Oecologia

, Volume 178, Issue 1, pp 275–284 | Cite as

DNA left on browsed twigs uncovers bite-scale resource use patterns in European ungulates

  • Ruth V. Nichols
  • Joris P. G. M. Cromsigt
  • Göran Spong
Community ecology - Original research

Abstract

Fine-scale resource use by large herbivores is often difficult to quantify directly. This is particularly true for browsing ungulates due to the challenges in observing shy subjects in forested environments of low visibility. As a consequence we know relatively little about resource use by diverse browsing ungulates. When browsing, ungulates leave behind saliva on the browsed twig that includes their DNA, which can be used to identify the species that was responsible for browsing the twig. We used this method, which we term “biteDNA”, to study bite-scale browsing patterns in a temperate ungulate community. This approach provides a level of detail in browsing patterns across species that was previously very hard to attain. We found that all deer species largely overlapped in terms of the tree species they used. Moose browsed larger diameters than red deer and roe deer, but these latter two species did not differ. Moose browsed at higher heights than red deer, and red deer higher than roe deer. Although the deer species differed in mean browsing height, species were comparable in terms of their minimum browsing height of ~20 cm. This means that height and diameter ranges of the smaller species were found to be completely inside the ranges of the larger species. Hence, while moose may access exclusive food resources in terms of browse height and diameter, red and roe deer cannot.

Keywords

Alces alces Capreolus capreolus Cervidae Dama dama Cervus elaphus Resource use Molecular ecology Browsing Environmental DNA 

