Advertisement

Mammalian Biology

, Volume 79, Issue 2, pp 123–131 | Cite as

Factors and mechanisms that explain coexistence in a Mediterranean carnivore assemblage: An integrated study based on camera trapping and diet

  • J. BarrullEmail author
  • I. Mate
  • J. Ruiz-Olmo
  • J. G. Casanovas
  • J. Gosàlbez
  • M. Salicrú
Original Investigation

Abstract

To promote management and conservation, it is useful to identify the factors that determine species distribution and to understand the mechanisms that regulate the organization of species assemblages or influence the dynamics of communities. Using information provided by 842 camera-trap photos and 8175 scats, we studied the factors that favour the coexistence of European badgers (Meles meles), red foxes (Vulpes vulpes) and stone martens (Martes foina) in a Mediterranean, agroforestry environment in the Iberian Peninsula. With extensive, simultaneous occupation of the space, and simultaneous activity during a broad time period (basically nocturnal and crepuscular activity patterns), the carnivores displayed different strategies depending on the availability of resources. In summer when plant resources were abundant and easy to access, there was a high overlap in patterns of diet and activity, and the temporal avoidance of the superior competitor allowed joint use of the same plots. In autumn, when there were fewer resources (although still sufficient) that were harder to access, the maintenance of food overlap was compensated for by avoidance and a reduction in overlapping activity. In winter and spring, the differentiation in response behaviour was evident in the partial substitution of plant resources.

Differentiation in niche dimensions has been linked to complementarity, the differential needs and capacities of each species, and their biology. Differentiation in response behaviour was compatible with the hierarchical structure of the carnivores: European badger; red fox; stone marten. Knowledge of these factors and mechanisms increases our understanding and can help in the prediction of responses to disturbances. Consequently, it helps to improve management and conservation actions.

