Is reintroduction a tool for the conservation of the jaguar Panthera onca? A case study in the Brazilian Pantanal
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Is reintroduction a tool for the conservation of the jaguar Panthera onca? A case study in the Brazilian Pantanal ROSE LILIAN GASPARINI-MORATO, LEONARDO SARTORELLO, LILIAN RAMPIM CARLOS EDUARDO FRAGOSO, JOARES ADENILSON MAY JR, PEDRO TELES M A R I O H A B E R F E L D , R O G É R I O C U N H A D E P A U L A and R O N A L D O G O N Ç A L V E S M O R A T O Abstract To evaluate the feasibility of reintroduction as a survival of the species in this biome will depend on reduc- tool for conservation of the jaguar Panthera onca, we ing jaguar mortality and reconnecting the subpopulations adapted the IUCN soft release protocol to reintroduce two (Paviolo et al., ). However, some of these are isolated jaguars in the southern Pantanal, Brazil. After being kept at and the cost of establishment of suitable corridors may be rescue centres for months, the jaguars were moved to a prohibitive (Paviolo et al., ), and alternative strategies, -ha enclosure with native vegetation on a , ha ranch such as supplementation and reintroduction, may be re- in the Pantanal, where hunting is not allowed and prey is quired (Galetti et al., ). abundant. In the enclosure, the animals were fed with meat, Reintroductions of apex predators, including the few dead animals (roadkill) and then, progressively, live wild attempts to reintroduce jaguars, have generally been poorly prey. After months, the jaguars were fitted with collars documented and measurement of failure or success has equipped with GPS/VHF (recording one location per hour) been hampered by the lack of prior definition of expected and accelerometers, and released in the same area. The outcomes (Breitenmoser et al., ). To evaluate reintro- animals established residence near the enclosure, with duction as a tool for conservation of the jaguar, we adapted home ranges, movement parameters, daily activity patterns the IUCN () soft release protocol to reintroduce two res- and prey consumption similar to that recorded in previous cued jaguars in the southern Pantanal, Brazil (Fig. ). We studies. Social interaction and reproduction indicated the chose this area based on five criteria: () rescued animals reintroduction was successful, and that it can be a tool for were from the same region, () knowledge of the species’ the species’ survival in areas where the jaguar population biology in the Pantanal was available, including for the re- is in decline. lease site (Cavalcanti & Gese, ), () availability of suit- able habitat (de Paula et al., ), () prey availability Keywords Brazil, home range, jaguar, Pantanal, Panthera (Perilli et al., ), and () acceptance by the local com- onca, reintroduction munity. Our expected outcomes were that the two jaguars would: () prey on wild species (to evaluate this, we compared the T he historical range of the jaguar Panthera onca has con- tracted and many populations are now threatened (De la Torre et al., ), including the subpopulations in the species preyed upon with the reported feeding habits of ja- guars in the same area; Perilli et al., ), () establish resi- Atlantic Forest (Morato et al., ). The last c. indivi- dence (establishment of residence may be an indicator of duals in this forest occur in seven subpopulations, and the acclimation, and jaguars have resident ranges; Rabinowitz & Nottingham, ), () have similar home ranges and movement to those reported for jaguars in the Pantanal ROSE LILIAN GASPARINI-MORATO* (Corresponding author, orcid.org/0000- (Morato et al., ), () have daily activity patterns com- 0003-2885-0034), ROGÉRIO CUNHA DE PAULA ( orcid.org/0000-0003-1943- parable to that of resident jaguars, () exhibit social interac- 8320) and RONALDO GONÇALVES MORATO ( orcid.org/0000-0002-8304-9779) Instituto Chico Mendes de Conservação da Biodiversidade – Centro Nacional tions (Kanda et al., ), and () reproduce. de Pesquisa e Conservação de Mamíferos Carnívoros, Estrada Municipal In June , during the flood season, a female jaguar and Hisaichi Takebayashi 8600, 12952-011, Atibaia, São Paulo, Brazil E-mail rose.morato@icmbio.gov.br her two -month old female cubs were forced to seek refuge in an urban area of Corumbá, in the state of Mato Grosso do Sul, LEONARDO SARTORELLO* ( orcid.org/0000-0001-7607-9577), LILIAN RAMPIM ( orcid.org/0000-0001-8121-3152), CARLOS EDUARDO FRAGOSO ( orcid.org/ in the southern Brazilian Pantanal, climbing a tree c. m from 0000-0001-8971-2896), JOARES ADENILSON MAY JR ( orcid.org/0000-0002- a house. An attempt to capture the jaguars resulted in the ac- 0007-9690), PEDRO TELES ( orcid.org/0000-0003-0754-2470) and MARIO HABERFELD ( orcid.org/0000-0001-9360-6658) Associação Onçafari, São cidental death of the mother. The two orphans were moved to Paulo, Brazil a wildlife rescue centre in Campo Grande, where they spent *Contributed equally months. We then moved them to a new facility in São Paulo Received October . Revision requested December . state, with better infrastructure and minimum contact with Accepted May . First published online March . people, where they stayed for months. 