Skip to main content

Advertisement

Log in

Temperature Affects Chemical Defense in a Mite-Beetle Predator-Prey System

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Temperature influences all biochemical and biophysiological processes within an organism. By extension, it also affects those ecological interactions that are mediated by gland-produced chemical compounds, such as reservoir-based chemical defense. Herein, we investigate how environmental temperature affects the regeneration of defensive secretions and influences the efficacy of chemical defense in a model predator-prey system: the oribatid mite Archegozetes longisetosus and the predaceous rove beetle Stenus juno. Through a combination of chemical analyses, non-linear regression modeling and theoretical simulations we show that the amount of defensive secretion responded to temperature in a unimodal optimum curve: the regeneration rate followed a positive, linear relationship up to 35 °C, but rapidly broke down beyond this temperature (“tipping point” effect). Using functional response simulations, there is an initially positive dampening effect on the predation rate when regeneration is optimal, but at higher temperatures chemical defense does not counteract the previously described effects of elevated predatory pressure. In a larger context, our results demonstrate the need to integrate relevant environmental factors in predator-prey modeling approaches.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aoki J (1965) Oribatiden (Acarina) Thailands I. Nat Life Southeast Asia 4:129–193

    Google Scholar 

  • Bartoń K (2018) MuMIn: Multi-Model Inference (Version 1.42. 1)

  • Běhrádek J (1930) Temperature coefficients in biology. Biol Rev 5:30–58

    Article  Google Scholar 

  • Binzer A, Guill C, Brose U, Rall BC (2012) The dynamics of food chains under climate change and nutrient enrichment. Philos Trans R Soc Lond Ser B Biol Sci 367:2935–2944

    Article  Google Scholar 

  • Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML (2002) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28

    Article  Google Scholar 

  • Brückner A, Heethoff M (2017a) A chemo-ecologists’ practical guide to compositional data analysis. Chemoecology 27:33–46

    Article  CAS  Google Scholar 

  • Brückner A, Heethoff M (2017b) The ontogeny of oil gland chemistry in the oribatid mite Archegozetes longisetosus Aoki (Oribatida, Trhypochthoniidae). Int J Acarol 43:337–342

    Article  Google Scholar 

  • Brückner A, Heethoff M (2018) Nutritional effects on chemical defense alter predator–prey dynamics. Chemoecology 28:1–9

    Article  CAS  Google Scholar 

  • Brückner A, Parker J (2020) Molecular evolution of gland cell types and chemical interactions in animals. J Exp Biol 223:jeb211938

    Article  Google Scholar 

  • Clarke K, Gorley R (2015) Getting started with PRIMER v7 PRIMER-E: Plymouth, Plymouth Marine Laboratory:20

  • Cornish-Bowden A (2012) Fundamentals of enzyme kinetics vol 510. Wiley-Blackwell, Weinheim

    Google Scholar 

  • Deutsch CA, Tewksbury JJ, Huey RB, Sheldon KS, Ghalambor CK, Haak DC, Martin PR (2008) Impacts of climate warming on terrestrial ectotherms across latitude. PNAS 105:6668–6672

    Article  Google Scholar 

  • Englund G, Öhlund G, Hein CL, Diehl S (2011) Temperature dependence of the functional response. Ecol Lett 14:914–921

    Article  Google Scholar 

  • Florez LV, Biedermann PHW, Engl T, Kaltenpoth M (2015) Defensive symbioses of animals with prokaryotic and eukaryotic microorganisms. Nat Prod Rep 32:904–936

    Article  CAS  Google Scholar 

  • Hartig F (2017) DHARMa: residual diagnostics for hierarchical (multi-level/mixed) regression models R package version 0.15

  • Hedrick MS, Hillman SS (2016) What drove the evolution of endothermy? J Exp Biol 219:300–301

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Heethoff M, Rall BC (2015) Reducible defence: chemical protection alters the dynamics of predator–prey interactions. Chemoecology 25:53–61

    Article  Google Scholar 

  • Heethoff M, Raspotnig G (2012a) Investigating chemical communication in oribatid and astigmatid mites in bioassays - pitfalls and suggestions. Soil Org 84:409–421

    Google Scholar 

  • Heethoff M, Raspotnig G (2012b) Triggering chemical defense in an oribatid mite using artificial stimuli. Exp Appl Acarol 56(4):287–295

    Article  CAS  Google Scholar 

  • Hoekman D (2010) Turning up the heat: temperature influences the relative importance of top-down and bottom-up effects. Ecology 91:2819–2825

    Article  Google Scholar 

  • Holling CS (1959) Some characteristics of simple types of predation and parasitism. Can Entomolo 91:385–398

    Article  Google Scholar 

  • Jones CG, Hess TA, Whitman DW, Silk PJ, Blum MS (1986) Idiosyncratic variation in chemical defenses among individual generalist grasshoppers. J Chem Ecol 12:749–761

    Article  CAS  Google Scholar 

  • Kingsolver JG, Higgins JK, Augustine KE (2015) Fluctuating temperatures and ectotherm growth: distinguishing non-linear and time-dependent effects. J Exp Biol 218:2218–2225

