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Assessing landscape connectivity for South-Central Argentine pumas dispersing under genetic source-sink dynamics

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Abstract

Context

Identification of areas with high connectivity is crucial for large carnivores’ management and conservation, especially where landscape has been modified by human activities. Partially under legal hunting control, south-central Argentine pumas (Puma concolor) have been described to be structured into two distinct groups with an inverse correlation between gene flow and hunting pressure.

Objectives

To further assess puma genetic structure and test whether isolation-by-distance and/or isolation-by-resistance could explain the previously reported putative correlation between gene flow and hunting pressure.

Methods

We explored spatial segregation of pumas by testing for hierarchical structure within previously identified clusters, genetic differentiation among sampling regions, and isolation-by-distance among individuals. Using a land cover resistance-based approach, we assessed landscape influence on puma connectivity to analyze landscape permeability between sampling sites.

Results

Our study added a third genetic group to the previously identified clusters, reporting significant genetic differentiation among sampling regions. We also observed a significant correlation among geographic and genetic distances, supporting genetic structure and gene flow pattern of connectivity. We identified a continuous high current flow across the landscape where shrublands are the primary habitat, whereas landscape permeability declined as grassland cover increases.

Conclusions

Genetic structure and gene flow among south-central Argentine pumas can be partially related to the landscape connectivity pattern observed in the area. These results are extremely important for puma conservation in the area because the identification of high-permeability linkage zones can now be used to gather ecological fine-scale data to support more appropriate conservation strategies, aiming to preserve important dispersal areas for this apex predator.

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References

  • Anderson CR, Lindzey FG (2005) Experimental evaluation of population trend and harvest composition in a Wyoming cougar population. Wildl Soc Bull 33:179–188

    Article  Google Scholar 

  • Anderson CR, Lindzey FG, McDonald DB (2004) Genetic Structure of Cougar Populations Across the Wyoming Basin: Metapopulation or Megapopulation. J Mammal 85:1207–1214

    Article  Google Scholar 

  • Andreasen AM, Stewart KM, Longland WS et al (2012) Identification of source-sink dynamics in mountain lions of the Great Basin. Mol Ecol 21:5689–5701

    Article  PubMed  Google Scholar 

  • De Angelo C, Llanos R, Guerisoli M de las M, et al (2019) Puma concolor. In: Categ. 2019 los mamíferos Argentina según su riesgo extinción. https://cma.sarem.org.ar/es/especie-nativa/puma-concolor. Accessed 4 Jul 2020

  • Balasubramaniam KN, Bliss-Moreau E, Beisner BA et al (2021) Addressing the challenges of research on human-wildlife interactions using the concept of coupled natural & human systems. Biol Conserv 257:109095

    Article  Google Scholar 

  • Baldi R, Novaro A, Funes M et al (2010) Guanaco management in Patagonian rangelands: a conservation opportunity on the brink of collapse. In: Du Toit J, Kock R, Deutsch J (eds) Conserving Wildlife while Maintaining Livestock in Semi-Arid Ecosystems. Blackwell Publishing, Oxford, pp 266–290

    Chapter  Google Scholar 

  • Balkenhol N, Holbrook JD, Onorato D et al (2014) A multi-method approach for analyzing hierarchical genetic structures: a case study with cougars Puma concolor. Ecography 37:552–563

    Article  Google Scholar 

  • Blecha KA, Boone RB, Alldredge MW (2018) Hunger mediates apex predator’s risk avoidance response in wildland–urban interface. J Anim Ecol 87:609–622

    Article  PubMed  Google Scholar 

  • Brown A, Martinez Ortiz U, Acerbi M, Corcuera J (eds) (2006) La Situación Ambiental Argentina 2005. Fundación Vida Silvestre Argentina, Buenos Aires

  • Castilho CS, Marins-Sá LG, Benedet RC, Freitas TO (2011) Landscape genetics of mountain lions (Puma concolor) in southern Brazil. Mamm Biol 76:476–483

    Article  Google Scholar 

  • Castilho CS, Marins-Sá LG, Benedet RC, Freitas TRO (2012) Genetic structure and conservation of mountain lions in the South-Brazilian Atlantic Rain Forest. Genet Mol Biol 35:65–73