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. IP address: and reproduction in any medium, provided 46.4.80.155, on 20isMay the original work 2021cited. properly at 06:03:48, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms . https://doi.org/10.1017/S0030605320000460 Oryx, 2021, 55(3), 461–465 © The Author(s), 2021. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605320000460
462 R. L. Gasparini‐Morato et al. FIG. 1 The estimated home range (with % CI bands) of jaguars Panthera onca and in the southern Pantanal, Brazil. Note the high overlap in their home ranges. Pre-release, the two jaguars were tested for all relevant in- home range and spatial overlap, we used months of tel- fectious and parasitic diseases. At c. months old, having emetry data (June –September ). We also performed been confirmed healthy, they were moved on July visual appraisals using images captured by a c. km grid to a ha enclosure with native vegetation (Plate ) in the of camera traps. We observed that jaguar no. suffered Caiman Ecological Refuge, a , ha private ranch in initial loss of weight but recovered days after release. The Miranda, Mato Grosso do Sul (Fig. ). The ranch is a enclosure door remained open for months and both ja- mixed enterprise, with cattle ranching and ecotourism. It guars returned several times. We fitted a continuous-time follows jaguar-friendly best practices (Rampim et al., ), stochastic movement model (ctmm; Calabrese et al., ) and hunting is not allowed on the property. As a result, po- in R .. (R Core Team, ) to evaluate movement behav- tential prey is abundant and the estimated density of jaguars iour and estimate home range. This method accounts for the is c. per km (Soisalo & Cavalcanti, ). In the first inherent serial autocorrelation of our data and could handle months in the enclosure the jaguars were fed meat and dead irregularities in the sample schedule (Fleming et al., ). animals (roadkill), to facilitate acclimation. After this, live Range residence behaviour was checked by visual inspection wild prey was captured and presented, one animal at a of a semi-variogram (function variogram in R). Movement time. Prey was released into the enclosure through one of models were fit with maximum likelihood (function ctmm. six guillotine gates. These gates were covered with wooden fit) and ranked based on the Aikake information criteria plates to prevent the jaguars associating the arrival of food (function ctmm.select). We estimated home range condi- with people. We observed that hunting was better after tional on the fitted model for both individuals using the days without food. After months the two jaguars were akde function (autocorrelated kernel density estimator). able to chase, surprise and kill all the animals offered. On We estimated spatial overlap using the overlap function. a few occasions we offered two prey, of the same species, Daily activity patterns were evaluated using Activity Pat- simultaneously, to evaluate hunting behaviour. In total, tern Software (Lotek, Newmarket, Canada) after recovering the jaguars captured and consumed prey, including white- the accelerometer data from the GPS collars. lipped peccaries Tayassu pecari, capybaras Hydrochoerus We adapted the method described by Cavalcanti & Gese hydrochaeris, caimans Caiman yacare and feral pigs Sus () to identify prey consumed. When . consecutive scrofa scrofa (Table ). After fitting collars equipped with locations were found , m from each other this was clas- GPS/VHF, recording one location per hour, and acceler- sified as a kill site, where we then searched for prey remains ometers, the jaguars were monitored for days inside the to identify the species. Social behaviour, interactions and enclosure, to provide baseline data on activity patterns and reproduction were investigated by observation and camera- social behaviour. trap images. Range residence was confirmed after visual The two jaguars were released at c. months old, on inspection of a semi-variogram, months post release June . To evaluate movement behaviour and estimate (Morato et al., ). Home range estimates were . km Oryx, 2021, 55(3), 461–465 © The Author(s), 2021. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605320000460 Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 20 May 2021 at 06:03:48, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms . https://doi.org/10.1017/S0030605320000460
