Osteological comparisons of appendicular skeletons: a case study on Patagonian huemul deer and its implications for conservation
Werner T. Flueck A B C and Jo M. Smith-Flueck BA National Council of Scientific and Technological Research (CONICET), Buenos Aires; Swiss Tropical Institute, University Basel; DeerLab, C.C. 592, 8400 Bariloche, Argentina.
B Institute of Natural Resources Analysis – Patagonia, Universidad Atlantida Argentina, C.C. 592, 8400 Bariloche, Argentina.
C Corresponding author. Email: wtf@deerlab.org
Animal Production Science 51(4) 327-339 https://doi.org/10.1071/AN10174
Submitted: 10 September 2010 Accepted: 15 October 2010 Published: 8 April 2011
Abstract
Early explorers described huemul (Hippocamelus bisulcus) as stocky, massive and short-legged deer of mountains, comparing them to ibex (Cabra ibex), chamois (Rupicapra rupicapra), mountain sheep (Ovis canadensis) and mountain goats (Oreamnos americanus). Subsequent key paleontological work also claimed that huemul are mountain deer. However, all these comparisons of huemul to other ungulates were done without any supporting data. These historic events lead to: (i) the continued prevailing claim that huemul are mountain deer; and (ii) that their natural range is the Andean mountains, as evidenced by the current distribution. We found that early writings about huemul generally reported their rareness, disappearance or near extinction. References to stocky and short-legged huemul were casual remarks made about deer found mainly in refuge areas. Paleontological comparisons were based on a new fossil labelled as mountain deer which, however, has been shown to be a construct and declared a ‘nomen nudum’. Behaviour like the aggressive horseshoe stance and thick long hair dissimulate stockiness by distorting body shape. Comparing leg morphometrics of huemul and 12 other ungulates revealed that huemul cannot be associated with rock climbing species. Intraspecific proportional leg length is not static and is influenced by ecogeography, nutrition, physiology and factors affecting exercise. Thus, climate, altitudinal hypoxia and locomotor pattern employed according to terrain, predation and forage affect the appendicular skeleton. Nutritional deficiencies occurring in Andean mountains are notorious for affecting bone development, causing osteopathology and altering body shape. Frequent underdeveloped huemul antlers and high incidence of osteopathology support the effect from mineral deficiencies. Skeletal proportions are affected by numerous factors, causing large intraspecific variation. Relative metapodial length varies up to 70% in better studied cervids, and populations from different environments can be clearly distinguished. Huemul morphology does not overlap with rock climbing species previously considered analogous, but falls within the range of other cervids. We caution against the rigid application of modern huemul occurrences in interpreting past habitat use. The few historic extra-Andean accounts cannot be considered abnormal outliers. Huemul ecology must be interpreted in terms of first principles rather than applying direct analogues from the present. This allows us to begin to use the past to understand the present instead of repeating the fallacy of imposing the present on the past. Current efforts to recover remaining huemul are distinctly based on the assumption that huemul foremost belong in rugged mountains, because of their supposed special adaptions and resemblance to stereotype ungulates, also erroneously believed to only occur in rugged mountains elsewhere. We conclude that the present empirical comparisons support many other lines of evidence that huemul existed in treeless habitat and colonised Andean forests and higher altitudes secondarily. Habitat breath of huemul is thus more like that found in other closely related Odocoilines, promising tremendous new opportunities for recovery efforts.
Additional keywords: adaptation, epigenetics, Hippocamelus bisulcus, morphometry, skeletal ratios.
References
[1] Eisenberg JF. The evolutionary history of the Cervidae with special reference to the South American radiation. In Wemmer CM, editor. Biology and management of the Cervidae. Washington, DC: Smithsonian Institution Press; 1987. pp. 60–64.[2] Iriarte A. Mamiferos de Chile. Barcelona, Spain: Lynx Ediciones; 2008.
