Advertisement

Oecologia

, Volume 179, Issue 3, pp 835–842 | Cite as

Upscaling the niche variation hypothesis from the intra- to the inter-specific level

  • Marjorie Bison
  • Sébastien Ibanez
  • Claire Redjadj
  • Frédéric Boyer
  • Eric Coissac
  • Christian Miquel
  • Delphine Rioux
  • Sonia Said
  • Daniel Maillard
  • Pierre Taberlet
  • Nigel Gilles Yoccoz
  • Anne Loison
Community ecology - Original research

Abstract

The “niche variation hypothesis” (NVH) predicts that populations with wider niches should display higher among-individual variability. This prediction originally stated at the intra-specific level may be extended to the inter-specific level: individuals of generalist species may differ to a greater extent than individuals of a specialist species. We tested the NVH at intra- and inter-specific levels based on a large diet database of three large herbivore feces collected in the field and analyzed using DNA metabarcoding. The three herbivores (roe deer Capreolus capreolus, chamois Rupicapra rupicapra and mouflon Ovis musimon) are highly contrasted in terms of sociality (solitary to highly gregarious) and diet. The NVH at the intraspecific level was tested by relating, for the same population, diet breadth and inter-individual variation across the four seasons. Compared to null models, our data supported the NVH both at the intra- and inter-specific levels. Inter-individual variation of the diet of solitary species was not larger than in social species, although social individuals feed together and could therefore have more similar diets. Hence, the NVH better explained diet breadth than other factors such as sociality. The expansion of the population niche of the three species was driven by resource availability, and achieved by an increase in inter-individual variation, and the level of inter-individual variability was larger in the generalist species (mouflon) than in the specialist one (roe deer). This mechanism at the base of the NVH appears at play at different levels of biological organization, from populations to communities.

Keywords

Individual heterogeneity Sociality Large herbivores DNA metabarcoding Null models 

Notes

Acknowledgments

We warmly thank J.-M. Jullien and T. Chevrier for collecting the feces during the animal captures and field workers for feces sampling in the field. We also thank ONCFS and CNRS for funding the barcoding analyses and the Natural Regional Park of Bauges massif for data provision.

Author contribution statement

AL, DM and SS originally developed the idea. MB, SI, NGY, AL analyzed the data and wrote the first draft of the manuscript. SI and NGY developed the mathematical model of a new null model. CM, PT, CR, DR developed the DNA metabarcoding methods and applied it on feces. CR performed the feces sampling, laboratory experiments (DNA metabarcoding on feces), database treatment and preliminary analyses. FB and EC performed the statistical analyses and the database treatment of DNA sequences. All authors commented and approved the ms.

Supplementary material

442_2015_3390_MOESM1_ESM.docx (92 kb)
Supplementary material 1 (DOCX 91 kb)

