, Volume 25, Issue 2, pp 53–61 | Cite as

Reducible defence: chemical protection alters the dynamics of predator–prey interactions

  • Michael Heethoff
  • Björn C. Rall
Research Paper


Morphological and chemical defences are widespread anti-predator mechanisms in most domains of life, and play an important role in understanding predator–prey interactions. Classical concepts of dynamical protection (‘inducible defence’) include the morphological changes in certain crustaceans or the production of chemicals in many plants. Permanently stored defensive secretions are, to our knowledge, ignored in food web ecology. We show that this kind of chemical defence is highly dynamic and may loose its effect over time (‘reducible defence’). Combining experimental and theoretical approaches, we show that chemical defence also changes the time budget of predators and decreases the strength of the functional response. However, this may be counteracted by increasing predator density—an effect we call ‘apparent facilitation’. The interplay of ‘reducible defence’ and ‘apparent facilitation’ may substantially contribute to stability in terrestrial ecosystems.


Oribatida Archegozetes Stenus Functional response Chemical defence Stability Apparent facilitation 



We thank Lars Koerner for providing Stenus juno specimens, Ulrich Brose for discussion on the model and Nico Blüthgen and Andrew D. Barnes for discussion on the manuscript.


  1. Abrams PA, Walters CJ (1996) Invulnerable prey and the paradox of enrichment. Ecology 77:1125–1133CrossRefGoogle Scholar
  2. Altwegg R, Eng M, Caspersen S, Anholt BR (2006) Functional response and prey defence level in an experimental predator–prey system. Evol Ecol Res 8:115–128Google Scholar
  3. Binzer A, Guill C, Brose U, Rall BC (2012) The dynamics of food chains under climate change and nutrient enrichment. Philos Trans R Soc B Biol Sci 367:2935–2944. doi: 10.1098/rstb.2012.0230 CrossRefGoogle Scholar
  4. Boit A, Martinez ND, Williams RJ, Gaedke U (2012) Mechanistic theory and modelling of complex food-web dynamics in Lake Constance. Ecol Lett 15:594–602. doi: 10.1111/j.1461-0248.2012.01777.x CrossRefPubMedGoogle Scholar
  5. Burnham KP, Anderson DR (2004) Multimodel Inference. Sociol Methods Res 33:261–304. doi: 10.1177/0049124104268644 CrossRefGoogle Scholar
  6. Caro T (2005) Antipredator defenses in birds and mammals. University of Chicago Press, ChicagoGoogle Scholar
  7. Core Team R (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  8. Crawley MJ (2007) The R Book, Auflage, 1st edn. Wiley, New YorkCrossRefGoogle Scholar
  9. Eisner T, Eisner M, Siegler M (2005) Secret weapons—defenses of insects, spiders, scorpions, and other many-legged creatures. The Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  10. Fussmann KE, Schwarzmüller F, Brose U et al (2014) Ecological stability in response to warming. Nat Clim Change 4:206–210. doi: 10.1038/nclimate2134 CrossRefGoogle Scholar
  11. Genkai-Kato M, Yamamura N (1999) Unpalatable prey resolves the paradox of enrichment. Proc R Soc B Biol Sci 266:1215–1219. doi: 10.1098/rspb.1999.0765 CrossRefGoogle Scholar
  12. Giller PS (1996) The diversity of soil communities, the ‘poor man’s tropical rainforest’. Biodivers Conserv 5:135–168. doi: 10.1007/BF00055827 CrossRefGoogle Scholar
  13. Hammill E, Petchey O, Anholt B (2010) Predator functional response changed by induced defenses in prey. Am Nat 176:723–731. doi: 10.1086/657040 CrossRefPubMedGoogle Scholar
  14. Heethoff M (2012) Regeneration of complex oil-gland secretions and its importance for chemical defense in an oribatid mite. J Chem Ecol 38:1116–1123. doi: 10.1007/s10886-012-0169-8 CrossRefPubMedGoogle Scholar
  15. Heethoff M, Raspotnig G (2012a) Expanding the “enemy-free space” for oribatid mites: evidence for chemical defense of juvenile Archegozetes longisetosus against the rove beetle Stenus juno. Exp Appl Acarol 56:93–97. doi: 10.1007/s10493-011-9501-1 CrossRefPubMedGoogle Scholar
