Sympatric snow leopards and Tibetan wolves: coexistence of large carnivores with human-driven potential competition

  • Anna Bocci
  • Sandro Lovari
  • Muhammad Zafar Khan
  • Emiliano Mori
Original Article

Abstract

The snow leopard Panthera uncia coexists with the wolf Canis lupus throughout most of its distribution range. We analysed the food habits of snow leopards and wolves in their sympatric range in the Karakoram mountains of Pakistan. A total of 131 genotyped scats (N = 74, snow leopard; N = 57, Tibetan wolf) were collected during the cold periods (i.e. winter and spring) of 2011 and 2012 in the Hushey valley. Large mammals, i.e. livestock and ibex, accounted for 84.8 and 83.1% of the diet (relative frequency) of the snow leopard and the wolf, respectively. Domestic prey was the staple of the diet of both snow leopards (66.6%) and wolves (75.1%). Ibex Capra ibex, the only wild ungulate in our study area, contributed 18.2 and 16.9% of relative frequencies in the diets of the snow leopard and the wolf, respectively. In winter, the snow leopard heavily relied on domestic sheep (43.3%) for food, whereas the wolf preyed mainly on domestic goats (43.4%). Differently from other study areas, both snow leopards and wolves showed no apparent prey preference (Jacobs index: snow leopard min. − 0.098, max. 0.102; Tibetan wolf min. − 0.120, max. 0.03). In human depauperate areas, with livestock and only a few wild prey, should competitive interactions arise, two main scenarios could be expected, with either predator as a winner. In both cases, the best solution could primarily impinge on habitat restoration, so that a balance could be found between these predators, who have already coexisted for thousands of years.

Keywords

Panthera uncia Canis lupus filchneri Competition Large-carnivore coexistence Siberian ibex 

References

  1. Anwar MB, Jackson R, Nadeem MS, Janečka JE, Hussain S, Beg M, Muhammad G, Qayyum M (2011) Food habits of the snow leopard Panthera uncia (Schreber, 1775) in Baltistan, Northern Pakistan. Eur J Wildl Res 57(5):1077–1083. https://doi.org/10.1007/s10344-011-0521-2 CrossRefGoogle Scholar
  2. Aryal A, Babu Shrestha U, Ji W, Ale SB, Shrestha S, Ingty T, Maraseni T, Cockfield G, Raubenheimer D (2016) Predicting the distributions of predator (snow leopard) and prey (blue sheep) under climate change in the Himalaya. Ecol Evol 6(12):4065–4075. https://doi.org/10.1002/ece3.2196 PubMedPubMedCentralCrossRefGoogle Scholar
  3. Bagchi S, Mishra C (2006) Living with large carnivores: predation on livestock by the snow leopard (Uncia uncia). J Zool (Lond) 268(3):217–224. https://doi.org/10.1111/j.1469-7998.2005.00030.x CrossRefGoogle Scholar
  4. Blumestein DT (1993) Dhee Sar—portrait of a high alpine meadow. WWF-Pakistan. Natura 18:4–7Google Scholar
  5. Bothma JDP (1966) Food of the silver fox Vulpes chama. Zool Afr 2(2):205–210. https://doi.org/10.1080/00445096.1966.11447343 CrossRefGoogle Scholar
  6. Butler JRA, du Toit JT, Bingham J (2004) Free-ranging domestic dogs (Canis familiaris) as predators and prey in rural Zimbabwe: threat of competition and disease to large wild carnivores. Biol Conserv 115(3):369–378. https://doi.org/10.1016/S0006-3207(03)00152-6 CrossRefGoogle Scholar
