Skip to main content
SpringerLink
Log in

Behavioral response of a generalist predator to chemotactile cues of two taxonomically distinct prey species

  • Original Article
  • Published:
Chemoecology Aims and scope Submit manuscript

Abstract

Chemotactile cues unintentionally left by animals can play a major role in predator–prey interactions. Specialized predators can use them to find their prey, while prey individuals can assess predation risk. However, little is known to date about the importance of chemotactile cues for generalist predators such as ants. Here, we investigated the response of a generalized predatory ant, Formica polyctena, to cues of two taxonomically distinct prey: a spider (Pisaura mirabilis) and a cricket (Nemobius sylvestris). In analogy, we studied whether crickets and spiders showed antipredator behavior in response to ant cues. When confronted with cues of the two prey species, Formica polyctena workers showed increased residence time and reduced movement speed, which suggests success-motivated searching behavior and thus increased foraging effort. The ants’ response did not differ between cues of the two prey species, coinciding with similar aggression and consumption rates of dead prey. However, the cuticular hydrocarbons, which likely resemble part of the potential cues, differed strongly between the species, with only few methyl-branched alkanes in common. This suggests that ants respond to multiple compounds left by other organisms with prey-search behavior. The two prey species, in turn, showed no detectable antipredator behavior in response to ant cues. Our study shows that ants can detect and respond to chemotactile cues of taxonomically and ecologically distinct prey species, probably to raise their foraging success. Using such chemotactile cues for prey detection may drastically increase their foraging efficiency and thus contribute to the high ecological success of ants.

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
Fig. 4

Similar content being viewed by others

References

  • Agarwala BK, Yasuda H, Kajita Y (2003) Effect of conspecific and heterospecific feces on foraging and oviposition of two predatory ladybirds: role of fecal cues in predator avoidance. J Chem Ecol 29:357–376

    Article  CAS  PubMed  Google Scholar 

  • Akino T, Yamaoka R (2005) Trail discrimination signal of Lasius japonicus (Hymenoptera: Formicidae). Chemoecology 15:21–30

    Article  CAS  Google Scholar 

  • Al Abassi S, Birkett MA, Pettersson J et al (2000) Response of the seven-spot ladybird to an aphid alarm pheromone and an alarm pheromone inhibitor is mediated by paired olfactory cells. J Chem Ecol 26:1765–1771

    Article  Google Scholar 

  • Baudoin C, Haim A, Durand J-L (2013) Effect of conspecific and heterospecific urine odors on the foraging behavior of the golden spiny mouse. Integr Zool 8(Suppl 1):1–8

    Article  PubMed  Google Scholar 

  • Bell RD, Rypstra AL, Persons MH (2006) The effect of predator hunger on chemically mediated antipredator responses and survival in the wolf spider Pardosa milvina (Araneae: Lycosidae). Ethology 112:903–910

    Article  Google Scholar 

  • Binz H, Bucher R, Entling MH, Menzel F (2014a) Knowing the risk: crickets distinguish between spider predators of different size and commonness. Ethology 120:99–110

    Article  Google Scholar 

  • Binz H, Foitzik S, Staab F, Menzel F (2014b) The chemistry of competition: exploitation of heterospecific cues depends on the dominance rank in the community. Anim Behav 94:45–53

    Article  Google Scholar 

  • Blomquist GJ, Bagnères A-G (2010) Insect hydrocarbons: biology, biochemistry, and chemical ecology. Cambridge University Press, New York

    Book  Google Scholar 

  • Bucher R, Binz H, Menzel F, Entling MH (2014) Effects of spider chemotactile cues on arthropod behavior. J Insect Behav 27:567–580

    Article  Google Scholar 

  • Buehlmann C, Graham P, Hansson BS, Knaden M (2014) Desert ants locate food by combining high sensitivity to food odors with extensive crosswind runs. Curr Biol 24:960–964

    Article  CAS  PubMed  Google Scholar 

  • Cárdenas M, Jiroš P, Pekár S (2012) Selective olfactory attention of a specialised predator to intraspecific chemical signals of its prey. Naturwissenschaften 99:597–605

    Article  PubMed  Google Scholar 

  • Clemente CJ, McMaster KA, Fox E et al (2010) The visual system of the Australian wolf spider Lycosa leuckartii (Araneae: Lycosidae): Visual acuity and the functional role of the eyes. J Arachnol 38:398–406

    Article  Google Scholar 

  • Collett TS, Collett M (2002) Memory use in insect visual navigation. Nat Rev Neurosci 3:542–552

    Article  CAS  PubMed  Google Scholar 

  • Czaczkes TJ, Heinze J, Ruther J (2015) Nest etiquette—where ants go when nature calls. PLoS One 10(2):e0118376. doi:10.1371/journal.pone.0118376