[3] Guérin C, Faure M. The Cervidae (Mammalia, Artiodactyla) of the Upper Pleistocene/Lower Holocene deposits of the Serra da Capivara National Park Region (Piaui, Brazil). Geobios 2009; 42 169–95.
[4] Muñoz-Pedreros A, Valenzuela JY. Mamiferos de Chile. Segunda edicion. Valdivia, Chile: CEA Ediciones; 2009.
[5] Vila AR, Saucedo C, Aldridge D, Ramilo E, Corti P. South Andean huemul Hippocamelus bisulcus (Molina 1782). In Barbanti M, González S, editors. Neotropical Cervidology. Brazil: FUNEP; 2010. pp. 89–100.
[6] Osgood WH. The mammals of Chile. Field Museum of Natural History. Zoological Series 1943; 30 1–268.
[7] Díaz NI. Changes in the range distribution of Hippocamelus bisulcus in Patagonia. Z Saugetierkd 1993; 58 344–51.
[8] Flueck WT, Smith-Flueck JM. Predicaments of endangered huemul deer, Hippocamelus bisulcus, in Argentina: a review. Eur J Wildl Res 2006; 52 69–80.
| Predicaments of endangered huemul deer, Hippocamelus bisulcus, in Argentina: a review.Crossref | GoogleScholarGoogle Scholar |
[9] Kurten B. A new pleistocene genus of American mountain deer. J Mammal 1975; 56 507–8.
| A new pleistocene genus of American mountain deer.Crossref | GoogleScholarGoogle Scholar |
[10] Morejohn GV, Dailey DC. The identity and postcranial osteology of Odocoileus lucasi (Hay) 1927. Sierra College Natural History Museum Bulletin 2004; 1 1–54.
[11] Klein DR. Range-related differences in growth of deer reflected in skeletal ratios. J Mammal 1964; 45 226–35.
| Range-related differences in growth of deer reflected in skeletal ratios.Crossref | GoogleScholarGoogle Scholar |
[12] McMahon TA. Allometry and biomechanics: limbbones in adult ungulates. Am Nat 1975; 109 547–63.
| Allometry and biomechanics: limbbones in adult ungulates.Crossref | GoogleScholarGoogle Scholar |
[13] Scott KM. Allometric trends and locomotor adaptations in the Bovidae. Bull Am Mus Nat Hist 1985; 179 197–288.
[14] Fernandez H, Monchot H. Sexual dimorphism in limb bones of Ibex (Capra ibex L.): mixture analysis applied to modern and fossil data. Int J Osteoarchaeol 2007; 17 479–91.
| Sexual dimorphism in limb bones of Ibex (Capra ibex L.): mixture analysis applied to modern and fossil data.Crossref | GoogleScholarGoogle Scholar |
[15] Whistler DP, Webb SD. New goatlike camelid from the late Pliocene of Tecopa lake basin, California. Contrib Sci 2005; 503 1–40.
[16] Philippi RA. Über den Guemul von Molina. Archiv für Naturgeschichte 1857; 23 135–6.
[17] Gigoux EE. El huemul. Rev Chil Hist Nat 1929; 23 573–82.
[18] Wolffsohn JW. Notas sobre el huemul. Rev Chil Hist Nat 1910; 14 227–34.
[19] Latcham RE. Expedicion cientifica Macqueen al Aysen. Boletin del Museo Nacional (Chile) 1935; 14 7–31.
[20] De Agostini AM. Andes Patagónicos: Viajes de Exploración a la Cordillera Patagónica Austral. Buenos Aires: Talleres Gráficos Guillermo Kraft Ltda; 1941.
[21] Ringuelet RA. Serie Técnica y Didáctica Nr. 2: Temas de Ciencia Naturales. La Plata, Argentina: ProBiotA 2003, División Zoología Vertebrados, Museo de La Plata; 1946.
[22] Grosse A. El huemul – ciervo de los Andes y emblema del escudo Chileno. [Revista Chileno Alemana] Condor 1949; 12 10–12.
