecology on its own terms: do Cerrado brasileiro. Relatório técnico não publicado. Margolis et al. revisited. Journal of Parasitology Conservação Internacional, Brasília. 83:575-583. Marshall, A. G. 1981. The ecology of ectoparasitic insects. Cloutier, D., & D. W. Thomas. 1992. Carollia perspicillata. Academic Press, London Mammalian species 417:1-9. Matlack, G. R. 1993. Microenvironment variation within Diaz, M. M., S. Solari, L. F. Aguirre, L. M. S. Aguiar, and among forest edge sites in the eastern United & R. M. Barquez. 2016. Clave de identificacion de los States. Biological Conservation 66:185-194. murciélagos de sudamérica. Publicacion Especial no 2, Mbora, D. N. M., & M. A. McPeek. 2009. Host density and PCMA (Programa de Conservacion de los Murciélagos human activities mediate increased parasite prevalence de Argentina), Tucumán, Argentina. and richness in primates threatened by habitat loss and Dick, C. W. 2007. High host specificity of obligate fragmentation. Journal of Animal Ecology 78:210-218. ectoparasites. Ecological Entomology 32:446-450. Patterson, B. D., C. W. Dick, & K. Dittmar. 2007. Dick, C. W., & B. D. Patterson. 2007. Against all odds: Roosting habits of bats affect their parasitism by bat explaining high host specificity in dispersal-prone flies (Diptera: Streblidae). Journal of Tropical Ecology parasites. International Journal of Parasitology 23:177-189. 37:871-876. Patterson, B. D., C. W. Dick, & K. Dittmar. 2008. Sex Fleming, T. H. 1988. The short-tailed fruit bat: A study biases in parasitism of neotropical bats by bat flies in plant-animal interactions. University of Chicago (Diptera: Streblidae). Journal of Tropical Ecology Press, Chicago, Illinois. 24:387-396. Frank, H. K., C. D. Mendenhall, S. D. Judson, G. C. Pilosof, S., C. W. Dick, C. Korine, B. D. Patterson, Daily, & E. A. Hadly. 2016. Anthropogenic impacts & B. R. Krasnov. 2012. Effects of anthropogenic on Costa Rican bat parasitism are sex specific. Ecology disturbance and climate on patterns of bat fly and Evolution 6:4898-4909. parasitism. PLoS ONE 7:e41487. Fritz, G. N. 1983. Biology and ecology of bat flies (Diptera: R Core Team. 2015. R: A language and environment Streblidae) on bats in the genus Carollia. Journal of for statistical computing. R Foundation for Statistical Medical Entomology 20:1-10. Computing, Vienna.
Wenzel, R. L., V. J. Tipton, & A. Kiewlicz. 1966. The Willig, M. R. et al. 2007. Phyllostomid bats of lowland streblid bat flies of Panama (Diptera: Calyptera: Amazonia: effects of habitat alteration on abundance. Streblidae). Ectoparasites of Panama (R. L. Wenzel & Biotropica 39:737-746. V. J. Tipton, eds.). Field Museum of Natural History, Chicago, Illinois.