Ecological Research

, Volume 24, Issue 4, pp 897–908 | Cite as

Clues to the cause of the Tsushima leopard cat (Prionailurus bengalensis euptilura) decline from isotopic measurements in three species of Carnivora

  • Naho Mitani
  • Shozo Mihara
  • Nobuo Ishii
  • Hiroko Koike
Original Article

Abstract

The estimated population of the Tsushima leopard cat Prionailurus bengalensis euptilura is only 80–110 individuals. However, the cause of the population decline is not clear. We investigated temporal changes in the food habits of the cat and two other species of Carnivora (marten and weasel) inhabiting the Tsushima Islands by measuring δ13C and δ15N values in hair samples. Hair samples of the cat were collected not only from specimens and furs, but also from feces. The gathering of hair from cat feces was most efficient when the feces were collected in the spring. The food habit of male cats seemed to be more diverse and tended to comprise prey of higher trophic levels than the food habits of the females. The δ13C and δ15N measurements suggested that the trophic level of the food sources has been decreasing over the last several decades for the cat and weasel, but not for the marten. Increased consumption of prey from lower trophic levels in the food habit of the cat seems to be related to the decline of the cat population because these phenomena occurred simultaneously.

Keywords

Leopard cat Isotopic measurements Trophic level Conservation 

Notes

Acknowledgments

We are grateful to the Ministry of the Environment for issuing permits to collect samples of the Tsushima leopard cat. Other samples for this study were obtained in cooperation with the National Science Museum, the Kitakyushu Museum of Natural History and Human History, the Osaka Museum of Natural History, the Historical Museum of Izuhara Town, the Mine Town Museum of History and Folklore, the Public Hall of Kamiagata Town, the Prefectural Museum of History and Folklore of Tsushima, and residents in Tsushima.

