National Parks Influence Habitat Use of Lowland Tapirs in Adjacent Private Lands in the Southern Yungas of Argentina

National parks influence habitat use of lowland tapirs in adjacent private lands in the Southern Yungas of Argentina

L UIS O SVALDO R IVERA,SEBASTIAN M ARTINUZZI,NATALIA P OLITI S OFIA B ARDAVID,SOLEDAD DE B USTOS,SILVIA C HALUKIAN L EONIDAS L IZÁRRAGA,VOLKER R ADELOFF and A NNA P IDGEON

Abstract Protected areas are cornerstones of conservation in the persistence of lowland tapir populations on adjacent efforts worldwide. However, protected areas do not act in private lands. isolation because they are connected with surrounding, Keywords National park, occupancy, potential habitat, unprotected lands. Few studies have evaluated the effects private land, road, Southern Yungas, Tapir Conservation of protected areas on wildlife populations inhabiting pri- Unit, Tapirus terrestris vate lands in the surrounding landscapes. The lowland tapir Tapirus terrestris is the largest terrestrial mammal of the Supplementary material for this article is available at Neotropics and is categorized as Vulnerable on the IUCN doi.org/./S Red List. It is necessary to understand the influence of landscape characteristics on the tapir’s habitat use to enable effective conservation management for this species. Our  objectives were to ( ) determine the potential distribution Introduction of the lowland tapir’s habitat in the Southern Yungas of Argentina, and () evaluate the role of protected areas and rotected areas are set aside to conserve species and other covariates on tapir habitat use in adjacent private Ptheir habitats, and they are cornerstones of biodiver- lands. We used records of lowland tapirs to model the spe- sity conservation worldwide (Ewers & Rodrigues, ). cies’ potential distribution and determined habitat use with Biodiversity is typically higher and deforestation lower occupancy modelling. Based on the covariates found to be inside protected areas compared to the surrounding land- significant in our models, we constructed predictive maps scape, highlighting the effectiveness of area-based conserva- of probability of habitat use and assessed the area of poten- tion (Joppa & Pfaff, ; Geldman et al., ; Gray et al., tial habitat remaining for the species. Probability of habitat ). However, protected areas do not work in isolation use was higher in the vicinity of two national parks and because they are embedded within wider landscapes and small households than further away from them. We found are connected with surrounding unprotected lands through that in % of the lowland tapir’s potential distribution the fluxes of organisms, energy and nutrients (Hansen & DeFries, probability of habitat use is high (. .). These areas are ). Protected areas may act as refugia that sustain wild- near the three national parks in the study area. The prob- life populations in the surrounding landscapes, especially ability of detecting lowland tapirs increased with distance for large mammals. Wildlife conservation across landscapes to roads. We conclude that national parks play a key role thus requires a clear understanding of the interactions between protected areas and the surrounding unprotected lands (McNeely, ; DeFries et al., ). Private lands have long been recognized as essential LUIS OSVALDO RIVERA (Corresponding author, orcid.org/0000-0003-2960- for large mammal conservation (Simonetti, ; Hilty & 9779), NATALIA POLITI ( orcid.org/0000-0002-8283-3262) and SOFIA BARDAVID Merenlender, ; Soares-Filho et al., ) because lim- Instituto de Ecorregiones Andinas, Consejo Nacional de Investigaciones Científicas y Técnicas, Universidad Nacional de Jujuy, San Salvador de Jujuy, itations in area and representation of habitats in protected Argentina. E-mail [email protected] areas can impede long-term conservation of populations SEBASTIAN MARTINUZZI ( orcid.org/0000-0003-3433-0561), VOLKER RADELOFF and species. However, land use around protected areas is and ANNA PIDGEON ( orcid.org/0000-0002-0090-3352), Department of Forest considered a major threat to biodiversity (Joppa et al., and Wildlife Ecology, University of Wisconsin-Madison, Madison, USA ; Radeloff et al., ). Increasing human popula- SOLEDAD DE BUSTOS Biodiversity Program, Secretary of Environment of Salta Province, Salta, Argentina tions, agricultural expansion and infrastructure development around protected areas reduce wildlife habitat, limit species SILVIA CHALUKIAN Grupo Argentino de Tapires, IUCN Tapir Specialist Group, Bariloche, Argentina movements, affect population source–sink dynamics and

