1 | P a g e

A holistic inventory of mammalian species at Reserva Natural Laguna Blanca, Paraguay.

By

Simon Lowen BSc

(Internship period: 06.02.15 - 06.05.15)

2 | P a g e

Section 1: Introduction

The surge in camera trap use as a survey method for conservation and ecology is highlighted by a 50% annual increase in the number of scientific publications that have adopted them as research tools between 1998 and 2008 (Rowcliffe & Carbone, 2008). Ironically, camera trap applications for analysing species abundance originated from sport hunting devices (Rovero et al., 2013). Such demand for passive animal observation has increased the commercial availability of camera technologies to the extent that reliable, digital camera traps are now generally available for both scientific and non-scientific purposes.

Camera trap applications range throughout field research including collecting species inventories including the detection of elusive species (Sanderson & Trolle, 2005; Tobler et al., 2008); investigating activity patterns (Jacomo et al., 2003); and estimating animal density/relative abundance predominantly through photographic rate calculations (Carbone et al., 2001). For example, Jacomo et al (2003) successfully combined camera traps with canid scat analysis to better define the niche breadths and resultant ecological overlaps of the Maned Wolf, Crab-eating Fox and Hoary Fox in Emas National Park, Brazil.

The rise of this technology has opened avenues in ecology, especially in the detection of elusive species (Kelly, 2008). There are however a plethora of methodological issues, primarily regarding the manner in which the cameras are set in the field (Trolle & Kéry., 2003). The surrounding environment and the height & angle at which the cameras are set can both impact the observational efficiency of variously sized mammals. Likewise, changes in climate have been known to inadvertently trigger camera-traps (Acrenaz et al., 2012).

Conversely, camera traps do bring a number of benefits to field biology. They have been notably valuable as they provide a constant level of effort, loosely depend on the surveyor’s experience with animal observations and can be left in the field for long periods without requiring breaks between surveys (Silveira et al., 2003). Similarly, the passive nature of this method allows the surveyor to observe large areas over a relatively short period particularly in environments with problematic terrain where other field methods have commonly failed (O’Brien, Kinnaird & Wibisono., 2003).

As with many younger survey technologies, the manner in which camera traps can be adopted for species inventories is far from uniform. Some investigations suggest placing cameras in conjunction with scent lures as to enhance animal detection (Giman et al., 2007). Others question the validity of such methods and suggest the stringent use of an overlying grid system to establish camera locations for representative data (Séquin et al., 2003). The literature advises continued investigation into the use of camera traps for improved guidelines regardless of the target species’ or ecosystem (Hamel et al., 2013).

In this report, a continuation of the initial camera trap inventory at Reserva Natural Laguna Blanca (RNLB), Paraguay is evaluated focusing purely on the detection of medium to large mammals. Data was separately considered from subsidiary herpetology and primatology projects. Environmental and anthropogenic stressors that may have created any fluctuation in mammalian populations are considered in the analysis. The on-site environmental station, Para La Tierra (PLT), was established in 2010. Prior to this, there had been no scientific investigation into the ecology of the reserve leaving a great need to establish an on-going inventory of the environment. An underlying aim of this project is to consider previous complications with camera trapping surveys and to establish a set of standardised and reliable methods allowing for continued analysis.

3 | P a g e

Section 2: Sampling design

2a. Study areaThe study was implemented at Para La Tierra Ecological Station (PLT) located within Reserva Natural Laguna Blanca (RNLB) (S23°48’45.4”, W56°17’41.7”). The reserve is positioned roughly 25 km east of Santa Rosa Del Aguaray in San Pedro Department, Paraguay. There are three major habitats within the reserve: The Cerrado, the Atlantic Forest and an area of transitional forest located on their frontier. The majority of the northern section of the reserve is occupied by the southern extent of the Cerrado habitat which continues north into Brazil; this environment is characterised by scrub and grassland growing on dry, nutrient-deficient earth (Hebblethwaite, 2014). To the south of the reserve lies a patch of degraded but rehabilitating Atlantic Forest which has previously been encroached upon by soy field development on the east and western sides. A patch of semi-deciduous, semi-humid gallery ‘Transitional Forest’ (Smith et al., 2014) separates the Cerrado from Paraguay’s only spring-fed natural lake named Laguna Blanca.