References

  1. Aniya M (1997) The relationship between the environmental utilization, and the distribution and density of the prey. Graduation thesis, The University of the Ryukyus (in Japanese)Google Scholar
  2. Araki R, Suda T (1998) Approach from the aspect of biodiversity, the relationship between the density of deer and status of plants, rodents and birds. Wildl Forum 4:14–15 (in Japanese)Google Scholar
  3. Baker KP (1974) Hair growth and replacement in the cat. Br Vet J 130:327–335PubMedGoogle Scholar
  4. Ben-David M, Titus K, Beier LR (2004) Consumption of salmon by Alaskan brown bears: a trade-off between nutritional requirements and the risk of infanticide? Oecologia 138:465–474. doi:10.1007/s00442-003-1442-x PubMedCrossRefGoogle Scholar
  5. Bocherens H, Fizet M, Mariotti A (1994) Diet, physiology and ecology of fossil mammals as inferred from stable carbon and nitrogen isotope biogeochemistry: implications for Pleistocene bears. Palaeogeogr Palaeoclimatol Palaeoecol 107:203–225. doi:10.1016/0031-0182(94)90095-7 CrossRefGoogle Scholar
  6. Branch LC, Pessino M, Villarreal D (1996) Response of pumas to a population decline of the plains vizcacha. J Mammal 77:1132–1140. doi:10.2307/1382795 CrossRefGoogle Scholar
  7. Caut S, Angulo E, Courchamp F (2008a) Discrimination factors (Δ15N and Δ13C) in an omnivorous consumer: effect of diet isotopic ratio. Funct Ecol 22:255–263. doi:10.1111/j.1365-2435.2007.01360.x CrossRefGoogle Scholar
  8. Caut S, Angulo E, Courchamp F (2008b) Caution on isotopic model use for analyses of consumer diet. Can J Zool 86:438–445. doi:10.1139/Z08-012 CrossRefGoogle Scholar
  9. DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506. doi:10.1016/0016-7037(78)90199-0 CrossRefGoogle Scholar
  10. DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351. doi:10.1016/0016-7037(81)90244-1 CrossRefGoogle Scholar
  11. Environment Agency, Nagasaki Prefecture (1997) Report of the second special research on the Tsushima leopard cat (in Japanese)Google Scholar
  12. Fox-Dobbs K, Bump JK, Peterson RO, Fox DL, Koch PL (2007) Carnivore-specific stable isotope variables and variation in the foraging ecology of modern and ancient wolf populations: case studies from Isle Royale, Minnesota, and La Brea. Can J Zool 85:458–471. doi:10.1139/Z07-018 CrossRefGoogle Scholar
  13. Fry B (1988) Food web structure on George Bank from stable C, N, and S isotopic compositions. Limnol Oceanogr 33:1182–1190Google Scholar
  14. Fry B, Sherr EB (1984) δ13C Measurements as indicators of carbon flow in marine and freshwater ecosystems. Contrib Mar Sci 27:13–47Google Scholar
  15. Hesslein RH, Capel MD, Fox DE, Hallard KA (1992) Stable isotopes of sulfur, carbon and nitrogen as indicators of trophic level and fish migration in the lower MacKenzie River Basin, Canada. Can J Fish Aquat Sci 48:2258–2265CrossRefGoogle Scholar
  16. Hilderbrand GV, Farley SD, Robbins CT, Hanley TA, Titus K, Servheen C (1996) Use of stable isotopes to determine diets of living and extinct bears. Can J Zool 74:2080–2088. doi:10.1139/z96-236 CrossRefGoogle Scholar
  17. Hirons AC, Scell DM, Finney BP (2001) Temporal records of δ13C and δ15N in North Pacific pinnipeds: inferences regarding environmental change and diets. Oecologia 129:591–601Google Scholar
  18. Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor 94:181–188. doi:10.2307/1368807 CrossRefGoogle Scholar
  19. Hobson KA, Welch HE (1992) Determination of trophic relationships within a high Arctic marine food web using δ13C and δ15N analysis. Mar Ecol Prog Ser 84:9–18. doi:10.3354/meps084009 CrossRefGoogle Scholar
  20. Hobson KA, McLellan BN, Woods JG (2000) Using stable carbon (δ13C) and nitrogen (δ15N) isotopes to infer trophic relationships among black and grizzly bears in the upper Columbia River basin, British Columbia. Can J Zool 78:1332–1339. doi:10.1139/cjz-78-8-1332 CrossRefGoogle Scholar
  21. Inoue T (1972) The food habit of the Tsushima leopard cat, Felis bengalensis spp., analyzed from their scats. J Mammal Soc Jpn 5:155–169 (in Japanese with English Summary)Google Scholar