References

  1. Arsenault R, Owen-Smith N (2008) Resource partitioning by grass height among grazing ungulates does not follow body size relation. Oikos 117:1711–1717CrossRefGoogle Scholar
  2. Bell RHV (1970) The use of the herb layer by grazing ungulates in the Serengeti. In: Watson A (ed) Animal populations and relations to their food resources. Blackwell, Oxford, pp 111–124Google Scholar
  3. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate—a practical and powerful approach to multiple testing. J R Stat Soc Ser B-Methodol 57:289–300Google Scholar
  4. Bergqvist G, Bergström R, Edenius L (2001) Patterns of stem damage by moose (Alces alces) in young Pinus sylvestris stands in Sweden. Scand J For Res 16:363–370CrossRefGoogle Scholar
  5. Brown MB, Forsythe AB (1974) Robust tests for the equality of variances. J Am Stat Assoc 69:364–367CrossRefGoogle Scholar
  6. Cameron EZ, du Toit JT (2007) Winning by a neck: tall giraffes avoid competing with shorter browsers. Am Nat 169:130–135CrossRefPubMedGoogle Scholar
  7. Clauss M, Kaiser T, Hummel J (2008) The morphophysiological adaptations of browsing and grazing mammals. In: Gordon IJ, Prins HHT (eds) The ecology of browsing and grazing, vol 195. Springer, Berlin, Heidelberg, pp 47–88CrossRefGoogle Scholar
  8. Clauss M, Steuer P, Müller DW, Codron D, Hummel J (2013) Herbivory and body size: allometries of diet quality and gastrointestinal physiology, and implications for herbivore ecology and dinosaur gigantism. PLoS One 8:e68714CrossRefPubMedCentralPubMedGoogle Scholar
  9. Cromsigt JPGM, Olff H (2006) Resource partitioning among savanna grazers mediated by local heterogeneity: an experimental approach. Ecology 87:1532–1541CrossRefPubMedGoogle Scholar
  10. Cromsigt JPGM, Prins HHT, Olff H (2009) Habitat heterogeneity as a driver of ungulate diversity and distribution patterns: interaction of body mass and digestive strategy. Divers Distrib 15:513–522CrossRefGoogle Scholar
  11. du Toit JT (1990) Feeding-height stratification among African browsing ruminants. Afr J Ecol 28:55–61CrossRefGoogle Scholar
  12. du Toit JT, Owen-Smith N (1989) Body size, population metabolism, and habitat specialization among large african herbivores. Am Nat 133:736–740CrossRefGoogle Scholar
  13. Duncan P, Tixier H, Hofmann RR, Lechner-Doll M (1998) Feeding strategies and the physiology of digestion in roe deer. In: Andersen R, Duncan P, Linell J (eds) The European roe deer: the biology of success. Scandinavian University Press, Oslo, pp 91–116Google Scholar
  14. Gagnon M, Chew AE (2000) Dietary preferences in extant african bovidae. J Mammal 81:490–511CrossRefGoogle Scholar
  15. Gordon IJ, Illius AW (1996) The nutritional ecology of African ruminants: a reinterpretation. J Anim Ecol 65:18–28CrossRefGoogle Scholar
  16. Gordon IJ, Prins HH (2008) The ecology of browsing and grazing. Springer, Berlin, HeidelbergCrossRefGoogle Scholar
  17. Hagström T, Hagström E (2010) Däggdjuren i Norden. Ica, SwedenGoogle Scholar
  18. Hofmann RR (1989) Evolutionary steps of ecophysiological adaptation and diversification of ruminants: a comparative view of their digestive system. Oecologia 78:443–457CrossRefGoogle Scholar
  19. Holmen (2014) Holmens Viltskötselområde Östergötland, StockholmGoogle Scholar
  20. Jarman PJ (1974) Social-organization of antelope in relation to their ecology. Behaviour 48:215CrossRefGoogle Scholar
  21. Jia J, Niemelä P, Danell K (1995) Moose Alces alces bite diameter selection in relation to twig quality on four phenotypes of Scots pine Pinus sylvestris. Wildl Biol 1:47–55Google Scholar
  22. Lande US, Loe LE, Skjaerli OJ, Meisingset EL, Mysterud A (2014) The effect of agricultural land use practice on habitat selection of red deer. Eur J Wildl Res 60:69–76CrossRefGoogle Scholar
  23. Leuthold W (1978) Ecological separation among browsing ungulates in Tsavo East National Park, Kenya. Oecologia 35:241–252CrossRefGoogle Scholar
  24. McNaughton SJ, Georgiadis NJ (1986) Ecology of African grazing and browsing mammals. Annu Rev Ecol Syst 17:39–65CrossRefGoogle Scholar
  25. Miller RS (1967) Pattern and process in competition. Adv Ecol Res 4:1–74CrossRefGoogle Scholar
  26. Mysterud A (2000a) Diet overlap among ruminants in Fennoscandia. Oecologia 124:130–137CrossRefGoogle Scholar
  27. Mysterud A (2000b) The relationship between ecological segregation and sexual body size dimorphism in large herbivores. Oecologia 124:40–54CrossRefGoogle Scholar
  28. Nichols RV, Spong G (2014) Ungulate browsing on conifers during summer as revealed by DNA. Scand J For Res 29:650–652CrossRefGoogle Scholar
  29. Nichols RV, Königsson H, Danell K, Spong G (2012) Browsed twig environmental DNA: diagnostic PCR to identify ungulate species. Mol Ecol Resour 12:983–989CrossRefPubMedGoogle Scholar
  30. Nugent G (1990) Forage availability and the diet of fallow deer (Dama dama) in the Blue Mountains, Otago. N Z J Ecol 13:83–95Google Scholar
  31. Obidziński A, Kiełtyk P, Borkowski J, Bolibok L, Remuszko K (2013) Autumn-winter diet overlap of fallow, red, and roe deer in forest ecosystems, Southern Poland. Cent Eur J Biol 8:8–17CrossRefGoogle Scholar
  32. Ogram A, Sayler GS, Barkay T (1987) The extraction and purification of microbial DNA from sediments. J Microbiol Methods 7:57–66CrossRefGoogle Scholar
  33. Parra-Frutos I (2013) Testing homogeneity of variances with unequal sample sizes. Comput Stat 28:1269–1297CrossRefGoogle Scholar
  34. Renaud PC, Verheyden-Tixier H, Dumont B (2003) Damage to saplings by red deer (Cervus elaphus): effect of foliage height and structure. For Ecol Manage 181:31–37CrossRefGoogle Scholar
  35. Ritchie ME, Olff H (1999) Spatial scaling laws yield a synthetic theory of biodiversity. Nature 400:557–560CrossRefPubMedGoogle Scholar
  36. Searle KR, Shipley LA (2008) The comparative feeding bahaviour of large browsing and grazing herbivores. In: Gordon IJ, Prins HHT (eds) The ecology of browsing and grazing. Springer, Berlin, Heidelberg, pp 117–148CrossRefGoogle Scholar
  37. Seaton CT, Paragi TF, Boertje RD, Kielland K, DuBois S, Fleener CL (2011) Browse biomass removal and nutritional condition of moose Alces alces. Wildl Biol 17:55–66CrossRefGoogle Scholar
  38. Senft RL, Coughenour MB, Bailey DW, Rittenhouse LR, Sala OE, Swift DM (1987) Large herbivore foraging and ecological hierarchies. Bioscience 37:789CrossRefGoogle Scholar
  39. Shipley LA (2007) The influence of bite size on foraging at larger spatial and temporal scales by mammalian herbivores. Oikos 116:1964–1974CrossRefGoogle Scholar
  40. Shipley LA, Illius AW, Danell K, Hobbs NT, Spalinger DE (1999) Predicting bite size selection of mammalian herbivores: a test of a general model of diet optimization. Oikos 84:55–68CrossRefGoogle Scholar
  41. SMHI (2013) Swedish Meteorological and Hydrological Institute, vol 2013, NorrköpingGoogle Scholar
  42. Steuer P et al (2014) Does body mass convey a digestive advantage for large herbivores? Funct Ecol 28:1127–1134CrossRefGoogle Scholar
  43. Taberlet P, Coissac E, Hajibabaei M, Rieseberg LH (2012) Environmental DNA. Mol Ecol 21:1789–1793CrossRefPubMedGoogle Scholar
  44. Van Soest PJ (1996) Allometry and ecology of feeding behavior and digestive capacity in herbivores: a review. Zoo Biol 15:455–479CrossRefGoogle Scholar
  45. Wilson SL, Kerley GIH (2003) Bite diameter selection by thicket browsers: the effect of body size and plant morphology on forage intake and quality. For Ecol Manage 181:51–65CrossRefGoogle Scholar
  46. Woolnough A, du Toit J (2001) Vertical zonation of browse quality in tree canopies exposed to a size-structured guild of African browsing ungulates. Oecologia 129:585–590CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Ruth V. Nichols
    • 1
  • Joris P. G. M. Cromsigt
    • 1
    • 2
  • Göran Spong
    • 1
  1. 1.Molecular Ecology Group, Department of Wildlife, Fish and Environmental StudiesSwedish University of Agricultural SciencesUmeåSweden
  2. 2.Department of Zoology, Centre for African Conservation EcologyNelson Mandela Metropolitan University, NMMUPort ElizabethSouth Africa

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