[23] Pefáur J, Hermosilla W, DiCastri F, González R, Salinas F. Estudio preliminar de mamíferos silvestres chilenos: su distribución, valor económico e importancia zoonótica. Revista de la Sociedad Medicina Veterinaria (Chile) 1968; 18 3–15.
[24] Franke FR. Mein Inselparadies. Bern, Switzerland; Verlag A. Francke AG; 1949.
[25] Krieg H. Biologische Reisestudien in Südamerika. V. Die chilenischen Hirsche. Z Morphol Oekol Tiere 1925; 4 585–97.
| Biologische Reisestudien in Südamerika. V. Die chilenischen Hirsche.Crossref | GoogleScholarGoogle Scholar |
[26] Kolliker Frers A. Das Waidwerk und die autochthonen Cerviden in Argentinien. In Vogel CA, editor. Parque Diana. München, Germany: Stefan Schwarz Verlag; 1969. pp. 25–31.
[27] Frädrich H. Bemerkungen über Nord-Andenhirsche (Hippocamelus antisensis) im Berliner Zoo. Bongo, Berlin 1978; 2 81–8.
[28] Kurten B. A stilt-legged deer Sangamona of the North-American Pleistocene. Boreas 1979; 8 313–21.
| A stilt-legged deer Sangamona of the North-American Pleistocene.Crossref | GoogleScholarGoogle Scholar |
[29] Povilitis A. The Chilean Huemul Project – a case history (1975–1976). In Threatened Deer. Gland, Switzerland; IUCN; 1978. pp. 109–128.
[30] Povilitis A. The huemul in Chile: national symbol in jeopardy? Oryx 1983; 17 34–40.
| The huemul in Chile: national symbol in jeopardy?Crossref | GoogleScholarGoogle Scholar |
[31] Delegacion Regional Patagonia. Programa conservación del huemul de la Administración de Parques Nacionales en Argentina (15 años: 1993–2007). Informe 2007; 1–19.
[32] Webb SD. A cranium of Navahoceros and its phylogenetic place among New World Cervidae. Ann Zool Fenn 1992; 28 401–10.
[33] Webb SD. Evolutionary history of New World Cervidae. In Vrba ES, Schaller GB, editors. Antelopes, deer, and relatives. New York: Yale University Press; 2000. pp. 38–64.
[34] Barnosky AD, Hadly EA, Maurer BA, Christie MI. Temperate terrestrial vertebrate faunas in North and South America: interplay of ecology, evolution, and geography with biodiversity. Conserv Biol 2001; 15 658–674.
| Temperate terrestrial vertebrate faunas in North and South America: interplay of ecology, evolution, and geography with biodiversity.Crossref | GoogleScholarGoogle Scholar |
[35] Churcher CS. Sangamona: the furtive deer. In Genoways HH, Dawsen MR, editors. Contributions in quarternary vertebrate paleonotology: a volume in memorial to John D. Guilday. Carnegie Museum of Natural History, Special Publication 1984; 8: 316–31.
[36] Wheatley PV, Ruez DR. Pliocene Odocoileus from Hagerman Fossil Beds National Monument, Idaho, and comments on the taxonomic status of Odocoileus brachyodontus. J Vertebr Paleontol 2006; 26 462–5.
| Pliocene Odocoileus from Hagerman Fossil Beds National Monument, Idaho, and comments on the taxonomic status of Odocoileus brachyodontus.Crossref | GoogleScholarGoogle Scholar |
[37] Smith-Flueck JM. The current situation of the Patagonian huemul. In Díaz NI, Smith-Flueck JM, editors. The Patagonian huemul: a mysterious deer on the brink of extinction. Buenos Aires: LOLA; 2000. pp. 67–146.
[38] Brandborg SM. Life history and management of the mountain goat in Idaho. Wildlife Bulletin, Department of Fish and Game, State of Idaho, Boise, Idaho 1955; 2 1–142.