  7. Chakrabarti S, Jhala YV, Dutta S, Qureshi Q, Kadivar RF, Rana VJ (2016) Adding constraints to predation through allometric relation of scats to consumption. J Anim Ecol 85(3):660–670. https://doi.org/10.1111/1365-2656.12508 PubMedCrossRefGoogle Scholar
  8. Champion HG, Seth SK, Khattak GM (1965) Forest types of Pakistan. Pakistan Forest Institute, PeshawarGoogle Scholar
  9. Chetri M, Odden M, Wegge P (2017) Snow leopards and Himalayan wolf: food habits and prey selection in the Central Himalayas, Nepal. Plos ONE 12(2):e0170549. https://doi.org/10.1371/journal.pone.0170549 PubMedPubMedCentralCrossRefGoogle Scholar
  10. Chundawat RS, Rawat GS (1994) Food habits of the snow leopard in Ladakh. In: Fox JL, Jizeng D (eds) International snow leopard trust and northwest plateau. Institute of Biology, Seattle, pp 127–132Google Scholar
  11. Clemens J, Nusser M (1997) Resource management in Rupal Valley, Northern Pakistan: the utilization of forests and pastures in the Nanga Parbat area. In: Stellrecht I, Winiger M (eds) Perspectives on history and change in the Karakoram, Hindukush and Himalaya, vol 3. Culture Area Karakoram Scientific Studies, Cologne, pp 1–17Google Scholar
  12. Donadio E, Buskirk SW (2006) Diet, morphology and interspecific killing in Carnivora. Am Nat 167(4):524–536. https://doi.org/10.1086/501033 PubMedCrossRefGoogle Scholar
  13. Forrest JL, Wikramanayake E, Shrestha R, Areendran G, Gyeltshen K, Maheshwari A, Mazumdar S, Naidoo R, Thapa K (2012) Conservation and climate change: assessing the vulnerability of snow leopard habitat to treeline shift in the Himalaya. Biol Conserv 150(1):129–135. https://doi.org/10.1016/j.biocon.2012.03.001 CrossRefGoogle Scholar
  14. Fox JL, Sinha SP, Chundawat RS, Das PK (1991) Status of snow leopard (Panthera uncia) in northwest India. Biol Conserv 55(3):283–298. https://doi.org/10.1016/0006-3207(91)90033-6 CrossRefGoogle Scholar
  15. Hass CC (2009) Competition and coexistence in sympatric bobcats and pumas. J Zool (Lond) 278(3):174–180. https://doi.org/10.1111/j.1469-7998.2009.00565.x CrossRefGoogle Scholar
  16. Hoppe-Dominik B (1988) Grass-eating leopards: wolves turned into sheep? Naturwissenschaften 75(1):49–50. https://doi.org/10.1007/BF00367444 PubMedCrossRefGoogle Scholar
  17. Jackson RM (1996) Home range, movements and habitat use of snow leopard (Uncia uncia) in Nepal. (Ph.D. Thesis) University of London (External Programme), LondonGoogle Scholar
  18. Jacobs J (1974) Quantitative measurement of food selection-a modification of the forage ratio and Ivlev’s electivity index. Oecologia 14(4):413–417. https://doi.org/10.1007/BF00384581 PubMedCrossRefGoogle Scholar
  19. Johansson O, McCarthy T, Samelius G, Andren H, Tumursukh L, Mishra C (2015) Snow leopard predation in a livestock dominated landscape in Mongolia. Biol Conserv 184:251–258. https://doi.org/10.1016/j.biocon.2015.02.003 CrossRefGoogle Scholar
  20. Jumabay-Uulu K, Wegge P, Mishra C, Sharma K (2013) Large carnivores and low diversity of optimal prey: a comparison of the diet of snow leopard Panthera uncia and wolf Canis lupus in Sarychat-Ertash Reserve in Kyrgyzstan. Oryx 48:529–535CrossRefGoogle Scholar
