Skip to main content
SpringerLink
Log in

Risk Odors Deriving from Predator Abdominal Gland Secretions Mediate Non-Consumptive Effects on Prey

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

Abstract

Prey can detect the presence of predators by predator-released cues and then flexibly alter their phenotypical traits to mitigate the risk, thus non-consumptive effects emerge. Non-consumptive effects have been widely studied in many ecosystems, however, the mechanisms underlying these effects are poorly understood, leaving questions as to the nature of the risk cues and how prey detect the predator. Here, we used a Y-tube olfactometer to examine whether small brown planthoppers, Laodelphax striatellus (Fallén), could detect the presence of rove beetles (Paederus fuscipes Curtis) via odor from rove beetle abdominal gland secretion. We further identified the chemicals of abdominal gland secretion by gas chromatography-mass spectrometry. Chemicals identified were exposed to a planthopper to test their effects on planthopper behavior. Female or male planthoppers could distinguish the predation risk odors of rove beetle or rove beetle abdominal gland secretion from odor without predation risks. Through gas chromatography-mass spectrometry, sixteen of the most abundant chemicals were found in female and male abdominal gland secretion. Five of them (n-undecane, n-pentadecane, n-hexadecane, n-eicosane, and n-heneicosane) individually or collectively reduced the activity level of planthoppers. These findings enhance our understanding of the role of abdominal gland secretion in mediating non-consumptive predator effects, with significant implications for pest management, and the evolution of chemical signals.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aflitto NC, Thaler JS (2020) Predator pheromone elicits a temporally dependent non-consumptive effect in prey. Ecol Entomol 45:1190–1199

    Article  Google Scholar 

  • Aldrich JR, Lusby WR, Kochansky JP, Abrams CB (1984) Volatile compounds from the predatory insect Podisus maculiventris (Hemiptera: Pentatomidae): male and female metathoracic scent gland and female dorsal abdominal gland secretions. J Chem Ecol 10:561–568

    Article  PubMed  CAS  Google Scholar 

  • Arteaga-Torres JD, Wijmenga JJ, Mathot KJ (2020) Visual cues of predation risk outweigh acoustic cues: a field experiment in black-capped chickadees. Proc R Soc B 287:20202002

    Article  PubMed  PubMed Central  Google Scholar 

  • Auld JR, Relyea RA (2011) Adaptive plasticity in predator-induced defenses in a common freshwater snail: altered selection and mode of predation due to prey phenotype. Evol Ecol 25:189–202

    Article  Google Scholar 

  • Beleznai O, Tholt G, Tóth Z, Horváth V, Marczali Z, Samu F (2015) Cool headed individuals are better survivors: non-consumptive and consumptive effects of a generalist predator on a sap feeding insect. PLoS One 10(8):e0135954

    Article  PubMed  PubMed Central  Google Scholar 

  • Benard MF (2004) Predator-induced phenotypic plasticity in organisms with complex life histories. Annu Rev Ecol Evol Syst 35:651–673

    Article  Google Scholar 

  • Bray A, Nieh J (2014) Non-consumptive predator effects shape honey bee foraging and recruitment dancing. PLoS One 9:e87459

    Article  PubMed  PubMed Central  Google Scholar 

  • Breviglieri CPB, Oliveira PS, Romero GQ (2017) Fear mediates trophic cascades: nonconsumptive effects of predators drive aquatic ecosystem function. Am Nat 189:490–500

    Article  PubMed  Google Scholar 

  • Buskirk JV, Yurewicz KL (1998) Effects of predators on prey growth rate: relative contributions of thinning and reduced activity. Oikos 82:20–28

    Article  Google Scholar 

  • Culshaw-Maurer M, Sih A, Rosenheim JA (2020) Bugs scaring bugs: enemy-risk effects in biological control systems. Ecol Lett 23:1693–1714

    Article  PubMed  PubMed Central  Google Scholar 

  • Da Silva MR, Vidal DM, Figueiredo L, Bandeira PT, Bergmann J, Zarbin PHG (2020) Tergal gland secretion of the rove beetle Aleochara pseudochrysorrhoa (Staphylinidae: Aleocharinae): chemical composition and biological roles. Chem Biodivers 17:e2000483

    Article  PubMed  Google Scholar 

  • Dennis SR, Carter MJ, Hentley WT, Beckerman AP (2010) Phenotypic convergence along a gradient of predation risk. Proc Royal Soc B 278:1687–1696

    Article  Google Scholar 

  • Dixon AFG, Agarwala BK (1999) Ladybird-induced life-history changes in aphids. Proc R Soc B 266:1549–1553

    Article  PubMed Central  Google Scholar 

  • Ferrari MCO, Sih A, Chivers DP (2009) The paradox of risk allocation: a review and prospectus. Anim Behav 78:579–585