Keywords

Martes foina Meles meles Vulpes vulpes Carnivore assemblage Coexistence mechanisms 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ables, E.D., 1969. Activity studies of red foxesin southern Wisconsin. J.Wildl. Manag. 33, 145–153.CrossRefGoogle Scholar
  2. Ables, E.D., 1975. Ecology of the red fox in North America. In: Fox, M.W. (Ed.), The Wild Canids. Their Systematics, Behavioral Ecology and Evolution. Litton Educational Publishing, Washington, pp. 216–236.Google Scholar
  3. Amarasekare, P., 2009. Competition and coexistence in animal communities. In: Levin, S.A. (Ed.), The Princeton Guide to Ecology. Princeton University Press, Princeton, NJ, pp. 196–201.CrossRefGoogle Scholar
  4. Artois, M., 1989. Encyclopédie des Carnivores de France. Vol. 3. Le renard roux. Société Franc¸ aise pour l’Étude et la Protection des Mammifères, Bourges.Google Scholar
  5. Bang, P., Dahlstrøm, P., 2007. Animal Tracks and Signs. Oxford University Press, New York.Google Scholar
  6. Barrientos, R., Virgós, E., 2006. Reduction of potential food interference in two sym-patric carnivores by sequential use of shared resources. Acta Oecol. 30 (1), 107–116.CrossRefGoogle Scholar
  7. Barrull, J., Mate, I., 2007a. Fauna vertebrada del Parc Natural de la Serra de Montsant. Diputació de Tarragona, Tarragona.Google Scholar
  8. Barrull, J., Mate, I., 2007b. La guineu a Catalunya. Agulla de Cultura Popular, Tarragona.Google Scholar
  9. Barrull, J., Mate, I., Soler, J., 2007. Atles dels amfibis i rèptils del Parc Natural de la Serra de Montsant. Generalitat de Catalunya, Departament de Medi Ambient i Habitatge, Barcelona.Google Scholar
  10. Barrull, J., Mate, I., Casanovas, J.G., Salicrú, M., Gosàlbez, J., 2011. Selectivity of mammalian predator control in managed hunting areas: an example in a Mediterranean environment. Mammalia 75 (4), 363–369,  https://doi.org/10.1515/MAMM.2011.052.CrossRefGoogle Scholar
  11. Beja, P., Gordinho, L., Reino, L., Loureiro, F., Santos-Reis, M., Borralho, R., 2009. Predator abundance in relation to small game management in southern Portugal: conservation implications. Eur. J. Wildl. Res. 55, 227–238,  https://doi.org/10.1007/s10344-008-0236-1.CrossRefGoogle Scholar
  12. Biknevicius, A.R., Van Valkenburgh, B., 1996. Desing for killing: craniodental adaptations of predators. In: Gittleman, J.L. (Ed.), Carnivore Behavior, Ecology, and Evolution, vol. 2. Cornell University Press, Ithaca, New York, pp. 393–428.Google Scholar
  13. Blanco, J.C., 1986. On the diet, size and use of home range and activity patterns of a red fox in Central Spain. Acta Theriol. 31 (40), 547–556.CrossRefGoogle Scholar
  14. Boitani, L., Vinditti, R.M., 1988. La volpe rosa. Edagricole, Bologna.Google Scholar
  15. Brashares, J.S., Prugh, L.R., Stoner, C.J., Epps, C.W., 2010. Ecological and conservation implications of mesopredator release. In: Terborgh, J., Estes, J.A. (Eds.), Trophic Cascades: Predators, Preys, and the Changing Dynamics of Nature. Island Press, Washington, pp. 221–240.Google Scholar
  16. Canova, L., Rosa, P., 1993. Badger Meles meles and fox Vulpes vulpes food in agricultural land in the western Po plain (Italy). Hystrix (n.s.) 5 (1–2), 73–78.Google Scholar
  17. Casanovas, J.G., Barrull, J., Mate, I., Zorrilla, J.M., Ruiz-Olmo, J., Gosàl-bez, J., Salicrú, M., 2012. Shaping carnivore communities by predator control: competitor released revisited. Ecol. Res. 27 (3), 603–614,  https://doi.org/10.1007/s11284-012-0931-y.CrossRefGoogle Scholar