  21. Khan B (2012) Pastoralism-Wildlife Conservation Conflict in Climate Change Context—a study of climatic factors influencing fragile mountain ecosystems and pastoral livelihoods in the Karakoram Pamir trans-border area between China and Pakistan. Ph.D thesis, Graduate University of the Chinese Academy of Sciences, ChinaGoogle Scholar
  22. Khan MZ, Awan MS, Bocci A, Khan B, Abbas SY, Khan G, Abbas S (2014) Population structure and grouping tendency of Asiatic ibex Capra sibirica in the Central Karakoram National Park, Pakistan. J Bio Env Sci 5:542–554Google Scholar
  23. Khan MZ, Khan B, Awan MS, Begum F (2017) Livestock depredation by large predators and its implications for conservation and livelihoods in the Karakoram Mountains of Pakistan. Oryx 1–7. https://doi.org/10.1017/S0030605316001095
  24. Khatoon R (2010) Diet selection of snow leopard Uncia uncia in Chitral Area. Master Thesis. Department of Wildlife Management, Faculty of Forestry, Range Management and Wildlife, Pir Mehr Ali Shah Arid Agriculture University, RawalpindiGoogle Scholar
  25. Krebs CJ (1999) Ecological methodology, 2nd edn. Addison Wesley Longman, Menlo ParkGoogle Scholar
  26. Kruuk H (1989) The social badger: ecology and behaviour of group-living carnivore (Meles meles). Oxford University Press, OxfordGoogle Scholar
  27. Kruuk H, Parish T (1981) Feeding specialization of the European badger Meles meles in Scotland. J. Anim Ecol 50:773–788CrossRefGoogle Scholar
  28. Lescureux N (2006) Towards the necessity of a new interactive approach integrating ethnology, ecology, and ethology in the study of the relationship between Kyrgyz stockbreeders and wolves. Soc Sci Inform 45:463–478CrossRefGoogle Scholar
  29. Levins R (1968) Evolution in changing environments. Princeton University Press, PrincetonGoogle Scholar
  30. Lovari S, Mishra C (2016) Living on the edge: depletion of wild prey and survival of the snow leopard. In: McCarthy T, Mallon D (eds) Snow leopards. Elsevier Academic Press, Amsterdam, pp 69–76CrossRefGoogle Scholar
  31. Lovari S, Boesi R, Minder I, Mucci N, Randi E, Dematteis A, Ale SB (2009) Restoring a keystone predator may endanger a prey species in a human-altered ecosystem: the return of the snow leopard to Sagarmatha National Park. Anim Conserv 12(6):559–570. https://doi.org/10.1111/j.1469-1795.2009.00285.x CrossRefGoogle Scholar
  32. Lovari S, Ventimiglia M, Minder I (2013a) Food habits of two leopard species, competition, climate change and upperline: a way to the decrease of an endangered species? Ethol Ecol Evol 25(4):305–318. https://doi.org/10.1080/03949370.2013.806362 CrossRefGoogle Scholar
  33. Lovari S, Minder I, Ferretti F, Mucci N, Randi E, Pellizi B (2013b) Common and snow leopards share prey, but not habitat: competition avoidance by large predators? J Zool (Lond) 291(2):127–135. https://doi.org/10.1111/jzo.12053 CrossRefGoogle Scholar
  34. Lovari S, Pokheral CP, Jnavali SR, Fusani L, Ferretti F (2015) Coexistence of the tiger and the common leopard in a prey-rich area: the role of prey partitioning. J Zool (Lond) 295(2):122–131. https://doi.org/10.1111/jzo.12192 CrossRefGoogle Scholar
  35. Lucherini M, Crema G (1995) Seasonal variation in the food habits of badgers in an Alpine valley. Hystrix 7:165–171Google Scholar