LEONIDAS LIZÁRRAGA National Park Administration of Argentina, Salta, expose wildlife to anthropogenic threats such as hunting, Argentina poaching, invasive exotic species and diseases. These factors Received  May . Accepted  June . First published online  April . potentially limit the conservation value of protected areas

This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, Downloadeddistribution, from https://www.cambridge.org/core and reproduction in any medium,. IP address: provided 170.106.40.40 the original work, onis 30 properly Sep 2021 cited. at 21:53:22, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/termsOryx, 2021, 55(4), 625–634 ©. https://doi.org/10.1017/S0030605319000796The Author(s), 2020. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605319000796 626 L. O. Rivera et al.

(Hansen & DeFries, ). Researchers commonly compare (Tobler, ; Medici, ). They keep away from infra- habitats and wildlife populations inside vs outside protected structure, including roads and oil and gas developments, areas to assess the effectiveness of protected areas (DeFries and are unlikely to persist in areas with human densities  et al., ; Blake et al., ; Geldmann et al., ). . /km (Naveda et al., ; Taber et al., ). Well- However, most studies assessing the interaction between protected areas such as national parks are probably strong- protected areas and surrounding lands have focused on holds for the species (Novaro et al., ;Chalukianetal., the effects of land use and anthropogenic pressures in the ). In north-west Argentina the lowland tapir inhabits surrounding landscape on wildlife populations within pro- both dry Chaco and Southern Yungas forests, at –, m tected areas (Woodroffe & Ginsberg, ; Setsaas et al., altitude (Taber et al., ; Chalukian et al., ). Forest ; Balme et al., ; Harrison, ; Häkkilä et al., loss and fragmentation, illegal hunting, and competition ). High levels of anthropogenic disturbance in areas with livestock are the main factors responsible for popula- surrounding protected lands usually have a negative effect tion declines of lowland tapirs, and they are also chased and on species within protected areas (Metzger et al., ; killed by dogs (Naveda et al., ;Chalukianetal.,). In Laurance et al., ; Häkkilä et al., ). Argentina, the species’ range has declined by %intheth In contrast, the effects of protected areas on wildlife century, remaining populations are small and highly frag- populations inhabiting adjacent private lands have rarely mented (Chalukian et al., ), and the species is categorized been analysed, especially not in a spatially explicit manner. as Endangered nationally (Ojeda et al., ). Fifty-one Tapir Typically, the presence of charismatic mammals such as the Conservation Units, areas with important or critical habitat jaguar Panthera onca, Baird’s tapir Tapirus bairdii, primates for the conservation of the species, have been identified and ungulates declines with distance from protected areas, globally based on expert opinion (Taber et al., ). but factors such as land-cover type, distance from human The mountainous, forested region of north-west Ar- settlements and prey richness also influence habitat use gentina known as the Southern Yungas contains four (Licona et al., ; Carretero-Pinzón et al., ; Schank Tapir Conservation Units and three national parks, but et al., ; Petracca et al., ). Nonetheless, habitats out- most of the land is privately owned. Here, we sought to de- side protected areas can have a high probability of wild- termine how much potential habitat remains for the low- life occupancy, as has been reported for the jaguar in land tapir in both the Tapir Conservation Units and in Nicaragua (Zeller et al., ). Understanding the distribu- the Southern Yungas of Argentina. We also assessed the in- tion patterns of charismatic species in landscapes that con- fluence of small human settlements, roads and rivers, and tain a mosaic of patches with different ownership is useful whether properties were categorized as private reserves, on for understanding the extent of influence of protected areas tapir habitat use in private properties adjacent to national and the role of adjacent private lands, and for informing parks. We expected a higher degree of human influence conservation decisions. This is particularly applicable in at the landscape scale, expressed as shorter distances from regions with high levels of biodiversity, and where large human settlements and roads, to be associated with lower mammals can serve as indicators of the status of more cryp- habitat use by lowland tapirs. Conversely, proximity to na- tic species. Such information is also vital in places such tional parks and to water, and categorization as private re- as South America, which support high biodiversity and serves, were expected to be associated with higher values where land is mostly privately owned but that often lack of habitat use by lowland tapirs. the spatially explicit species-level information required for effective conservation and management. The lowland tapir Tapirus terrestris is the largest Neo- Study area tropical land mammal, occurring in forests from northern South America to northern Argentina (Emmons, The Southern Yungas in north-west Argentina is the south- ; Eisenberg & Redford, ). Lowland tapirs can ernmost Neotropical montane forest (Cabrera, ). It oc- weigh up to  kg, with one young produced at most curs along the eastern Andean slopes between the Chaco dry every  months, are herbivorous and, although typically forests to the east and the Puna highlands to the west. The occurring at low densities, can be locally abundant around area is considered a biodiversity hotspot with high species water sources and salt licks (Padilla & Dowler, ; richness and endemism (Myers et al., ). Human activ- Naveda et al., ). The species has an important role as ities in the lowlands have transformed % of the Southern a disperser of tree seeds, thereby engineering the struc- Yungas forest into agriculture (Brown & Malizia, ). We ture and diversity of forests (Bodmer, ; Fragoso, ; carried out our study in the provinces of Salta and Jujuy, in Chalukian et al., ), and is categorized as Vulnerable forests that cannot be transformed to other land use accord- on the IUCN Red List, with a declining population ing to the current land-use planning scheme (Martinuzzi (Naveda et al., ). Lowland tapirs use riparian forests et al., ) and that contain the four Tapir Conservation and avoid open areas such as grasslands and crops Units of the Southern Yungas ecoregion (Fig. ). The study

