Abstract
Ungulates often adjust their diet when food availability varies over time. However, it is poorly understood when and to what extent individuals change their diet and, if they do so, if all individuals of a population occupy distinct or similar dietary niches. In the arid Namibian Kunene Region, we studied temporal variations of individual niches in grazing gemsbok (Oryx gazella gazella) and predominantly browsing springbok (Antidorcas marsupialis). We used variation in stable C and N isotope ratios of tail hair increments as proxies to estimate individual isotopic dietary niches and their temporal plasticity. Isotopic dietary niches of populations of the two species were mutually exclusive, but similar in breadth. Isotopic niche breadth of gemsbok was better explained by within-individual variation than by between-individual variation of stable isotope ratios, indicating that gemsbok individuals were facultative specialists in using isotopically distinct local food resources. In contrast, inter- and intra-individual variations contributed similarly to the isotopic niche breadth of the springbok population, suggesting a higher degree of individual isotopic segregation in a more generalist ungulate. In both species, between-individual variation was neither explained by changes in plant primary productivity, sex, geographical position nor by group size. Within species, individual dietary niches overlapped partially, suggesting that both populations included individuals with distinct isotopic dietary niches. Our study provides the first evidence for isotopic dietary niche segregation in individuals of two distinct desert ungulates. Similar, yet isotopically distinct dietary niches of individuals may facilitate partitioning of food resources and thus individual survival in desert ecosystems.
Similar content being viewed by others
References
Appleby MC (1980) Social rank and food access in red deer stags. Behaviour 74:294–309
Ayliffe LK, Cerling TE, Robinson T, West AG, Sponheimer M, Passey BH, Hammer J, Roeder BM, Dearing D, Ehleringer JR (2004) Turnover of carbon isotopes in tail hair and breadth CO2 of horses fed an isotopically varied diet. Oecologia 139:11–22
Barbehenn RV, Chen Z, Karowe DN, Spickard A (2004) C3 grasses have higher nutritional quality than C4 grasses under ambient and elevated atmospheric CO2. Glob Change Biol 10(9):1565–1575
Bates D, Maechler M, Bolker B, Walker S (2013) lme4: linear mixed-effects models using Eigen and S4. R package version 1.0-5. http://CRAN.R-project.org/package=lme4
Bender MM (1971) Variations in the δ13C ratios of plants in relation to the pathway of photosynthetic carbon dioxide fixation. Phytochemistry 10(6):1239–1244
Bolnick DI, Svanbäack R, Fordyce JA, Yang LH, David JM, Hulsey CD, Forister ML (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28
Bolnick DI, Svanbäck R, Araùjo MS, Persson L (2007) Comparative support for the niche variation hypothesis that more generalized populations also are more heterogeneous. Proc Natl Acad Sci USA 104:10075–10079
Côté SD (2000) Determining social rank in ungulates: a comparison of aggressive interactions recorded at a bait site and under natural conditions. Ethology 106:945–955
Cerling TE, Harris JM (1999) Carbon isotope fractionation between diet and bioapatite in ungulates mammals and implications for ecological and paleoecological studies. Oecologia 120:347–363
Cerling TE, Wittemyer G, Ehleringer JR, Remien CH, Douglas-Hamilton I (2009) History of animals using isotope records (HAIR): a 6-year dietary investigation of one family of African elephants. Proc Natl Acad Sci USA 106:8093–8100
Cherel Y, Kernaléguen L, Richard P, Guinet C (2009) Whisker isotopic signature depicts migration patterns and multi-year intra-and inter-individual foraging strategies in fur seals. Biol Lett 5(6):830–832
Child G, Le Riche JD (1969) Recent springbok treks (mass movements) in south-western Botswana. Mammalia 33(3):499–504