  36. Lumetsberger T, Ghoddousi A, Appel A, Khorozyan I, Waltert M, Kiffner C (2017) Re-evaluating models for estimating prey consumption by leopards. J Zool (Lond) 302(3):201–210. https://doi.org/10.1111/jzo.12449 CrossRefGoogle Scholar
  37. Lyngdoh S, Shrotriya S, Goyal SP, Clements H, Hayward MW, Habib B (2014) Prey preferences of the snow leopard (Panthera uncia): regional diet specificity holds global significance for conservation. PLoS One 9(2):e88349. https://doi.org/10.1371/journal.pone.0088349 PubMedPubMedCentralCrossRefGoogle Scholar
  38. Macdonald DW (1992) The velvet claw: a natural history of carnivores. BBC Book, LondonGoogle Scholar
  39. Mech LD (1970) The wolf: the ecology and behaviour of an endangered species. Natural History Press, New YorkGoogle Scholar
  40. Meriggi A, Lovari S (1996) A review of wolf predation in southern Europe: does the wolf prefer wild prey to livestock? J Appl Ecol 33(6):1561–1571. https://doi.org/10.2307/2404794 CrossRefGoogle Scholar
  41. Mishra C (1997) Livestock depredation by large carnivores in the Indian trans-Himalaya: conflict perceptions and conservation prospects. Environ Conserv 24(4):338–343. https://doi.org/10.1017/S0376892997000441 CrossRefGoogle Scholar
  42. Namgail T, Fox JL, Bhatnagar YV (2007) Carnivore-caused livestock mortality in trans-Himalaya. Environ Manag 39(4):490–496. https://doi.org/10.1007/s00267-005-0178-2 CrossRefGoogle Scholar
  43. Nawaz MA (2009) Draft management plan for CKCC; sub-plan Species Management. IUCN, Karachi 24ppGoogle Scholar
  44. Newsome TM, Boitani L, Chapron G, Ciucci P, Dickman CR, Dellinger JA, Lòpez-Bao JV, Peterson RO, Shores CR, Wirsing AJ, Ripple WJ (2016) Food habits of the world’s grey wolves. Mammal Rev 46(4):255–269. https://doi.org/10.1111/mam.12067 CrossRefGoogle Scholar
  45. Oli MK (1993) A key for the identification of hair of mammals of a snow leopard (Panthera uncia) habitat in Nepal. J Zool (Lond) 231(1):71–93. https://doi.org/10.1111/j.1469-7998.1993.tb05354.x CrossRefGoogle Scholar
  46. Oli MK, Taylor IR, Rogers ME (1993) The diet of snow leopard (Panthera uncia) in the Annapurna Conservation Area, Nepal. J Zool (Lond) 231(3):365–370. https://doi.org/10.1111/j.1469-7998.1993.tb01924.x CrossRefGoogle Scholar
  47. Palomares F, Caro TM (1999) Interspecific killing among mammalian carnivores. Am Nat 153(5):492–508. https://doi.org/10.1086/303189 CrossRefGoogle Scholar
  48. Palomares F, Ferreras P, Fedriani JM, Delibes M (1996) Spatial relationships between the Iberian lynx and other carnivores in an area of south-western Spain. J Appl Ecol 33(1):5–13. https://doi.org/10.2307/2405010 CrossRefGoogle Scholar
  49. Peiman K, Robinson B (2010) Ecology and evolution of resource-related heterospecific aggression. Q Rev Biol 85(2):133–158. https://doi.org/10.1086/652374 PubMedCrossRefGoogle Scholar
  50. Pianka ER (1974) Niche overlap and diffuse competition. Proc Nat Ac Sci 71(5):2141–2145. https://doi.org/10.1073/pnas.71.5.2141 CrossRefGoogle Scholar
  51. Reynolds J, Aebischer NJ (1991) Comparison and quantification of carnivore diet by faecal analysis: a critique, with recommendations, based on a study of red fox Vulpes vulpes. Mammal Rev 21(3):97–121. https://doi.org/10.1111/j.1365-2907.1991.tb00113.x CrossRefGoogle Scholar
  52. Schaller GB (1977) Mountain monarchs. Wild sheep and goats of the Himalaya. The University of Chicago Press, ChicagoGoogle Scholar