[39] Honess RF, Frost NM. A Wyoming bighorn sheep study. Wyoming Game and Fish Department Bulletin 1942; 1 1–127.
[40] Cowan IMcT, Geist V. Aggressive behavior in deer of the genus Odocoileus. J Mammal 1961; 42 522–6.
| Aggressive behavior in deer of the genus Odocoileus.Crossref | GoogleScholarGoogle Scholar |
[41] Bubenik AB. Significance of antlers in the social life of barren ground caribou. Biological Papers, University of Alaska. Special Report 1975; 1 436–61.
[42] Crichton V. The horseshoe posture in moose – a reaction to perceived threats. Alces 2002; 38 109–11.
[43] Texera WA. Algunos aspectos de la biología del huemul (Hippocamelus bisulcus) (Mammalia: Artiodactyla, Cervidae) en cautividad. Anales del Instituo de la Patagonia. Punta Arenas (Chile) 1974; 5 155–88.
[44] Guineo P, Guineo Garay R, Garay G. Conociendo al huemul de Torres del Paine. Punta Arenas, Chile: La Prensa Austral; 2008.
[45] Garland T, Janis CM. Does metatarsal femur ratio predict maximal running speed in cursorial mammals. J Zool 1993; 229 133–51.
| Does metatarsal femur ratio predict maximal running speed in cursorial mammals.Crossref | GoogleScholarGoogle Scholar |
[46] Christiansen P. Locomotion in terrestrial mammals: the influence of body mass, limb length and bone proportions on speed. Zool J Linn Soc 2002; 136 685–714.
| Locomotion in terrestrial mammals: the influence of body mass, limb length and bone proportions on speed.Crossref | GoogleScholarGoogle Scholar |
[47] Geist V. Deer of the world. Pennsylvania, USA; Stackpole Books; 1998.
[48] Christiansen P. Scaling of the limb long bones to body mass in terrestrial mammals. J Morphol 1999; 239 167–90.
| Scaling of the limb long bones to body mass in terrestrial mammals.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M7js1yqsA%3D%3D&md5=29385d757e6a089f9738375ec0103542CAS | 9951716PubMed |
[49] Palsson H, Verges JB. Effects of the plane of nutrition on growth and development of carcass quality in lambs. Part I. The effects of high and low planes of nutrition at different ages. J Agric Sci 1952; 42 1–92.
| Effects of the plane of nutrition on growth and development of carcass quality in lambs. Part I. The effects of high and low planes of nutrition at different ages.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG2cXks1ykuw%3D%3D&md5=06a421161075f722ce1d18e4ca39f5aeCAS |
[50] Nilsson O, Baron J. Fundamental limits on longitudinal bone growth: growth plate senescence and epiphyseal fusion. Trends Endocrinol Metab 2004; 15 370–4.
| 1:CAS:528:DC%2BD2cXnslGjtbc%3D&md5=534e75b76478b05c4a85059601665a38CAS | 15380808PubMed |
[51] Flueck M. Functional, structural and molecular plasticity of mammalian skeletal muscle in response to exercise stimuli. J Exp Biol 2006; 209 2239–48.
| Functional, structural and molecular plasticity of mammalian skeletal muscle in response to exercise stimuli.Crossref | GoogleScholarGoogle Scholar | 16731801PubMed |
[52] Putman R, Flueck WT. Intraspecific variation in biology and ecology of deer: magnitude and causation. 2011; 51 277–91.
| Intraspecific variation in biology and ecology of deer: magnitude and causation.Crossref | GoogleScholarGoogle Scholar | 20735763PubMed |
[53] Scott KM. Allometry and habitat-related adaptions in the postcranial skeleton of Cervidae. In Wemmer CM, editor. Biology and management of the Cervidae. Washington, DC: Smithsonian Institution Press; 1987. pp. 65–80.
