ABSTRACT:

The aim of this study was to correlate Streblidae parasitism rates with temperature and humidity as well as sex, age and reproductive condition of Artibeus bats. Streblidae specimens were collected during two years in the Tinguá Biological Reserve and in two areas inside buffer zone, located in Nova Iguaçu, Rio de Janeiro State and preserved as wet specimens. The abundance of Streblidae species parasitizing Artibeus was analyzed, and no differences were found between them. However, the number of females parasitizing Artibeus fimbriatus was higher. Moreover, regarding sex, Artibeus females were more parasitized, particularly A. fimbriatus and A. lituratus. There was no correlation between mean intensity of infestation and body mass index of Artibeus species, even when correlated to abiotic data. This study contributes to better understand the parasitism on Artibeus by Streblidae, and based on results, it is clear that Streblidae show no preferences in terms of reproductive condition, body size, age, sex, temperature and humidity in parasitizing Artibeus species.

Key words:
parasitism; bat flies; Paratrichobius longicrus; bats

RESUMO:

O objetivo deste estudo foi de correlacionar as taxas de parasitismo de Streblidae com a temperatura e umidade, bem como sexo, idade e condução reprodutiva dos morcegos Artibeus. Os espécimes de Streblidae foram coletados durante dois anos na Reserva Biológica do Tinguá e em duas áreas dentro da zona de amortecimento, localizadas em Nova Iguaçu, estado do Rio de Janeiro, e preservados em coleção úmida. A abundância de espécies de Streblidae que parasitaram Artibeus foi analisada e não foram encontradas diferenças entre elas. No entanto, o número de fêmeas que parasitaram Artibeus fimbriatus foi maior. Além disso, em relação ao sexo, as fêmeas de Artibeus foram mais parasitadas, principalmente, A. fimbriatus e A. lituratus. Não houve correlação entre a intensidade média de infestação e o índice de corpóreo das espécies de Artibeus, mesmo quando correlacionados com dados abióticos. Este estudo contribui para uma melhor compreensão do parasitismo em Artibeus por Streblidae e, com base nos resultados, as moscas Streblidae não demostraram preferências em termos de condição reprodutiva, tamanho corporal, idade, sexo, temperatura e umidade ao parasitar as espécies de Artibeus.

Palavras-chave:
parasitismo; streblideos; Paratrichobius longicrus; morcegos

INTRODUCTION:

Among bat ectoparasites, Streblidae (Diptera) stand out. Exclusive to bats, these flies establish a relationship of dependency with their hosts considering their blood-sucking habit and the fact that a large part of their life cycle occurs on these bats (OVERAL, 1980OVERAL, W.L. Host-relations of the bat fly Megistopoda aranea (Diptera: Streblidae) in Panama. University of Kansas Science Bulletin, v.52, p.1-20, 1980.). Bats can harbor more than one Streblidae species, which generally are found on the body and/or wing membranes (LINHARES & KOMENO, 2000LINHARES, A; C. A. KOMENO. Trichobius joblingi, Aspidoptera falcata and Megistopoda proxima (Diptera: Streblidae) parasitic on Carollia perspicillata and Sturnira lilium (Chiroptera: Phyllostomidae) in Southestern Brazil: sex ratios, seasonality, host site preference, and effect of parasitism on the host. Journal of Parasitology, v.86, p.167-170, 2000.).

Many aspects can influence the abundance of Streblidae. Among the factors linked to the host are type of refuge, behavior, condition stage and body size (LINHARES & KOMENO, 2000LINHARES, A; C. A. KOMENO. Trichobius joblingi, Aspidoptera falcata and Megistopoda proxima (Diptera: Streblidae) parasitic on Carollia perspicillata and Sturnira lilium (Chiroptera: Phyllostomidae) in Southestern Brazil: sex ratios, seasonality, host site preference, and effect of parasitism on the host. Journal of Parasitology, v.86, p.167-170, 2000.), while temperature and humidity are abiotic attributes that can also affect the population of these parasites (RUI & GRACIOLLI, 2005RUI, A.M.; GRACIOLLI, G. Moscas ectoparasitas (Diptera, Streblidae) de morcegos (Chiroptera, Phyllostomidae) no sul do Brasil: associações hospedeiros-parasito e taxas de infestação. Revista Brasileira de Zoologia , v.22, n.2, p.438-445, 2005.; ESBERÁRD et al., 2012ESBERÁRD, C.E.L. et al. Do young Carollia perspicillata (Chiroptera: Phyllostomidae) present higher infestation rates of Streblidae (Diptera)?, Brazilian Journal Biology, v.72, n.3, p.617-621, 2012.). In the Neotropics, parasitism by Streblidae on Phyllostomidae bats is well known. Nevertheless, there are still few studies about the host-parasite relationship between Artibeus and Streblidae species (GRACIOLLI & DICK, 2004GRACIOLLI, G.; DICK, C.W. A new species of Metelasmus (Diptera: Streblidae: Streblinae) from southern South America. Zootaxa, v.509, p.1-8, 2004.).