  53. Schaller GB (2016) Foreword. In: McCarthy T, Mallon D (eds) Snow leopards. Elsevier Academic Press, Amsterdam, pp 23–27Google Scholar
  54. Sharma RK, Bhatnagar YV, Mishra C (2015) Does livestock benefit or harm snow leopards? Biol Conserv 190:8–13. https://doi.org/10.1016/j.biocon.2015.04.026 CrossRefGoogle Scholar
  55. Sheikh KM, Molur S (2004) Status and red list of Pakistan mammals. Conservation assessment and management plan. IUCN Pakistan, KarachiGoogle Scholar
  56. Shrestha B (2008) Prey abundance and prey selection by snow leopard (Uncia uncia) in Sagarmatha (Mt. Everest) National Park, Nepal. Report for International Snow Leopard Trust, Snow Leopard Conservancy and snow leopard network, Forum of Natural Resource Managers, Nepal, 34ppGoogle Scholar
  57. Stephens DW, Krebs JR (1986) Foraging theory. Princeton University Press, PrincetonGoogle Scholar
  58. Sugimoto T, Aramilev VV, Nagata J, McCullough DR (2016) Winter food habits of sympatric carnivores, Amur tigers and Far East leopards, in the Russian Far East. Mammal Biol 81(2):214–218. https://doi.org/10.1016/j.mambio.2015.12.002 CrossRefGoogle Scholar
  59. Suryawanshi KR, Bhatnagar YV, Redpath S, Mishra C (2013) People, predators and perceptions: patterns of livestock depredation by snow leopards and wolves. J Appl Ecol 50(3):550–560. https://doi.org/10.1111/1365-2664.12061 CrossRefGoogle Scholar
  60. Tannerfeldt M, Elmhagen B, Angerbjörn A (2002) Exclusion by interference competition? The relationship between red and arctic foxes. Oecologia 132(2):213–220. https://doi.org/10.1007/s00442-002-0967-8 PubMedCrossRefGoogle Scholar
  61. Teerink BJ (1991) Hair of West-European mammals. Cambridge University Press, CambridgeGoogle Scholar
  62. Turner A, Anton M (1997) The big cats and their fossil relatives: an illustrated guide to their evolution and natural history. Columbia University Press, New YorkGoogle Scholar
  63. Ud Din J, Ali H, Ali Nawaz M (2016) The current state of snow leopard conservation in Pakistan. In: McCarthy T, Mallon D (eds) Snow leopards. Elsevier Academic Press, Amsterdam, pp 486–492Google Scholar
  64. Wang J, Laguardia A, Damerell PJ, Riordan P, Shi K (2014) Dietary overlap of snow leopard and other carnivores in the Pamirs of Nortwestern China. Chin Sci Bull 59(25):3162–3168. https://doi.org/10.1007/s11434-014-0370-y CrossRefGoogle Scholar
  65. Watts HE, Holekamp KE (2008) Interspecific competition influences reproduction in spotted hyenas. J Zool (Lond) 276(4):402–410. https://doi.org/10.1111/j.1469-7998.2008.00506.x CrossRefGoogle Scholar
  66. WWF-Pakistan (2008) Land cover mapping of the Central Karakoram National Park. WWF Pakistan, LahoreGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  • Anna Bocci
    • 1
    • 2
  • Sandro Lovari
    • 1
    • 2
    • 3
  • Muhammad Zafar Khan
    • 4
  • Emiliano Mori
    • 1
  1. 1.Dept. of Life Sciences-Research Unit of Behavioural Ecology, Ethology and Wildlife ManagementUniversity of SienaSienaItaly
  2. 2.Ev-K2-CNRBergamoItaly
  3. 3.Museo di Storia Naturale della MaremmaGrossetoItaly
  4. 4.Department of Environmental SciencesKarakoram International UniversityGilgitPakistan

Personalised recommendations