Abstract

Ocelots play a key role in ecological communities as mesopredators affecting the lower trophic level and other mesopredators. They show great variability in ecological traits across their distribution, but knowledge of this species is missing in several regions where it occurs. Here, we present the first study of ocelot in the Brazilian semiarid of Caatinga. Arid habitats might keep carnivore population density low and therefore vulnerable to environmental shocks and to human-induced changes, at risk of local extinction. To assess their population status, we used camera traps between September 2009 and January 2010. We estimated the density of ocelots using a spatially explicit capture-recapture method (SECR) to be 3.16 ± 0.46 individuals per 100 km². This is a low-density estimate for ocelots, which might reflect the harsh conditions of the arid habitat. A longer population study of the ocelot can answer if this low population density is enough for a long-term persistence of this species in this and other arid environments.

Keywords
Arid environments; Brazil; Density; Ocelot; SECR

Resumo

Jaguatiricas possuem um papel fundamental em comunidades ecológicas como mesopredadores, afetando níveis tróficos inferiores e também outros mesopredadores. Esta espécie possui uma grande variabilidade em suas características ecológicas em toda a sua distribuição, no entanto, o conhecimento desta espécie possui lacunas em vários locais onde ela ocorre. Neste trabalho, nós apresentamos o primeiro estudo desta espécie no semiárido brasileiro da Caatinga. Ambientes áridos podem afetar negativamente as espécies carnívoras e, aliado a alterações antrópicas, esta espécie pode ser levada a extinção local se sua densidade populacional é baixa. Portanto, para verificar o nível populacional da jaguatirica em uma região protegida da Caatinga, instalamos armadilhas fotográficas, entre setembro de 2009 e janeiro de 2010. Com os dados obtidos, calculamos a densidade desta espécie através de métodos espacialmente explícitos (SECR). A densidade estimada da jaguatirica foi de 3.16 ± 0.46 indivíduos por 100 km². Esta estimativa é muito baixa para esta espécie, o que pode ser um reflexo das condições áridas deste ambiente. Um estudo populacional de maior duração pode ajudar a responder se esta baixa densidade é o suficiente para a persistência desta espécie a longo prazo tanto neste, quanto em outros ambientes áridos onde ela ocorre.

Palavras-chave
Ambientes áridos; Brasil; Densidade; Jaguatirica; SECR

Introduction

The ocelot (Leopardus pardalis) occurs from southern Texas to north Argentina (Murray & Gardner 1997MURRAY, J.L. & GARDNER, G.L. 1997. Leopardus pardalis. Mamm. Species 1–10.) in open environments, flood plains, dry coniferous forests, and rainforests (Emmons & Feer 1997EMMONS, L.H. & FEER, F. 1997. Neotropical Rainforest Mammals: A Field Guide, 2nd ed. University of Chicago Press, Chicago.). Besides the existence of many studies focused on this species through its distribution (de Villa Meza et al. 2002DE VILLA MEZA, A., MEYER, E.M. & GONZÁLEZ, C.L. 2002. Ocelot (Leopardus pardalis) food habits in a tropical deciduous forest of Jalisco, Mexico. Am. Midl. Nat. 148:146–154., Haines et al. 2005HAINES, A.M., TEWES, M.E. & LAACK, L.L. 2005. Survival and sources of mortality in ocelots. J. Wildl. Manage. 69:255–263., Maffei & Noss 2008MAFFEI, L. & NOSS, A.J. 2008. How Small is too Small? Camera Trap Survey Areas and Density Estimates for Ocelots in the Bolivian Chaco. Biotropica 40: 71-75., Kolowski & Alonso 2010KOLOWSKI, J. & ALONSO, A. 2010. Density and activity patterns of ocelots (Leopardus pardalis) in northern Peru and the impact of oil exploration activities. Biol. Conserv. 143:917–925.), very few have addressed this species in arid habitats (Laack 1991, González et al. 2003, Harveson et al. 2004, Maffei et al. 2005MAFFEI, L., NOSS, A.J., CUÉLLAR, E. & RUMIZ, D.I. 2005. Ocelot (Felis pardalis) population densities, activity, and ranging behaviour in the dry forests of eastern Bolivia: data from camera trapping. J. Trop. Ecol. 21:349–353.).