    Article  Google Scholar 

  • Creel S, Rotella JJ (2010) Meta-analysis of relationships between human offtake, total mortality and population dynamics of gray wolves (Canis lupus). PLoS ONE 5:e12918

    Article  PubMed  PubMed Central  Google Scholar 

  • Crooks KR, Burdett CL, Theobald DM et al (2011) Global patterns of fragmentation and connectivity of mammalian carnivore habitat. Philos Trans R Soc B Biol Sci 366:2642–2651

    Article  Google Scholar 

  • Cushman SA, Mckelvey KS, Hayden J, Schwartz MK (2006) Gene flow in complex landscapes: testing multiple hypotheses with causal modeling. Am Nat 168:486–499

    Article  PubMed  Google Scholar 

  • Del Valle HF, Elissalde NO, Gagliardini DA, Milovich J (1998) Status of desertification in the Patagonian region: assessment and mapping from satellite imagery. Arid Soil Res Rehabil 12:95–121

    Google Scholar 

  • Delibes M, Gaona P, Ferreras P (2001) Effects of an attractive sink leading into maladaptive habitat selection. Am Nat 158:277–285

    Article  CAS  PubMed  Google Scholar 

  • Dickson BG, Jenness JS, Beier P (2005) Influence of vegetation, topography, and roads on cougar movement in Southern California. J Wildl Manage 69:264–276

    Article  Google Scholar 

  • Dickson BG, Roemer GW, McRae BH, Rundall JM (2013) Models of regional habitat quality and connectivity for pumas (Puma concolor) in the Southwestern United States. PLoS ONE. https://doi.org/10.1371/journal.pone.0081898

    Article  PubMed  PubMed Central  Google Scholar 

  • Dolrenry S, Stenglein J, Hazzah L et al (2014) A metapopulation approach to African lion (Panthera leo) conservation. PLoS ONE 9:e88081

    Article  PubMed  PubMed Central  Google Scholar 

  • Earl DA, vonHoldt BM (2012) Structure harvester: a website and program for visualizing structure output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Elbroch L, Wittmer H (2012) Puma spatial ecology in open habitats with aggregate prey. Mamm Biol 77:377–384

    Article  Google Scholar 

  • Elbroch M, Wittmer HU, Saucedo C, Corti P (2009) Long-distance dispersal of a male puma (Puma concolor puma) in Patagonia. Rev Chil Hist Nat 82:459–461

    Article  Google Scholar 

  • Ernest HB, Boyce WM, Bleich VC et al (2003) Genetic structure of mountain lion (Puma concolor) populations in California. Conserv Genet 4:353–366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ernest HB, Vickers TW, Morrison SA et al (2014) Fractured genetic connectivity threatens a Southern California puma (Puma concolor) population. PLoS ONE. https://doi.org/10.1371/journal.pone.0107985

    Article  PubMed  PubMed Central  Google Scholar 

  • Fahrig L, Merriam G (1994) Conservation of fragmented populations. Conserv Biol 8:50–59

    Article  Google Scholar 

  • Frankham R (2006) Genetics and landscape connectivity. In: Crooks KR, Sanjayan M (eds) Connectivity conservation. Cambridge University Press, Cambridge, pp 72–96

    Chapter  Google Scholar 

  • Frantz AC, Cellina S, Krier A et al (2009) Using spatial Bayesian methods to determine the genetic structure of a continuously distributed population: clusters or isolation by distance? J Appl Ecol 46:493–505

    Article  Google Scholar 

  • Gallo O, Castillo DF, Godinho R, Casanave EB (2020) Genetic diversity, population structure, and immigration, in a partially hunted puma population of south-central Argentina. J Mammal 101:766–778

    Article  Google Scholar 

  • Golluscio RA, Deregibus VA, Paruelo JM (1998) Sustainability and range management in the Patagonian steppes. Ecol Austral 8:265–284

    Google Scholar 

  • Guillot G, Mortier F, Estoup A (2005) Geneland: a computer package for landscape genetics. Mol Ecol Notes 5:712–715

    Article  CAS  Google Scholar 

  • Guillot G, Renaud S, Ledevin R et al (2012) A Unifying Model for the Analysis of Phenotypic, Genetic, and Geographic Data. Syst Biol 61:897–911