Oryx, 2021, 55(4), 625–634 © The Author(s), 2020. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605319000796 Downloaded from https://www.cambridge.org/core. IP address: 170.106.40.40, on 30 Sep 2021 at 21:53:22, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605319000796 Habitat use of lowland tapirs in Argentina 627

  area comprises , km of forests and , km of Species distribution model transformed land (mostly agriculture and urban develop-  ment). Land tenure in the Southern Yungas is characterized We used Maxent (Phillips et al., ) to map the lowland  ’ by large private properties, some . , km in size, with- tapir s potential distribution. We obtained occurrence data in which local people occupy small households (so-called from camera traps used in this study, and also used oc-  puestos), where they grow crops for subsistence and practice currence data from previous studies (Taber et al., ;  extensive cattle ranching (Reboratti, ). There are three Fundación CEBio, ). To minimize sample bias caused national parks in the study area (Calilegua, Baritu and El by double counting of individual tapirs, we used only re- $   Rey National Parks) that have implemented enforcement cords that were km apart. We used eight -km reso- against human activities, except research and tourism lution bioclimatic variables as predictors, following the (Burkart, ). precedent of other distribution models for species in the Southern Yungas: annual precipitation (BIO), annual mean temperature (BIO), seasonality of precipitation (BIO) and temperature (BIO), extreme data for precipitation of wettest quarter (BIO), precipitation of driest Methods quarter (BIO), maximum temperature of warmest month (BIO) and minimum temperature of coldest month Camera-trap data (BIO; Pidgeon et al., , Martinuzzi et al., ). These – Camera traps are effective for detecting tapir presence and variables represented conditions in the area during   have been used extensively throughout the Neotropics (Hijmans et al., ). After testing different buffer    (Trolle et al., ;Coveetal.,;Cruzetal.,). We sizes, we selected a km buffer and generated , selected  camera-trap sites within a matrix of Southern pseudo-absences within the selected buffer for model train-  Yungasforests,andsurveyedthemsequentiallyingroupsof ing in Maxent (VanDerWal et al., ). When running  – sites. Camera-trap sites were located in private proper- Maxent, we set all other options to default (Phillips, )  ties, within a ° latitudinal range, and represented different and assessed model performance with a -fold cross-  land management objectives (i.e. protection for wildlife vs validation (Bateman et al., ) and the area under the human use of forest). We did not set up any camera traps with- receiver operating curve (AUC). To create a map of the ’ in the national parks. Three of the sampled properties are species potential distribution, we transformed predictions designated as private reserves, where the only permitted hu- from Maxent into a binary map of suitable vs unsuitable  man activities are tourism and scientific research. However, habitat, using the th percentile presence logistic threshold. there is no enforcement against hunting, poaching or cattle Because in the Southern Yungas lowland tapirs occur only ’ grazing, all of which commonly occur, so private reserves in forests, we deleted non-forested areas from the species are less protected than national parks. We set up one camera potential distribution map by intersecting the potential dis-  trap (Bushnell Trophy Cam Aggressor, Bushnell, Overland tribution with a land-cover map (Martinuzzi et al., ). Park, USA) at each site to record lowland tapir presence. We did not include topographic variables in our modelling Each camera trap was active continuously for  days during because climate and elevation are often highly correlated  May–November  and was attached to a tree c.  cm (Martinuzzi et al., ). Finally, we calculated the total above the ground. We positioned camera traps to max- area of potential habitat for the species in the study area imize detection of lowland tapirs, by placing them along and in each Tapir Conservation Unit, and the area of trans- forest trails used by large mammals. Camera traps were formed land