Rewilding with large herbivores: Positive direct and delayed effects of carrion on plant and arthropod communities

Autoři: Roel van Klink aff001;  Jitske van Laar-Wiersma aff001;  Oscar Vorst aff002;  Christian Smit aff001
Působiště autorů: Groningen Institute for Evolutionary Life Sciences (GELIFES), Conservation Ecology Group, University of Groningen, Groningen, The Netherlands aff001;  Independent Researcher, Utrecht, The Netherlands aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article


Carrion of large animals is an extremely nutrient rich, ephemeral resource that is essential for many species, but is scarce in the anthropogenic Western-European landscape due to legislative restrictions. Rewilding, a novel conservation strategy that aims at restoring natural processes with minimal human intervention, is increasing in popularity and could lead to increased carrion availability in the landscape. It is therefore important to understand the effects of carrion on biodiversity. We investigated the direct and delayed (five months) effects of red deer (Cervus elaphus) carcasses on plants and arthropods in the Oostvaardersplassen, the Netherlands, one of the oldest rewilding sites in Europe. Specifically, we tested whether carrion has a positive direct effect on the abundances and diversity of various arthropod functional groups, as well as a delayed effect on the vegetation and arthropods through the increased nutrient availability. During the active decomposition stage in spring, we, not surprisingly, observed higher abundances of carrion associated species (scavengers and their specialized predators) at the carrion sites than at control sites without carrion, but no higher abundances of predators or detritivores. In late summer, after near-complete decomposition, plant biomass was five times higher, and nutritional plant quality (C:N ratio) was higher at the carrion sites than at the control sites. Arthropod abundance and diversity were also manifold higher, owing to higher numbers of herbivorous and predatory species. Regression analysis showed that abundances of herbivores and detritivores were positively related to plant biomass, and predator abundances were positively related to abundances of herbivores and detritivores, suggesting bottom-up effects propagating through the food chain. Our results show that even in a naturally nutrient-rich ecosystem like the Oostvaardersplassen, carrion can have strong positive effects on local plant biomass and nutritional quality and arthropod abundances, lasting the whole growing season. We found evidence that these effects were first directly caused by the presence of carrion, and later by the enhanced nutrient availability in the soil. This highlights the importance of the indirect pathways by which carrion can structure arthropod communities.

Klíčová slova:

Arthropoda – Biomass – Deer – Herbivory – Invertebrates – Nutrients – Plant-herbivore interactions – Spring


1. Barton PS, Cunningham SA, Lindenmayer DB, Manning AD. The role of carrion in maintaining biodiversity and ecological processes in terrestrial ecosystems. Oecologia. 2013;171: 761–72. doi: 10.1007/s00442-012-2460-3 23007807

2. Van Klink R, Van der Plas F, Van Noordwijk CGET, WallisDeVries MF, Olff H. Effects of large herbivores on grassland arthropod diversity. Biol Rev. 2015;90: 347–366. doi: 10.1111/brv.12113 24837856

3. European Commission. Regulation (EC) No 1774/2002 of the European Parliament and of the Council of 3 October 2002 laying down health rules concerning animal by-products not intended for human consumption. 2002.

4. European Commission. Regulation (EC) No 1069/2009 of the European Parliament and of the Council of 21 October 2009 laying down health rules as regards animal by-products and derived products not intended for human consumption and repealing regulation (EC) No 1774/2002. 2009.

5. European Commission. Regulation 2005/830/EC: Commission decision of 25 November 2005 amending decision 2003/322/EC as regards the feeding of certain necrophagous birds with certain category 1 material (notified under document number C(2005) 4521). 2005.

6. Fielding D, Newey S, Van der Wal R, Irvine RJ. Carcass provisioning to support scavengers: evaluating a controversial nature conservation practice. Ambio. 2014;43: 810–819. doi: 10.1007/s13280-013-0469-4 24366570

7. Colijn EO. Kevers op kadavers in Nederland, de stand van zaken. Entomol Ber. 2014;74: 60–67.

8. Paine RT. A note on trophic complexity and community stability. Am Nat. 1969;103: 91–93. doi: 10.1086/282586

9. Svenning J-C, Pedersen PBM, Donlan J, Ejrnaes R, Faurby S, Galetti M, et al. Science for a wilder Anthropocene -synthesis and future directions for rewilding research. Proc Natl Acad Sci. 2016;113: 898–906. doi: 10.1073/pnas.1502556112 26504218

10. Sandom C, Donlan CJ, Svenning J-C, Hansen D. Rewilding. In: Macdonald DW, Willis KJ, editors. Key Topics in Conservation Biology 2. John Wiley & Sons, Ltd.; 2013. pp. 430–451.