Ocelot densities vary across its distribution, ranging from 2.3 to 75.2 individuals per 100 km² (Table 1) and are thought to decrease with lower precipitation and increasing distance from the equator (Di Bitetti et al. 2008DI BITETTI, M.S., PAVIOLO, A., DE ANGELO, C.D. & DI BLANCO, Y.E. 2008. Local and continental correlates of the abundance of a neotropical cat, the ocelot (Leopardus pardalis). J. Trop. Ecol. 24:189–200.). This is because a lower precipitation may decrease productivity (Chesson et al. 2004CHESSON, P., GEBAUER, R.L.E., SCHWINNING, S., HUNTLY, N., WIEGAND, K., ERNEST, M.S.K., SHER, A., NOVOPLANSKY, A. & WELTZIN, J.F. 2004. Resource pulses, species interactions, and diversity maintenance in arid and semi-arid environments. Oecologia 141:236–53.) which in turn, might decrease carnivore prey densities (Herfindal et al. 2005HERFINDAL, I., LINNELL, J.D.C., ODDEN, J., NILSEN, E.B. & ANDERSEN, R. 2005. Prey density, environmental productivity and home-range size in the Eurasian lynx (Lynx lynx). J. Zool. 265:63–71., Pettorelli et al. 2009, Sandom et al. 2013), and higher latitudes often correlates with a lower precipitation (Prince & Goward 1995, Di Bitetti et al. 2008DI BITETTI, M.S., PAVIOLO, A., DE ANGELO, C.D. & DI BLANCO, Y.E. 2008. Local and continental correlates of the abundance of a neotropical cat, the ocelot (Leopardus pardalis). J. Trop. Ecol. 24:189–200.). However, arid environments might present different challenges to species in those regions.

The semiarid of the Caatinga, in northeastern Brazil (Figure 1), for instance, is a harsh environment where ocelots occurs (Oliveira & Cassaro 2005OLIVEIRA, T.G. & CASSARO, K. 2005. Guia de campo dos felinos do Brasil. Instituto Pró-Carnivoros, Brazil.). This region has a high annual mean temperature (26^o to 30^o) and the lowest precipitation (300-1,000 mm/year) of Brazil (Prado 2008PRADO, D.E. 2008 As caatingas da America do Sul. In: Ecologia e Conservação da caatinga (Leal, I.R., Tabarelli, M. & Silva, J.M.C., eds) 3rd ed. Editora Universitária da UFPE, Recife, p. 3–74.). Furthermore, this habitat is under heavily negative human induced changes like deforestation for ranches and plantations (Castelletti et al. 2004CASTELLETTI C, SILVA JMC, TABARELLI M, SANTOS AMM (2004) Quanto ainda resta da Caatinga? Uma estimativa preliminar. Biodiversidade da Caatinga áreas e ações prioritárias para a Conservação. UFPE, Petrolina, Brazil.). However, there is almost no knowledge of ocelots' population status in the Caatinga.

Figure 01
Map of Serra da Capivara National Park with camera locations.

Ocelots are ecologically important as mesopredators, not only affecting prey species, but potentially other carnivore species as well (de Oliveira & Pereira 2013), it is essential to conduct studies in this region where not only the ocelot, but also others species, faces a harsh environment that is being severely modified by human activities (Leal et al. 2008LEAL, I.R., TABARELLI, M. & DA SILVA, J.M.C. (2008) Ecologia e conservação da caatinga. 3rd ed. Editora Universitária da UFPE, Recife.). Therefore, this study aims to contribute to the knowledge of ocelot populations in arid habitats by estimating its abundance and density in one of the few conservation units in the Caatinga (Leal et al. 2008LEAL, I.R., TABARELLI, M. & DA SILVA, J.M.C. (2008) Ecologia e conservação da caatinga. 3rd ed. Editora Universitária da UFPE, Recife.).

Material and Methods

The study was conducted at the Serra da Capivara National Park (SCNP), in southern Piauí state (Figure 1), covering an area of 1,291 km² (FUMDHAM 1994FUMDHAM (Fundação Museu do Homem Americano).1994. Parque Nacional da Serra da Capivara. Alinea Publicações Editora, Teresina.). Local mean annual rainfall is approximately 644 mm with temperatures ranging from 12-45^oC and annual mean of 26^oC (Pellerin 1991PELLERIN, J. 1991. Aspectos Físicos. Plano Manejo Parque Nacional da Serra da Capivara. IBAMA, Brasília.). To make up for the lack of permanent natural water sources, the park's administration conducts artificial water hole management in which a water truck fills, periodically, artificial ponds distributed in the park.