inside each Unit, by intersecting the potential separated by at least  km (there is no information available distribution with the land-cover map. on home range sizes of lowland tapirs in the Southern Yungas). Occupancy modelling Our approach was similar to a hierarchical framework (Pearson et al., ), and consisted of fitting a model We used occupancy modelling (MacKenzie et al., )to with bioclimatic variables at a larger scale and with low reso- estimate the probability of the species occurring at a site (ψ, lution in Maxent .. (Phillips et al., ), followed by oc- probability of habitat use), and the probability of the species cupancy modelling at a more local scale and with a higher being detected if present (p, detection probability), using re- resolution (MacKenzie et al., ). Occupancy modelling cords in a detection history matrix. We identified biologi- has recently been proposed as a tool for estimating probabil- cally meaningful variables known to influence the detection ity of occupancy, habitat use, or as a surrogate of abundance, of the species and included these variables in the occupancy using co-variables that can influence those parameters at a models (Long et al., ). more local scale, allowing the inference about conservation We partitioned the detection history of each -day potential (MacKenzie et al., ). camera-trap period into -day blocks for a maximum of

FIG. 1 (a) Study area in the Southern Yungas of Argentina, showing national parks (NP), camera-trap sites, non-forested areas, and Tapir Conservation Units (TCU). (b) Detail of (a) showing camera-trap sites in relation to roads, rivers and puestos.

six repeated lowland tapir surveys of each site. Camera de- correlation coefficient of variable pairs (Supplementary tections of lowland tapirs were defined as independent when Table ), and removed one of each pair when correlation they occurred at intervals .  hour (Cove et al., ; Cruz was . . (McDonald et al., ;Steenwegetal.,). et al., ). We retained distance from camera traps to nearest roads, We selected covariates based on previous studies (Norris, puestos, water courses and national park borders. We stan- ; Ferreguetti et al., ) that identified relevant an- dardized these variables by converting them to Z scores thropogenic and environmental variables influencing pres- (to vary between + and −;Donovan&Hines,). Pro- ence and occupancy of lowland tapirs. Variables used were tection of private properties was included as a binary variable distances to settlements, agricultural lands, roads, water (properties without protection = , private reserves = ). courses and national park boundaries. We did not consider We developed  a priori models, including a constant forest cover as a variable, given that all camera traps were (null) and global set (Supplementary Table ), to estimate placed within forests. We calculated Euclidian distances (in the influence of the five variables on the probability of km) from camera traps to settlements, agricultural lands, lowland tapir habitat use (ψ). We selected the best models roads, water courses and national park boundaries in based on the Akaike information criterion (AIC; Burnham ArcGIS . (Esri, Redlands, USA). We obtained spatial data- & Anderson, ). Rather than choosing the single high- sets of settlements, roads, water courses and national park est-ranked model, we estimated the mean of the high- boundaries from governmental datasets (IGN, ), and est-ranked models (i.e. models with ΔAIC ,  with respect to of agricultural lands from the available land-cover map the top-ranked model; MacKenzie et al., ). We deter- (Martinuzzi et al., ). Settlements were differentiated mined co-variable effects on ψ and p using the model aver- into two types: () puestos, which are isolated small house- aged parameter estimate. If the % confidence intervals for holds inhabited by one or few people, in some instances a parameter estimate excluded zero, its effect was considered inhabited only seasonally, and () urban centres, defined significant (MacKenzie et al., ). as settlements with . , people (IGN, ). To avoid We fitted detection histories and covariates in a single- collinearity between covariates we calculated the Pearson season occupancy model implemented in PRESENCE .