[54] Lee MMC, Chu PC, Chan HC. Effects of cold on the skeletal growth of albino rats. Am J Anat 1969; 124 239–49.
| Effects of cold on the skeletal growth of albino rats.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF1M7jslarsQ%3D%3D&md5=58525fd13e0ef0761b380737c6543504CAS | 5774652PubMed |
[55] Holliday TW, Ruff CB. Relative variation in human proximal and distal limb segment lengths. Am J Phys Anthropol 2001; 116 26–33.
| Relative variation in human proximal and distal limb segment lengths.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3Mvpt1Oisw%3D%3D&md5=8d74fbdf1a68d0dc575cd8879f4cf0fcCAS | 11536114PubMed |
[56] Lilje KE, Tardieu C, Fischer MS. Scaling of long bones in ruminants with respect to the scapula. J Zoological Syst Evol Res 2003; 41 118–26.
| Scaling of long bones in ruminants with respect to the scapula.Crossref | GoogleScholarGoogle Scholar |
[57] McCutchen HE. Desert bighorn zoogeography and adaptation in relation to historic land use. Wildl Soc Bull 1981; 9 171–9.
[58] Weaver M, Ingram D. Morphological changes in swine associated with environmental temperature. Ecology 1969; 50 710–3.
| Morphological changes in swine associated with environmental temperature.Crossref | GoogleScholarGoogle Scholar |
[59] Weinstein KJ. Body proportions in ancient Andeans from high and low altitudes. Am J Phys Anthropol 2005; 128 569–85.
| Body proportions in ancient Andeans from high and low altitudes.Crossref | GoogleScholarGoogle Scholar | 15895419PubMed |
[60] Bailey SM, Xu J, Feng JH, Hu X, Zhang C, Qui S. Tradeoffs between oxygen and energy in tibial growth at high altitude. Am J Hum Biol 2007; 19 662–8.
| Tradeoffs between oxygen and energy in tibial growth at high altitude.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2svms12itg%3D%3D&md5=4ffc15b491a6bf56db8dc4b1e17a17c9CAS | 17636531PubMed |
[61] Harrison AP, Tivey DR, Clausen T, Duchamp C, Dauncey MJ. Role of thyroid hormones in early postnatal development of skeletal muscle and its implications for undernutition. Br J Nutr 1996; 76 841–55.
| Role of thyroid hormones in early postnatal development of skeletal muscle and its implications for undernutition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlslaksA%3D%3D&md5=48eaae21d531ad3abcdc8f134ec5ac87CAS | 9014653PubMed |
[62] Oestreich AE. The acrophysis: a unifying concept for understanding enchondral bone growth and its disorders. II. Abnormal growth. Skeletal Radiol 2004; 33 119–28.
| The acrophysis: a unifying concept for understanding enchondral bone growth and its disorders. II. Abnormal growth.Crossref | GoogleScholarGoogle Scholar | 14689243PubMed |
[63] McLean RM, Podell DN. Bone and joint manifestations of hypothyroidism. Semin Arthritis Rheum 1995; 24 282–90.
| Bone and joint manifestations of hypothyroidism.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M3lvVOruw%3D%3D&md5=9cdcc1178be7f647a2878e43d3792d48CAS | 7740308PubMed |
[64] Obendorf PJ, Oxnard CE, Kefford BJ. Are the small human-like fossils found on Flores human endemic cretins? Proc Biol Sci 2008; 275 1287–96.
| Are the small human-like fossils found on Flores human endemic cretins?Crossref | GoogleScholarGoogle Scholar | 18319214PubMed |
[65] Crile R. The comparative anatomy of the thyroid and adrenal glands in wild animals. Ohio J Sci 1937; 37 42–61.