Chirima GJ, Owen-Smith N, Erasmus BNF, Parrini F (2013) Distributional niche of relatively rare sable antelope in a South African savanna: habitat versus biotic relationships. Ecography 36:068–079
Codron D, Lee-Thorp JA, Sponheimer M, Codron J (2007) Stable carbon isotope reconstruction of ungulate diet changes through the seasonal cycle. S Afr J Wildl Res 37(2):117–125
Codron J, Codron D, Sponheimer M, Kirkman K, Duffy KJ, Raubenheimer EJ, Mélice JL, Grant R, Clauss M, Lee-thorp JA (2012) Stable isotope series from elephant ivory reveal lifetime histories of a true dietary generalist. Proc R Soc Lond B 279:2433–2441
Codron J, Kirkman K, Duffy KJ, Sponheimer M, Lee-Thorp JA, Ganswindt A, Clauss M, Codron D (2013) Stable isotope turnover and variability in tail hairs of captive and free-ranging African elephants (Loxodonta Africana) reveal dietary niche differences within populations. Can J Zool 91:124–134
Dammhahn M, Kappeler PM (2014) Stable isotope analyses reveal dense trophic species packing and clear niche differentiation in a Malagasy primate community. Am J Phys Anthropol 153(2):249–259
Darimont CT, Paquet PC, Reimchen TE (2009) Landscape heterogeneity and marine subsidy generate extensive intrapopulation niche diversity in a large terrestrial vertebrate. J Anim Ecol 78:126–133
Dungan JD, Wright RG (2005) Summer diet composition of moose in Rocky Mountain National Park, Colorado. Alces 41:139–146
Dunnett M, Lees P (2003) Trace element, toxin and drug elimination in hair with particular reference to the horse. Res Vet Sci 75(2):89–101
Digital Atlas of Namibia (2002) Directorate of Environmental Affairs, Ministry of Environment and Tourism of Namibia. http://www.uni-koeln.de/sfb389/e/e1/download/atlas_namibia
du Toit JT (2003) Large herbivores and savanna heterogeneity. In: du Toit JT, Rogers KH, Biggs HC (eds) The Kruger experience: ecology and management of savanna heterogeneity. Island Press, Washington, DC, pp 292–309
du Toit (2005) Sexual segregation in vertebrates. In: Ruckstuhl KE, Neuhaus (eds) Ecology of the two sexes. Cambridge University Press, Cambridge, pp 35–50
Estes RD (1991) Behaviour guide to African mammals: including hoofed mammals, carnivores, primates. University of California Press, Oakland
Estes JA, Riedman ML, Staedler MM, Tinker MT, Lyon BE (2003) Individual variation in prey selection by sea otters: patterns, causes, and implications. J Anim Ecol 72:144–155
Flaherty EA, Ben-David M (2010) Overlap and partitioning of the ecological and isotopic niches. Oikos 119:1409–1416
Gonfiantini R, Stichler W, Rozansky K (1995) Intercomparison materials for stable isotopes of light elements. International Atomic Energy Agency, Vienna, p 13
Gordon IJ, Illius AW, Milne JD (1996) Sources of variations in the foraging efficiency of grazing ruminants. Funct Ecol 10:219–226
Hensman MC, Owen-Smith N, Parrini F, Bonyongo CM (2013) Resource use and the nutritional status of sable antelope in the Okavango Delta region of northern Bostwana. Afr J Ecol. doi:10.1111/aje.12113
Hopcraft JGC, Anderson TM, Pérez-Villa S, Mayemba E, Olff H (2012) Body size and the division of niche space: food and predation differentially shape the distribution of Serengeti grazers. J Anim Ecol 81:201–2013
Hutchinson GE (1978) An introduction to population ecology. Yale University Press, New Haven
Inger R, Ruxton GD, Newton J, Colhoun K, Robinson JA, Jackson AL, Bearhop S (2006) Temporal and intrapopulation variation in prey choice of wintering geese determined by stable isotope analysis. J Anim Ecol 75:1190–1200
IUCN (2014) The IUCN Red List of threatened species. Version 2014.3. www.iucnredlist.org
Jackson AL, Inger R, Parnell AX, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER-stable isotope Bayesian ellipses in R. J Anim Ecol 80:595–602