We deployed 70 camera trap stations between September 1^st 2009 and January 19^th 2010 in roads and trails inside the park (Figure 1). We chose to install the stations in this way because several studies have demonstrated that big cats (Emmons 1988EMMONS, L. 1988. A field study of ocelots (Felis pardalis) in Peru. Rev. Ecol. (Terre Vie) 43:133–158., Carbone & Christie 2001CARBONE, C. & CHRISTIE, S. 2001. The use of photographic rates to estimate densities of tigers and other cryptic mammals. Anim. Conserv. 4:75–79., Maffei et al. 2005MAFFEI, L., NOSS, A.J., CUÉLLAR, E. & RUMIZ, D.I. 2005. Ocelot (Felis pardalis) population densities, activity, and ranging behaviour in the dry forests of eastern Bolivia: data from camera trapping. J. Trop. Ecol. 21:349–353.) and ocelots (Trolle & Kéry 2005TROLLE, M. & KÉRY, M. 2005. Camera-trap study of ocelot and other secretive mammals in the northern Pantanal. Mammalia 69:409–416.) have higher capture rates on roads and trails than on forested habitats. Additionally, the dense thorny vegetation and dramatic relief present in the park made it very difficult to install trap stations in other areas. Each station had two cameras (LeafRiver – Leaf River Outdoor Products, Taylorville, MS, US) facing each other in order to photograph both sides of the animal, which facilitates posterior individual identification. Cameras were set to operate continuously, with a 5-minute delay between consecutive photos. Each trap was spaced from the others by a mean distance of 2.9 ± 0.4 km (SD). Like other ocelot studies (Maffei et al. 2005MAFFEI, L., NOSS, A.J., CUÉLLAR, E. & RUMIZ, D.I. 2005. Ocelot (Felis pardalis) population densities, activity, and ranging behaviour in the dry forests of eastern Bolivia: data from camera trapping. J. Trop. Ecol. 21:349–353., Di Bitetti et al. 2006DI BITETTI, M.S., PAVIOLO, A. & DE ANGELO, C. 2006. Density, habitat use and activity patterns of ocelots (Leopardus pardalis) in the Atlantic Forest of Misiones, Argentina. J. Zool. 270:153–163., Maffei & Noss 2008MAFFEI, L. & NOSS, A.J. 2008. How Small is too Small? Camera Trap Survey Areas and Density Estimates for Ocelots in the Bolivian Chaco. Biotropica 40: 71-75.), the present study was originally designed for jaguars (Silveira et al. 2009SILVEIRA, L., JÁCOMO, A.T.A., ASTETE, S., SOLLMANN, R., TORRES, N.M., FURTADO, M.M. & MARINHO-FILHO, J. 2009. Density of the Near Threatened jaguar Panthera onca in the caatinga of north-eastern Brazil. Oryx 44:104.) and we opportunistically gathered important data on ocelots.

To estimate density we applied spatially explicit capture-recapture (SECR) Maximum-likelihood methods (Borchers & Efford 2008) implemented in software R 3.0.1 through the package "secr" (Efford 2011). These models estimates the density ($\widehat{D}$), assuming the existence of a relation of the animal detection probability to the distance (d) from each animal home range center. This follows a two-parameters function, g(d), with g₀ being the detection probability when d = 0, and a spatial scale σ, related to home range diameter (O'Brien & Kinnaird 2011). We considered six models with different effects on detection: (1) No variation in detection [g₀ (.)σ(.)], (2) variation after the first capture [g₀ (b)σ(.)], (3) variation with time [g₀ (T)σ(.)], (4) differences between sexes [g₀ (sex)σ(.)] (5) The conjoint effect of sex and time [g₀ (sex+T)σ(.)] and (6) behavior and time [g₀ (b+T)σ(.)]. We selected between models by using the Akaike Information Criterion adjusted for small samples (AICc).

Results

We registered 316 pictures of ocelots comprising 51 individuals. (Two researchers identified each picture independently). It is possible to identify sex easily in ocelot's pictures due the conspicuousness of the male's scrotum, and we found a sex ratio of 1.5:1 males to females (31 males and 20 females). We found 38 individuals (74.5%) at more than one station, 27 at more than two (52.9%) and 11 individuals (21.5%) had no recaptures (i.e. registered at only one photograph). There were also several pictures of juveniles and cubs; however, we did not include them in the analysis because we could not identify them individually. Model selection highlighted the difference between sexes on detection probability (Table 2), consistent with other studies that find ocelots are a territorial species with variation in home range and activity between sexes (Dillon & Kelly 2008DILLON, A. & KELLY, M.J. 2008. Ocelot home range, overlap and density: comparing radio telemetry with camera trapping. J. Zool. 275:391–398.). The highest-ranked model estimated 3.16 ± 0.46 ocelots/100 km².