  18. Cavallini, P., 1994. Faeces count as an index of fox abundance. Acta Theriol. 39 (4), 417–424.CrossRefGoogle Scholar
  19. Chase, J.M., Leibold, M.A., 2003. Ecological Niches: Linking Classical and Contemporary Approaches. Chicago University Press, Chicago.CrossRefGoogle Scholar
  20. Chesson, P., 2000. Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Syst. 31, 343–366,  https://doi.org/10.1146/annurev.ecolsys.31.1.343.CrossRefGoogle Scholar
  21. Creel, S., Spong, G., Creel, N., 2001. Interspecific competition and the population biology of extinction-prone carnivores. In: Gittleman, J.L., Funk, S.M., Macdon-ald, D., Wayne, R.K. (Eds.), Carnivore Conservation. Cambridge University Press, Cambridge, pp. 35–60.Google Scholar
  22. Davison, A., Birks, J.D.S., Brookes, R.C., Braithwaite, T.C., Messenger, J.E., 2002. On the origin of faeces: morphological versus molecular methods for surveying rare carnivores from their scats. J. Zool. 257, 141–143.CrossRefGoogle Scholar
  23. Dierenfeld, E.S., Alcorn, H.L., Jacobsen, K.L., 2002. Nutrient Composition of Whole Vertebrate Prey (Excluding Fish) Fed in Zoos. US Department of Agricultu, Agricultural Research Service, National Agricultural Library, Animal Welfare Information Center, Beltsville.Google Scholar
  24. Donadio, E., Buskirk, S.W., 2006. Diet, morphology, and interspecific killing in car-nivora. Am. Nat. 167 (4), 524–536,  https://doi.org/10.1086/501033.CrossRefGoogle Scholar
  25. Ferrari, N., (Ph.D. thesis) 1997. Eco-éthologie du blaireau européen (Meles meles L. 1758) dans le Jura suisse: comparaison de deux populations vivant en milieu montagnard et en milieu cultivé de plaine. Faculty of Science, University of Neuchâtel, Neuchâtel.Google Scholar
  26. Fraigneau, C., 2007. Reconnaître facilement les plumes. Delachaux et Niestlé, Paris. Frye, F.L., 1991. Reptile Diseases An Atlas of Care and Treatment. TFH Publishing, Inc., Neptune City.Google Scholar
  27. Genovesi, P., Secchi, M., Boitani, L., 1996. Diet of stone martens: an example of ecological flexibility. J. Zool. 238, 545–555,  https://doi.org/10.1111/j.1469-7998.1996.tb05412.x.CrossRefGoogle Scholar
  28. Genovesi, P., Sinibaldi, J., Boitani, L., 1997. Spacing patterns and territoriality of the stone marten. Can. J. Zool. 75, 1966–1971,  https://doi.org/10.1139/z97-828.CrossRefGoogle Scholar
  29. Güthlin, D., Kröschel, M., Küchenhoff, H., Storch, I., 2012. Faecal sampling along trails: a questionable standard for estimating red fox Vulpes vulpes abundance. Wildl. Biol. 18, 374–382,  https://doi.org/10.2981/11-065.CrossRefGoogle Scholar
  30. Harde, K.W., Severa, F., 1998. A Field Guide in Colour to Beetles. Blitz Editions, Leicester.Google Scholar
  31. Harmsen, B.J., (Ph.D. thesis) 2006. The Use of Camera Traps for Estimating Abundance and Studying the Ecology of Jaguars (Panthera onca). Department of Biology, University of Southampton, Southampton.Google Scholar
  32. Henry, C., Lafontaine, L., Mouches, A., 1988. Le blaireau (Meles meles L., 1758). Ency-clopèdie des Carnivores de France, vol. 7. Société Franc¸ aise pour l’Étude et la Protection des Mammifères, Bohallard.Google Scholar
  33. Jȩdrzejewski, W., Sidorovich, V., 2010. The Art of Tracking Animals. Mammal Research Institute Polish Academy of Science, Białowiez˙ a.Google Scholar
  34. Johnson, W.E., Franklin, W.L., 1994. Spatial resource partitioning by sympatric grey fox (Dusicyon griseus) and culpeo fox (Dusicyon culpaeus) in southern Chile. Can. J. Zool. 72, 1788–1793,  https://doi.org/10.1139/z94-242.CrossRefGoogle Scholar