Jackson MC, Donohue I, Jackson AL, Britton JR, Harper DM, Grey J (2012) Population-level metrics of trophic structure based on stable isotopes and their application to invasion ecology. PLoS One 7:e31757
Jarman PJ (1974) The social organization of antelope in relation to their ecology. Behaviour 48(3/4):215–267
Kim SL, Tinker MT, Estes JA, Koch PL (2013) Ontogenetic and among-individual variation in foraging strategies of northeast pacific white sharks based on stable isotope analysis. PLoS One 7(9):e45068
Lehmann D, Mfune JKE, Gewers E, Cloete J, Brain C, Voigt CC (2013) Dietary plasticity of generalist and specialist ungulates in the Namibian desert: a stable isotopes approach. PLoS One 8(8):e72190
Lindström J (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14(9):343–348
Macdonald DW (1983) The ecology of carnivore social behaviour. Nature 301:379–384
Matich P, Heithaus MR, Layman CA (2010) Contrasting patterns of individual specialization and trophic coupling in two marine apex predators. J Anim Ecol 80:294–305
del Rio MC, Sabat P, Anderson-Sprecher R, Gonzalez SP (2009) Dietary and isotopic specialization: the isotopic niche of three Cinclodes ovenbirds. Oecologia 161(149):159
McEachern BM, Eagles-Smith AC, Efferson CM, Van Vuren DH (2006) Evidence for local specialization in a generalist mammalian herbivore Neotoma fuscipes. Oikos 113(3):440–448
Murray IW, Wolf BO (2013) Desert tortoise (Gopherus agassizii) dietary specialization decreases across a precipitation gradient. PloS one 8(6):e66505
Namibia Association of CBNRM Support Organizations NACSO (2012) http://www.nacso.org.na/index.php
Newsome SD, del Rio CM, Bearhop S, Phillips DL (2007) A niche for isotope ecology. Front Ecol Environ 5:429–436
Newsome SD, Tinker MT, Monson DH, Oftedal OT, Ralls K, Staedler MM, Fogel ML, Estes JA (2009) Using stable isotopes to investigate individual diet specialization in California sea otters (Enhydra lutris nereis). Ecology 90:961–974
Newsome SD, Yeakel JD, Wheatley PV, Tinker MT (2012) Tools for quantifying isotopic niche space and dietary variation at the individual and population level. J Mammal 93(2):329–341
Owen-Smith N (2008) Effects of temporal variability in resources on foraging behaviour. In: Prins HHT, Van Langevelde F (eds) Resource ecology: spatial and temporal dynamics of foraging. Springer, Dordreht, pp 159–181
Owen-Smith N, Le Roux E, Macandza V (2013) Are relatively rare antelope narrowly selective feeders? A sable antelope and zebra comparison. J Zool. doi:10.1111/jzo.12058
Osmond CB (1978) Crassulacean acid metabolism: a curiosity in context. Annu Rev Plant Physiol 29(1):379–414
Parnell AC, Jackson A (2013) SIAR: stable isotope analysis in R. R package version 4.2. Available at http://CRAN.R-project.org/package=siar-project.org/package=siar
Quevedo M, Svanbäck R, Eklov P (2009) Intrapopulation niche partitioning in a generalist predator limits food web connectivity. Ecology 90:2263–2274
Remien CH, Adler FR, Chesson LA, Valenzuela LO, Ehleringer JR, Cerling TE (2014) Deconvolution of isotope signals from bundles of multiple hairs. Oecologia 175(3):781–789
Roughgarden J (1972) Evolution of niche width. Am Nat 106:683–718
Ruckstuhl KE, Festa-Bianchet M, Jorgenson JT (2003) Bite rates in Rocky Mountain bighorn sheep (Ovis canadensis): effects of season, age, sex and reproductive status. Behav Ecol Sociobiol 54:167–173
Saitoh M, Uzuka M, Sakamotot M, Kobory T (1969) Rate of hair growth. In: Montagna W, Dobson RL (eds) Hair growth. Pergamon, Oxford, pp 183–201
Schwertl M, Matthew C, Auerswald K, Schnyder H, Crook K (2003) Isotopic composition of cow tail switch hair as an information archive of the animal environment. In: Proceedings of the New Zealand Grassland Association, vol 65. New Zealand Grassland Association, pp 147–152
Sih A, Christiansen B (2001) Optimal diet theory: when does it work, and when and why does it fail? Anim Behav 61:379–390