4 | P a g e

The holistic approach adopted for this study allowed data to be gathered from a variety of flexible sampling designs as described below. Each design is written as a standardised guideline due to the variable nature of camera trap surveying and the affects that many anthropogenic and natural confounding factors have on surveying efficiency. They are also written to allow for future continuations of the inventory. The study ran throughout the period of 07/02/15 to the 06/05/15.

2b. Primary designRepresentative sampling sites were developed by dividing the reserve into 33 0.5km2 grid-squares. The coordinates for the central point of each square were calculated and noted as the camera sites (figure i). This sampling design was inspired by the initial inventory as performed by Declan Crace during the period 05/04/12 to 14/06/12.A total of 6 ‘Bushnell Trophy Cam’ camera traps were available at the disposal of this project. The initial aim was to obtain 5 nights of data (camera nights) at each survey site. This was considered flexible due to the requirements of side projects and general maintenance issues with the cameras. The cameras were installed under the recommendations of Rovero & Marshall (2009) and Tobler et al (2008). The former suggested that camera placement should be opportunistic using wildlife trails and sleeping/eating sites as camera trap locations. The latter concluded that installing a dual camera set-up instead of a single camera will increase capture probability by less than 50%; efficiency is therefore enhanced when adopting a single camera method.

In light of the literature, single cameras were installed at ‘areas of interest’ located within 50m of the specific coordinates as to keep the data representative. Human manipulation such as baiting was avoided whilst establishing these ’areas of interest’ as to avoid issues with ecological validity. Once a position was located, the cameras were mainly secured to trees however other such reliable structures could be used depending on availability. The cameras were secured 20-30 cm off the ground as advised by Tobler et al (2008).

Figure i: Camera trap positioning as dictated by the 0.5km2 grid-square sampling design

5 | P a g e

2c. Secondary designBetween the dates 09/03/15 and 22/03/15, additional data was gathered from a separate camera trap study focusing on observations of lizards, frogs and other herpetofauna that populate a seasonal pond located near the lake’s edge (S23°49’30.6” W56°17’24.97”). The cameras were primarily set using bamboo structures (figure ii) along pathways or in open spaces. The ponds’ surrounding foliage e.g. trees, shrubs & reed beds were occasionally used as structures to bind the cameras to. The cameras were set at dusk and removed at dawn in harmony with animal behaviour and to avoid theft of equipment. The locations of the cameras around the pond were not pre-empted but placed in areas of interest where previous sightings had occurred as dictated by the herpetologist who managed the study.

2d. Tertiary designThe final portion of data was extracted from an ongoing primatology study based around man-made baiting platforms. The platforms stood approximately 2m off the ground and were capable of carrying the weight of several monkeys plus the desired bait (often corn or fruit.) Two baiting tables were located in the southern and northern sections of the Atlantic Forest respectively, in natural openings with enough canopy and reliable structures to suitably position the camera traps. The height and angle at which the traps were bound to the tree was assessed onsite depending on their orientation to the baiting tables as shown in figure iii.

Figure ii: An image showing a typical bamboo structure

Figure iii: An image showing a camera set-up at one of the baiting stations in the Atlantic Forest

Baiting station

Camera-trap positioning

6 | P a g e

Section 3: Results

3a. Primary resultsThis ‘secondary inventory’ (14.02.15 – 21.04.15) observed a total of 5 different medium to large mammalian species. This suggests a significant decrease in the number of species occupying the reserve compared to Declan’s previous survey (initial inventory) which observed 10 species during the period 04.04.12 to 20.06.12. Despite the lack of diversity, abundance levels were higher for some species in the second inventory as demonstrated in figure iv.

SpeciesInitial inventory

sightingsSecondary inventory

sightings

Crab-eating Fox 12 20

Red Brocket Deer 5 4

Brazilian Cotton Tail 4 1

Six-Banded Armadillo 3 n/a

Azara’s Agouti 2 4

Nine-banded Armadillo 2 6

Coati 2 n/a

Lesser Grison 1 n/a

Little Spotted Cat 1 n/a

Southern Tamandua 1 n/a

Both inventories suggest a high abundance of the Crab-eating Fox; this was more significant for the second inventory however compared to all other species throughout both inventories, this was definitely the most common.