References

  1. Abbas F, Picot D, Merlet J, Cargnelutti B, Lourtet B, Angibault JM, Daufresne T, Aulagnier S, Verheyden H (2013) A typical browser, the roe deer, may consume substantial quantities of grasses in open landscapes. Eur J Wildl Res 59(1):69–75CrossRefGoogle Scholar
  2. Ainsworth CH, Kaplan IC, Levin PS, Mangel M (2010) A statistical approach for estimating fish diet compositions from multiple data sources: Gulf of california case study. Ecol Appl 20(8):2188–2202CrossRefPubMedGoogle Scholar
  3. Araújo M, Gonzaga M (2007) Individual specialization in the hunting wasp Trypoxylon (Trypargilum) albonigrum (Hymenoptera, Crabronidae). Behav Ecol Sociobiol 61(12):1855–1863CrossRefGoogle Scholar
  4. Araújo MS, dos Reis SF, Giaretta AA, Machado G, Bolnick DI (2007) Intrapopulation diet variation in four frogs (Leptodactylidae) of the Brazilian Savannah. Copeia 4:855–865CrossRefGoogle Scholar
  5. Araújo M, Guimarães P Jr, Svanbäck R, Pinheiro A, Guimarães P, Reis S, Bolnick D (2008) Network analysis reveals contrasting effects of intraspecific competition on individual vs. population diets. Ecology 89(7):1981–1993CrossRefPubMedGoogle Scholar
  6. Araújo M, Bolnick D, Martinelli L, Giaretta A, Dos Reis S (2009) Individual-level diet variation in four species of Brazilian frogs. J Anim Ecol 78(4):848–856CrossRefPubMedGoogle Scholar
  7. Araújo MS, Bolnick DI, Layman CA (2011) The ecological causes of individual specialisation. Ecol Lett 14(9):948–958CrossRefPubMedGoogle Scholar
  8. Bertolino S, Di Montezemolo N, Bassano B (2009) Food–niche relationships within a guild of alpine ungulates including an introduced species. J Zool 277(1):63–69CrossRefGoogle Scholar
  9. Bolnick D, Yang L, Fordyce J, Davis J, Svanbäck R (2002) Measuring individual-level resource specialization. Ecology 83(10):2936–2941CrossRefGoogle Scholar
  10. Bolnick D, Svanbäck R, Fordyce J, Yang L, Davis J, Hulsey C, Forister M (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161(1):1–28CrossRefPubMedGoogle Scholar
  11. Bolnick D, Svanbäck R, Araújo M, Persson L (2007) Comparative support for the niche variation hypothesis that more generalized populations also are more heterogeneous. Proc Natl Acad Sci USA 104(24):10075–10079Google Scholar
  12. Bolnick DI, Ingram T, Stutz WE, Snowberg LK, Lau OL, Paull JS (2010) Ecological release from interspecific competition leads to decoupled changes in population and individual niche width. Proc R Soc Lond B 277(1689):1789–1797CrossRefGoogle Scholar
  13. Boschi C, Nievergelt B (2003) The spatial patterns of alpine chamois (Rupicapra rupicapra rupicapra) and their influence on population dynamics in the Swiss National Park. Mamm Biol 68:16–30Google Scholar
  14. Castle EJ (1956) The rate of passage of foodstuffs through the alimentary tract of the goat. Br J Nutr 10(02):115–125CrossRefPubMedGoogle Scholar
  15. Chase JM, Kraft NJ, Smith KG, Vellend M, Inouye BD (2011) Using null models to disentangle variation in community dissimilarity from variation in α-diversity. Ecosphere 2(2):art24Google Scholar
  16. Clauss M, Lechner-Doll M, Streich W (2003) Ruminant diversification as an adaptation to the physicomechanical characteristics of forage. Oikos 102(2):253–262CrossRefGoogle Scholar
  17. Clavel J, Julliard R, Devictor V (2010) Worldwide decline of specialist species: toward a global functional homogenization? Front Ecol Environ 9(4):222–228CrossRefGoogle Scholar
  18. Costa GC, Mesquita DO, Colli GR, Vitt LJ (2008) niche expansion and the niche variation hypothesis: does the degree of individual variation increase in depauperate assemblages? Am Nat 172(6):868–877CrossRefPubMedGoogle Scholar
  19. Cransac N, Gerard JF, Maublanc ML, Pépin D (1998) An example of segregation between age and sex classes only weakly related to habitat use in mouflon sheep (ovis gmelini). J Zool 244(03):371–378CrossRefGoogle Scholar
  20. Darmon G, Calenge C, Loison A, Jullien JM, Maillard D, Lopez JF (2012) Spatial distribution and habitat selection in coexisting species of mountain ungulates. Ecography 35(1):44–53CrossRefGoogle Scholar
  21. Devictor V, Clavel J, Julliard R, Lavergne S, Mouillot D, Thuiller W, Venail P, Villeger S, Mouquet N (2009) Defining and measuring ecological specialization. J Appl Ecol 47(1):15–25CrossRefGoogle Scholar
  22. Duparc A, Redjadj C, Viard-Crétat F, Lavorel S, Austrheim G, Loison A (2012) Co-variation between plant above-ground biomass and phenology in sub-alpine grasslands. Appl Veg Sci 16(2):305–316Google Scholar
  23. Dzieciolowski R (1979) Structure and spatial-organization of deer populations. Acta Theriol 24(1–11):3–21CrossRefGoogle Scholar
  24. Ferrari S, Cribari-Neto F (2004) Beta regression for modelling rates and proportions. J Appl Stat 31:799–815CrossRefGoogle Scholar
  25. Fritz H, Loison A (2006) Large herbivores across biomes. In: Dannell K, Duncan O, Bergström R, Pastor R (eds) Large herbivores ecology, ecosystem dynamics and conservation. Cambridge Unversity Press, London, pp 19–49Google Scholar
  26. Gerardo Herrera ML, Korine C, Fleming TH, Arad Z (2008) Dietary implications of intrapopulation variation in nitrogen isotope composition of an old world fruit bat. J Mammal 89(5):1184–1190CrossRefGoogle Scholar