In order to complement knowledge about how host or environmental factors can influence the relationship between Streblidae flies and Artibeus bats, it was analyzed data on sex, body size, reproductive condition and host age, as well as environmental temperature and humidity.

MATERIALS AND METHODS:

Streblidae flies came from a previous study about bat ectoparasites conducted in Tinguá Biological Reserve and two areas inside buffer zone, in Nova Iguaçu, state of Rio de Janeiro, Brazil. The database (Microsoft Excel) built and partly published by LOURENÇO et al. (2014LOURENÇO, E.C. et al. Streblidae (Diptera) on bats (Chiroptera) in an area of Atlantic Forest, state of Rio de Janeiro. Revista Brasileira de Parasitologia Veterinária, v.23, n.2, p.1-7, 2014. Available from: <Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1984-29612014000200164 >. Accessed: Nov. 25 2014. doi: 10.1590/S1984-29612014029.
http://www.scielo.br/scielo.php?script=s... ) was used to obtain data related to bat captures (number of bats and temperature).

Records on bat specimens included species name, capture location, morphometric data, reproductive condition and sex. Records also contained the host classification by age (infant, young or adult), and reproductive status (males with existing or abdominal scrotum; sexually inactive females, with palpable fetuses or secreting nipples) (COSTA et al., 2007COSTA, L.M.; ESBERAD, C.E.L. Datas of reproduction the Platyrrhinus lineatus in long-term study in the state of Rio de Janeiro (Mammalia, Chiroptera, Phyllostomidae). Iheringia, Série Zoologia, v.97, n.2, p.152-156, 2007.).

Streblidae flies collected were stored in a wet collection (70% ethanol), organized in jars containing identification of the host species and date of each capture. They were identified, counted and sexed with the aid of a stereoscopic microscope. The identification was made using a dichotomous key (GRACIOLLI & CARVALHO, 2001GRACIOLLI, G; CARVALHO, C.G.B. Flies ectoparasites (Diptera, Hippoboscoidea, Streblidae) of bats (Mammalia: Chiroptera) of Paraná, Brazil. II. Streblidae. Pictorial key to genera and species. Revista Brasileira de Zoologia, v.18, p.907-960, 2001.).

The abundance (number of specimens registered) of each sex of Streblidae on the host species and the abundance and prevalence (number of parasitized hosts divided by the total number of hosts) of the Streblidae species parasitizing males and females of different Artibeus species were compared using the Chi-square test with degree of freedom of one, with the R program (R DEVELOPMENT CORE TEAM, 2014TEAM. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing, 2014. ISBN 3-900051-07-0. Available from: <Available from: http://www.Rproject.org/ >. Accessed: Jan. 21, 2014.
http://www.Rproject.org/... ). The mean intensity of Streblidae (number of Streblidae specimens divided by the number of parasitized bats) was compared with sex of Artibeus using the Mann-Whitney test with the Past 3.0 program (HAMMER et al., 2006HAMMER, O. et al. Paleontological statistics - PAST ver. 1.92. 2006. Available from: <Available from: http://www.folk.uio.no/ohammer/past >. Accessed: Jun. 06, 2013.
http://www.folk.uio.no/ohammer/past... ).

The body mass index (BMI), resulting from the division of host weight by the length of forearm, was calculated to correlate parasite load of Streblidae with the host size.