Figure iv: A table listing the species sightings for each inventory

7 | P a g e

4 16 28 36 48 60 72 84 96108

120132

144156

168180

188200

212224

236248

260272

0

2

4

6

8

10

12

Initial inventorySecondary inventory

Survey effort (camera nights)

Num

ber o

f spe

cies

The initial inventory adopted twenty-seven camera trap locations, 6 of which were in the Transitional Forest, fourteen in the Cerrado and 7 in the Atlantic Forest. Similarly, the secondary inventory had a total of thirty-three trap locations with a spatial variation of 5 locations in the Transitional Forest, eighteen in the Cerrado and 10 in the Atlantic Forest. The mean time a camera was set at each location was 4.9 (2 s.f.) camera nights.

4 6 8 10 12 14 16 18 200

0.5

1

1.5

2

2.5

3

3.5

4

4.5Initial Cerrado inventory

Initial Atlantic Forest inven-tory

Initial Transitional Forest inventory

Secondary Transitional Forest inventory

Secondary Atlantic Forest inventory

Secondary Cerrado inven-tory

Number of camera trap locations

Num

ber o

f spe

cies

Fluctuations between the three distinct habitats are demonstrated in figure R3. The most significant variation is between the initial and secondary inventories of the Cerrado habitat. Despite the vastly greater survey effort, only 1 species (Crab-eating Fox) was observed in the secondary inventory compared to 8 species in the initial inventory; this constituted 80% of the total number of species sighted throughout that inventory. The trend shown in figure R3 would suggest a negative correlation between the number of camera trap locations and the number of species observed within that habitat.

Figure v: Comparative species abundance lines for two inventories at Reserva Natural Laguna Blanca, Paraguay.

Figure vi: A chart to show the number of camera trap locations for each habitat compared to the number of observed species

8 | P a g e

3b. Secondary resultsThere was only 1 recorded individual that fell under the category of ‘medium to large mammal’ throughout the duration of this subsidiary project. 2 birds-eye viewed images showed the back and front feet of a potential adult Southern Raccoon. This is possibly the first pictorial evidence of the species within the reserve; further scientific verification is ongoing to confirm the sighting.

3c. Tertiary resultsThe ongoing primatology project at Laguna Blanca has deduced the current Capuchin Monkey population within the reserve to be fifteen in ‘group O’ and 8 in ‘group F’. The survey period considered for this research ran from 07.02.15 to 06.05.15. During this time there were 3 recorded visits to the feeding tables. One by ‘F group’ at the tables in the northern section of the Atlantic Forest in which there were 4 sighted individuals. The other 2 recorded visits occurred at the feeding tables in the southern section of the Atlantic Forest; Across these 2 visits there were 9 sighted individuals all of which were members of ‘O group’. It should be noted that the camera traps were not active throughout the entire survey period; the data was extrapolated from a total of sixteen camera nights. We can deduce that 50% of ‘group O’ and 60% of ‘group F’ were observed during the period of this study.

9 | P a g e

Section 4: Discussion

4a. Variation as a result of changing habitatsReserva Natural Laguna Blanca boasts a variety of natural habitats and sub-habitats. Figure vi

suggest a significant variation in useable observations between the Cerrado, Atlantic Forest and Transitional Forest. This variation is likely the result of species niches and respective populations within the given habitat e.g. the Red Brocket Deer were only recorded in the degraded section of the Atlantic Forest where vegetation is sparse; this is possibly the result of response to high ground-water levels in the south of the Atlantic Forest however such ungulates are comfortable eating such a woody browse diet (Bodmer, 1990). Similarly, the Azara’s Agouti were only recorded in the Transitional Forest and the Atlantic Forest due to their frugivorous diet; evolutionary adaptations have given this species exceptionally sharp teeth allowing them to eat fallen nuts and seeds which are common in these dense environments (Ribeiro & Vieira, 2014).