  35. Johnson, W.E., Eizirik, E., Lento, G.M., 2001. The control, exploitation, and conservation of carnivores. In: Gittleman, J.L., Funk, S.M., Macdonald, D., Wayne, R.K. (Eds.), Carnivore Conservation. Cambridge University Press, Cambridge, pp. 196–219.Google Scholar
  36. Kays, R.W., Slauson, K.M., 2008. Remote cameras. In: Long, R.A., MacKay, P., Zielinski, W.J., Ray, J.C. (Eds.), Noninvasive Survey Methods for Carnivores. Island Press, Washington, pp. 110–140.Google Scholar
  37. Kronfeld-Schor, N., Dayan, T., 2003. Partitioning of time as ecological resource. Annu. Rev. Ecol. Syst. 34, 153–181,  https://doi.org/10.1146/annurev.ecolsys.34.011802.132435.CrossRefGoogle Scholar
  38. Lenth, R.V., 1989. Quick and easy analysis of unreplicated factorials. Technome 31, 469–473.CrossRefGoogle Scholar
  39. Libois, R., Waechter, A., 1991. Le fouine (Martes foina Erxleben, 1777). Encyclopèdie des Carnivores de France, vol. 10. Société Franc¸ aise pour l’Étude et la Protection des Mammifères, Paris.Google Scholar
  40. Lindström, E.R., Brainerd, S.M., Helldin, J.O., Overskaug, K., 1995. Pine marten–red fox interactions: a case intraguild predation? Ann. Zool. Fenn. 32, 123–130.Google Scholar
  41. Litvaitis, J.A., 2000. Investigating food habits of terrestrial vertebrates. In: Boitani, L., Fuller, T.K. (Eds.), Research Techniques in Animal Ecology. Controversies and Consequences. Columbia University Press, New York, pp. 165–190.Google Scholar
  42. Long, R.A., Zielinski, W.J., 2008. Designing effective noninvasive carnivore surveys. In: Long, R.A., MacKay, P., Zielinski, W.J., Ray, J.C. (Eds.), Noninvasive Survey Methods for Carnivores. Island Press, Washington, pp. 8–44.Google Scholar
  43. López-Martín, J.M., 2006. Comparison of feeding behaviour between stone marten and common genet: living in coexistence. In: Santos-Reis, M., Birks, J.D.S., O’Doherty, E.C., Proulx, G. (Eds.), Martes in Carnivore Communities. Alpha Wildlife Publications, Sherwood Park, Alberta, pp. 137–155.Google Scholar
  44. Lucherini, M., Reppucci, J.I., Walter, R.S., Villalba, M.L., Wurstten, A., Gallardo, G., Iriarte, A., Villalobos, R., Perovic, P., 2009. Activity pattern segregation of carnivores in the High Andes. J. Mammal. 90 (6), 1404–1409,  https://doi.org/10.1644/09-MAMM-A-002R.1.CrossRefGoogle Scholar
  45. MacArthur, R.H., Levins, R., 1967. The limiting similarity, convergence and divergence of coexisting species. Am. Nat. 101, 377–385.CrossRefGoogle Scholar
  46. Macdonald, D.W., 1987. Runnig with the fox. Unwin Hyman, London.Google Scholar
  47. Macdonald, D.W., Buesching, C.D., Stopka, P., Henderson, J., Ellwood, S.A., Baker, S.E., 2004. Encounters between two sympatric carnivores: red foxes (Vulpes vulpes) and European badgers (Meles meles). J. Zool. (Lond.) 263 (4), 385–392,  https://doi.org/10.1017/S0952836904005400.CrossRefGoogle Scholar
  48. Maffei, L., Cuellar, E., Noss, A., 2004. One thousand jaguars (Panthera onca) in Bolivia’s Chaco? Camera trapping in Kaalya National Park. J. Zool. (Lond.) 262 (3), 295–304,  https://doi.org/10.1017/S0952836903004655.CrossRefGoogle Scholar
  49. Mangas, J.G., Lozano, J., Cabezas-Díaz, S., Virgós, E., 2008. The priority value of scrubland habitats for carnivore conservation in Mediterranean ecosystems. Biodivers. Conserv. 17, 43–51,  https://doi.org/10.1007/s10531-007-9229-8.CrossRefGoogle Scholar
  50. Mate, I., Barrull, J., 2010. Primera cita de visón americano Neovison vison (Schreber, 1777) en el río Montsant (Tarragona). Galemys 22, 63–65.Google Scholar