The average minimum and maximum temperature and relative humidity were correlated with the mean intensity of Streblidae infestation found in different Artibeus species by Spearman's rs with the Past 3.0 program (HAMMER et al., 2006HAMMER, O. et al. Paleontological statistics - PAST ver. 1.92. 2006. Available from: <Available from: http://www.folk.uio.no/ohammer/past >. Accessed: Jun. 06, 2013.
http://www.folk.uio.no/ohammer/past... ).

RESULTS:

Five species of Streblidae - Megistopoda aranea (Coquillett, 1899), Paratrichobius longicrus (Miranda Ribeiro, 1907), Aspidoptera falcata Wenzel, 1976, Aspidoptera phyllostomatis (Perty, 1833) and Metelasmus pseudopterus Coquillet, 1907 - and four Artibeus, Leach, 1821 bat species - Artibeus fimbriatus Gray, 1838 Artibeus lituratus (Olfers, 1818), Artibeus obscurus (Schinz, 1821) and Artibeus planirostris (Spix, 1823) were correlated (Table 1).

Regarding the abundance of Streblidae males and females on host species, there was a higher number of female parasites (N=50) than males (N=27) only on A. fimbriatus (χ2= 6.87; P=0.008) (Table 1).

When considering hosts sex, the total number of females parasitized by flies (61.25%) (χ2= 11.25; P=0.0007) was higher than males, especially on A. fimbriatus (χ2= 8.24; P=0.003) and A. lituratus (χ2=36.5; P=0.000) (Table 2). The abundance of a few flies was too low to calculate or compare their prevalence and mean intensities. Megistopoda aranea and A. phyllostomatis were more prevalent on male A. fimbriatus specimens (♂P=30.00%; ♀P=20.75%; χ2= 41.20; P<0.005) and (♂P=30.00%; ♀P=26.42; χ2=19.6; P<0.005), respectively. In contrast, P. longicrus was more prevalent on females of A. lituratus (♂P=24.05%; ♀P=38.43; χ2=45.11; P<0.005).

The highest mean infestation intensities of A. phyllostomatis and P. longicrus were observed on female A. fimbriatus (♂MI=1.57; ♀MI=1.68; U=10; P=0.001) and A. lituratus (♂MI=1.71; ♀MI=2; U=416; P=0.005) respectively. There was no difference between A. fimbriatus sex and mean intensity of infestation by M. aranea (♂MI=1.12; ♀MI=1.83; U=30; P=0.15).

Average intensities of Streblidae were compared between the hosts considering their reproductive condition. The highest values were observed for M. aranea parasitizing A. lituratus inactive females (MI=4.0). The second highest values were noted for A. phyllostomatis parasitizing A. obscurus post-lactation females (MI=3.0), followed by P. longicrus parasitizing A. lituratus (MI=2.1)and A. planirostris (MI=2.0) males with existing scrotum (Table 3). Concerning flies' preference according to host age, the highest mean parasitism intensity was observed for P. longicrus (MI=2.7) on young individuals of A. lituratus (Table 3).

No relationship was found between the abundance of Streblidae and BMI when considering all individuals of Artibeus (N=188; R=-0.02; P=0.74), even when considering A. fimbriatus (N=36; R=0.16; P=0.33), A. lituratus (N=132; R=0.002; P=0.75), A. obscurus (N=5; R=0.78; P=0.2) and A. planirostris (N=15; R=0.4; P=0.2). Also, no correlation was found between the abundance of Streblidae and relative humidity (N=50; R=-0.16584; P=0.2487), minimum temperature (N=50; R=-0, 16584; P=0.2487), mean temperature (N=48; R=-0.2432; P=0.095) and maximum temperature (N=48; R=0.2485; P=0.093).

DISCUSSION:

Data about the sex of Streblidae species that parasitize Artibeus in Atlantic Forest fragments in Rio de Janeiro were added by this study. We did not expect a higher abundance of Streblidae females parasitizing A. fimbriatus since previous reports in the literature suggest a greater abundance of males (LINHARES & KOMENO, 2000LINHARES, A; C. A. KOMENO. Trichobius joblingi, Aspidoptera falcata and Megistopoda proxima (Diptera: Streblidae) parasitic on Carollia perspicillata and Sturnira lilium (Chiroptera: Phyllostomidae) in Southestern Brazil: sex ratios, seasonality, host site preference, and effect of parasitism on the host. Journal of Parasitology, v.86, p.167-170, 2000.; RUI & GRACIOLLI, 2005RUI, A.M.; GRACIOLLI, G. Moscas ectoparasitas (Diptera, Streblidae) de morcegos (Chiroptera, Phyllostomidae) no sul do Brasil: associações hospedeiros-parasito e taxas de infestação. Revista Brasileira de Zoologia , v.22, n.2, p.438-445, 2005.; BERTOLA et al., 2005BERTOLA, P.B. et al. Bat flies (Diptera: Streblidae, Nycteribiidae) parasitic on bats (Mammalia: Chiroptera) at Parque Estadual da Cantareira, São Paulo, Brazil: parasitism rates and host-parasite associations. Memórias Instituto Oswaldo Cruz, v.100, n.1, p.25-32, 2005.; DICK & PATERSON, 2008DICK, C.W.; PATTERSON, B.D. An excess of males: skewed sex ratios in bat flies (Diptera: Streblidae). Evolutionary Ecology, v.22, p.757-769, 2008.).

The predominance of Streblidae males is explained by the fact they remain on the host body throughout their life cycle, including during mating (OVERAL, 1980OVERAL, W.L. Host-relations of the bat fly Megistopoda aranea (Diptera: Streblidae) in Panama. University of Kansas Science Bulletin, v.52, p.1-20, 1980.), while females leave the host for larviposition. According to Fritz (1983FRITZ, G.N. Biology and ecology of bat flies (Diptera: Streblidae) on bats in the genus Carollia. Journal of Medical Entomology, v.20, n.1, p.1-10, 1983.), larviposition occurs mainly during foraging, when most capture method are applied, which explains the greater number of male parasites (DITTMAR et al., 2009DITTMAR, K. et al. Pupal deposition and ecology of Bat flies (Diptera: Streblidae): Trichobius sp. (Caecus Group) in a Mexican Cave Habitat. Journal of Parasitology, v.95, p.308-314, 2009. Available from: <Available from: http://www.journalofparasitology.org/doi/abs/10.1645/GE-1664.1 >. Accessed: Nov. 3, 2014. doi: 10.1645/GE-1664.
http://www.journalofparasitology.org/doi... ). When captures are directed to bat shelters, the probability of finding a greater number of Streblidae females on the host increases (DITTMAR et al., 2011DITTMAR, K. et al. E. Spatial and temporal complexities of reproductive behavior and sex ratios: a case from parasitic insects. PLoS ONE, v.6, n.5, e19438, 2011. Available from: <Available from: http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0019438 >. Accessed: Nov. 21, 2014. doi: 10.1371/journal.pone.0019438.
http://journals.plos.org/plosone/article... ), since males are more susceptible to predation by another host through grooming.

It is well known that in dioic animals the birth probability of males and females is equal. However, studies with some ectoparasites such as ticks, fleas, lice and flies have shown that females are more abundant than males (DICK & PETTERSON, 2008DICK, C.W.; PATTERSON, B.D. An excess of males: skewed sex ratios in bat flies (Diptera: Streblidae). Evolutionary Ecology, v.22, p.757-769, 2008.) For Streblidae in Brazil, there are few studies that report a greater abundance of females (RUI & GRACIOLLI, 2005RUI, A.M.; GRACIOLLI, G. Moscas ectoparasitas (Diptera, Streblidae) de morcegos (Chiroptera, Phyllostomidae) no sul do Brasil: associações hospedeiros-parasito e taxas de infestação. Revista Brasileira de Zoologia , v.22, n.2, p.438-445, 2005.).

Preference of hematophagous arthropods according to host sex sometimes follows a pattern. For example, fleas have preference for male rodents (KOWALSKI et al., 2014KOWALSKI, K. et al. Sex differences in flea infections among rodent hosts: is there a male bias? Parasitology Reserch, v.114, p.337-341 2014. Available from: <Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4281372/pdf/436_2014_Article_4231.pdf >. Accessed: Nov. 21, 2014. doi: 10.1007/s00436-014-4231-z.
http://www.ncbi.nlm.nih.gov/pmc/articles... ; KIFFNER et al., 2014KIFFNER, C. et al. Variable effects of host characteristics on species richness of flea infracommunities in rodents from three continents. Parasitology Research, v.113, p.2777-2788, 2014..). This is explained by the fact that high testosterone rates of males during the breeding season reduce their immune response, and they become more susceptible to parasitism when compared to healthy females (ZUK & MCKEAN, 1996ZUK, M.; McKEAN, K.A. Sex differences in parasite infections: patterns and processes. International, Journal of Parasitology v.26, n.10, p.1009-1024, 1996.).