As the results suggest from figure vi, a negative correlation was found between the number of camera trap locations and the number of recorded species for each given habitat. Perhaps a lack of data from many of the locations could be avoided by following a ‘clustered’ design where there are high concentrations of camera trap locations as opposed to the representative design adhered to in this inventory. These ‘clustered’ designs should be positioned in each of the sub-habitats as to increase the recording efficiency of species with varied ecological characteristics (Kelly & Holub, 2008) e.g. the Atlantic Forest should be divided into the Flooded Forest, North Atlantic, South Atlantic and degraded territories.

As discussed in section 2b, ‘areas of interest’ were located onsite and in most cases were unnatural influencers such as roads or footpaths. It was pre-empted that these paths were active habitat corridors for mammals especially in dense floral environments (Bennett, 1990). It was conversely noted that the majority of recordings were limited to night time possibly the result of a learned response by mammalian species to recognise and avoid odours of sympatric predators (Swihart, 1991). In light of this, it is advised that ‘areas of interest’ are more carefully pre-empted and positioned in harmony with the respective natural attractors of each sub-habitat.

10 | P a g e

4b. Targeting specific speciesWhen comparing the primary and secondary results to the tertiary results it is clear that the

efficiency of lures when attracting mammals cannot be understated. This is demonstrated by high photographic detection success of the reserve’s Azara’s Capuchin populations over a relatively short sampling period (16 camera nights). The corn used in this primatology project not only attracted the monkeys but during each visit, there were sightings of at least two Plush Crested Jays. Conversely, the results from the primary and secondary designs are comparatively random in detecting mammals e.g. the initial and secondary inventory from the primary design shared the same number of camera nights however the number of species recorded is significantly greater in the initial inventory (figure v). We can deduce that lures provide sufficient incentive in a natural environment to increase capture rate and improve survey reliability.

Rovero et al., (2010) used a variety of scented lures at an Acacia plantation in central Sarawak to monitor terrestrial mammal populations. Some lures failed due to heavy rainfall however oily lures such as Fish Oils e.g. Magna Gland produces a strong odour which remained pungent to the researcher for one month even during the rainy season. The benefits of natural lures such as Wheat, oats, millet, canary seed, and hemp are effective in increasing capture rates of elusive species (Blair, 1941) however introducing anthropogenic elements could create unrepresentative data when researching population dynamics as intelligent species may return to the point of attraction as some capture-recapture models would suggest (Karanth et al., 2004) . In this project, lures would have been beneficial as the aim was to further a basic inventory as opposed to understanding the complexities of various mammalian species.

From an ethical standpoint, the importance of choosing appropriate lures has been highlighted by Schlexer (2008). His research considers the serious health threats associated with raw fish bait, commonly used to survey carnivores. Salmon poisoning disease (SPD) and Elokomin fluke fever (EFF) were both shown to be acute infectious diseases transferred through the ingestion of salmon and other common fish, ‘SPD can kill up to 90% of infected animals, while EFF usually manifests in a milder form’ (Aiello, 1998). To avoid this ethical issue, researching the diet of each targeted mammal species could offer educated insight into safe and effective lures.

11 | P a g e

4c. Survey intensificationFigures v & vi would both suggest no positive relationship between increased survey effort and

mammal capture rate. The data from figure vi would actually suggest a significant negative correlation between the number of onsite camera locations and the number of species observed e.g. only 4 of the 18 camera sites in the secondary Cerrado inventory recorded collectable data. Considering each site was allocated ≥5 camera nights, the results would suggest an inefficiency of survey effort.

As a relatively modern ecological tool there are still questions regarding the ideal survey design to adopt for camera trap studies. Soria-Diaz et al., (2010) discussed the variation of abundance and density of Puma concolor in zones of high and low concentration of camera traps in Sierra Nanchititla Natural Reserve, Central Mexico i.e. a representative or intensive survey design. The representative design was more expansive (an average distance between cameras of 4.6 km with 56-618 trap days) compared to the intensive design (an average distance between cameras of1.6 km with 491-618 trap days). The representative design recorded an average of 1.21±0.41 (individuals/100 km²) whereas the representative design recorded an average of 5.49±0.54 (individuals/100 km²).