[66] Moreno-Reyes R, Suetens C, Mathieu F, Begaux F, Zhu D, Rivera MT, Boelaert M, Nève J, Perlmutter N, Vanderpas J. Kashin-Beck osteoarthropathy in rural Tibet in relation to selenium and iodine status. N Engl J Med 1998; 339 1112–20.
| Kashin-Beck osteoarthropathy in rural Tibet in relation to selenium and iodine status.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1cvjt1Cmsw%3D%3D&md5=55cbe5cbfa4a3ee57df7e33fd2598b1fCAS | 9770558PubMed |
[67] Ren FL, Guo X, Zhang RJ, Wang SJ, Zuo H, Zhang ZT, Geng D, Yu Y, Su M. Effects of selenium and iodine deficiency on bone, cartilage growth plate and chondrocyte differentiation in two generations of rats. Osteoarthritis Cartilage 2007; 15 1171–7.
| Effects of selenium and iodine deficiency on bone, cartilage growth plate and chondrocyte differentiation in two generations of rats.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2srjvFCqug%3D%3D&md5=3d4dd568e2aa882af9f315b85ab076bfCAS | 17490897PubMed |
[68] Flueck WT, Smith-Flueck JM. Why the Patagonian huemul deer in Argentina fails to recover: an ecological hypothesis. In Bartos L, Dusek A, Kotrba R, Bartosova J, editors. Advances in deer biology: deer in a changing world. Praha, Czech Republic: Research Institute of Animal Production; 2006. pp. 181–185.
[69] Flueck WT, Smith-Flueck JM. Age-independent osteopathology in skeletons of a South American cervid, the Patagonian huemul (Hippocamelus bisulcus). J Wildl Dis 2008; 44 636–48.
| 18689649PubMed |
[70] Flueck WT, Smith-Flueck JM. Recent advances in the nutritional ecology of the Patagonian huemul: implications for recovery. Anim Prod Sci 2011; 51 311–26.
| Recent advances in the nutritional ecology of the Patagonian huemul: implications for recovery.Crossref | GoogleScholarGoogle Scholar |
[71] Peterson RO, Vucetich JA, Fenton G, Drummer TD, Larsen CS. Ecology of arthritis. Ecol Lett 2010; 13 1124–8.
| Ecology of arthritis.Crossref | GoogleScholarGoogle Scholar | 20618843PubMed |
[72] Lehoczki R, Erdélyi K, Sonkoly K, Szemethy L, Csányi S. Iodine distribution in the environment as a limiting factor for roe deer antler development. Biol Trace Elem Res 2010; 139 168–76.
| Iodine distribution in the environment as a limiting factor for roe deer antler development.Crossref | GoogleScholarGoogle Scholar | 20195916PubMed |
[73] Rusconi C. Anomalias en las cornamentas del huemul. Anales Sociedad Cientifica Argentina 1936; 122 288–96.
[74] Grayson DK, Meltzer DJ. Clovis hunting and large mammal extinction: a critical review of the evidence. J World Prehist 2002; 16 313–59.
| Clovis hunting and large mammal extinction: a critical review of the evidence.Crossref | GoogleScholarGoogle Scholar |
[75] Haller H. Der Rothirsch im Schweizerischen Nationalpark und dessen Umgebung. Eine alpine population von Cervus elaphus zeitlich und räumlich dokumentiert. Nationalpark-Forschung Schweiz 2002; 91 1–144.
[76] Luccarini S, Mauri L, Ciuti S, Lamberti P, Apollonio M. Red deer (Cervus elaphus) spatial use in the Italian Alps: home range patterns, seasonal migrations, and effects of snow and winter feeding. Ethol Ecol Evol 2006; 18 127–45.
| Red deer (Cervus elaphus) spatial use in the Italian Alps: home range patterns, seasonal migrations, and effects of snow and winter feeding.Crossref | GoogleScholarGoogle Scholar |
[77] Hornaday WT. The extermination of the American bison. Report, US National Museum, The Smithsonian Institution. Washington DC: Government Printing Office; 1889.
[78] Flueck WT, Smith-Flueck JM, Naumann CM. The current distribution of red deer (Cervus elaphus) in southern Latin America. Eur J Wildl Res 2003; 49 112–9.
[79] Geist V. On Pleistocene bighorn sheep: some problems of adaption, and relevance to today’s American megafauna. Wildl Soc Bull 1985; 13 351–9.