(Hines, ). Lowland tapirs are large-bodied mammals ψ of Tapir Conservation Unit  was almost half of the capable of travelling long distances between sites (Fragoso, value of the other Tapir Conservation Units (Supplementary ), therefore, ψ was considered to represent habitat use Table ). The model-averaged estimate for all sites, based instead of occurrence (MacKenzie et al., ). We deter- on the five models with ΔAIC , , was ψ = . ± SE . mined a naïve occupancy estimate for the lowland tapir and p = . ± SE .. Variables in these well supported as the proportion of cameras at which the species was re- models included distances to national parks, roads and corded. Finally, we generated a spatially explicit map of es- puestos, and protection of forests in private reserves. Dis- timated habitat use, based on the model averaged variables. tance to nearest watercourses was not included in the For our maps, we established a hexagonal grid of  km diam- best models (Table ). Distance to national park borders eter cells over the study area. We calculated the value of each and distance to puestos were significantly negatively asso- variable included in the averaged model for each hexagon ciated with ψ (Table ). Detection probability p was sig- using the centroid of each hexagon as the reference point nificantly positively associated with increasing distance to for determining the distances to the nearest national parks, roads (Table ). roads and puestos. Given the small size of the hexagons we The spatially explicit map of estimated habitat use showed assumed that conditions at the centroids were representa- that the majority (%) of the area with potential lowland tive of conditions in the entire hexagon. We constructed the tapir distribution has a high probability (. .) of habitat spatially explicit map of estimated habitat use considering use (Fig. ). Areas with the highest probability of habitat only the area within the potential distribution of the low- use were located near the three national parks (Fig. ). Con- land tapir determined with Maxent. versely, the area of the Southern Yungas with the lowest probability of habitat use was the north-eastern part of the study area, where there are no national parks (Fig. ). Results