  16. Heethoff M, Raspotnig G (2012b) Triggering chemical defense in an oribatid mite using artificial stimuli. Exp Appl Acarol 56:287–295. doi: 10.1007/s10493-012-9521-5 CrossRefPubMedGoogle Scholar
  17. Heethoff M, Laumann M, Bergmann P (2007) Adding to the reproductive biology of the parthenogenetic oribatid mite, Archegozetes longisetosus (Acari, Oribatida, Trhypochthoniidae). Turk J Zool 31:151–159. doi: 10.3906/zoo-0601-7 Google Scholar
  18. Heethoff M, Koerner L, Norton RA, Raspotnig G (2011) Tasty but protected—first evidence of chemical defense in oribatid mites. J Chem Ecol 37:1037–1043. doi: 10.1007/s10886-011-0009-2 CrossRefPubMedGoogle Scholar
  19. Heethoff M, Bergmann P, Laumann M, Norton RA (2013) The 20th anniversary of a model mite: a review of current knowledge about Archegozetes Longisetosus (acari, Oribatida). Acarologia 53:353–368. doi: 10.1051/acarologia/20132108 CrossRefGoogle Scholar
  20. Holling CS (1959) Some characteristics of simple types of predation and parasitism. Can Entomol 91:385–398. doi: 10.4039/Ent91385-7 CrossRefGoogle Scholar
  21. Jeschke JM (2006) Density-dependent effects of prey defenses and predator offenses. J Theor Biol 242:900–907. doi: 10.1016/j.jtbi.2006.05.017 CrossRefPubMedGoogle Scholar
  22. Jeschke JM, Tollrian R (2000) Density-dependent effects of prey defences. Oecologia 123:391–396. doi: 10.1007/s004420051026 CrossRefGoogle Scholar
  23. Jeschke JM, Kopp M, Tollrian R (2002) Predator functional responses: discriminating between handling and digesting prey. Ecol Monogr 72:95–112. doi: 10.2307/3100087 CrossRefGoogle Scholar
  24. Kalinkat G, Rall BC, Vucic-Pestic O, Brose U (2011) The allometry of prey preferences. PLoS One 6:e25937. doi: 10.1371/journal.pone.0025937 CrossRefPubMedCentralPubMedGoogle Scholar
  25. Kalinkat G, Schneider FD, Digel C et al (2013) Body masses, functional responses and predator–prey stability. Ecol Lett 16:1126–1134. doi: 10.1111/ele.12147 CrossRefPubMedGoogle Scholar
  26. Kefi S, Berlow EL, Wieters EA et al (2012) More than a meal… integrating non-feeding interactions into food webs. Ecol Lett 15:291–300. doi: 10.1111/j.1461-0248.2011.01732.x CrossRefGoogle Scholar
  27. Koen-Alonso M (2007) A process-oriented approach to the multispecies functional response. Energ Ecosyst Dyn Struct Ecol Syst, pp 1–36Google Scholar
  28. Kopp M, Tollrian R (2003) Reciprocal phenotypic plasticity in a predator–prey system: inducible offences against inducible defences? Ecol Lett 6:742–748. doi: 10.1046/j.1461-0248.2003.00485.x CrossRefGoogle Scholar
  29. Kratina P, Vos M, Anholt BR (2007) Species diversity modulates predation. Ecology 88:1917–1923. doi: 10.1890/06-1507.1 CrossRefPubMedGoogle Scholar
  30. MacArthur R (1955) Fluctuations of animal populations, and a measure of community stability. Ecology 36:533–536CrossRefGoogle Scholar
  31. Maraun M, Martens H, Migge S et al (2003) Adding to “the enigma of soil animal diversity”: fungal feeders and saprophagous soil invertebrates prefer similar food substrates. Eur J Soil Biol 39:85–95. doi: 10.1016/S1164-5563(03)00006-2 CrossRefGoogle Scholar
  32. May RM (1972) Will a large complex system be stable. Nature 238:413–414. doi: 10.1038/238413a0 CrossRefPubMedGoogle Scholar
  33. McCann K (2000) The diversity–stability debate. Nature 405:228–233CrossRefPubMedGoogle Scholar
  34. McCann KS, Hastings A, Huxel GR (1998) Weak trophic interactions and the balance of nature. Nature 395:794–798. doi: 10.1038/27427 CrossRefGoogle Scholar
  35. McCauley E, Murdoch WW (1990) Predator-prey dynamics in environments rich and poor in nutrients. Nature 343:455–457. doi: 10.1038/343455a0 CrossRefGoogle Scholar
  36. Murdoch WW, Oaten A (1975) Predation and population stability. Adv Ecol Res 9:1–131CrossRefGoogle Scholar