The Streblidae preference for female hosts have a behavioral explanation, since females spend more time in refuges due to parental care (ESBERÁRD et al., 2012ESBERÁRD, C.E.L. et al. Do young Carollia perspicillata (Chiroptera: Phyllostomidae) present higher infestation rates of Streblidae (Diptera)?, Brazilian Journal Biology, v.72, n.3, p.617-621, 2012.). It should be recalled that larviposition, development of pupae and emergence of new Streblidae individuals occurs in the refuge.

Although young bats were only slightly parasitized by Streblidae (1.42% prevalence), it is known that young bats usually host a large number of parasites (RUI & GRACIOLLI, 2005RUI, A.M.; GRACIOLLI, G. Moscas ectoparasitas (Diptera, Streblidae) de morcegos (Chiroptera, Phyllostomidae) no sul do Brasil: associações hospedeiros-parasito e taxas de infestação. Revista Brasileira de Zoologia , v.22, n.2, p.438-445, 2005.). However, the mean intensity of P. longicrus parasitizing young specimens of A. lituratus was considered high. High parasite loads in young individuals may be an ectoparasite strategy for the dispersion of new colonies, as these individuals, especially males, will form new colonies (LINHARES & KOMENO, 2000LINHARES, A; C. A. KOMENO. Trichobius joblingi, Aspidoptera falcata and Megistopoda proxima (Diptera: Streblidae) parasitic on Carollia perspicillata and Sturnira lilium (Chiroptera: Phyllostomidae) in Southestern Brazil: sex ratios, seasonality, host site preference, and effect of parasitism on the host. Journal of Parasitology, v.86, p.167-170, 2000.; BERTOLA et al., 2005BERTOLA, P.B. et al. Bat flies (Diptera: Streblidae, Nycteribiidae) parasitic on bats (Mammalia: Chiroptera) at Parque Estadual da Cantareira, São Paulo, Brazil: parasitism rates and host-parasite associations. Memórias Instituto Oswaldo Cruz, v.100, n.1, p.25-32, 2005.).

About Streblidae preference regarding reproductive condition of the host, while the highest mean intensity was inactive on females parasitized by M. aranea on A. lituratus (MI=4.0), this result needs to be carefully analyzed due to the high worm burden of a single individual. Other studies report that inactive females are less parasitized, because they spend less time in refuges, and are more active than pregnant and lactating females, making them less attractive to ectoparasites (MUNOZ-ROMO, 2006MUÑOZ-ROMO, M. Ethogram and diurnal activities of a colony of Artibeus lituratus (Phyllostomidae: Stenodermatinae). Acta Chiropterologica, v.8, p.231-238, 2006.; ESBERÁRD et al., 2012ESBERÁRD, C.E.L. et al. Do young Carollia perspicillata (Chiroptera: Phyllostomidae) present higher infestation rates of Streblidae (Diptera)?, Brazilian Journal Biology, v.72, n.3, p.617-621, 2012.).

Lactating females have closer contact with their young, increasing the surface area for fly infestation, since both can share ectoparasites. Additionally, both spend more time in refuges (ESBERÁRD et al., 2012ESBERÁRD, C.E.L. et al. Do young Carollia perspicillata (Chiroptera: Phyllostomidae) present higher infestation rates of Streblidae (Diptera)?, Brazilian Journal Biology, v.72, n.3, p.617-621, 2012.). Although RUI & GRACIOLLI (2005RUI, A.M.; GRACIOLLI, G. Moscas ectoparasitas (Diptera, Streblidae) de morcegos (Chiroptera, Phyllostomidae) no sul do Brasil: associações hospedeiros-parasito e taxas de infestação. Revista Brasileira de Zoologia , v.22, n.2, p.438-445, 2005.) concluded that there are no behavioral differences related to sex and age of the host that favor or impair infestation by P. longicrus of A. lituratus. BERTOLA et al. (2005BERTOLA, P.B. et al. Bat flies (Diptera: Streblidae, Nycteribiidae) parasitic on bats (Mammalia: Chiroptera) at Parque Estadual da Cantareira, São Paulo, Brazil: parasitism rates and host-parasite associations. Memórias Instituto Oswaldo Cruz, v.100, n.1, p.25-32, 2005.) reported higher prevalence of P. longicrus on A. lituratus in adult females, especially post-lactating specimens, and the greatest abundance and mean intensity were on pregnant females, corroborating with data presented in this study.

