Speed of extirpation of the huemul in the history of human occupation in Patagonia
Melina E. Zuliani
A * , Jo Anne M. Smith-Flueck B C , Werner T. Flueck C D E and Adrian J. Monjeau A D
A Departamento de Análisis de Sistemas Complejos, Fundación Bariloche, Bariloche 8400, Argentina.
B Laboratorio de Teriogenología ‘Dr Héctor H. Morello’, Facultad de Ciencias Agrarias, Universidad Nacional del Comahue, Cinco Saltos 8303, Argentina.
C Fundación Shoonem, Parque Protegido Shoonem, Alto RíoSenguer 9033, Argentina.
D National Council of Scientific and Technological Research (CONICET), Buenos Aires 1425, Argentina.
E Swiss Tropical and Public Health Institute, University of Basel, Basel 4001, Switzerland.
Animal Production Science 63(16) 1697-1704 https://doi.org/10.1071/AN23048
Submitted: 7 February 2023 Accepted: 15 June 2023 Published: 17 July 2023
Abstract
The Patagonian huemul, an endangered Odocoilinedeer, has an estimated 350–500 individuals remaining in Argentina. Today’s population size, representing a numerical reduction of >99% of original estimates, is fragmented into small groups along ~2000 km of Andean mountains. The species’ numbers were heavily reduced by past overexploitation and they disappeared in areas of high anthropogenic activity, predominantly the fertile valley bottoms.
This research delineates the current potential distribution of Patagonian huemul by using climatic indicators, topographic and vegetational proxies, and anthropogenic pressure, to determine the relevance of the climatic envelope on current distribution.
Occurrence records (latitude and longitude) were compiled (n = 159) by consulting the literature. Twenty environmental variables were used (WorldClim database) and two other representative environmental variables (normalised difference vegetation index (NDVI) and enhanced vegetation index (EVI)) were added to test their predictive power. We added the human footprint index (HFP) as a variable to control for model bias. Using the maximum entropy algorithm (MaxEnt), we modelled the species’ potential distribution. We designated the historical distribution as area M. Additionally, we calculated three areas of distribution: current, historical and potential. Finally, we calculated distributional retraction of the species and area lost per year.
The model showed good predictive power (AUCTest = 0.764 ± 0.091). However, low values were obtained for AUCtrain and AUCprom for the different predictor scenarios. Although the model shows the interaction among several climatic, environmental, and topographic variables, the human footprint index (39.9%) was the variable that most influenced the current potential distribution of this species.
Our model shows that most of Patagonia’s surface is climatically suitable for huemul. This suggests that the causes of distributional retraction are not related to limitations imposed by the climate envelope, but rather concur with recent research showing impact owing to the species’ behavioural response to anthropogenic activity.
Current populations are small, fragmented, and confined to poor-quality sites. Although the species is currently found mainly within protected areas, management actions must be initiated that promote innovative strategies in unprotected areas, as well as high-value habitats, particularly as protected areas contain limited fertile lower-valley habitats.
Keywords: climate envelope, conservation, distribution model, endangered species, historical distribution, Patagonian huemul, potential distribution, retraction.
References
Anderson RP, Martínez-Meyer E (2004) Modeling species’ geographic distributions for preliminary conservation assessments: an implementation with the spiny pocket mice (Heteromys) of Ecuador. Biological Conservation 116(2), 167-179.
| Crossref | Google Scholar |
Barve N, Barve V, Jiménez-Valverde A, Lira-Noriega A, Maher SP, Peterson AT, Soberón J, Villalobos F (2011) The crucial role of the accessible area in ecological niche modeling and species distribution modeling. Ecological Modelling 222(11), 1810-1819.
| Crossref | Google Scholar |
Bessera EM (2006) La Colonia Nahuel Huapi y los origenes de la actividad turistica en la region Andino-Patagonica. In ‘Trabajo presentado en “Historia de la Patagonia. 2das Jornadas” (CD-ROM).’ (Universidad Nacional del Comahue: Neuquén, Argentina) Recuperado de http://www.hechohistorico.com.ar/Trabajos/Jornadas%20de%20Roca%20-%202006/Bessera.pdf
Brown JH (1995) Macroecology. Journal of Mammalogy 78(1), 257-260.