  27. Hofmann R (1989) Evolutionary steps of ecophysiological adaptation and diversification of ruminants: a comparative view of their digestive system. Oecologia 78(4):443–457CrossRefGoogle Scholar
  28. Hutchinson G (1957) Concluding remarks. Cold Spring Harb Symp Quant Biol 22:415–427CrossRefGoogle Scholar
  29. Jarman P (1974) The social organisation of antelope in relation to their ecology. Behaviour 48:215–267CrossRefGoogle Scholar
  30. Knudsen R, Amundsen P, Primicerio R, Klemetsen A, Sorensen P (2007) Contrasting niche-based variation in trophic morphology within arctic charr populations. Evol Ecol Res 9(6):1005–1021Google Scholar
  31. Martins E, Araújo M, Bonato V, Reis S (2008) Sex and season affect individual-level diet variation in the neotropical marsupial Gracilinanus microtarsus (didelphidae). Biotropica 40(1):132–135Google Scholar
  32. Pires MM, Martins EG, Araújo MS, Reis SF (2013) Between-individual variation drives the seasonal dynamics in the trophic niche of a neotropical marsupial. Austral Ecol 38:664–671CrossRefGoogle Scholar
  33. Pompanon F, Deagle B, Symondson W, Brown D, Jarman S, Taberlet P (2012) Who is eating what: diet assessment using next generation sequencing. Mol Ecol 21:1931–1950CrossRefPubMedGoogle Scholar
  34. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  35. Rayé G, Miquel C, Coissac E, Redjadj C, Loison A, Taberlet P (2011) New insights on diet variability revealed by DNA barcoding and high-throughput pyrosequencing: chamois diet in autumn as a case study. Ecol Res 26(2):265–276CrossRefGoogle Scholar
  36. Redjadj C (2010) Etude inter-et intra-spécifique des variations spatio-temporelles de l’utilisation des ressources alimentaires au sein d’une communauté de grands herbivores de montagne. PhD thesis, Université de Grenoble, GrenobleGoogle Scholar
  37. Redjadj C, Darmon G, Maillard D, Chevrier T, Bastianelli D, Verheyden H, Loison A, Saïd S (2014) Intra-and interspecific differences in diet quality and composition in a large herbivore community. PloS ONE 9(2):e84756PubMedCentralCrossRefPubMedGoogle Scholar
  38. Roughgarden J (1972) Evolution of niche width. Am Nat 106:683–718CrossRefGoogle Scholar
  39. Roughgarden J (1974) niche width: biogeographic patterns among anolis lizard populations. Am Nat 108:429–442CrossRefGoogle Scholar
  40. Schoener TW (1968) The anolis lizards of bimini: resource partitioning in a complex fauna. Ecology 49:704–726CrossRefGoogle Scholar
  41. Svanbäck R, Bolnick DI (2007) Intraspecific competition drives increased resource use diversity within a natural population. Proc R Soc Lond B 274(1611):839–844CrossRefGoogle Scholar
  42. Taberlet P, Coissac E, Pompanon F, Gielly L, Miquel C, Valentini A, Vermat T, Corthier G, Brochmann C, Willerslev E (2007) Power and limitations of the chloroplast trnl (UAA) intron for plant DNA barcoding. Nucleic Acids Res 35(3):e14–e14PubMedCentralCrossRefPubMedGoogle Scholar
  43. Tinker MT, Bentall G, Estes JA (2008) Food limitation leads to behavioral diversification and dietary specialization in sea otters. Proc Natl Acad Sci USA 105(2):560–565PubMedCentralCrossRefPubMedGoogle Scholar
  44. Tur C, Vigalondo B, Trøjelsgaard K, Olesen JM, Traveset A (2014) Downscaling pollen–transport networks to the level of individuals. J Anim Ecol 83(1):306–317CrossRefPubMedGoogle Scholar
  45. Van Valen L (1965) Morphological variation and width of ecological niche. Am Nat 99:377–390CrossRefGoogle Scholar
  46. Willerslev E, Davison J, Moora M, Zobel M, Coissac E, Edwards ME, Lorenzen ED, Vestergård M, Gussarova G, Haile J et al (2014) Fifty thousand years of arctic vegetation and megafaunal diet. Nature 506(7486):47–51CrossRefPubMedGoogle Scholar
  47. Wilson M, Shmida A (1984) Measuring beta diversity with presence-absence data. J Ecol 72:1055–1064CrossRefGoogle Scholar
  48. Yoccoz N (2012) The future of environmental DNA in ecology. Mol Ecol 21(8):2031–2038CrossRefPubMedGoogle Scholar
  49. Zaccarelli N, Bolnick DI, Mancinelli G (2013) Rinsp: an r package for the analysis of individual specialization in resource use. Methods Ecol Evol 4(11):1018–1023CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Marjorie Bison
    • 1
    • 5
  • Sébastien Ibanez
    • 1
  • Claire Redjadj
    • 1
    • 3
  • Frédéric Boyer
    • 2
  • Eric Coissac
    • 2
  • Christian Miquel
    • 2
  • Delphine Rioux
    • 2
  • Sonia Said
    • 4
  • Daniel Maillard
    • 3
  • Pierre Taberlet
    • 2
  • Nigel Gilles Yoccoz
    • 5
  • Anne Loison
    • 1
  1. 1.Laboratoire d’Ecologie Alpine, CNRS UMR 5553Université de SavoieLe Bourget-du-LacFrance
  2. 2.Laboratoire d’Ecologie Alpine, UMR CNRS 5553Université J. FourierGrenoble Cedex 9France
  3. 3.Office National de la Chasse et de la Faune Sauvage, Centre National d’Etudes et de Recherche Appliquée Faune de MontagneJuvignacFrance
  4. 4.Office National de la Chasse et de la Faune Sauvage, Centre National d’Etudes et de Recherche Appliquée Cervidés-SangliersBirieuxFrance
  5. 5.Department of Arctic and Marine BiologyUiT The Arctic University of NorwayTromsøNorway

Personalised recommendations