11. Moleón M, Sánchez-Zapata JA, Selva N, Donázar JA, Owen-Smith N. Inter-specific interactions linking predation and scavenging in terrestrial vertebrate assemblages. Biol Rev. 2014;89: 1042–1054. doi: 10.1111/brv.12097 24602047

12. Devault TL, Rhodes OE, Shivik JA. Scavenging by vertebrates: behavioral, ecological, and evolutionary perspectives on an important energy transfer pathway in terrestrial ecosystems. Oikos. 2003;102: 225–234.

13. Wilmers CC, Crabtree RL, Smith DW, Murphy KM, Getz WM. Trophic facilitation by introduced top predators: grey wolf subsidies to scavengers in Yellowstone National Park. J Anim Ecol. 2003;72: 909–916.

14. Elbroch LM, Wittmer HU. Table scraps: inter-trophic food provisioning by pumas. Biol Lett. 2012;8: 776–779. doi: 10.1098/rsbl.2012.0423 22696284

15. Turner KL, Abernethy EF, Conner LM, Rhodes OE, Beasley JC. Abiotic and biotic factors modulate carrion fate and vertebrate scavenging communities. Ecology. 2017;98: 2413–2424. doi: 10.1002/ecy.1930 28628191

16. Olson ZH, Beasley JC, Rhodes OE. Carcass type affects local scavenger guilds more than habitat connectivity. PLoS One. 2016;11: 1–19. doi: 10.1371/journal.pone.0147798 26886299

17. Benecke M. A brief history of forensic entomology. Forensic Sci Int. 2001;120: 2–14. doi: 10.1016/s0379-0738(01)00409-1 11457602

18. Michaud J-P, Schoenly KG, Moreau G. Rewriting ecological succession history: did carrion ecologists get there first? Q Rev Biol. 2015;90: 45–66. doi: 10.1086/679763 26434165

19. Gu X, Haelewaters D, Krawczynski R, Vanpoucke S, Wagner H-G, Wiegleb G. Carcass ecology—more than just beetles. Entomol Ber. 2014;74: 68–74. Available:

20. Melis C, Teurlings I, Linnell JC, Andersen R, Bordoni A. Influence of a deer carcass on Coleopteran diversity in a Scandinavian boreal forest: a preliminary study. Eur J Wildl Res. 2004;50: 146–149. doi: 10.1007/s10344-004-0051-2

21. Barry JM, Elbroch LM, Aiello-Lammens ME, Sarno RJ, Seelye L, Kusler A, et al. Pumas as ecosystem engineers: ungulate carcasses support beetle assemblages in the Greater Yellowstone Ecosystem. Oecologia. 2019;in press. doi: 10.1007/s00442-018-4315-z 30506303

22. Pechal JL, Benbow ME, Crippen TL, Tarone AM, Tomberlin JK. Delayed insect access alters carrion decomposition and necrophagous insect community assembly. Ecosphere. 2014;5: 1–21. doi: 10.1890/es14-00022.1

23. Payne JA. A summer carrion study of the baby pig Sus scrofa Linnaeus. Ecology. 1965;46: 592–602.

24. Reed HB. A study of dog carcass communities in Tennessee, with special reference to the insects. Am Midl Nat. 1958;59: 213–245.