Reintroduction of the jaguar 463 TABLE 1 Total amount of meat consumed and dead and live prey offered to the two female jaguars Panthera onca during days in an enclosure in the Caiman Ecological Refuge, in Miranda, Mato Grosso do Sul, Brazil. kg (no. of carcasses/individuals) Meat Beef 137 Chicken 118 Pig 13 Dead prey Capybara Hydrochoerus hydrochaeris 55 (2) Giant anteater Myrmecophaga trydactila 30 (1) Caiman Caiman yacare 23 (1) Live prey Capybara 400 (15) White-lipped peccary Tayassu pecari 345 (16) Caiman 185 (8) Pig 110 (6) Feral pig Sus scrofa scrofa 5 (1) TABLE 2 Details of the and prey killed by female jaguars and , respectively, after release (January –December ) and, for comparison, the mean per cent of total prey killed by jaguars in an earlier study in the southern Pantanal. Female 1 Female 2 Mean % of Prey (% of total) (% of total) kills (range)1 Caiman 32 (61) 18 (56) 36 (10–52) Capybara 1 (2) 4 (12) 3 (0–17) White-lipped 9 (17) 3 (10) 30 (0–57) peccary Armadillo Dasypus 1 (2) 3 (10) 2 (0–15) novemcinctus Coati Nasua nasua 5 (10) 2 (6) 2 (0–11) Raccoon Procyon 1 (3) 1 (0–4) cancrivorus Crab eating fox 1 (3) 1 (0–3) Cerdocyon thous Giant anteater 2 (4) 4 (0–17) Deer Mazama sp. 1 (2) 2 (0–5) Bird 1 (2) 1 (0–3) From Cavalcanti & Gese (). (% CI .–.) for jaguar , and . km (% CI .– .) for jaguar (Fig. ). Both individuals anchored their home range around the enclosure and showed high spatial overlap with each other (%, % CI –%; Fig. ). The home ranges included areas with ecotourism and cattle PLATE 1 The ha enclosure in the Caiman Ecological Refuge ranching activities, areas with wild prey, and well-preserved (Fig. ): (a) . m high eucalyptus posts, m apart; (b) cm deep trench excavated around the perimeter of the enclosure and natural vegetation. Directionality in movement paths, repre- filled with cement, to prevent any animal digging into or out of sented by the velocity autocorrelation timescale (h), were the enclosure; (c) c. m deep, m pond; (d) galvanized wire . (% CI .–.) and . (% CI .–.) for jag- perimeter fence of . mm gauge and × cm mesh, with uar and , respectively. Mean distances travelled per day electric wires at , and cm, both inside and outside were . and . km for jaguar and , respectively. Daily and on the top of the fence; (e) aerial view. Oryx, 2021, 55(3), 461–465 © The Author(s), 2021. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605320000460 Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 20 May 2021 at 06:03:48, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms . https://doi.org/10.1017/S0030605320000460
464 R. L. Gasparini‐Morato et al. As a pre-condition for reintroduction, the highest prior- ity must be to address the threats that are causing jaguar population declines. Firstly, some jaguar subpopulations are proximal to areas where people are active, potentially resulting in negative interactions. Jaguars involved in such interactions are often killed by members of the affected community (Inskip et al., ). In such areas, law enforce- ment to prevent killing of jaguars, and alleviation of nega- tive interactions with ranchers, are required and should play a central role in planning any reintroduction (Caruso & Pérez, ). Secondly, in areas that have undergone deforestation (Ribeiro et al., ) or defaunation (Jorge et al., ), it is important to evaluate habitat quality and prey availability before establishing a reintroduction programme. Thirdly, social interaction is a key compo- nent. The absence of intersexual territoriality (Crawshaw & Quigley, ) suggests that reintroducing female jaguars is likely to increase the success of reintroductions in areas where male jaguars are present. Fourthly, jaguars tend to move in areas with which they are familiar, evidence of cog- nitive capacity and spatial memory (Kanda et al., ), and therefore building enclosures in the release area and keeping individuals there prior to release may facilitate acclimation. PLATE 2 (a) Jaguar with her – month old cub, photo-trapped Fifthly, the cost of reintroduction needs to be compared to in December , and (b) Jaguar and her two – month old cubs, photo-trapped in December . alternative strategies. The total cost for reintroducing the two female jaguars was c. USD ,, without considering activity was similar to that previously reported for jaguars, the costs of previous studies of the species’ behaviour in with both individuals moving (hunting and transiting) dur- the