  51. McNab, B.K., 1989. Basal rate of metabolism, body size and food habits in the order Carnivora. In: Gittleman, J.L. (Ed.), Carnivore Behavior, Ecology, and Evolution, vol. 1. Cornell University Press, Ithaca, New York, pp. 335–354.CrossRefGoogle Scholar
  52. Mouches, A., (Thèse de doctorat) 1981. Éco-éthologie du blaireau européen Meles meles L.: stratégies d’utilitsation de l’habitat et des resources alimentaires. Uni-vesité de Rennes I, pp. 130.Google Scholar
  53. Mulder, J.L., 1990. The stoat Mustela erminea in the Duch dune region, its local extinction, and possible cause: the arrival of the red fox Vulpes vulpes. Lutra 33, 1–21.Google Scholar
  54. Olmo, J.M., 2006. Atles dels ortòpters de Catalunya i llibre vermell. Generalitat de Catalunya, Departament de Medi Ambient i Habitatge, Barcelona.Google Scholar
  55. Ozolins, J., Pilats, V., 1995. Distribution and status of small and medium-sized carnivores in Latvia. Ann. Zool. Fennici 32, 21–29.Google Scholar
  56. Padial, J.M., Ávila, E., Gil-Sánchez, J.M., 2002. Feeding habits and overlap among red fox (Vulpes vulpes) and stone marten (Martes foina) in two Mediterranean mountain habitats. Mamm. Biol. Z. Saügertierk 67, 137–146.CrossRefGoogle Scholar
  57. Palomares, F., Caro, T.M., 1999. Interspecific killing among mammalian carnivores. Am. Nat. 153 (5), 492–508,  https://doi.org/10.1086/303189.PubMedCrossRefPubMedCentralGoogle Scholar
  58. Posillico, M., Serafini, P., Lovari, S., 1995. Activity patternsof the stone marten Martes foina Erxleben, 1777, in relation to some environmental factors. Hystryx (n.s.) 7 (1–2), 79–97.Google Scholar
  59. Posluszny, M., Pilot, M., Goszczynski, J., Gralak, B., 2007. Diet of sympatric pine marten(Martesmartes)andstonemarten(Martesfoina)identifiedbygenotyping of DNA from faeces. Ann. Zool. Fennici 44, 269–284.Google Scholar
  60. Prigioni, C., Balestrieri, A., Remonti, L., Cavada, L., 2008. Differential use of food and habitat by sympatric carnivores in the eastern Italian Alps. Ital. J. Zool. 75, 173–184,  https://doi.org/10.1080/11250000701885521.CrossRefGoogle Scholar
  61. Rabinowitz, A.R., Nottingham, G., 1986. Ecology and behaviour of the jaguar (Panthera onca) in Belize, Central America. J. Zool. (Lond.) 210 (1), 149–159,  https://doi.org/10.1111/j.1469-7998.1986.tb03627.x.CrossRefGoogle Scholar
  62. Randa, L.A., Cooper, D.M., Meserve, P.L., Yunger, J.A., 2009. Prey switching of sym-patric canids in response to variable prey abundance. J. Mammal. 90 (3), 594–603,  https://doi.org/10.1644/08-MAMM-A-092R1.1.CrossRefGoogle Scholar
  63. Roberts, M.J., 1995. Field Guide Spiders of Britain and Northern Europe. Harper Collins, London.Google Scholar
  64. Roper, T.J., 2010. Badger. Collins, London.Google Scholar
  65. Rosalino, L.M., Santos-Reis, M., 2001. Fruits and mesocarnivores in Mediterranean Europe. In: Rosalino, L.M., Gheler-Costa, G. (Eds.), Middle-Sized Carnivores in Agricultural Landscapes. Nova Science Publishers, New York, pp. 69–82.Google Scholar
  66. Rosenzweig, M.L., 1966. Community structure in sympatric carnivora. J. Mammal. 47 (4), 602–612.CrossRefGoogle Scholar
  67. Ruiz-Olmo, J., 1988. El poblament dels grans mamífers a Catalunya. I. Carnívors: Distribució i requeriments ambientals. Butll. Inst. Cat. Hist. Nat. 58 (8), 87–98.Google Scholar
  68. Salicrú, M., Fleurent, C., Armengol, J.M., 2011. Timetable-based operation in urban transport: run-time optimisation and improvements in the operating process. Transport. Res. A 45, 721–740.Google Scholar
