Private forest reserves can aid in preserving
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Private forest reserves can aid in preserving the community of medium and large-sized vertebrates in the Amazon arc of deforestation Nuno Negro˜ es • Eloy Revilla • Carlos Fonseca • Amadeu M. V. M. Soares • Anah T. A. Ja´ como • Leandro Silveira Abstract Due to the advancing agricultural frontier in the Brazilian Amazon, the present rate of deforestation engenders a pessimistic scenario for vertebrate diversity in the area. Protected areas are an essential conservation tool to limit biodiversity loss, but their efficiency have yet to be proven. Here, we used camera-trap data on the presence of medium and large-size vertebrates in a protected area (Canta˜o State Park) and a neigh- bouring private forest reserve (Santa Fe´ Ranch) to evaluate their effectiveness in protecting biodiversity. We also gathered information on seasonality and activity patterns. A total sampling effort of 7929 trap-nights revealed a diverse vertebrate fauna in the region. A total of 34 mammal species, belonging to 8 different orders was detected in the study area, some of which have a high level of conservation interest and value. The photographic index showed that diversity was more abundant outside the protected area of Canta˜o State Park, where seasonality could play a major role in vertebrate occurrence. Overall, the influence of seasonality on distribution appears to be species-specific. During the wet season around 40% of the common species were not detected inside the park, whereas in Santa Fe´ Ranch most species (62.5%) suffered only a slight decrease in relative abundance probably due to changes in the availability of food resources. Our results highlight the importance of private land for vertebrate conservation in the Amazon and alert to the need for increased law enforcement in these areas to secure biodiversity preservation.
CESAM and Biology Departament, Aveiro University, Campus Universita´rio de Santiago, 3810-193 Aveiro, Portugal e-mail: nunonegroes@gmail.com N. Negro˜ es A. T. A. Ja´como L. Silveira Jaguar Conservation Fund, 193 GO-341 km 84, Zona Rural, Mineiros, GO 75.830-000, Brazil N. Negro˜ es E. Revilla Department of Conservation Biology, Estacio´ n Biolo´ gica de Don˜ ana CSIC, Calle Americo Vespucio s/n, 41092 Seville, Spain Introduction With a growing human population and a higher demand for natural resources, protected areas represent one of the main conservation measures used to avoid species extinction and habitat loss (Cardillo et al. 2004; Joppa et al. 2009). Despite covering over 12% of earth’s terrestrial surface, there are still some issues concerning the efficiency of protected areas in securing species richness preservation (Parrish et al. 2003). One of the questions that remain open is the usefulness of private reserves in preserving the extraordinary biodi- versity of tropical forests, such as in the Amazon. In Brazil, the agricultural frontier is quickly advancing, with a concomitant fragmentation of the Amazon forest. By law, new farms and ranches must establish a private forest reserve that covers 80% of the private land accessioned. In theory, this legal requirement preserves, by far, much more land than the more traditional public protected areas. However, it is not clear how useful they are in preserving biodiversity because most of our conservation and scientific efforts are focused towards public reserves. The Amazon basin represents one of the most important regions in the world in terms of biodiversity (Costa et al. 2005; Stone et al. 2009). This, the largest rainforest on the planet, harbours the greatest number of endemic species per unit area and one of the highest diversities of vertebrates (IUCN et al. 2008). Habitat loss is the most important threat to vertebrate species and, even if relatively well known, only a small number of studies provide information on their status in this tropical forest (Voss and Emmons 1996; Fonseca et al. 1999). The rate of deforestation of Brazilian Amazonia has reached considerably high rates in recent years and it is estimated that the advance of the agricultural frontier over the region could cause a reduction by 50% of its forest cover in a few decades and, with it, the majority of its vertebrate diversity (Laurence et al. 2001; Azevedo-Ramos et al. 2006). This scenario highlights the imperativeness of establishing an effective network of pro- tected areas (Schulman et al. 2007). In particular, within the ‘‘arc of deforestation’’ the eastern/south-eastern region of the Amazon, where increased human pressure results in a highly fragmented landscape of agricultural farms and forest patches, evaluation of the conservation value of the remaining forest fragments is needed (Lopes and Ferrari 2000; Morton et al. 2006). There has been an increase in research on the distribution and ecology of medium and large-sized mammals and birds in the tropics, but their biological characteristics (noctur- nal, low density and cryptic) make them difficult to census and study (Silveira et al. 2003; Lyra-Jorge et al. 2008). The use of camera trapping in surveys has been intensified recently due to the advantages of being cost-effective for detecting animals with inconspicuous habits and its reduced disturbance (Zielinski et al. 1995; Kelly 2008; Rowcliffe and Carbone 2008). It constitutes a non-invasive method that provides considerable informa- tion on occurrence, population density and other biological parameters (sociality, activity or reproduction) of target and non-target species (Silveira et al. 2003; Go´ mez et al. 2005; Stein et al. 2008). This research is part of a long-term monitoring programme for jaguar density. Our intensive sampling effort over several years has resulted in a considerable number of photos of medium to large-sized vertebrates (mostly mammals, and to a limited extend birds) within Canta˜o State Park (CS-Park) and the adjacent Santa Fe´ Ranch (SF-Ranch). We use this information to report on vertebrate species richness, their activity patterns and the influence of seasonality and flooding both in a public reserve (CS-Park) and in a private forest fragment within a cattle ranch (SF-Ranch) in the Amazon arc of deforestation.  Materials and methods
Study area The study was carried out in the middle Araguaia river basin in two areas on opposite sides of the river: the Canta˜o State Park (CS-Park) on the right river bank and the Santa Fe´ Ranch (SF-Ranch) on the left river bank (Fig. 1). Canta˜o State Park (09°360 S, 50°030 W) is an 89,000 ha conservation unit situated in the transitional area between the Amazon and Cerrado biomes. Water abundance undergoes dramatic cyclical changes due to an extended network of rivers, canals and lakes. The dynamics created by the wet season (November–March) and the prolonged dry season (April–October) influences vegetation structure (SPMA 2000; Vitt et al. 2007). With an annual average precipitation of 1,710 mm/year and a difference of more than 4 m in river level between seasons (data from Santa Fe´ Ranch), flooding conditions influence available resources (food and shelter) for the fauna (Fig. 2). The vegetation, mainly represented by secondary growth tropical rainforest with some small grassland areas, suffers partial flooding during the wet season. 