| Crossref | Google Scholar |
Bunin JS, Jamieson IG (1995) New approaches toward a better understanding of the decline of Takahe (Porphyrio mantelli) in New Zealand. Conservation Biology 9(1), 100-106.
| Crossref | Google Scholar |
Channell R, Lomolino MV (2000) Dynamic biogeography and conservation of endangered species. Nature 403(6765), 84-86.
| Crossref | Google Scholar |
Chauvenet ALM, Barnes M (2016) Expanding protected areas is not enough. Science 353(6299), 551-552.
| Crossref | Google Scholar |
Curran SC (2015) Exploring Eucladoceros ecomorphology using geometric morphometrics. Anatomical Record 298(1), 291-313.
| Crossref | Google Scholar |
Dormann CF, Schymanski SJ, Cabral J, Chuine I, Graham C, Hartig F, Kearney M, Morin X, Römermann C, Schröder B, Singer A (2012) Correlation and process in species distribution models: bridging a dichotomy. Journal of Biogeography 39(12), 2119-2131.
| Crossref | Google Scholar |
Elith J, Leathwick JR (2009) Species distribution models: ecological explanation and prediction across space and time. Annual Review of Ecology, Evolution, and Systematics 40, 677-697.
| Crossref | Google Scholar |
Elith J, Graham CH, Anderson RP, Dudík M, Ferrier S, Guisan A, Hijmans RJ, Huettmann F, Leathwick JR, Lehmann A, Li J, Lohmann LG, Loiselle BA, Manion G, Moritz C, Nakamura M, Nakazawa N, Overton JMM, Peterson AT, Phillips SJ, Richardson K, Scachetti-Pereira R, Schapire RE, Soberón J, Williams S, Wisz MS, Zimmermann NE (2006) Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29(2), 129-151.
| Crossref | Google Scholar |
Escobar LE, Lira-Noriega A, Medina-Vogel G, Townsend Peterson A (2014) Potential for spread of the white-nose fungus (Pseudogymnoascus destructans) in the Americas: use of Maxent and NicheA to assure strict model transference. Geospatial Health 9(1), 221-229.
| Crossref | Google Scholar |
Flueck WT, Smith-Flueck JAM (2011a) Recent advances in the nutritional ecology of the Patagonian huemul: implications for recovery. Animal Production Science 51(4), 311-326.
| Crossref | Google Scholar |
Flueck WT, Smith-Flueck JA (2011b) Osteological comparisons of appendicular skeletons: a case study on Patagonian huemul deer and its implications for conservation. Animal Production Science 51(4), 327-339.
| Crossref | Google Scholar |
Flueck WT, Smith-Flueck JAM (2012) Huemul heresies: beliefs in search of supporting data. 1. Historical and zooarcheological considerations. Animal Production Science 52(8), 685-693.
| Crossref | Google Scholar |
Flueck W, Smith-Flueck J, Escobar M, Zuliani M, Fuchs B, Geist V, Heffelfinger J, Black-Decima P, Gizejewski Z, Vidal F, Barrio J, Molinuevo S, Monjeau A, Hoby S, Jiménez J (2022) Loss of migratory traditions makes the endangered Patagonian Huemul deer a year-round refugee in its summer habitat. Conservation 2(2), 322-348.
| Crossref | Google Scholar |
González B, Brook F, Martin GM (2021) Distribución y conservación de las especies de Marmosini (Didelphimorphia, Didelphidae) de Colombia. PREPRINT (Versión 1) disponible en Research Square.
| Crossref | Google Scholar |
Gutiérrez EE, Boria RA, Anderson RP (2014) Can biotic interactions cause allopatry? Niche models, competition, and distributions of South American mouse opossums. Ecography 37(8), 741-753.
| Crossref | Google Scholar |
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25(15), 1965-1978.
| Crossref | Google Scholar |
Huemul Task Force (HTF) (2012) Reassessment of morphology and historical distribution as factors in conservation efforts for the Endangered Patagonian Huemul Deer Hippocamelus bisulcus (Molina 1782). Journal of Threatened Taxa 4(14), 3302-3311.