same area. This reintroduction was in an area where ing the night and resting during the day (Kanda et al., ). spatial ecology, habitat and prey preferences were known We identified species preyed upon by the two jaguars (Cavalcanti & Gese, , ; Morato et al., ). In (Table ). Social interactions were observed between the the Atlantic Forest on the Argentina–Brazil border the two jaguars and nine other individual jaguars), including main strategy for the southernmost jaguar subpopulation mating, fighting and paired movement. Jaguar gave birth was to reduce persecution and poaching by means of edu- to a cub in c. June and jaguar gave birth to two cubs in cation and law enforcement. The annual cost of the pro- c. August (Plate ). gramme was c. USD , and after years the jaguar The two jaguars established residence near the enclo- population increased from an estimated to individuals sure, with home ranges, and movement and activity patterns (Paviolo et al., ). similar to those reported for free living individuals (Morato In conclusion, reintroduction can be an important tool et al., ), and prey consumption similar to that recorded in areas where the jaguar population is in severe decline. in a previous study in the same area (Cavalcanti & Gese, It is the only option where the species has been extirpated ), including a high consumption of caimans. The exhib- and the management goal is reintroduction, residency and ition of social interactions, and reproduction, indicate that recovery. This study defines some of the practices and para- the reintroduction was successful. meters that led to a successful outcome in the Pantanal. The main objective of a reintroduction is usually to re- establish or supplement an extinct or declining population Acknowledgements We thank Centro de Reabilitação de Animais (Cheyne, ). We released two individuals in an area Silvestres de Campo Grande and Instituto de Meio Ambiente de Mato where jaguars are not facing a high risk of extinction Grosso do Sul for rescuing the jaguars; Mantenedor Santa Rosa for (Morato et al., ) and threats are low. Our intention was hosting and caring for them; Caiman Ecological Refuge for allowing to evaluate a protocol that could be applied to other subpo- us to build the training facility and release the jaguars on their prop- pulations across the species’ range, and specifically for the erty; Alexandre Bossi, Camila Martins, Écio Silva, Fernando Von Zuben, Márcia Reed, Pedro Lacerda Camargo, Raphael Klabin, Critically Endangered subpopulation of the Atlantic Forest Robert Kozmann Jr, and Roberto Klabin and Instituto SOS Pantanal (Morato et al., ). Despite the success of this reintroduc- for their support; Log Materials and Bushnell Corporation for donat- tion in the Pantanal we need to be cautious in using this tool ing camera traps; and Tetrapak for donating materials to build the for the species’ long-term survival. enclosure. Oryx, 2021, 55(3), 461–465 © The Author(s), 2021. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605320000460 Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 20 May 2021 at 06:03:48, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms . https://doi.org/10.1017/S0030605320000460
Reintroduction of the jaguar 465 Author contributions Study design: RLG-M, LS, LR, PT, MH, G A L E T T I , M., E I Z I R I K , E., B E I S I E G E L , B., F E R R A Z , K., C AVA L C A N T I , S., RCdP, RGM; fieldwork: LS, LR, CEF, JAMJ, MH, RCdP; data analysis, S R B E K -A R A U J O , A.C. et al. () Atlantic rainforest’s jaguars in writing: RLG-M, LS, RGM; revision: LS, LR, CEF, JAMJ, PT, MH, RCdP. decline. Science, , . I N S K I P , C., R I D O U T , M., F A H A D , Z., T U L LY , R., B A R LOW , A., B A R LO W , Conflicts of interest The authors have no relationship with Log C.G. et al. () Human–tiger conflict in context: risks to lives Materials, Bushnell Corporation or Tetrapak, who donated equipment and livelihoods in the Bangladesh sundarbans. Human Ecology, for research purposes only. , –. IUCN () Guidelines for Reintroductions and other Conservation Ethical standards All research protocols were approved by Instituto Translocations. IUCN, Gland, Switzerland. issg.org/pdf/ Chico Mendes de Conservação da Biodiversidade and Sistema de publications/RSG_ISSG-Reintroduction-Guidelines-.pdf Autorização e Informação em Biodiversidade (licenses 46508, 47979, [accessed July ]. 