Fig. 1 Study area showing the Santa Fe´ Ranch and Canta˜o State Park and their ecotonal location in the Brazilian biomes of the Amazon and Cerrado 
Fig. 2 Average precipitation and river level recorded for the Canta˜o State Park region, central Brazil (data from Santa Fe´ Ranch) Santa Fe´ Ranch (09°340 S, 50°210 W) is a 65,000 ha beef cattle ranch in southeast Para´ State, bordering the Araguaia River. Around 65% of the ranch represents a continuous, semi-deciduous seasonal tropical forest (similar as the CS-Park) patch that extrapolates the farm boundaries, while the other 35% is occupied almost entirely by pastures. Field methods We conducted five camera trap surveys between July 2005 and November 2007 during both the dry (three surveys) and wet (two surveys) seasons. A variable number of stations (from 10 to 22) were established throughout each study area, with a distance of 1–3 km between stations (Rabinowitz and Nottigham 1986; Karanth and Nicholds 2002; Silver et al. 2004). One passive infra-red camera was placed approximately 50–70 cm above ground on dirt roads or trails (animal or human made) at each station, except during the 2007 dry season survey at SF-Ranch when two cameras per station were used (Silver 2004). Two different camera types were used: Camtrakker® (Cam Trakker, Watkinsville, USA) and C1-BU® (Vibrashine Inc., Taylorsville, MS 3968, USA). Each camera was programmed to take photographs 24 h/day with a 5-min interval between photos. All stations were checked on a regular basis (5–20 days) throughout all surveys for mainte- nance. In addition to camera trapping, field observations contributed data on the occurrence of primates and aquatic mammals during the expeditions for camera installation and monitoring. Data analysis Species identification, number of individuals, sex, age, date and hour were determined, where possible, for each photograph. Following O’Brien et al. (2003), photos were con- sidered independent events only if they met at least one of three criteria: consecutive photographs of different individuals of the same or different species; consecutive photo- graphs of individuals of the same species taken more than 1 h apart; non-consecutive photos of individuals of the same species. The relative abundance index (RAI) was determined for all species by dividing the number of independent photo captures, by effort (trap-nights) times 100 (O’Brien et al. 2003; Kawanishi and Sunquist 2004). A photographic base index of abundance is con- sidered a consistent method to infer the relative abundance of cryptic mammals, assuming that the cameras did not affect the rates of movement of animals (Carbone et al. 2001; Goulart et al. 2009). The criteria used to set-up the cameras was always to maximise jaguar detection and, therefore, we assume that the same bias in species detection occurs across the entire study area, making the data comparable between sites and over time (Stein et al. 2008). We anticipated that populations would remain relatively stable during our short study period (3 years) and also within seasons in the absence of any catastrophic phenomenon (Krebs 1994; Harmsen 2006). Taking this into account, results from different surveys were pooled and we compared RAI for the most frequent species between seasons (dry and wet) for both areas (SF-Ranch and CS-Park) using Mann–Whitney tests. Factors affecting diversity and species detection Using generalised linear mixed models (GLMM), we evaluated the factors that could affect species richness according to sampling features (year, season, area: CS-Park vs. SF-Ranch) and environmental predictors (distance to water, distance to pasture, camera location i.e. road vs. trail), considering the number of different species as the dependent variable and trap station included as a random variable. We also analysed the factors affecting RAI according to some species characteristics: weight, conservation status, trophic niche (predator vs. prey) and social behaviour (solitary vs. group-living), using RAI as the dependent variable. We used R v.8.2 free statistical software and the Lme4 package for mixed models (Bates and Sarkar 2006) to fit the statistical models. Activity patterns We generated the activity pattern in 1-h intervals for those species with more than 10 inde- pendent photographic events. We used Chi-square tests to compare data from CS-Park and SF- Ranch, pooling them for further analysis if they were not significantly different (P [ 0.05). Then, each capture was classified into three categories: nocturnal (18:31–05:00 h), diurnal (06:31–17:00 h), and crepuscular (17:01–18.30 and 05:01–06:30 h) (Schaik and Griffiths 1996).
Results Species richness A total sampling effort of 7929 trap-nights were conducted over several, continuous, two- month periods (average 61 days), with a variable number of camera stations (average 15; range 10–22) and trap nights (965 trap-nights; 525–1681) at each site (Table 1). Camera trap effort on CS-Park was lower (3183 trap nights) than in SF-Ranch (4746 trap nights), but sampling season lasted on average 61 days in both areas, and the average number of camera stations established on each site was slightly higher in CS-Park (18) than in SF- Ranch (15). In 2007 we only sampled SF-Ranch.   
 Table 1 Sampling effort (No. stations, No. trap-nights, average number of days of effective camera use), total number of photos and number of photos (and percentage) for main vertebrate Classes in Canta˜o State Park and Santa Fe´ Ranch in central Brazil, as determined from camera traps
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