| Crossref | Google Scholar |
Kuemmerle T, Radeloff VC, Perzanowski K, Kozlo P, Sipko T, Khoyetskyy P, Bashta A-T, Chikurova E, Parnikoza I, Baskin L, Angelstam P, Waller DM (2011) Predicting potential European bison habitat across its former range. Ecological Applications 21(3), 830-843.
| Crossref | Google Scholar |
Laliberte AS, Ripple WJ (2004) Range contractions of North American carnivores and ungulates. BioScience 54(2), 123-138.
| Crossref | Google Scholar |
Leon RJC, Bran D, Collantes M, Paruelo JM, Soriano A (1998) Grandes unidades de vegetacion de la Patagonia extra andina. Ecologia Austral 8(2), 125-144.
| Google Scholar |
Loiselle BA, Howell CA, Graham CH, Goerck JM, Brooks T, Smith KG, Williams PH (2003) Avoiding pitfalls of using species distribution models in conservation planning. Conservation Biology 17(6), 1591-1600.
| Crossref | Google Scholar |
Lütolf M, Kienast F, Guisan A (2006) The ghost of past species occurrence: improving species distribution models for presence-only data. Journal of Applied Ecology 43(4), 802-815.
| Crossref | Google Scholar |
Merow C, Smith MJ, Silander JA, Jr (2013) A practical guide to MaxEnt for modeling species’ distributions: what it does, and why inputs and settings matter. Ecography 36(10), 1058-1069.
| Crossref | Google Scholar |
Mills JA, Lavers RB, Lee WG (1984) The takahe – a relict of the Pleistocene grassland avifauna of New Zealand. New Zealand Journal of Ecology 7, 57-70.
| Google Scholar |
Muscarella R, Galante PJ, Soley-Guardia M, Boria RA, Kass JM, Uriarte M, Anderson RP (2014) ENMeval: an R package for conducting spatially independent evaluations and estimating optimal model complexity for Maxent ecological niche models. Methods in Ecology and Evolution 5(11), 1198-1205.
| Crossref | Google Scholar |
Nuñez-Penichet C, Cobos Cobos ME, Amaro JG, Cañamero AB (2016) Distribución potencial del género Omphalea (Euphorbiaceae) en Cuba: aproximación a su distribución real/potential distribution of the genus Omphalea (Euphorbiaceae) in Cuba: approach to its actual distribution. Revista del Jardín Botánico Nacional 37, 165-175 Available at tinyurl.com/2r2565wz.
| Google Scholar |
Onelli C (1905) El huemul. Su patria: Su vida. Revista del Jardín Zoológico de Buenos Aires [1] 370-374.
| Google Scholar |
Pardiñas UFJ, Teta P, Cirignoli S, Podesta DH (2003) Micromamíferos (Didelphimorphia y Rodentia) de Norpatagonia extra andina, Argentina: taxonomía alfa y biogeografía. Mastozoología Neotropical 10(1), 69-113.
| Google Scholar |
Paruelo JM, Beltran A, Jobbagy E, Sala OE, Golluscio RA (1998) The climate of Patagonia: general patterns and controls on biotic processes. Ecologia Austral 8(2), 85-101.
| Google Scholar |
Pastore H, Aprile G (2019) Hippocamelus bisulcus. In ‘Categorización 2019 de los mamíferos de Argentina según su riesgo de extinción. Lista Roja de los mamíferos de Argentina’. (Ed. SAyDS–SAREM) Versión digital http://cma.sarem.org.ar
Patton JL, Pardiñas UFJ, D’Elía G (2015) ‘Mammals of South America. Vol. 2.’ (University of Chicago Press) doi:10.7208/chicago/9780226169606.001.0001
Pearson RG, Dawson TP (2003) Predicting the impacts of climate change on the distribution of species: are bioclimate envelope models useful? Global Ecology and Biogeography 12(5), 361-371.
| Crossref | Google Scholar |
Phillips SJ, Dudík M, Schapire RE (2004) A maximum entropy approach to species distribution modeling. In ‘ICML’04 Proceedings of the 21st International Conference on Machine Learning’. pp. 655–662. (ACM Press: New York) doi:10.1145/1015330.1015412
Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecological Modelling 190, 231-259.