  • Lang B, Rall BC, Brose U (2012) Warming effects on consumption and intraspecific interference competition depend on predator metabolism. J Anim Ecol 81:516–523

    Article  Google Scholar 

  • Li J, Lehmann S, Weißbecker B, Naharros IO, Schütz S, Joop G, Wimmer EA (2013) Odoriferous defensive stink gland transcriptome to identify novel genes necessary for quinone synthesis in the red flour beetle, Tribolium castaneum. PLoS Gen 9:e1003596

    Article  CAS  Google Scholar 

  • Lomnicki A (1988) Population ecology of individuals. Princeton University Press

  • Luxton M (1972) Studies on oribatid mites of a Danish beech wood soil .I. Nutritional biology. Pedobiologia 12:434–463

    Google Scholar 

  • Luxton M (1975) Studies on the oribatid mites of a Danish beech wood soil. II. Biomass, calorimetry, and respirometry. Pedobiologia 15:161–200

    Google Scholar 

  • McCoull C, Swain R, Barnes R (1998) Effect of temperature on the functional response and components of attack rate in Naucoris congrex Stål (Hemiptera: Naucoridae). Aust J Entomol 37:323–327

    Article  Google Scholar 

  • Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142

    Article  Google Scholar 

  • Norton RA (1994) Evolutionary aspects of oribatid mite life histories and consequences for the origin of the Astigmata. In: Houck MA (ed) Mites: ecological and evolutionary analyses of life-history patterns, Chapman & Hall edn. Chapman & Hall, New York, pp 99–135

    Chapter  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RC (2017) Nlme: linear and nonlinear mixed effects models. R package version 3:1–131 https://cran.r-project.org/web/packages/nlme/

  • Rall BC, Brose U, Hartvig M, Kalinkat G, Schwarzmuller F, Vucic-Pestic O, Petchey OL (2012) Universal temperature and body-mass scaling of feeding rates. Philos Trans R Soc Lond Ser B Biol Sci 367:2923–2934

    Article  Google Scholar 

  • Raspotnig G (2006) Chemical alarm and defence in the oribatid mite Collohmannia gigantea (Acari: Oribatida). Exp Appl Acarol 39:177–194

    Article  CAS  Google Scholar 

  • Rosenzweig ML, Mac Arthur RH (1963) Graphical representation and stability conditions of predator-prey interactions. Am Nat 97:209–223

    Article  Google Scholar 

  • Sakata T, Norton RA (2003) Opisthonotal gland chemistry of a middle-derivative oribatid mite, Archegozetes longisetosus (Acari: Trhypochthoniidae). Int J Acarol 29:345–350

    Article  Google Scholar 

  • Schmidt-Nielsen K (1997) Animal physiology: adaptation and environment. Cambridge University Press, Cambridge, UK

  • Schulte PM (2015) The effects of temperature on aerobic metabolism: towards a mechanistic understanding of the responses of ectotherms to a changing environment. J Exp Biol 218:1856–1866

    Article  Google Scholar 

  • Sentis A, Hemptinne J-L, Brodeur J (2013) Parsing handling time into its components: implications for responses to a temperature gradient. Ecology 94:1675–1680

    Article  CAS  Google Scholar 

  • Simeone JB, Sondheimer E (1970) Chemical ecology. Academic Press, New York

    Google Scholar 

  • Soetaert K, Petzoldt T, Setzer RW (2010) Solving differential equations in R: package deSolve. J Stat Soft 33:1–25

    Google Scholar 

  • Symonds MR, Elgar MA (2008) The evolution of pheromone diversity. Trends Ecol Evol 23:220–228

    Article  Google Scholar 

  • Thiel T, Brechtel A, Brückner A, Heethoff M, Drossel B (2018) The effect of reservoir-based chemical defense on predator-prey dynamics. Theo Ecol:1–14

  • Wong B, Candolin U (2015) Behavioral responses to changing environments. Behav Ecol 26:665–673

    Article  Google Scholar 

Download references

Acknowledgments

We want to thank Roy A. Norton for language editing and proofreading. AB was funded by the German Nation Academic Foundation and is a Simons Fellow of the Life Sciences Research Foundation (LSRF). The study was supported by the German Science Foundation (DFG; HE 4593/5–1).

Author information

Authors and Affiliations

Authors

Contributions

AB initial idea; AB, MH designed research; CM performed experiments and chemical analysis; CM, AB modeled and statistically analyzed the data; AB wrote the first draft with input from CM; AB revised the manuscript; MH, CM commented on the manuscript.

Corresponding author

Correspondence to Adrian Brückner.

Electronic supplementary material

ESM 1

(PDF 177 kb)

ESM 2

(XLSX 169 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Merkel, C., Heethoff, M. & Brückner, A. Temperature Affects Chemical Defense in a Mite-Beetle Predator-Prey System. J Chem Ecol 46, 947–955 (2020). https://doi.org/10.1007/s10886-020-01212-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-020-01212-3

Keywords

Navigation