Of the  camera traps set,  were active for  days, resulting in , trap nights. This trapping effort yielded Discussion  photographic records of lowland tapirs, with  independent records. Lowland tapirs were recorded at  camera Habitat use by the lowland tapir on private lands adjacent to traps in  of the  private properties. The mean nearest national parks was strongly negatively associated with in- distance from camera traps to puestos was . ± SE . km creasing distance to national park borders in the Southern (range .–.), to roads . ± SE . km (.–.), to a na- Yungas forests. A clear association between national parks tional park border . ± SE . km (.–.) and to water and tapir habitat use is further supported by the low pre- courses . ± SE .km (.–.). dicted habitat use values in the north-eastern sector of the study area, where there is no strictly protected area. This pattern of association with protected areas corresponds Potential tapir habitat with patterns of lowland tapir habitat use in the Peruvian Amazon (Bodmer, ; Bodmer & Robinson, ), and  We obtained a total of tapir locations for species distribu- with Baird’s tapir persistence in Costa Rica (Cove et al., tion modelling. The AUC value of the species distribution ). We suggest that national parks act as refugia for   model was . . Current forest area with potential distribu- tapirs, and as sources of tapir dispersal into unprotected    tion of the lowland tapir in the study area was , km , areas (Novaro et al., ), given that the national parks     with , km ( %) located within Tapir Conservation harbour healthy populations of lowland tapirs in the      Units (Supplementary Table ), and , km ( %) outside Southern Yungas (Chalukian et al., ). National parks  these Units. Privately owned properties represent %of in the Southern Yungas are strictly protected, with surveil- the total area of the four Tapir Conservation Units in the lance by park rangers and strong law enforcement (Burkart,  Southern Yungas of Argentina (Supplementary Table ), ). The continuous matrix of privately owned forests in     and %(, km ) of potential habitat have been lost which national parks are embedded provides habitat con- because of forest transformation to other land uses. nectivity and facilitates tapir dispersal into the unprotected areas near the national parks. In other regions, where areas Tapir habitat use immediately adjacent to national parks are exposed to high levels of land transformation and human disturbance, mor- The naïve occupancy estimate for the lowland tapir was tality of charismatic species is often high and population de- .. Our single season model assuming constant detec- clines are common in the surrounding landscape, as a result tion probability at all sites produced a habitat use estimate of edge effects, poaching and conflict with humans (Setsaas ψ = . ± SE . (β = . ± SE .) with a detection prob- et al., ; Balme et al., ; Häkkilä et al., ). For ex- ability p = . ± SE . (β = −. ± SE .). The value of ample, in Iguaçu National Park in Brazil, there are strong

TABLE 1 Top-ranked models for the probability of habitat use ψ and detection probability p of the lowland tapir Tapirus terrestris in the Southern Yungas forest of Argentina, based on Akaike’s information criterion (AIC) with a ΔAIC ,  (difference in AIC from the best-ranked model). The table shows the relative model weight (Akaike weight), the likelihood of each model being the best-performing model, the number of model parameters (k) and the − log-likelihood output from the occupancy model, implemented in PRESENCE . (Hines, ).

Model1 AIC ΔAIC Akaike weight Model likelihood k −2 log-likelihood ψ (NatParks, Puestos); p(Roads) 653.66 0.00 0.35 1.00 5 643.66 ψ (NatParks, Puestos); p(Roads, Puestos, Protection) 654.86 1.20 0.19 0.55 7 640.86 ψ (NatParks, Puestos); p(Roads, Protection) 655.07 1.41 0.17 0.49 6 643.07 ψ (NatParks, Puestos, Roads, Protection); p(Roads) 655.65 1.78 0.14 0.41 7 641.44 ψ (NatParks, Puestos, Roads); p(Roads) 655.94 1.99 0.13 0.37 6 643.65

 Variables: NatParks, distance of camera trap to the nearest national park border; Protection, designation as private reserves; Puestos, distance of camera trap to the nearest puestos (small households); Roads, distance of camera trap to the nearest road.