    Article  PubMed  Google Scholar 

  • Gustafson KD, Vickers TW, Boyce WM, Ernest HB (2017) A single migrant enhances the genetic diversity of an inbred puma population. R Soc Open Sci. https://doi.org/10.1098/rsos.170115

    Article  PubMed  PubMed Central  Google Scholar 

  • Gustafson KD, Gagne RB, Vickers TW et al (2019) Genetic source–sink dynamics among naturally structured and anthropogenically fragmented puma populations. Conserv Genet 20:215–227

    Article  Google Scholar 

  • Hawley JE, Rego PW, Wydeven AP et al (2016) Long-distance dispersal of a subadult male cougar from South Dakota to Connecticut documented with DNA evidence. J Mammal 97:1435–1440

    Article  Google Scholar 

  • Holmes BR, Laundré JW (2006) Use of open, edge and forest areas by pumas Puma concolor in winter: are pumas foraging optimally? Wildlife Biol 12:201–209

    Article  Google Scholar 

  • Jackson VL, Laack LL, Zimmerman EG (2005) Landscape metrics associated with habitat use by ocelots in South Texas. J Wildl Manage 69:733–738

    Article  Google Scholar 

  • Johnson JA, Bellinger MR, Toepfer JE, Dunn P (2004) Temporal changes in allele frequencies and low effective population size in greater prairie-chickens. Mol Ecol 13:2617–2630

    Article  CAS  PubMed  Google Scholar 

  • Jombart T (2008) Adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    Article  CAS  PubMed  Google Scholar 

  • Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet. https://doi.org/10.1186/1471-2156-11-94

    Article  PubMed  PubMed Central  Google Scholar 

  • Jorge MLSP, Galetti M, Ribeiro MC, Ferraz KMPMB (2013) Mammal defaunation as surrogate of trophic cascades in a biodiversity hotspot. Biol Conserv 163:49–57

    Article  Google Scholar 

  • LaRue MA, Nielsen CK (2008) Modelling potential dispersal corridors for cougars in midwestern North America using least-cost path methods. Ecol Modell 212:372–381

    Article  Google Scholar 

  • LaRue MA (2007) Predicting potential habitat and dispersal corridors for cougars in midwestern North America. Southern Illinois University, Carbondale, Illinois, USA

  • Llanos R, Travaini A, Montanelli S, Crespo E (2014) Estructura de edades de pumas (Puma concolor) cazados bajo el sistema de remoción por recompensas en patagonia. ¿Selectividad u oportunismo en la captura? Ecol Austral 24:311–319

    Article  Google Scholar 

  • Logan KA, Sweanor LL (2001) Desert Puma: Evolutionary Ecology and Conservation of an Enduring Carnivore. Island Press, Washington DC

    Google Scholar 

  • Lorenzana G, Heidtmann L, Haag T et al (2020) Large-scale assessment of genetic diversity and population connectivity of Amazonian jaguars (Panthera onca) provides a baseline for their conservation and monitoring in fragmented landscapes. Biol Conserv 242:108417

    Article  Google Scholar 

  • Loxterman JL (2011) Fine scale population genetic structure of pumas in the Intermountain West. Conserv Genet 12:1049–1059

    Article  Google Scholar 

  • Luque S, Saura S, Fortin MJ (2012) Landscape connectivity analysis for conservation: Insights from combining new methods with ecological and genetic data. Landsc Ecol 27:153–157

    Article  Google Scholar 

  • Lynch M, Ritland K (1999) Estimation of pairwise relatedness with molecular markers. Genetics 152:1753–1766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McRae BH (2006) Isolation by resistance. Evolution 60:1551–1561

    PubMed  Google Scholar 

  • McRae BH, Beier P (2007) Circuit theory predicts gene flow in plant and animal populations. Proc Natl Acad Sci U S A 104:19885–19890

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McRae BH, Beier P, Dewald LE et al (2005) Habitat barriers limit gene flow and illuminate historical events in a wide-ranging carnivore, the American puma. Mol Ecol 14:1965–1977

    Article  CAS  PubMed  Google Scholar 

  • McRae BH, Dickson BG, Keitt TH et al (2008) Using circuit theory to model connectivity in ecology, evolution, and conservation. Ecology 89:2712–2724