Skinner JD, Chimimba CT (2005). The mammals of the southern African sub-region. Oxford University Press, Oxford
Slater C, Preston T, Weaver LT (2001) Stable isotopes and the international system of units. Rapid Commun Mass Spectrom 15:1270–1273
Sponheimer M, Grant CC, de Ruiter DJ, Lee-Thorp JA, Codron DM, Codron J (2003) Diets of impala from Kruger National Park: evidence from stable carbon isotopes. Koedoe 46(1):101–106
Spalinger DE, Hobbs NT (1992) Mechanisms of foraging in mammalian herbivores: new models of functional response. Am Nat 140:325–348
Sutoh M, Koyama T, Yoneyama T (1987) Variations of natural 15N abundances in the tissues and digesta of domestic animals. Radioisotopes 36(2):74
Svanbäck R, Persson L (2004) Individual diet specialization, niche width, and population dynamics: implications for trophic polymorphisms. J Anim Ecol 73:973–982
Thaker M, Vanak AT, Owen CR, Ogden MB, Niemann SM, Slotow R (2011) Minimizing predation risk in a landscape of multiple predators: effects on the spatial distribution of African ungulates. Ecology 92(2):398–407
Tieszen LL, Boutton TW (1989) Stable carbon isotopes in terrestrial ecosystem research. In: Rundel PW, Ehleringer JR, Nagy KA (eds) Stable isotopes in ecological research. Springer, New York, pp 167–195
Tieszen LL, Senyimba MM, Imbamba SK, Troughton JH (1979) The distribution of C3 and C4 grasses and carbon isotope discrimination along an altitudinal and moisture gradient in Kenya. Oecologia 37(3):337–350
Urton EJM, Hobson KA (2005) Intrapopulation variation in grey wolf isotope (δ15N and δ13C) profiles: implications for the ecology of individuals. Oecologia 145:317–326
van de Pol M, Wright J (2009) A simple method for distinguishing within- versus between-subject effects using mixed models. Anim Behav 77:753–758
Vander Zanden HB, Bjomdal KA, Reich KJ, Bolten AB (2010) Individual specialists in a generalist population: results from a long-term stable isotope series. Biol Lett 6(5):711–714
Voigt CC, Matt F, Michener R, Kunz TH (2003) Low turnover rates of carbon isotopes in tissues of two nectar-feeding bat species. J Exp Biol 206(8):14191427
Watts DP (1984) Composition and variability of mountain gorilla diets in the central Virungas. Am J Primatol 7(4):323–356
West AG, Ayliffe LK, Cerling TE, Robinson TF, Karren B, Dearing MD, Eheleringer JR (2004) Short-term diet changes revealed using stable carbon isotopes in horsetail-hair. Funct Ecol 18:616–622
Acknowledgments
We would like to express our gratitude to the Ministry of Environment and Tourism of Namibia for granting us research permits (nos. 1534/2010 and 1676/2012). We are very grateful to the Torra Community-based Conservancy and its members for allowing this study to be performed on their communal territory. We thank Wilderness Safari Namibia for support in the field with logistics and field vehicle maintenance. We are thankful to the team of Damaraland Camp for assisting with logistics, especially Pascolena Florry, Maggie Vries, Efreida Hebach and Johann Cloete. We thank Anja Luckner, Karin Sörgel and Doris Fichte for preparing and analysing the samples in the stable isotope laboratory. We are grateful to Alexandre Courtiol for statistical advice. We thank Emilia Haimbili from the University of Namibia for assisting in data collection. We thank Ortwin Aschenborn, Bettina Wachter and Joerg Melzheimer for logistical advice and support in the field. We thank Norman Owen-Smith for providing useful comments. This study was approved by the Institutional Committee for Ethics and Animal Welfare of the IZW (no. 2009-10-01).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Peggy Ostrom.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Lehmann, D., Mfune, J.K.E., Gewers, E. et al. Individual variation of isotopic niches in grazing and browsing desert ungulates. Oecologia 179, 75–88 (2015). https://doi.org/10.1007/s00442-015-3335-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-015-3335-1