  22. Izawa M, Doi T, Ono Y (1991) Ecological study on the two species of Felidae in Japan. In: Maruyama N, Bobek B, Ono Y, Regelin W, Bartos L, Ratcliffe PR (eds) Wildlife conservation: present trends and perspectives for the 21st century, proceedings of the fifth international congress on ecology, Yokohama. Japan Wildlife Research Center, Tokyo, pp 141–143Google Scholar
  23. Kelly JK (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can J Zool 78:1–27. doi:10.1139/cjz-78-1-1 CrossRefGoogle Scholar
  24. Kurle CM, Worthy GAJ (2001) Stable isotope assessment of temporal and geographic differences in feeding ecology of northern fur seals (Callorhinus ursinus) and their prey. Oecologia 126:254–265. doi:10.1007/s004420000518 CrossRefGoogle Scholar
  25. Kurose N, Masuda R, Tatara M (2005) Fecal DNA analysis for identifying species and sex of sympatric carnivores: a noninvasive method for conservation on the Tsushima Islands, Japan. J Hered 96:688–697. doi:10.1093/jhered/esi124 PubMedCrossRefGoogle Scholar
  26. Long ES, Richard AS, Diefenbach DR, Ben-David M (2005) Controlling for anthropogenically induced atmospheric variation in stable carbon isotope studies. Oecologia 146:148–156. doi:10.1007/s00442-005-0181-6 PubMedCrossRefGoogle Scholar
  27. Maruyama N, Watanabe Y (1993) Increase of the Tsushima-sika population in the Tsushima-sika reserve, Tsushima Islands. In: Ohtaishi N, Sheng H (eds) Deer of China. Elsevier, Amsterdam, pp 258–272Google Scholar
  28. Masuda R, Yoshida MC (1995) Two Japanese wildcats, the Tsushima cat and the Iriomote cat, show the same mitochondrial DNA lineage as the leopard cat Felis bengalensis. Zool Sci 12:655–659PubMedCrossRefGoogle Scholar
  29. McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390. doi:10.1034/j.1600-0706.2003.12098.x CrossRefGoogle Scholar
  30. Michael S, Auerswald SK, Schnyder H (2003) Reconstruction of the isotopic history of animal diets by hair segmental analysis. Rapid Commun Mass Spectrom 17:1312–1318. doi:10.1002/rcm.1042 CrossRefGoogle Scholar
  31. Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta 48:1135–1140. doi:10.1016/0016-7037(84)90204-7 CrossRefGoogle Scholar
  32. Ministry of Agriculture, Forestry and Fisheries of Japan (2002) The world census of agriculture and forestry 2000 (in Japanese)Google Scholar
  33. Ministry of the Environment (2006) Report of the project on rehabilitation of natural habitats and the maintenance for the Tsushima leopard cat (in Japanese)Google Scholar
  34. Mitani N (2005) Food habit of the Tsushima leopard cat, Felis bengalensis euptilura, estimated from carbon and nitrogen stable isotope measurements. PhD thesis, Kyushu UniversityGoogle Scholar
  35. Mitani N, Mihara S, Ishii S, Koike H (2006) Natural distribution of δ13C and δ15N values of flora and fauna in Tsushima. Bull Grad Sch Soc Cult Stud Kyushu Univ 12:25–38Google Scholar
  36. Mizukami RN, Goto M, Izumiyama S, Yoh M, Ogura N, Hayashi H (2005) Temporal diet changes recorded by stable isotopes in Asiatic black bear (Ursus thibetanus) hair. Isotopes Environ Health Stud 41:87–94. doi:10.1080/10256010412331304211 PubMedCrossRefGoogle Scholar
  37. Moleón M, Gil-Sánchez JM (2003) Food habits of the wildcat (Felis silvestris) in a peculiar habitat: the Mediterranean high mountain. J Zool (Lond) 260:17–22Google Scholar
  38. Nowell K, Jackson P (eds) (1996) Wild cats: status survey and conservation action plan. IUCN, GlandGoogle Scholar
  39. Peterson B, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320. doi:10.1146/annurev.es.18.110187.001453 CrossRefGoogle Scholar
  40. Peterson B, Howarth RW (1987) Sulfur, carbon and nitrogen isotopes used to trace organic matter flow in the salt-marsh estuaries of Sapelo Islands, Georgia. Limnol Oceanogr 32:1195–1213CrossRefGoogle Scholar
  41. Phillips DL (2001) Mixing models in analyses of diet using multiple stable isotopes: a critique. Oecologia 127:166–170. doi:10.1007/s004420000571 CrossRefGoogle Scholar