    Article  PubMed  Google Scholar 

  • McRae BH, Shah VB, Mohapatra TK (2013) Circuitscape 4 User Guide. The Nature Conservancy. https://circuitscape.org/docs/. Accessed 4 Jul 2020

  • Meirmans PG (2012) The trouble with isolation by distance. Mol Ecol 21:2839–2846

    Article  PubMed  Google Scholar 

  • Miotto RA, Cervini M, Figueiredo MG et al (2011) Genetic diversity and population structure of pumas (Puma concolor) in southeastern Brazil: implications for conservation in a human-dominated landscape. Conserv Genet 12:1447–1455

    Article  Google Scholar 

  • Morrison CD, Boyce MS, Nielsen SE (2015) Space-use, movement and dispersal of sub-adult cougars in a geographically isolated population. PeerJ 2015:e1118

    Article  Google Scholar 

  • Naude VN, Balme GA, O’Riain J et al (2020) Unsustainable anthropogenic mortality disrupts natal dispersal and promotes inbreeding in leopards. Ecol Evol 10:3605–3619

    Article  PubMed  PubMed Central  Google Scholar 

  • Nei M (1977) F-statistics and analysis of gene diversity in subdivided populations. Ann Hum Genet 41:225–233

    Article  CAS  PubMed  Google Scholar 

  • Newby JR, Scott Mills L, Ruth TK et al (2013) Human-caused mortality influences spatial population dynamics: pumas in landscapes with varying mortality risks. Biol Conserv 159:230–239

    Article  Google Scholar 

  • Nielsen C, Thompson D, Kelly M, Lopez-Gonzalez CA (2015) Puma concolor (errata version published in 2016). IUCN Red List Threat Species. https://doi.org/10.2305/IUCN.UK.2015-4.RLTS.T18868A50663436.en

    Article  Google Scholar 

  • Oliva G, Paredes P, Ferrante D et al (2019) Remotely sensed primary productivity shows that domestic and native herbivores combined are overgrazing Patagonia. J Appl Ecol 56:1575–1584

    Article  Google Scholar 

  • Oyarzabal M, Clavijo J, Oakley L et al (2018) Unidades de vegetación de la Argentina. Ecol Austral 28:040–063

    Article  Google Scholar 

  • Packer C, Kosmala M, Cooley HS et al (2009) Sport hunting, predator control and conservation of large carnivores. PLoS ONE 4:e5941

    Article  PubMed  PubMed Central  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinforma Appl 28:2537–2539

    Article  CAS  Google Scholar 

  • Perez MF, Franco FF, Bombonato JR et al (2018) Assessing population structure in the face of isolation by distance: are we neglecting the problem? Divers Distrib 24:1883–1889

    Article  Google Scholar 

  • Peri PL, Lencinas MV, Bousson J et al (2016) Biodiversity and ecological long-term plots in Southern Patagonia to support sustainable land management: the case of PEBANPA network. J Nat Conserv 34:51–64

    Article  Google Scholar 

  • Peterman WE (2018) ResistanceGA: An R package for the optimization of resistance surfaces using genetic algorithms. Methods Ecol Evol 9:1638–1647

    Article  Google Scholar 

  • Porini G, Ramadori D (2007) Knowledge estate about foxes management of economic interest in Argentine. Dirección Nacional de Fauna Silvestre, Buenos Aires

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rambaut A, Drummond AJ (2005) Tracer. MCMC trace analysis tool. https://beast.community/tracer. Accessed 27 Mar 2020

  • Reddy PA, Puyravaud JP, Cushman SA, Segu H (2019) Spatial variation in the response of tiger gene flow to landscape features and limiting factors. Anim Conserv 22:472–480

    Article  Google Scholar 

  • Riley SPD, Pollinger JP, Sauvajot RM et al (2006) FAST-TRACK: A southern California freeway is a physical and social barrier to gene flow in carnivores. Mol Ecol 15:1733–1741

    Article  CAS  PubMed  Google Scholar 

  • Robinson HS, Wielgus RB, Cooley HS, Cooley SW (2008) Sink populations in carnivore management: cougar demography and immigration in a hunted population. Ecol Appl 18:1028–1037