[80] Fairbanks WS, Bailey JA, Cook RS. Habitat use by a low-elevation, semicaptive bighorn sheep population. J Wildl Manage 1987; 51 912–5.
| Habitat use by a low-elevation, semicaptive bighorn sheep population.Crossref | GoogleScholarGoogle Scholar |
[81] Senn J, Suter W. Ungulate browsing on silver fir (Abies alba) in the Swiss Alps: beliefs in search of supporting data. For Ecol Manage 2003; 181 151–64.
| Ungulate browsing on silver fir (Abies alba) in the Swiss Alps: beliefs in search of supporting data.Crossref | GoogleScholarGoogle Scholar |
[82] Miracle P, Sturdy D. Chamois and the Karst of Herzegovina. J Archaeol Sci 1991; 18 89–108.
| Chamois and the Karst of Herzegovina.Crossref | GoogleScholarGoogle Scholar |
[83] Phoca-Cosmetatou N. Site function and the ‘ibex-site phenomenon’: myth or reality? Oxf J Archaeol 2004; 23 217–42.
| Site function and the ‘ibex-site phenomenon’: myth or reality?Crossref | GoogleScholarGoogle Scholar |
[84] Phoca-Cosmetatou N. Landscape use in Northeast Italy during the Upper Palaeolithic. Preistoria Alpina 2005; 41 23–49.
[85] Molinari-Jobin A, Molinari P, Breitenmoser-Wursten C, Breitenmoser U. Significance of lynx Lynx lynx predation for roe deer Capreolus capreolus and chamois Rupicapra rupicapra mortality in the Swiss Jura Mountains. Wildl Biol 2002; 8 109–15.
[86] Baumann M, Babota C, Schibler J. Native or naturalized? Validating Alpine chamois habitat models with archaeozoological data. Ecol Appl 2005; 15 1096–110.
| Native or naturalized? Validating Alpine chamois habitat models with archaeozoological data.Crossref | GoogleScholarGoogle Scholar |
[87] Choisy JP. Reintroduction de bouqetins Capra sp.: conditions de reussite, choix de massifs, enseignements. L’example du Vercors. Journal of Mountain Ecology 1994; 2 15–33.
[88] Phoca-Cosmetatou N. A zooarchaeological reassessment of the habitat and ecology of the ibex (Capra ibex). In Lauwerier RC, Plug I, editors. The future from the past. UK: Oxbow Books; 2004. pp. 64–78.
[89] Lyman RL. Paleozoology in the service of conservation biology. Evol Anthropol 2006; 15 11–9.
| Paleozoology in the service of conservation biology.Crossref | GoogleScholarGoogle Scholar |
[90] Choisy JP. Bouquetins d’Dans les falaises du royans. Parc Naturel Regional du Vercors Info 2001; 5 1–2.
[91] Dabbene R. Sobre la existencia del huemul de Bolivia y Perú, Odocoileus (Hippocamelus) antisensis (Orb.) y del avestruz petiso, Rhea darwini Gould en el N.W. de la República Argentina. Anales del Museo Nacional Buenos Aires, Serie 3 1911; 14 293–307.
[92] Smith-Flueck JM, Barrio J, Ferreyra N, Nuñez A, Tomas N, Guzman J, Flueck WT, Hinojosa A, Vidal F, Garay G, Jimenez J. Advances in ecology and conservation of Hippocamelus species in South America. Anim Prod Sci 2011; 51 378–83.
| Advances in ecology and conservation of Hippocamelus species in South America.Crossref | GoogleScholarGoogle Scholar |
[93] Nieminen M, Helle T. Variations in body measurements of wild and semidomestic reindeer (Rangifer tarandus) in Fennoscandia. Ann Zool Fenn 1980; 17 275–83.