  37. Neutel A-M, Heesterbeek JAP, de Ruiter PC (2002) Stability in real food webs: weak links in long loops. Science 296:1120–1123CrossRefPubMedGoogle Scholar
  38. Otto S, Rall BC, Brose U (2007) Allometric degree distributions stabilize food webs. Nature 450:1226–1229. doi: 10.1038/nature06359 CrossRefPubMedGoogle Scholar
  39. Pinheiro J, Bates D, DebRoy S, Sarkar D; R Core Team (2014) nlme: Linear and nonlinear mixed effects models. R package version 3.1–117.
  40. Quinn JL, Cresswell W (2012) Local prey vulnerability increases with multiple attacks by a predator. Oikos 121:1328–1334. doi: 10.1111/j.1600-0706.2011.20088.x CrossRefGoogle Scholar
  41. Rall BC, Guill C, Brose U (2008) Food-web connectance and predator interference dampen the paradox of enrichment. Oikos 117:202–213. doi: 10.1111/j.2007.0030-1299.15491.x CrossRefGoogle Scholar
  42. Rall BC, Brose U, Hartvig M et al (2012) Universal temperature and body-mass scaling of feeding rates. Philos Trans R Soc B Biol Sci 367:2923–2934. doi: 10.1098/rstb.2012.0242 CrossRefGoogle Scholar
  43. Raspotnig G (2006) Chemical alarm and defence in the oribatid mite Collohmannia gigantea (Acari: oribatida). Exp Appl Acarol 39:177–194. doi: 10.1007/s10493-006-9015-4 CrossRefPubMedGoogle Scholar
  44. Raspotnig G, Föttinger P (2008) Analysis of individual oil gland secretion profiles in oribatid mites (acari: oribatida). Int J Acarol 34:409–417. doi: 10.1080/17088180809434785 CrossRefGoogle Scholar
  45. Rosenzweig ML, Mac Arthur RH (1963) Graphical representation and stability conditions of predator–prey interactions. Am Nat 97:209. doi: 10.1086/282272 CrossRefGoogle Scholar
  46. Scheffer M, De Boer RJ (1995) Implications of spatial heterogeneity for the paradox of enrichment. Ecology 76:2270–2277CrossRefGoogle Scholar
  47. Schneider FD, Scheu S, Brose U (2012) Body mass constraints on feeding rates determine the consequences of predator loss. Ecol Lett 15:436–443. doi: 10.1111/j.1461-0248.2012.01750.x CrossRefPubMedGoogle Scholar
  48. Skalski GT, Gilliam JF (2001) Functional responses with predator interference: viable alternatives to the Holling type II model. Ecology 82:3083–3092. doi:10.1890/0012-9658(2001)082[3083:FRWPIV]2.0.CO;2CrossRefGoogle Scholar
  49. Soetaert K, Petzoldt T, Setzer R (2010) Solving differential equations in R: package deSolve. J Stat Softw 33:1–25Google Scholar
  50. Tollrian R, Harvell CD (eds) (1999) The ecology and evolution of inducible defenses. Princeton University Press, PrincetonGoogle Scholar
  51. Vos M, Kooi BW, DeAngelis DL, Mooij WM (2004) Inducible defences and the paradox of enrichment. Oikos 105:471–480. doi: 10.1111/j.0030-1299.2004.12930.x CrossRefGoogle Scholar
  52. Vucic-Pestic O, Birkhofer K, Rall BC et al (2010) Habitat structure and prey aggregation determine the functional response in a soil predator–prey interaction. Pedobiologia 53:307–312. doi: 10.1016/j.pedobi.2010.02.003 CrossRefGoogle Scholar
  53. Yodzis P (1981) The stability of real ecosystems. Nature 289:674–676. doi: 10.1038/289674a0 CrossRefGoogle Scholar
  54. Yodzis P, Innes S (1992) Body size and consumer–resource dynamics. Am Nat 139:1151–1175. doi: 10.1086/285380 CrossRefGoogle Scholar
  55. Zar JH (2009) Biostatistical analysis, 5th edn. Prentice Hall, New JerseyGoogle Scholar
  56. Zuur AF, Ieno EN, Walker NJ et al (2009) Mixed effects models and extensions in ecology with R, 1st edn. Springer, BerlinCrossRefGoogle Scholar

Copyright information

© Springer Basel 2015

Authors and Affiliations

  1. 1.Ecological NetworksTechnical University DarmstadtDarmstadtGermany
  2. 2.Systemic Conservation Biology, J.F. Blumenbach Institute of Zoology and AnthropologyGeorg-August-University GöttingenGöttingenGermany
  3. 3.German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-LeipzigLeipzigGermany
  4. 4.Institute of EcologyFriedrich Schiller University JenaJenaGermany

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