In the case of Soria-Diaz et al., (2010) we can deduce that a greater concentration of camera traps/unit area did increase the likelihood of registering the target species. It was noted however that consideration for the niche width and therefore recapture probability is essential to confirm improved survey design through intensification (Maffei et al., 2004). In this study, recapture rates are less of a concern as the aim was to establish a basic inventory whilst configuring the niche width of every possible mammalian species on the reserve would be ineffective. A more intensive design (as opposed to the 0.5km2 grid system) would therefore offer shorter distances between camera sites (allowing for simpler retrieval of devices & checking for technical issues) whilst possibly improving capture rates as previously discussed.

12 | P a g e

4d. Future researchAs previously discussed, a theme of this project was to find a set of standardised methods to allow for the continuous recording of mammalian species on the reserve. The core inventories of the ‘primary methodology’ were comparable due to their similar sampling designs. The results of the primary and secondary inventories suggest significant variation in species abundance when compared against survey effort and habitat (figures v & vi). The 0.5km2 grid-square sampling design is sound when assessing a general inventory of the reserve. Any future inventories using this style will only validate the previously discussed results. Standardising and carefully reciting this methodology will also create opportunities for volunteers who visit the reserve to contribute to an ongoing scientific project without necessarily possessing previous experience in Ecological principles.

A separate camera-trap project could be undertaken to improve the capture rate of mammals throughout the various habitats as depicted in figure vii. The ‘location indicators’ suggest sites for camera traps that are to be accompanied by non-lethal lures. Surrounding cameras should point inwards to the central camera. The central camera should be pointing in the optimum direction as dictated by the geography of the respective site. To establish valid results, 7-10 camera night surveys should be implemented in each of the various sub-habitats that the Cerrado, Atlantic Forest and Transitional forest possess e.g. the Cerrado is characterised by campo type vegetation, gallery forest and well-drained savannah type habitats. This design will give better survey area intensification whilst still considering the shifting mosaic that these habitats possess (Soria-Diaz et al., 2010). A less generalised survey area design will also improve the efficiency of the surveyor’s time in placing cameras in the field therefore increasing the number of recordable camera nights; an essential element of reliable data (Rovero et al., 2010).

Future developments to the herpetology camera trap study should involve changes to the bamboo structures that held the cameras in place. It was often the case that the structure had collapsed during the night possibly due to passing animals. Many of the pictures were also unclear because the cameras were set too close to the ground. Amending these issues with higher standing, more physically reliable structures could improve the capture rate of small herpetofauna; however, a significant change in survey design would have to occur to improve the capture rate of mammals, specifically larger mammals that would not fit through small ‘gate’ structures as shown in figure ii.

With regards to the primatology camera trap project, any considerations for future research should be sourced from the on-site primatologist. Due to the longstanding nature of this study, the Azara’s Capuchin population of ‘Group O’ and ‘Group F’ are reliably understood. Currently the project focuses on feeding behaviours as opposed to population changes. Perhaps a future project might involve using camera traps to observe the less studied Howler Monkey population that are occasionally heard in the Flooded Forest sub-habitat at the southern extent of the Atlantic Forest. Unfortunately, such research might be difficult due to the elusive nature of the species and the inaccessible environment that they populate.

Figure vii: A possible sampling design in light of research performed by Soria-Diaz et al., (2010)

& Rovero et al., (2010)

Location Indicators

13 | P a g e

ConclusionThis project gives evidence of the need for careful consideration when establishing an appropriate

survey design for an inventory. The holistic approach gave insight into a variety of techniques for recording medium to large mammals using camera traps.

Regarding the primary design, the initial inventory obtained a greater yield of usable images than the secondary inventory. The near identical designs used for both inventories would suggest that this variation is the result of natural factors as opposed to any anthropogenic issues. From a technical perspective, the initial inventory promoted the use of paths and roads as attractors for mammals whereas the secondary inventory suggested that natural attractors such as the educated implementation of diet-specific lures would offer a well-rounded view of the mammalian populations of each habitat. Further research into a variety of attractors is required to better understand where the cameras should be pointed towards. The grid-square design is unarguably representative as it covers the entire reserve in an equal manner; it should however be noted that 9 of the 33 camera trap locations from the secondary inventory yielded no usable images, a number that might be improved by adopting a more concentrated survey design.