25. Kočárek P. Decomposition and Coleoptera succession on exposed carrion of small mammal in Opava, the Czech Republic. Eur J Soil Biol. 2003;39: 31–45. doi: 10.1016/S1164-5563(02)00007-9

26. Braack LEO. Community dynamics of carrion-attendant arthropods in tropical african woodland. Oecologia. 1987;72: 402–409. doi: 10.1007/BF00377571 28311137

27. Macdonald BCT, Farrell M, Tuomi S, Barton PS, Cunningham SA, Manning AD. Carrion decomposition causes large and lasting effects on soil amino acid and peptide flux. Soil Biol Biochem. 2014;69: 132–140. doi: 10.1016/j.soilbio.2013.10.042

28. Towne EG. Prairie vegetation and soil nutrient responses to ungulate carcasses. Oecologia. 2000;122: 232–239. doi: 10.1007/PL00008851 28308377

29. Parmenter RR, MacMahon JA. Carrion decomposition and nutrient cycling in a semiarid shrub-steppe ecosystem. Ecol Monogr. 2009;79: 637–661. doi: 10.1890/08-0972.1

30. Barton PS, McIntyre S, Evans MJ, Bump JK, Cunningham SA, Manning AD. Substantial long-term effects of carcass addition on soil and plants in a grassy eucalypt woodland. Ecosphere. 2016;7: 1–11. doi: 10.1002/ecs2.1537

31. Melis C, Selva N, Teurlings I, Skarpe C, Linnell JDC, Andersen R. Soil and vegetation nutrient response to bison carcasses in Białowieża Primeval Forest, Poland. Ecol Res. 2007;22: 807–813. doi: 10.1007/s11284-006-0321-4

32. Bump JK, Webster CR, Vucetich JA, Peterson RO, Shields JM, Powers MD. Ungulate carcasses perforate ecological filters and create biogeochemical hotspots in forest herbaceous layers allowing trees a competitive advantage. Ecosystems. 2009;12: 996–1007. doi: 10.1007/s10021-009-9274-0

33. Carter DO, Yellowlees D, Tibbett M. Cadaver decomposition in terrestrial ecosystems. Naturwissenschaften. 2007;94: 12–24. doi: 10.1007/s00114-006-0159-1 17091303

34. Cobaugh KL, Schaeffer SM, DeBruyn JM. Functional and Structural Succession of Soil Microbial Communities below Decomposing Human Cadavers. Berg G, editor. PLoS One. 2015;10: e0130201. doi: 10.1371/journal.pone.0130201 26067226

35. Turner WC, Kausrud KL, Krishnappa YS, Cromsigt JPGM, Ganz HH, Mapaure I, et al. Fatal attraction: vegetation responses to nutrient inputs attract herbivores to infectious anthrax carcass sites. Proc Biol Sci. 2014;281. doi: 10.1098/rspb.2014.1785 25274365

36. Danell K, Berteaux D, Bråthen KA. Effect of muskox carcasses on nitrogen concentration in tundra vegetation. Arctic. 2002;55: 389–392. doi: 10.14430/arctic723

37. Vulink JT, Drost HJ, Jans L. The influence of different grazing regimes on Phragmites—and shrub vegetation in the well-drained zone of a eutrophic wetland. Appl Veg Sci. 2000;3: 73–80. doi: 10.2307/1478920

38. Cornelissen P, Bokdam J, Sykora K, Berendse F. Effects of large herbivores on wood pasture dynamics in a European wetland system. Basic Appl Ecol. 2014;15: 396–406. doi: 10.1016/j.baae.2014.06.006

39. Cornelissen P, Gresnigt MC, Vermeulen RA, Bokdam J, Smit R. Transition of a Sambucus nigra L. dominated woody vegetation into grassland by a multi-species herbivore assemblage. J Nat Conserv. 2014;22: 84–92. doi: 10.1016/j.jnc.2013.09.004

40. Cornelissen P, Kuipers J, Dekker J. Vegetatie, grote herbivoren, vogels en recreatie in de Oostvaardersplassen. Verslag van monitoring periode 1 mei 2012 t/m 30 april 2013. 2013.

41. ICMO. Natural processes, animal welfare, moral aspects and management of the Oostvaardersplassen. Report of the second International Commission on Management of the Oostvaardersplassen (ICMO2). The Hague / Wageningen; 2010.

42. Van Klink R, Ruifrok JL, Smit C. Rewilding with large herbivores: direct effects and edge effects of grazing refuges on plant and invertebrate communities. Agric Ecosyst Environ. 2016;234: 81–97.