    Article  Google Scholar 

  • Ferrari MCO, Wisenden BD, Chivers DP (2010) Chemical ecology of predator-prey interactions in aquatic ecosystems: a review and prospectus. Can J Zool 88:698–724

    Article  Google Scholar 

  • Freitas AVL, Oliveira PS (1996) Ants as selective agents on herbivore biology: effects on the behaviour of a non-myrmecophilous butterfly. J Anim Ecol 65:205–210

    Article  Google Scholar 

  • Godin JJ, Briggs SE (1996) Female mate choice under predation risk in the guppy. Anim Behav 51:117–130

    Article  Google Scholar 

  • Hermann SL, Landis DA (2017) Scaling up our understanding of non-consumptive effects in insect systems. Curr Opin Insect Sci 20:54–60

    Article  PubMed  Google Scholar 

  • Hermann SL, Thaler J (2014) Prey perception of predation risk: volatile chemical cues mediate non-consumptive effects of a predator on a herbivorous insect. Oecologia 176:669–676

    Article  PubMed  Google Scholar 

  • Jandricic SE, Schmidt D, Bryant G, Frank SD (2016) Non-consumptive predator effects on a primary greenhouse pest: predatory mite harassment reduces western flower thrips abundance and plant damage. Biol Control 95:5–12

    Article  Google Scholar 

  • Jefson M, Meinwald J, Nowicki S, Hicks K, Eisner T (1983) Chemical defense of a rove beetle (Creophilus maxillosus). J Chem Ecol 9:159–180

    Article  PubMed  CAS  Google Scholar 

  • Jones EI, Dornhaus A (2011) Predation risk makes bees reject rewarding flowers and reduce foraging activity. Behav Ecol Sociobiol 65:1505–1511

    Article  Google Scholar 

  • Koch BJ, Hall RO Jr, Peckarsky BL (2020) Nonconsumptive effects of brook trout predators reduce secondary production of mayfly prey. Freshw Sci 39:549–558

    Article  Google Scholar 

  • Kohler S, McPeek M (1989) Predation risk and the foraging behavior of competing stream insects. Ecology 70:1811–1825

    Article  Google Scholar 

  • Lima SL, Bednekoff PA (1999) Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am Nat 153:649–659

    Article  PubMed  Google Scholar 

  • Moraes MCB, Pareja M, Laumann RA, Borges M (2008) The chemical volatiles (semiochemicals) produced by Neotropical stink bugs (Hemiptera: Pentatomidae). Neotrop Entomol 37:489–505

    Article  PubMed  CAS  Google Scholar 

  • Otuka A, Matsumura M, Sanada-Morimura S, Takeuchi H, Watanabe T, Ohtsu R, Inoue H (2008) The 2008 overseas mass migration of the small brown planthopper, Laodelphax striatellus, and subsequent outbreak of rice stripe disease in western Japan. Appl Entomol Zool 45:259–266

    Article  Google Scholar 

  • Otuka A, Zhou Y, Lee GS, Matsumura M, Zhu Y, Park HH, Liu Z, Sanada-Morimura S (2012) Prediction of overseas migration of the small brown planthopper, Laodelphax striatellus (Hemiptera: Delphacidae) in East Asia. Appl Entomol Zool 47:379–388

    Article  Google Scholar 

  • Pears JB, Emberts Z, Bateman PW (2018) The scent of danger: the impact of predator chemical cues on emergence from refuge and willingness to autotomize limbs in the house cricket (Acheta domesticus). J Insect Behav 31:416–426

    Article  Google Scholar 

  • Peschke K (1983) Defensive and pheromonal secretion of the tergal gland of Aleochara curtula II. Release and inhibition of male copulatory behavior J Chem Ecol 9:13–31

    PubMed  CAS  Google Scholar 

  • Peschke K (1986) Development, sex specificity, and site of production of aphrodisiac pheromones in Aleochara curtula. J Insect Physiol 32:687–693

    Article  CAS  Google Scholar 

  • Peschke K, Metzler M (1982) Defensive and pheromonal secretion of the tergal gland of Aleochara curtula: I. The chemical composition. J Chem Ecol 8:773–783

    Article  PubMed  CAS  Google Scholar 

  • Peschke K, Metzler M (1987) Cuticular hydrocarbons and female sex pheromones of the rove beetle, Aleochara curtula (Goeze) (Coleoptera:Staphylinidae). Insect Biochem 17:167–178

    Article  CAS  Google Scholar 

  • Preisser EL, Bolnick DI (2008) The many faces of fear: comparing the pathways and impacts of nonconsumptive predator effects on prey populations. PLoS One 3:e2465

    Article  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.r-project.org/

  • Rupert RLL, Kellner DK (1992) Comparative morphology of abdominal glands in Paederinae (Coleoptera: Staphylinidae). Int J Insect Morphol Embryol 21:117–135