The secondary survey design demonstrated an alternative means of hoisting the camera traps. The vertical images were often unclear due to the reflection from the ground and the relatively small bamboo frames meant that a lot of the larger mammals would not be able to fit through the structures. It should be noted that this could be considered the most successful of the three designs due to the possible sighting of a previously unseen species on the reserve; a Southern Racoon.

The tertiary design demonstrated how beneficial lures can be in enticing mammals. In this case, the use of feeding tables restricted the benefits of the lure to mobile species such as Capuchin Monkeys. A more accessible structure and a more universal lure e.g. fruits & nuts might demonstrate the true potential of lures in establishing a thorough inventory.

Overall, continued surveying of the reserve is essential in completing a full species inventory. It is clear that there are still unrecorded species that inhabit the reserve as demonstrated by section 3b. A continuation of the primary design would be advised however consideration for where the cameras are placed is important to improve survey efficiency. It is also important that data is collected from outside of the summer months to allow for seasonal variation. Incorporating all of the suggestions from each of the survey designs discussed within this project should give sufficient guidance to establish a set of reliable methods allowing for continued analysis of mammalian populations on the reserve.

14 | P a g e

Bibliography

Ancrenaz, M., Hearn, A. J., Ross, J., Sollmann, R., & Wilting, A. (2012). Handbook for wildlife monitoring using camera-traps. Sabah, Malaysai.

Carbone, C., Christie, S., Conforti, K., Coulson, T., Franklin, N., Ginsberg, J. R., & Wan Shahruddin, W. N. (2001). The use of photographic rates to estimate densities of tigers and other cryptic mammals. Animal Conservation, 4(01), 75-79.

De Almeida Jácomo, A. T., Silveira, L., & Diniz-Filho, J. A. F. (2004). Niche separation between the maned wolf (Chrysocyon brachyurus), the crab-eating fox (Dusicyon thous) and the hoary fox (Dusicyon vetulus) in central Brazil. Journal of Zoology, 262(01), 99-106.

Giman, B., Stuebing, R., Megum, N., Mcshea, W. J., & Stewart, C. M. (2007). A camera trapping inventory for mammals in a mixed use planted forest in Sarawak. Raffles Bulletin of Zoology, 55(1), 209-215.

Hamel, S., Killengreen, S. T., Henden, J. A., Eide, N. E., Roed‐Eriksen, L., Ims, R. A., & Yoccoz, N. G. (2013). Towards good practice guidance in using camera‐traps in ecology: influence of sampling design on validity of ecological inferences. Methods in Ecology and Evolution, 4(2), 105-113.

Kelly, M. J. (2008). Design, evaluate, refine: camera trap studies for elusive species. Animal Conservation, 11(3), 182-184.

O'Brien, T. G., Kinnaird, M. F., & Wibisono, H. T. (2003). Crouching tigers, hidden prey: Sumatran tiger and prey populations in a tropical forest landscape.Animal Conservation, 6(02), 131-139.

Rowcliffe, J. M., & Carbone, C. (2008). Surveys using camera traps: are we looking to a brighter future?. Animal Conservation, 11(3), 185-186.

Rovero, F., Zimmermann, F., Berzi, D., & Meek, P. (2013). " Which camera trap type and how many do I need?" A review of camera features and study designs for a range of wildlife research applications. Hystrix, the Italian Journal of Mammalogy, 24(2), 148-156.

Sanderson, J. G., & Trolle, M. (2005). Monitoring Elusive Mammals-Unattended cameras reveal secrets of some of the world's wildest places. American Scientist, 93(2), 148-155.

Séquin, E. S., Jaeger, M. M., Brussard, P. F., & Barrett, R. H. (2003). Wariness of coyotes to camera traps relative to social status and territory boundaries. Canadian Journal of Zoology, 81(12), 2015-2025.

Silveira, L., Jacomo, A. T., & Diniz-Filho, J. A. F. (2003). Camera trap, line transect census and track surveys: a comparative evaluation. Biological Conservation, 114(3), 351-355.