52734), and the research followed guidelines approved by the J O R G E , M.L.S.P., G A L E T T I , M., R I B E I R O , M.C., F E R R A Z , K.M.P.M.B. American Society of Mammalogists, and otherwise abided by the () Mammal defaunation as surrogate of trophic cascades in a Oryx guidelines on ethical standards. biodiversity hotspot. Biological Conservation, , –. K A N D A , C., O L I V E I R A -S A N T O S , L.G., M O R AT O , R.G., D E P A U L A , R.C., R A M P I M , L., S A R T O R E L LO , L. et al. () Unexpected spatial References overlap in a solitary carnivore is revealed by simultaneous GPS-tracking of jaguars (Panthera onca). Journal of Zoology, B R E I T E N M O S E R , U., B R E I T E N M O S E R -W U R S T E N , C., C A R B Y N , L.N. & , –. F U N K , S. () Assessment of carnivore reintroductions. M O R AT O , R.G., B E I S I E G E L , B.M., R A M A L H O , E.E. & B O U L H O S A , R.L.P. In Carnivore Conservation (eds J.L. Gittleman, S.M. Funk, () Avaliação de risco de extinção de onça pintada Panthera onca D. MacDonald & R.K. Wayne), pp. –. Cambridge University (Linnaeus, ) no Brasil. Biodiversidade Brasileira, , –. Press, Cambridge, UK. M O R AT O , R.G., S T A B AC H , J.A., F L E M I N G , C.H., C A L A B R E S E , J.M., D E C A L A B R E S E , J.M., F L E M I N G , C.H. & G U R A R I E , E. () Ctmm: an R P A U L A , R.C. et al. () Space use and movement of a neotropical package for analyzing animal relocation data as a continuous-time top predator: the Endangered jaguar. PLOS ONE, , e. stochastic process. Methods in Ecology and Evolution, , –. P AV I O LO , A., D E A N G E LO , C., F E R R A Z , K.M.P.M.B., M O R AT O , R.G., C A R U S O , F. & P É R E Z , I.J. () Tourism, local pride, and attitudes P A R D O , J.M. et al. () A biodiversity hotspot losing its top towards the reintroduction of a large predator, the jaguar Panthera onca predator: the challenge of jaguar conservation in the Atlantic Forest in Corrientes, Argentina. Endangered Species Research, , –. of South America. Scientific Reports, , . C AVA L C A N T I , S.M.C. & G E S E , E.M. () Spatial ecology and social P E R I L L I , M.L.L., L I M A , F., R O D R I G U E S , F.H.G. & C AVA L C A N T I , S.M.C. interactions of jaguars (Panthera onca) in the Southern Pantanal, () Can scat analysis describe the feeding habits of big cats? A Brazil. Journal of Mammalogy, , –. case study with jaguars (Panthera onca) in the Southern Pantanal, C AVA L C A N T I , S.M.C. & G E S E , E.M. () Kill rates and predation Brazil. PLOS ONE, , e. patterns of jaguars (Panthera onca) in the southern Pantanal, Brazil. R C O R E T E A M () R: A language and environment for statistical Journal of Mammalogy, , –. computing. R Foundation for Statistical Computing, Vienna, C H E Y N E , S.M. () Wildlife reintroduction: considerations of Austria. R-project.org [accessed July ]. habitat quality at the release site. BMC Ecology, , . R A B I N OW I T Z , A. & N OT T I N G H A M , B.G. () Ecology and behavior C R AW S H AW , P.G. & Q U I G L E Y , H.B. () Jaguar spacing, activity and of the jaguar (Panthera onca) in Belize. Journal of Zoology, habitat use in a seasonally flooded environment in Brazil. Journal , –. of Zoology, , –. R A M P I M , L.E, S A R T O R E L LO , L.R., F R A G O S O , C.E., H A B E R F E L D , M. & D E L A T O R R E , J.A., G O N Z Á L E Z -M AYA , J.F., Z A R Z A , H. & C E B A L LO S , D E V L I N , A.L. () Antagonistic interactions between predator G. () The jaguar’s spots are darker than they appear: assessing and prey: mobbing of jaguars by white-lipped peccaries. the global conservation status of the jaguar Panthera onca. Acta Ethologica, , –. Oryx, , –. R I B E I R O , M.C., M E T Z G E R , J.P., M A R T E N S E N , A.C., P O N Z O N I , F.J. & D E P A U L A , R.C., C AVA L C A N T I , S.M.C. & M O R A T O , R.G. () Plano H I R O TA , M.M. () The Atlantic Rainforest: how much is left, de Ação para a Conservação da Onça Pintada. Instituto Chico and how is the remaining forest distributed? Implications for Mendes de Conservação da Biodiversidade, Brasília, Brazil. conservation. Biological Conservation, , –. F L E M I N G , C..H., F A G A N , W.F., M U E L L E R , T., O L S O N , K.A., S O I S A LO , M.K. & C AVA L C A N T I , S.M.C. (). Estimating the density L E I M G R U B E R , P. & C A L A B R E S E , J.M. () Rigorous home range of a jaguar population in the Brazilian Pantanal using camera-traps estimation with movement data: a new autocorrelated kernel density and capture-recapture sampling in combination with GPS estimator. Ecology, , –. radio-telemetry. Biological Conservation, , –. Oryx, 2021, 55(3), 461–465 © The Author(s), 2021. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605320000460 Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 20 May 2021 at 06:03:48, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms . https://doi.org/10.1017/S0030605320000460
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