    Article  Google Scholar 

  • Say-Sallaz E, Chamaillé-Jammes S, Fritz H, Valeix M (2019) Non-consumptive effects of predation in large terrestrial mammals: mapping our knowledge and revealing the tip of the iceberg. Biol Conserv 235:36–52

    Article  Google Scholar 

  • Schiwitz NC, Schalk CM, Saenz D (2020) Activity level-predation risk tradeoff in a tadpole guild: implications for community organization along the hydroperiod gradient. Am Midl Nat 183:223–232

    Google Scholar 

  • Silberbush A, Markman S, Lewinsohn E, Bar E, Cohen JE, Blaustein L (2010) Predator-released hydrocarbons repel oviposition by a mosquito. Ecol Lett 13:1129–1138

    Article  PubMed  Google Scholar 

  • Steidle JL, Dettner K (1995) Abdominal gland secretion of Bledius rove beetles as an effective defence against predators. Entomol Exp Appl 76:211–216

    Article  Google Scholar 

  • Stephan JG, Stenberg JA, Björkman C (2017) Consumptive and nonconsumptive effect ratios depend on interaction between plant quality and hunting behavior of omnivorous predators. Ecol Evol 7:2327–2339

    Article  PubMed  PubMed Central  Google Scholar 

  • Stökl J, Steiger S (2017) Evolutionary origin of insect pheromones. Curr Opin Insect Sci 24:36–42

  • Stoks R (2001) Food stress and predator-induced stress shape developmental performance in a damselfly. Oecologia 127:222–229

    Article  PubMed  Google Scholar 

  • Thaler JS, Griffin CAM (2008) Relative importance of consumptive and non-consumptive effects of predators on prey and plant damage: the influence of herbivore ontogeny. Entomol Exp Appl 128:34–40

    Article  Google Scholar 

  • Wen J, Ueno T (2021a) Predator cue-induced plasticity of morphology and behavior in planthoppers facilitate the survival from predation. Sci Rep 11:16760

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wen J, Ueno T (2021b) Application of predator-associated cues to control small brown planthoppers: non-consumptive effects of predators suppress the pest population. BioControl. https://doi.org/10.1007/s10526-021-10115-5

  • Werner EE, Peacor SD (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84:1083–1100

    Article  Google Scholar 

  • Wirsing AJ, Heithaus MR, Brown JS, Kotler BP, Schmitz OJ (2021) The context dependence of non-consumptive predator effects. Ecol Lett 24:113–129

    Article  PubMed  Google Scholar 

  • Wisenden BD (2000) Olfactory assessment of predation risk in the aquatic environment. Philos Trans R Soc Lond Ser B Biol Sci 355:1205–1208

    Article  CAS  Google Scholar 

  • Xiong X, Michaud JP, Li Z, Wu P, Chu Y, Zhang Q, Liu X (2015) Chronic, predator- induced stress alters development and reproductive performance of the cotton bollworm, Helicoverpa armigera. BioControl 60:827–837

    Article  Google Scholar 

  • Zacharuk RY, Shields VD (1991) Sensilla of immature insects. Annu Rev Entomol 36:331–354

    Article  Google Scholar 

Download references

Acknowledgements

We thank Emiko Matsunaga, of the Center for Advanced Instrumental and Educational Support, Faculty of Agriculture, Kyushu University, who helps us analyze the samples. We also gratefully acknowledge Hiroki Kusuhara, of the Faculty of Agriculture, Kyushu University Laboratory of Insect Natural Enemies, who kindly helped us to purchase the chemicals. We also thank Professor Robert A. Spicer, of the School of Environment, Earth and Ecosystem Sciences, The Open University, Milton Keynes, MK7 6AA, UK, for helping us edit the English in the draft manuscript.

Authors` Contributions

All authors collaboratively conceived and designed the research; J. W. conducted the laboratory work; J. W. analyzed the data and wrote the manuscript; T. U. and J. W. revised the manuscript.

Available of Data and Material

All data are available from the figshare. Dataset (https://doi.org/10.6084/m9.figshare.15052146.v1).

Author information

Authors and Affiliations

  1. Institute of Biological Control, Faculty of Agriculture, Kyushu University, Fukuoka, 819-0395, Japan

    Jian Wen & Takatoshi Ueno

Authors
  1. Jian Wen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Takatoshi Ueno
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jian Wen.

Ethics declarations

Conflict of Interest

We declare we have no competing interests.

Code Availability

All the data analyses were conducted in R version 4.0.3.

Ethics Approval

This article does not contain any studies with human participants or vertebrates performed by any of the authors.

Informed Consent

Informed consent was obtained from individual or guardian participants.

Supplementary Information

ESM 1

(PDF 327 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wen, J., Ueno, T. Risk Odors Deriving from Predator Abdominal Gland Secretions Mediate Non-Consumptive Effects on Prey. J Chem Ecol 48, 89–98 (2022). https://doi.org/10.1007/s10886-021-01331-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-021-01331-5

Keywords

Search

Navigation