TABLE 2 Model averaged beta values, standard errors, and % con- Conservation Units, but % remains outside. Therefore, fidence intervals for the variables that affected the probability of we recommend as a priority to evaluate the conservation habitat use (ψ) and the detection probability (p) of lowland tapirs status of the potential habitat area located outside Tapir in the Southern Yungas Forest of Argentina. Conservation Units. Only % of the forest area in the Parameter Tapir Conservation Units is within national parks, where- Variable estimates ± SE 95% CI as % is in private properties. The national parks in the Probability of habitat use (ψ) Southern Yungas are probably too small to maintain viable Distance to national park −1.23 ± 0.43* −2.07–−0.39 populations of lowland tapirs in the long term. It has been Distance to puestos −0.63 ± 0.31* −1.24–−0.01 estimated that the home range of lowland tapirs in semi-  Distance to roads −0.01 ± 0.09 −0.19–0.19 deciduous Atlantic Forest is . km and that  tapirs − ± − – Private reserve 0.24 0.17 0.58 0.10 would be required to ensure long-term population viability Detection probability (p) (Medici, ). Therefore, in the Southern Yungas the Distance to roads 0.41 ± 0.14* 0.15–0.68 Distance to puestos 0.05 ± 0.03 −0.01–0.12 conservation strategy for the lowland tapir should include Private reserve −0.09 ± 0.12 −0.33–0.14 private forests surrounding national parks in schemes of sustainable management. We found no evidence that tapir habitat use was higher edge effects from adjacent transformed lands inside the on protected private reserves than on private lands without protected area, affecting occupancy of several mammals, protection. This suggests that the protection level afforded including lowland tapirs (da Silva et al., ). In contrast, by protected private lands, which is lower than that of in the Southern Yungas the unprotected forests in private national parks, is not sufficient to influence habitat use by lands surrounding national parks appear to have low hu- tapirs. However, these findings must be interpreted cau- man disturbance levels, allowing tapirs to persist. tiously because our sample size was small. Currently, in The establishment of Tapir Conservation Units aims to Argentina the National Forest Law No. , (Seghezzo ensure the long-term viability of entire tapir populations, et al., ) provides a legal framework and financial support by prioritizing habitats for conservation and identifying for the protection of private land (Rivera et al., ), assist- and managing threats in those key areas. As we collect ing private land owners in supporting the populations of more information on the tapir’s habitat use and distribution tapirs and other wildlife. we can refine strategies and improve the delineation of the Contrary to our expectations, habitat use by the lowland existing Tapir Conservation Units. In three of the four Tapir tapir was higher closer to puestos. One possible explanation Conservation Units in our study area higher habitat use is that puestos are in relatively inaccessible locations, with values were partly attributable to the presence of national no association with distance to roads, cities, or agricultural parks (i.e. Tapir Conservation Unit  includes Baritú lands. Inaccessibility of puestos could offset the effect of National Park, Unit  includes Calilegua National Park, some human disturbance such as cattle grazing and small- and Unit  includes El Rey National Park). The lower va- scale crop farming. It is also possible that tapirs benefit from lues of habitat use in Unit , where there is no national small-scale forest disturbance caused by local people, as park, further highlight the importance of strict protection tapirs are known to forage in open and secondary forests of forests for the persistence of lowland tapir populations. (Painter, ). Another possible cause of the positive asso- The majority (%) of the potential lowland tapir ciation is that local people living in puestos persecute large habitat in the Southern Yungas is included in the Tapir predators to reduce cattle predation (Perovic et al., ),

FIG. 2 (a) Potential habitat for the lowland tapir, and (b) spatially explicit map of probability of habitat use for the lowland tapir in the study area.

which may also reduce predation pressure on the lowland poaching and illegal logging. Given that most of the land tapir. Local people also appear not to rely on hunting tapirs within the Tapir Conservation Units is privately owned, as a protein source. The only evidence of hunting in the collaboration with the private sector is required to protect study area is from areas with good accessibility by urban the lowland tapir and its habitat. This should happen within hunters (S.C. Chalukian, , pers. comm.), which is why the framework of the National Forest Law, which aims to roads affected lowland tapir detectability, as in other regions support land planning and forest management, including where roads have provided access for hunters (Licona et al., conservation and restoration of ecologically important ele- ; Cruz et al., ; Schank et al., ). Care is thus ne- ments. Connectivity between Tapir Conservation Units is cessary when planning and building new transport infra- threatened by land-use change, and thus strategies to main- structure in the Southern Yungas, to avoid increasing ac- tain the remaining structural connectivity are needed ur- cess to unprotected forested areas (Martinuzzi et al., ). gently, for the benefit of the lowland tapir and other species. Given the key role of national parks for the conservation More broadly, our study highlights the importance of of lowland tapir populations in the Southern Yungas, the protected areas for large mammals, not only by protecting management effectiveness and implementation of protec- populations inside the protected areas themselves, but also tion actions in these conservation areas must be maintained by potentially supporting populations outside, on adjacent or improved, with adequate funding and personnel. Tapir private lands. In addition, surrounding areas can increase Conservation Unit  is under increasing anthropogenic the total area of available habitat, and hence support larger pressure, with oil and gas prospecting, extensive cattle subpopulations with better chances for long-term survival. ranching, illegal forest logging and wildlife poaching (Salta However, we caution that studies based on camera traps, Government, ). We suggest that the lowland tapir and such as ours, cannot identify sink habitat, and we were other wildlife species would benefit from the creation of a not able to examine demographics and age structure of strictly protected area in Tapir Conservation Unit .Other- tapirs inside and outside protected areas. Nevertheless, we wise, if the creation of a strictly protected area is not pos- suggest that our findings highlight the broader importance sible, efforts should be made to limit the extent of cattle of national parks, and the need to carefully examine their ranching and strengthen the enforcement of laws against value for surrounding areas, especially if those areas are