  69. Sillero-Zubiri, C., 2009. Family Canidae (dogs). In: Wilson, D.E., Mittermeir, R.A. (Eds.), HandbookoftheMammalsofthe World. Vol.1.Carnivores. LynxEdicions, Barcelona, pp. 352–446.Google Scholar
  70. Schoener, T.W., 1970. Non-synchronous spatial overlap of lizards in patchy habitats.CrossRefGoogle Scholar
  71. Schoener, T.W., 1974. Resource partitioning in ecological communities. Science 185 (4145), 27–39,  https://doi.org/10.1126/science.185.4145.27.PubMedPubMedCentralCrossRefGoogle Scholar
  72. Schoener, T.W., 2009. Ecological niche. In: Levin, S.A. (Ed.), The Princeton Guide to Ecology. Princeton University Press, Princeton, New Jersey, pp. 3–13.CrossRefGoogle Scholar
  73. Sorensen, T., 1948. A method of establishing groups of equal amplitude in plant sociology based on similarity of species content and its application to analyses of the vegetation on Danish commons. Kong. Danish Vidensk. Selsk. Biol. Skr. (Copenhagen) 5, 1–34.Google Scholar
  74. Teerink, B.J., 1991. Atlas and Identification Key Hair of West-European Mammals. Cambridge University Press, Cambridge.Google Scholar
  75. Tokeshi, M., 1999. Species Coexistence. Ecological and Evolutionary Perspectives. Blackwell Science, Oxford.Google Scholar
  76. Tuyttens, F.A.M., Macdonald, D.W., 2000. Consequences of social perturbation for wildlife management and conservation. In: Gosling, M.L., Sutherland, W.J. (Eds.), Behaviour and Conservation. Cambridge University Press, Cambridge, pp. 315–329.Google Scholar
  77. Verdade, L.M., Rosalino, L.M., Gheler-Costa, C., Pedrosa, N.M., Lyra-Jorge, M.C., 2011. Adaptationofmesocarnivores(Mammalia:Carnivora)toagriculturallandscapes in Mediterranean Europe and southeastern Brazil: a trophic perspective. In: Rosalino, L.M., Gheler-Costa, C. (Eds.), Middle-Sized Carnivores in Agricultural Landscapes. Nova Science Publishers, New York, pp. 1–38.Google Scholar
  78. Virgós, E., 2001. Relative value of riparian woodlands in landscapes with different forest cover for medium-sized Iberian carnivores. Biodivers. Conserv. 10 (7), 1039–1049,  https://doi.org/10.1023/A:1016684428664.CrossRefGoogle Scholar
  79. Webbon, C.C., Baker, P.J., Harris, S., 2004. Faecal density counts for monitoring changes in red fox numbers in rural Britain. J. Appl. Ecol. 41 (4), 768–779,  https://doi.org/10.1111/j.0021-8901.2004.00930.x.CrossRefGoogle Scholar
  80. White, J., 1988. Basic Wildlife Rehabilitation. International Wildlife Rehabilitation Council, Suisun.Google Scholar
  81. Woodroffe, R., 2001. Strategies for carnivore conservation: lessons from contemporary extinctions. In: Gittleman, J.L., Funk, S.M., Macdonald, D., Wayne, R.K. (Eds.), Carnivore Conservation. Cambridge University Press, Cambridge, pp. 61–92.Google Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2014

Authors and Affiliations

  • J. Barrull
    • 1
    Email author
  • I. Mate
    • 1
  • J. Ruiz-Olmo
    • 2
  • J. G. Casanovas
    • 3
  • J. Gosàlbez
    • 1
  • M. Salicrú
    • 4
  1. 1.Department of Animal Biology, Faculty of BiologyUniversity of BarcelonaBarcelonaSpain
  2. 2.General Directorate of Natural Environment and Biodiversity, Department of AgricultureLivestock, Fisheries, Nourishment and Natural Environment, Generalitat of CataloniaBarcelonaSpain
  3. 3.Hydrobiology and Game, Superior Technical School of Forestry EngineersPolytechnic University of MadridMadridSpain
  4. 4.Department of Statistics, Faculty of BiologyUniversity of BarcelonaBarcelonaSpain

Personalised recommendations