Tobler, M. W., Carrillo‐Percastegui, S. E., Leite Pitman, R., Mares, R., & Powell, G. (2008). An evaluation of camera traps for inventorying large‐and medium‐sized terrestrial rainforest mammals. Animal Conservation, 11(3), 169-178.

Trolle, M., & Kéry, M. (2003). Estimation of ocelot density in the Pantanal using capture-recapture analysis of camera-trapping data. Journal of mammalogy, 84(2), 607-614.

Tobler, M. W., Carrillo‐Percastegui, S. E., Leite Pitman, R., Mares, R., & Powell, G. (2008). An evaluation of camera traps for inventorying large‐and medium‐sized terrestrial rainforest mammals. Animal Conservation, 11(3), 169-178.

Rovero, F., & Marshall, A. R. (2009). Camera trapping photographic rate as an index of density in forest ungulates. Journal of Applied Ecology, 46(5), 1011-1017.

Tobler, M. W., Carrillo‐Percastegui, S. E., Leite Pitman, R., Mares, R., & Powell, G. (2008). Further notes on the analysis of mammal inventory data collected with camera traps. Animal Conservation, 11(3), 187-189.

15 | P a g e

Hebblethwaite, M. (2014). Paraguay. Bradt travel guides.

Smith, P., Cacciali, P., Scott, N., del Castillo, H., Pheasey, H., & Atkinson, K. (2014). First record of the globally-threatened Cerrado endemic snake Philodryas livida (Amaral, 1923) (Serpentes, Dipsadidae) from Paraguay, and the importance of the Reserva Natural Laguna Blanca to its conservation. Cuadernos de Herpetología, 28(2).

Soria-Díaz, L., Monroy-Vilchis, O., Rodríguez-Soto, C., Zarco-González, M. M., & Urios, V. (2010). Variation of abundance and density of Puma concolor in zones of high and low concentration of camera traps in Central Mexico. Animal Biology, 60(4), 361-371.

Rovero, F., Tobler, M., & Sanderson, J. (2010). Camera-trapping for inventorying terrestrial vertebrates. Manual on field recording techniques and protocols for All Taxa Biodiversity Inventories and Monitoring. The Belgian National Focal Point to the Global Taxonomy Initiative, 100-128.

Schlexer, F. V. (2008). Attracting animals to detection devices. Noninvasive survey methods for carnivores, 263-292.

Blair, W. F. (1941). Techniques for the study of mammal populations. Journal of Mammalogy, 22(2), 148-157.

Aiello, S.E. (1998). The Merck Veterinary Manual, 8th Edition, Merck & Co., Inc, USA.

Maffei , L. & Noss , A. (2008) How small is too small? Camera trap survey areas and density estimates for ocelots in the Bolivian Chaco. Biotropica, 40 (1), 71-75.

Karanth, K. U., Chundawat, R. S., Nichols, J. D., & Kumar, N. (2004). Estimation of tiger densities in the tropical dry forests of Panna, Central India, using photographic capture–recapture sampling. Animal Conservation, 7(03), 285-290.

Bodmer, R. E. (1990). Responses of ungulates to seasonal inundations in the Amazon floodplain. Journal of tropical Ecology, 6(02), 191-201.

Ribeiro, J. F., & Vieira, E. M. (2014). Interactions between a seed‐eating neotropical rodent, the Azara's agouti (Dasyprocta azarae), and the Brazilian ‘pine’Araucaria angustifolia. Austral Ecology, 39(3), 279-287.

Kelly, M. J., & Holub, E. L. (2008). Camera trapping of carnivores: trap success among camera types and across species, and habitat selection by species, on Salt Pond Mountain, Giles County, Virginia. Northeastern Naturalist, 15(2), 249-262.

Bennett, A. F. (1990). Habitat corridors and the conservation of small mammals in a fragmented forest environment. Landscape Ecology, 4(2-3), 109-122.

Swihart, R. K., Pignatello, J. J., & Mattina, M. J. I. (1991). Aversive responses of white-tailed deer, Odocoileus virginianus, to predator urines. Journal of Chemical Ecology, 17(4), 767-777.