43. van Klink R, van Laar-Wiersma JM, Vorst O, Smit C. Oostvaardersplassen carrion experiment. In: Knowledge Network for Biocomplexity [Internet]. 2019. doi: 10.5063/F1NG4NZ3

44. Venables WN, Ripley BD. Modern applied statistics with S. Fourth edition. New York: Springer; 2002.

45. R Core Team. R: A language and environment for statistical computing. version 3.5.2. R Foundation for Statistical Computing. Vienna, Austria; <U></U>: R Foundation for Statistical Computing; 2019.

46. Barton PS, Cunningham SA, Macdonald BCT, McIntyre S, Lindenmayer DB, Manning AD. Species traits predict assemblage dynamics at ephemeral resource patches created by carrion. Kytöviita M-M, editor. PLoS One. 2013;8: e53961. doi: 10.1371/journal.pone.0053961 23326549

47. Arnaldos MI, Romera E, Presa JJ, Luna A, García MD. Studies on seasonal arthropod succession on carrion in the southeastern Iberian Peninsula. Int J Legal Med. 2004;118: 197–205. doi: 10.1007/s00414-004-0446-3 15114485

48. Matuszewski S, Bajerlein D, Konwerski S, Szpila K. Insect succession and carrion decomposition in selected forests of Central Europe. Part 1: Pattern and rate of decomposition. Forensic Sci Int. 2010;194: 85–93. doi: 10.1016/j.forsciint.2009.10.016 19914786

49. Matuszewski S, Frątczak K, Konwerski S, Bajerlein D, Szpila K, Jarmusz M, et al. Effect of body mass and clothing on carrion entomofauna. Int J Legal Med. 2016;130: 221–232. doi: 10.1007/s00414-015-1145-y 25874664

50. Moleón M, Sánchez-Zapata JA, Sebastián-González E, Owen-Smith N. Carcass size shapes the structure and functioning of an African scavenging assemblage. Oikos. 2015;124: 1391–1403. doi: 10.1111/oik.02222

51. Cortés-Avizanda A, Jovani R, Carrete M, Donázar JA. Resource unpredictability promotes species diversity and coexistence in an avian scavenger guild: A field experiment. Ecology. 2012;93: 2570–2579. doi: 10.1890/12-0221.1 23431588

52. Wilmers CC, Stahler DR, Crabtree RL, Smith DW, Getz WM. Resource dispersion and consumer dominance: Scavenging at wolf- and hunter-killed carcasses in Greater Yellowstone, USA. Ecol Lett. 2003;6: 996–1003. doi: 10.1046/j.1461-0248.2003.00522.x

53. Sugiura S, Tanaka R, Taki H, Kanzaki N. Differential responses of scavenging arthropods and vertebrates to forest loss maintain ecosystem function in a heterogeneous landscape. Biol Conserv. 2013;159: 206–213. doi: 10.1016/j.biocon.2012.11.003

54. Simmons T, Cross PA, Adlam RE, Moffatt C. The influence of insects on decomposition rate in buried and surface remains. J Forensic Sci. 2010;55: 889–892. doi: 10.1111/j.1556-4029.2010.01402.x 20412365

55. Komar D, Beattie O. Effects of carcass size on decay rates of shade and sun exposed carrion. J Can Soc Forensic Sci. 1998;31: 35–43. doi: 10.1080/00085030.1998.10757107

56. Moreno-Opo R, Margalida A. Carcasses provide resources not exclusively to scavengers: patterns of carrion exploitation by passerine birds. Ecosphere. 2013;4: 1–15. doi: 10.1890/es13-00108.1

57. Cortés-Avizanda A, Carrete M, Serrano D, Donázar JA. Carcasses increase the probability of predation of ground-nesting birds: A caveat regarding the conservation value of vulture restaurants. Anim Conserv. 2009;12: 85–88. doi: 10.1111/j.1469-1795.2008.00231.x

58. Cortés-Avizanda A, Selva N, Carrete M, Donázar JA. Effects of carrion resources on herbivore spatial distribution are mediated by facultative scavengers. Basic Appl Ecol. 2009;10: 265–272. doi: 10.1016/j.baae.2008.03.009

59. Van Geel PLBA, Poelman PJM, Van der List MJ, Externe Begeleidingscommissie beheer Oostvaardersplassen. Advies Beheer Oostvaardersplassen. Kaders voor provinciaal beleid Provincie Flevoland. 2018.

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