    Article  PubMed  Google Scholar 

  • Roques S, Sollman R, Jácomo A et al (2015) (2016) Effects of habitat deterioration on the population genetics and conservation of the jaguar. Conserv Genet 171(17):125–139

    Google Scholar 

  • Sergio F, Newton I, Marchesi L, Pedrini P (2006) Ecologically justified charisma: preservation of top predators delivers biodiversity conservation. J Appl Ecol 43:1049–1055

    Article  Google Scholar 

  • Stoner DC, Rieth WR, Wolfe ML et al (2008) Long-distance dispersal of a female cougar in a basin and range landscape. J Wildl Manage 72:933–939

    Article  Google Scholar 

  • Sweanor LL, Logan KA, Hornocker MG (2000) Cougar dispersal patterns, metapopulation dynamics, and conservation. Conserv Biol 14:798–808

    Article  Google Scholar 

  • Taylor PD, Fahrig L, Henein K, Merriam G (1993) Taylor, P. D.; Fahrig, L.; Henein, K.; Merriam, G. Connectivity is a vital element of landscape structure. Oikos 68:571–573

    Article  Google Scholar 

  • Trumbo DR, Salerno PE, Logan KA et al (2019) Urbanization impacts apex predator gene flow but not genetic diversity across an urban-rural divide. Mol Ecol 28:4926–4940

    Article  CAS  PubMed  Google Scholar 

  • Warren MJ, Wallin DO, Beausoleil RA, Warheit KI (2016) Forest cover mediates genetic connectivity of northwestern cougars. Conserv Genet 17:1011–1024

    Article  Google Scholar 

  • Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genet 163:1177–1191. https://doi.org/10.1093/genetics/163.3.1177

  • Wultsch C, Waits LP, Kelly MJ (2016) A Comparative Analysis of Genetic Diversity and Structure in Jaguars (Panthera onca), Pumas (Puma concolor), and Ocelots (Leopardus pardalis) in Fragmented Landscapes of a Critical Mesoamerican Linkage Zone. PLoS ONE 11:1–30

    Article  Google Scholar 

  • Zemanova MA, Perotto-Baldivieso HL, Dickins EL et al (2017) Impact of deforestation on habitat connectivity thresholds for large carnivores in tropical forests. Ecol Process 6:1–11

    Article  Google Scholar 

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Acknowledgements

The Dirección de Fauna y Flora Silvestre of Buenos Aires and Chubut provinces, and the Secretaría de Ambiente y Desarrollo Sustentable of Río Negro province provided sample collection permits. The authors thank Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, “La Plata” Museum, M. Guerisoli, R. Llanos, A. Andrade, R. D’Agostino, D. Udrizar Sauthier, and M. Faillá for contributing to sample collection for this study. We thank J. Campos for assistance with Ciscuitscape v4.0.

Funding

Fundings were provided by: The Wild Felid Research & Management Association (Wild Felid Legacy Scholarship, 2016), Conservation, Research and Education Opportunities International (2014), Agencia Nacional de Promoción Científica y Tecnológica (PICT 2283/2015), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET; PIP11220130100060CO01), Secretaría General de Ciencia y Tecnología—Universidad Nacional del Sur (PGI24/B234), Centro de Investigação em Biodiversidade e Recursos Genéticos (CIBIO/InBIO) through private funds, and Sociedad Argentina para el Estudio de los Mamíferos (SAREM). OG, DFC, and EBC were supported by CONICET; RG was supported by the Portuguese Foundation for Science and Technology (DL57/2016/CP1440/CT[SFRH/BPD/88496/2012]).

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OG: Software, formal analysis, writing—original draft, methodology. OG, DC, RG: data curation. DC, RG: validation. OG, DC, EC, EBC: project administration. DC, RG, EC: supervision. OG, DC, RG, EC: conceptualization, resources, funding acquisition, and writing—review & editing.

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Correspondence to Orlando Gallo.

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Gallo, O., Castillo, D.F., Godinho, R. et al. Assessing landscape connectivity for South-Central Argentine pumas dispersing under genetic source-sink dynamics. Landsc Ecol 38, 999–1012 (2023). https://doi.org/10.1007/s10980-022-01585-8

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