Among reproductive condition of Artibeus species, males with existing scrotum had the highest parasite load. This result can be explained by the fact that these animals had contact with females at mating time. In addition, they spend less time grooming, which decreases ectoparasite load. Another factor that may contribute is the immunosuppressive effect exerted by high levels of testosterone, making them more susceptible to parasitism (KLEIN, 2004KLEIN, S.L. Hormonal and immunological mechanisms mediating sex diferences in parasite infection. Parasite Immunology, v.26, p.247-264, 2004.).

Although we did not observe any relationship between the Streblidae parasite load and Artibeus species' BMI, LINHARES & KOMENO (2000LINHARES, A; C. A. KOMENO. Trichobius joblingi, Aspidoptera falcata and Megistopoda proxima (Diptera: Streblidae) parasitic on Carollia perspicillata and Sturnira lilium (Chiroptera: Phyllostomidae) in Southestern Brazil: sex ratios, seasonality, host site preference, and effect of parasitism on the host. Journal of Parasitology, v.86, p.167-170, 2000.) reported smaller bats to be more parasitized. When analyzing the relationship between the Streblidae intensity and BMI of A. planirostris, the smallest species among the four analyzed, we noted a tendency for smaller animals to be more parasitized. Artibeus planirostris was parasitized preferably by M. aranea and A. phyllostomatis, which have specific feeding behaviors on different anatomical regions of the same host (LINHARES & KOMENO, 2000LINHARES, A; C. A. KOMENO. Trichobius joblingi, Aspidoptera falcata and Megistopoda proxima (Diptera: Streblidae) parasitic on Carollia perspicillata and Sturnira lilium (Chiroptera: Phyllostomidae) in Southestern Brazil: sex ratios, seasonality, host site preference, and effect of parasitism on the host. Journal of Parasitology, v.86, p.167-170, 2000.).

Although there was no correlation between Streblidae parasite load and abiotic factors (temperature and air humidity), on days with lower minimum and average temperatures and lower mean relative humidity, there was a trend of hosts being more parasitized. It is known that the temperature and relative humidity are important factors, since they directly affect the reproduction and mortality of ectoparasites (RUI & GRACIOLLI, 2005RUI, A.M.; GRACIOLLI, G. Moscas ectoparasitas (Diptera, Streblidae) de morcegos (Chiroptera, Phyllostomidae) no sul do Brasil: associações hospedeiros-parasito e taxas de infestação. Revista Brasileira de Zoologia , v.22, n.2, p.438-445, 2005.). These effects may occur because abiotic factors also directly influence the hosts' behavior, causing more active warmer weather, as reported by MORRISON & McNAB, (1967MORRISON, P.; MCNAB, B.K. Temperature regulation in some Brazilian phyllostomid bats. Comparative biochemistry and physiology, v.21, n.1, p.207-221, 1967.). Due to host activity increase, they perform more often (MUÑOZ-ROMO, 2006MUÑOZ-ROMO, M. Ethogram and diurnal activities of a colony of Artibeus lituratus (Phyllostomidae: Stenodermatinae). Acta Chiropterologica, v.8, p.231-238, 2006.) which reduce parasite load (GIORGI et al., 2001GIORGI, M.S. et al. The energetic grooming costs imposed by a parasitic mite (Spinturnix myoti) upon its bat host (Myotis myotis). Proceedings of the Royal Society of London, v.268, p.2071-2075, 2001.).

CONCLUSION:

The parasitism rates by Streblidae were not influenced by morphophysiological factors such as BMI and the reproductive age of the host, only influenced by host sex, mainly at A. fimbriatus and A. lituratus. The abiotic factors showed no association with Streblidae parasitism in different species of Artibeus.

ACKNOWLEDGEMENTS

To Tinguá Biological Reserve, Entidade Ambientalista Onda Verde, Sindipetro Caxias and Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) (E-26/111.364/2011), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

REFERENCES:

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