[94] Kuzyk GW, Dehn MM, Farnell RS. Body-size comparisons of alpine- and forest-wintering woodland caribou herds in the Yukon. Can J Zool 1999; 77 1017–24.
| Body-size comparisons of alpine- and forest-wintering woodland caribou herds in the Yukon.Crossref | GoogleScholarGoogle Scholar |
[95] Kojola I, Huitu O, Toppinen K, Heikura K, Heikkinen S, Ronkainen S. Predation on European wild forest reindeer (Rangifer tarandus) by wolves (Canis lupus) in Finland. J Zool 2004; 263 229–35.
| Predation on European wild forest reindeer (Rangifer tarandus) by wolves (Canis lupus) in Finland.Crossref | GoogleScholarGoogle Scholar |
[96] Klein DR, Meldgaard M, Fancy SG. Factors determining leg length in Rangifer tarandus. J Mammal 1987; 68 642–55.
| Factors determining leg length in Rangifer tarandus.Crossref | GoogleScholarGoogle Scholar |
[97] Brisbin IL, Lenarz MS. Morphological comparisons of insular and mainland populations of southeastern white-tailed deer. J Mammal 1984; 65 44–50.
| Morphological comparisons of insular and mainland populations of southeastern white-tailed deer.Crossref | GoogleScholarGoogle Scholar |
[98] Parker KL, Robbins CT, Hanley TA. Energy expenditures for locomotion by mule deer and elk. J Wildl Manage 1984; 48 474–88.
| Energy expenditures for locomotion by mule deer and elk.Crossref | GoogleScholarGoogle Scholar |
[99] Klein DR, Strandgaard H. Factors affecting growth and body size of Roe deer. J Wildl Manage 1972; 36 64–79.
| Factors affecting growth and body size of Roe deer.Crossref | GoogleScholarGoogle Scholar |
[100] Van der Meuleun MC, Carter DR. Developmental mechanics determine long bone allometry. J Theor Biol 1995; 172 323–7.
| Developmental mechanics determine long bone allometry.Crossref | GoogleScholarGoogle Scholar | 7715201PubMed |
[101] Turner CH. Three rules for bone adaptation to mechanical stimuli. Bone 1998; 23 399–407.
| Three rules for bone adaptation to mechanical stimuli.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M%2FktVOkuw%3D%3D&md5=0cf4ad15930540a10009fab32ef74683CAS | 9823445PubMed |
[102] Kokshenev VB, Silva JKL, Garcia GJM. Long-bone allometry of terrestrial mammals and the geometric-shape and elastic-force constraints of bone evolution. J Theor Biol 2003; 224 551–6.
| Long-bone allometry of terrestrial mammals and the geometric-shape and elastic-force constraints of bone evolution.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3svhvVGmsg%3D%3D&md5=ff2fa62f22428ba9a41a4b5f0f6e7e32CAS | 12957126PubMed |
[103] Kokshenev VB, Christiansen P. Salient features in the locomotion of proboscideans revealed via the differential scaling of limb long bones. Biol J Linn Soc Lond 2010; 100 16–29.
| Salient features in the locomotion of proboscideans revealed via the differential scaling of limb long bones.Crossref | GoogleScholarGoogle Scholar |
[104] Ruff CB. Mechanical determinants of bone form: insights from skeletal remains. J Musculoskelet Neuronal Interact 2005; 5 202–12.
| 1:STN:280:DC%2BD2MrgtVGhtA%3D%3D&md5=5c820d4409d18b2348adbfb822043f9eCAS | 16172511PubMed |
[105] McKelvey KS, Aaubry KB, Schwartz MK. Using anecdotal occurrence data for rare or elusive species: the illusion of reality and a call for evidentiary standards. Bioscience 2008; 58 549–55.
| Using anecdotal occurrence data for rare or elusive species: the illusion of reality and a call for evidentiary standards.Crossref | GoogleScholarGoogle Scholar |
[106] Fedosenko AK, Blank DA. Ovis ammon. Mamm Species 2005; 773 1–15.
| Ovis ammon.Crossref | GoogleScholarGoogle Scholar |