  42. Phillips DL, Gregg JW (2003) Source partitioning using stable isotopes: coping with too many sources. Oecologia 136:261–269. doi:10.1007/s00442-003-1218-3 PubMedCrossRefGoogle Scholar
  43. Phillips DL, Koch PL (2002) Incorporating concentration dependence in stable isotope mixing models. Oecologia 130:114–125Google Scholar
  44. Schmidt K, Nakanishi N, Okamura M, Doi T, Izawa M (2003) Movement and use of home range in the Iriomote cat (Prionailurus bengalensis iriomotensis). J Zool (Lond) 261:273–283. doi:10.1017/S0952836903004205 CrossRefGoogle Scholar
  45. Schoeninger MJ, DeNiro MJ (1984) Nitrogen and carbon isotopic composition of bone collagen from marine and terrestrial animals. Geochim Cosmochim Acta 48:625–639. doi:10.1016/0016-7037(84)90091-7 CrossRefGoogle Scholar
  46. Suda K, Koganezawa M (2002) Natural population density of sika deer considering forest ecosystem biodiversity. Environ Res Q 126:44–49 (in Japanese with English Summary)Google Scholar
  47. Suda K, Araki R, Maruyama N (2001) The effect of sika deer on the structure and composition of the forests on the Tsushima Islands. Biosphere Conserv 4:13–22Google Scholar
  48. Sunde P, Kvam T (1997) Diet patterns of Eurasian lynx Lynx lynx: what causes sexually determined prey size segregation? Acta Theriol 42:189–201Google Scholar
  49. Tans PP, de Jong AFM, Mook WG (1979) Natural atmospheric 14C variation and the Suess effect. Nature 280:826–828. doi:10.1038/280826a0 CrossRefGoogle Scholar
  50. Tatara M, Doi T (1994) Comparative analysis on food habits of Japanese marten, Siberian weasel and leopard cat in the Tsushima Islands, Japan. Ecol Res 9:99–107. doi:10.1007/BF02347247 CrossRefGoogle Scholar
  51. Takeda T, Tanikawa T, Agata W, Hakoyama S (1985) Studies on the ecology and geographical distribution of C3 and C4 grasses: I. Taxonomic and geographical distribution of C3 and C4 grasses in Japan with special reference to climatic conditions. Jpn J Crop Sci 54:54–64 (in Japanese with English Summary)Google Scholar
  52. Thompson DR, Furness WR, Lewis SA (1995) Diets and long-term changes in δ15N and δ13C values in northern fulmars Fulmarus glacialis from two northeast Atlantic colonies. Mar Ecol Prog Ser 125:3–11. doi:10.3354/meps125003 CrossRefGoogle Scholar
  53. Vanderklift MA, Ponsard S (2003) Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136:169–182. doi:10.1007/s00442-003-1270-z PubMedCrossRefGoogle Scholar
  54. Wada E, Terazaki M, Kabaya Y, Nemoto T (1987) 15N and 13C abundances in the Antarctic Ocean with emphasis on the biogeochemical structure of the food web. Deep-Sea Res 34:829–841. doi:10.1016/0198-0149(87)90039-2 CrossRefGoogle Scholar
  55. Wada E, Mizutani H, Minagawa M (1991) The use of stable isotopes for food web analysis. Crit Rev Food Sci Nutr 30:361–371PubMedCrossRefGoogle Scholar
  56. Walker JL, Potter CW, Macko SA (1999) The diets of modern and historic bottlenose dolphin populations reflected through stable isotopes. Mar Mamm Sci 15:335–350. doi:10.1111/j.1748-7692.1999.tb00805.x CrossRefGoogle Scholar
  57. Yamaguchi T, Urata A (1970) Note on the distribution of Prionailurus bengalensis euptilurus (ELLIOT, 1871) in the Tsushima Islands Nagasaki Pre. Japan. Bull Fac Edu (Nat Sci) Nagasaki Univ 11:25–39 (in Japanese with English Summary)Google Scholar
  58. Yamaguchi T, Urata A (1976) The Tsushima leopard cat. In: Nagasaki Biological Society (ed) Life in Tsushima. Nagasaki Biological Society, Nagasaki, pp 155–166 (in Japanese)Google Scholar

Copyright information

© The Ecological Society of Japan 2009

Authors and Affiliations

  • Naho Mitani
    • 1
  • Shozo Mihara
    • 2
  • Nobuo Ishii
    • 3
  • Hiroko Koike
    • 4
  1. 1.Japan Wildlife Research CenterTokyoJapan
  2. 2.Research Facility Center for Science and TechnologyUniversity of TsukubaTsukubaJapan
  3. 3.College of Arts and SciencesTokyo Woman’s Christian UniversityTokyoJapan
  4. 4.Graduate School of Social and Cultural StudiesKyushu University, FukuokaFukuoka CityJapan

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