not heavily influenced by humans. In the oceans, marine BURKART,R.() Protected areas of Argentina. In Environmental protected areas have been shown to increase fisheries in Status of Argentina  (eds A. Brown, U. Martinez Ortiz, – the surrounding areas in some cases (McClanahan & M. Acerbi & J.F. Corcuera), pp. . FVSA (Fundación Vida    Silvestre Argentina), Buenos Aires, Argentina. Mangi, ; Roberts et al., ; Lester et al., ), and BURNHAM, K.P. & ANDERSON, D.R. () Model Selection and in terrestrial systems, theory and empirical data suggest Multimodel Inference: A Practical Information-Theoretic Approach. that spatial controls on hunting, such as those provided by nd edition. Springer Verlag, New York, USA. protected or sacred areas, can allow wild populations to CABRERA,A.() Argentine Encyclopedia of Agriculture and persist (McCullough, ; Brandt et al., ). It may be a Gardening: Phytogeographic Regions of Argentina. Acme, Buenos Aires, Argentina. missed opportunity that the benefits of protected areas for CARRETERO-PINZÓN, X., DEFLER, T.R., MCALPINE, C.A., & RHODES, wildlife populations in unprotected landscapes are not J.R. () The influence of landscape relative to site and patch typically considered in conservation planning (Margules & variables on primate distributions in the Colombian Llanos. Pressey, ; Naidoo et al., ; Keppel et al., ). Landscape Ecology, , –. CHALUKIAN, S., DE BUSTOS, S., LIZÁRRAGA, L., QUSE, V., PAVIOLO,A. Acknowledgements We thank the land owners who allowed us to &VARELA,D.() Action Plan for the Conservation of the Tapir conduct fieldwork on their properties; Francisco Molina and Mariano (Tapirus terrestris) in Argentina. Tapir Specialist Group, IUCN, Odetti for help with fieldwork; Fundación CEBio for logistical Salta, Argentina. support; and the Whitley Fund for Nature for financial support. CHALUKIAN, S., DE BUSTOS, S., DI BITETTI, M., DE ANGELO,C.& A Fulbright-CONICET (Consejo Nacional de Investigaciones Cien- PAVIOLO,A.() Order Perissodactyla. In Red Book of the tíficas y Técnicas) scholarship and CONICET supported the visit of Threatened Mammals of Argentina (eds R.A. Ojeda, V. Chillo & NP and LR to Silvis Lab at University of Wisconsin, Madison. G.B. Díaz Isenrath), pp. . SAREM (Sociedad Argentina para el Estudio de los Mamíferos), Mendoza, Argentina. Author contributions Study concept and design: all authors; data COVE, M.V., PARDO VARGAS, L.E., DE LA CRUZ, J.C., SPÍNOLA, R.M., collection: LR, NP, SB, SdB, SCH, LL; data analysis: LR, SM, NP, VR, JACKSON, V.L., SAENZ, J.C. & CHASSOT,O.() Factors AP; creation of habitat use maps: LR, SM, NP, VR, AP; writing: LR, SM, influencing the occurrence of the Endangered Baird’s tapir Tapirus NP, VR, AP; revisions: all authors. bairdii: potential flagship species for a Costa Rican biological corridor. 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