| Crossref | Google Scholar |
Pulliam HR (2000) On the relationship between niche and distribution. Ecology Letters 3(4), 349-361.
| Crossref | Google Scholar |
Quevedo P, von Hardenberg A, Pastore H, Álvarez J, Corti P (2017) Predicting the potential distribution of the Endangered huemul deer Hippocamelus bisulcus in North Patagonia. Oryx 51(2), 315-323.
| Crossref | Google Scholar |
Rapoport EH (1982) ‘Aerography: geographical strategies of species.’ (Pergamon Press). doi:10.2307/2844626
Riquelme C, Estay SA, López R, Pastore H, Soto-Gamboa M, Corti P (2018) Protected areas’ effectiveness under climate change: a latitudinal distribution projection of an endangered mountain ungulate along the Andes Range. PeerJ 6, e5222.
| Crossref | Google Scholar |
Rosas YM, Peri PL, Huertas Herrera A, Pastore H, Martínez Pastur G (2017) Modeling of potential habitat suitability of Hippocamelus bisulcus: effectiveness of a protected areas network in Southern Patagonia. Ecological Processes 6, 1-14.
| Google Scholar |
Ruiz Barlett T, Martin GM, Laguna MF, Abramson G, Monjeau A (2019) Climatic constraints and the distribution of Patagonian mice. Journal of Mammalogy 100(6), 1979-1991.
| Crossref | Google Scholar |
Sanderson EW, Jaiteh M, Levy MA, Redford KH, Wannebo AV, Woolmer G (2002) The Human Footprint and the Last of the Wild: the human footprint is a global map of human influence on the land surface, which suggests that human beings are stewards of nature, whether we like it or not. BioScience 52, 891-904.
| Crossref | Google Scholar |
Sepúlveda C, Moreira A, Villarroel P (1997) Conservación biológica fuera de las áreas silvestres protegidas. Ambiente y Desarrollo 13(2), 48-58.
| Google Scholar |
Smith-Flueck JM, Barrio J, Ferreyra N, Núñez A, Tomas N, Guzman J, Flueck WT, Hinojosa A, Vidal F, Garay G, Jimenez J (2011) Advances in ecology and conservation of Hippocamelus species in South America. Animal Production Science 51, 378-383.
| Crossref | Google Scholar |
Smith-Flueck JM, Gill R, Flueck WT (In press) Huemul Hippocamelus bisulcus (Molina 1782). Chapter 39. In ‘Deer of the world. Ecology, conservation and management’. (Eds M Melletti, S Focardi) (Springer) Available at https://link.springer.com/book/9783031177552
Soberon J, Peterson AT (2005) Interpretation of models of fundamental ecological Niches and Species’ distributional areas. Biodiversity Informatics 2, 1-10.
| Crossref | Google Scholar |
Vila AR, Lopez R, Pastore H, Faundez R, Serret A (2006) Current distribution and conservation of the huemul (Hippocamelus bisulcus) in Argentina and Chile. Mastozoologia Neotropical 13, 263-269.
| Google Scholar |
Warren DL, Seifert SN (2011) Ecological niche modeling in Maxent: the importance of model complexity and the performance of model selection criteria. Ecological Applications 21(2), 335-342.
| Crossref | Google Scholar |
Wintle BA, Kavanagh RP, McCarthy MA, Burgman MA (2005) Estimating and dealing with detectability in occupancy surveys for forest owls and arboreal marsupials. Journal of Wildlife Management 69(3), 905-917.
| Crossref | Google Scholar |
Wisz MS, Hijmans RJ, Li J, Peterson AT, Graham CH, Guisan A, NCEAS Predicting Species Distributions Working Group (2008) Effects of sample size on the performance of species distribution models. Diversity and Distributions 14(5), 763-773.
| Crossref | Google Scholar |
Zuliani ME, Monjeau A (2021) Modelos de distribución potencial de mamíferos nativos en la Patagonia. Ecología Austral 32(1), 019-032.
| Crossref | Google Scholar |