Discussion

Ocelot density in our study area was at the lower end for this species in relation to other regions (Table 1), which could make this population especially prone to environmental changes – man made or not – and local extinction (Purvis et al. 2000PURVIS, A., GITTLEMAN, J.L., COWLISHAW, G. & MACE, G.M. 2000. Predicting extinction risk in declining species. Proc. Biol. Sci. 267:1947–52.). Several characteristics of this arid region could be affecting ocelot populations. The first environmental factor that might play a role keeping this ocelot population at lower levels is the low productivity. In some regions, low productivity can limit prey species (East 1984EAST, R. 1984. Rainfall, soil nutrient status and biomass of large African savanna mammals. Afr. J. Ecol. 22:245–270., McNaughton et al. 1989MCNAUGHTON, S., OESTERHELD, M., FRANK, D. & WILLIAMS, K. 1989. Ecosystem-level patterns of primary productivity and herbivory in terrestrial habitats. Nature 341:142-144.), which in turn may suppresses carnivore populations, because of the lower density of prey (Carbone & Gittleman 2002CARBONE, C. & GITTLEMAN, J.L. 2002. A common rule for the scaling of carnivore density. Science 295:2273–6.). This bottom-up effect, was hypothesized to be a main driver of ocelot density throughout its distribution (Di Bitetti et al. 2008DI BITETTI, M.S., PAVIOLO, A., DE ANGELO, C.D. & DI BLANCO, Y.E. 2008. Local and continental correlates of the abundance of a neotropical cat, the ocelot (Leopardus pardalis). J. Trop. Ecol. 24:189–200.). However, dry environments may affect ocelots adversely. Other studies on ocelots densities in arid regions estimated highly varying densities: 1.6 to 51.7 ocelots/100 km² in the Bolivian dry forests (Noss et al. 2012), 30 ocelots/100 km² in Texas (Haines et al. 2006HAINES, A.M., TEWES, M.E., LAACK, L.L., HORNE, J.S. & YOUNG, J.H. 2006. A habitat-based population viability analysis for ocelots (Leopardus pardalis) in the United States. Biol. Conserv. 132:424–436.) and 5.7 ocelots/100 km² .In Sonora, Mexico (González et al. 2003).

It is also interesting to note that the lowest density estimated for ocelots (2.3 individuals per 100 km²) comes from a tropical pine forest in Belize (Dillon & Kelly 2007DILLON, A. & KELLY, M.J. 2007 Ocelot Leopardus pardalis in Belize: the impact of trap spacing and distance moved on density estimates. Oryx 41:469–477.). These same authors, however, found a higher ocelot density in forests that were not pine-dominated (25 individuals per 100 km²). Hence, vegetation structure may play an important role of this carnivore density across different regions. In our study, we estimated a low density in a region with a low productivity in an area with a dense vegetation structure, suggesting that in arid environments the productivity is a strong factor for ocelot density. However, we observed a high presence of rock cavies (Kerodon rupestris) during our survey. If this small rodent is an important part of ocelot's diet in this site, we do not believe low productivity is a main factor affecting ocelot density here. Unfortunately, the number of ocelot studies in arid regions are insufficient to verify a connection between productivity and density, as suggested by previously (Di Bitetti et al. 2008DI BITETTI, M.S., PAVIOLO, A., DE ANGELO, C.D. & DI BLANCO, Y.E. 2008. Local and continental correlates of the abundance of a neotropical cat, the ocelot (Leopardus pardalis). J. Trop. Ecol. 24:189–200.).

Several other factors may be relevant in arid landscapes. The interaction with other carnivore species can affect a species population (Palomares & Caro 1999, Caro & Stoner 2003, Dayan & Simberloff 2005, Donadio & Buskirk 2006). Ocelots co-occur with Jaguars and Pumas in the SCNP. These apex carnivores have a relatively high density in this park (Silveira et al. 2009SILVEIRA, L., JÁCOMO, A.T.A., ASTETE, S., SOLLMANN, R., TORRES, N.M., FURTADO, M.M. & MARINHO-FILHO, J. 2009. Density of the Near Threatened jaguar Panthera onca in the caatinga of north-eastern Brazil. Oryx 44:104.) and they might negatively affect ocelot densities through intraguild killing (Ritchie & Johnson 2009RITCHIE, E.G. & JOHNSON, C.N. 2009. Predator interactions, mesopredator release and biodiversity conservation. Ecol. Lett. 12:982–98.).

Continuous monitoring of this species would help elucidate whether this low density is the natural state of ocelots in the Caatinga or whether the population is declining. Even if the density remains constant during different years, it is still a very low estimative and likely to be subject to local extinction with environmental changes or increase in human activities in the region. This study provides background for future research concerning ocelots in these and other arid habitats.

Acknowledgments

This study was funded by the Jaguar Conservation Fund (JCF), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Fundação de Apoio à Pesquisa do Distrito Federal (FAPDF – Pronex 193000563-2009). We also would like to thank the reviewers that offered invaluable suggestions to improve this paper. We appreciate the support provided by the Fundação do Homem Americano and Park administration of Instituto Brasileiro de Meio Ambiente e Recursos Naturais Renováveis. A Scholarship grant to G.P. was provided by Coordenação de Aperfeiçoamento de Pesssoal de Nível Superior (CAPES) and to S.A. by CAPES and CNPQ.

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