    Article  PubMed  PubMed Central  Google Scholar 

  • Dall SRX, Giraldeau L-A, Olsson O et al (2005) Information and its use by animals in evolutionary ecology. Trends Ecol Evol 20:187–193

    Article  PubMed  Google Scholar 

  • Dangles O, Magal C, Pierre D et al (2005) Variation in morphology and performance of predator-sensing system in wild cricket populations. J Exp Biol 208:461–468

    Article  PubMed  Google Scholar 

  • Dangles O, Ory N, Steinmann T et al (2006) Spider’s attack versus cricket’s escape: velocity modes determine success. Anim Behav 72:603–610

    Article  Google Scholar 

  • Domisch T, Finér L, Neuvonen S et al (2009) Foraging activity and dietary spectrum of wood ants (Formica rufa group) and their role in nutrient fluxes in boreal forests. Ecol Entomol 34:369–377

    Article  Google Scholar 

  • Drechsler P, Federle W (2006) Biomechanics of smooth adhesive pads in insects: influence of tarsal secretion on attachment performance. J Comp Physiol A 192:1213–1222

    Article  Google Scholar 

  • Driessen GJ, Van Raalte AT, De Bruyn GJ (1984) Cannibalism in the red wood ant, Formica polyctena (Hymenoptera: Formicidae). Oecologia 63:13–22

    Article  Google Scholar 

  • Dupuy F, Casas J, Body M, Lazzari CR (2011) Danger detection and escape behavior in wood crickets. J Insect Physiol 57:865–871

    Article  CAS  PubMed  Google Scholar 

  • Durant SM (2000) Living with the enemy: avoidance of hyenas and lions by cheetahs in the Serengeti. Behav Ecol 11:624–632

    Article  Google Scholar 

  • Eigenbrode SD, Espelie KE (1995) Effects of plant epicuticular lipids on insect herbivores. Annu Rev Entomol 40:171–194

    Article  Google Scholar 

  • Ekner A, Tryjanowski P (2008) Do small hole nesting passerines detect cues left by a predator? A test on winter roosting sites. Acta Ornithol 43:107–111

    Article  Google Scholar 

  • Eltz T (2006) Tracing pollinator footprints on natural flowers. J Chem Ecol 32:907–915. doi:10.1007/s10886-006-9055-6

    Article  CAS  PubMed  Google Scholar 

  • Evans TA, Inta R, Lai JCS et al (2009) Termites eavesdrop to avoid competitors. Proc R Soc B Biol Sci 276:4035–4041

    Article  Google Scholar 

  • Federle W (2006) Why are so many adhesive pads hairy? J Exp Biol 209:2611–2621

    Article  PubMed  Google Scholar 

  • Federle W, Riehle M, Curtis AS, Full RJ (2002) An integrative study of insect adhesion: mechanics and wet adhesion of pretarsal pads in ants. Integr Comp Biol 42:1100–1106

    Article  PubMed  Google Scholar 

  • Foelix RF (2011) Biology of Spiders, 3rd edn. Oxford University Press, New York

    Google Scholar 

  • Folgarait PJ (1998) Ant biodiversity and its relationship to ecosystem functioning: a review. Biodivers Conversat 7:1221–1244

    Article  Google Scholar 

  • Geiselhardt SF, Geiselhardt S, Peschke K (2009) Comparison of tarsal and cuticular chemistry in the leaf beetle Gastrophysa viridula (Coleoptera: Chrysomelidae) and an evaluation of solid-phase microextraction and solvent extraction techniques. Chemoecology 19:185–193

    Article  CAS  Google Scholar 

  • Geiselhardt SF, Geiselhardt S, Peschke K (2011) Congruence of epicuticular hydrocarbons and tarsal secretions as a principle in beetles. Chemoecology 21:181–186

    Article  CAS  Google Scholar 

  • Greene MJ, Gordon DM (2003) Cuticular hydrocarbons inform task decisions. Nature 423:32

    Article  CAS  PubMed  Google Scholar 

  • Hawes C, Stewart AJA, Evans HF (2002) The impact of wood ants (Formica rufa) on the distribution and abundance of ground beetles (Coleoptera: Carabidae) in a scots pine plantation. Oecologia 131:612–619

    Article  Google Scholar 

  • Hergenröder R, Barth FG (1983) The release of attack and escape behavior by vibratory stimuli in a wandering spider (Cupiennius salei Keys.). J Comp Physiol A 152:347–358

    Article  Google Scholar 

  • Hölldobler B, Wilson EO (1977) Colony-specific territorial pheromone in the African weaver ant Oecophylla longinoda (Latreille). Proc Natl Acad Sci USA 74:2072–2075

    Article  PubMed  PubMed Central  Google Scholar 

  • Hölldobler B, Wilson EO (1990) The Ants. Harvard University Press, Cambridge

    Book  Google Scholar 

  • Horstmann K (1982) Die Energiebilanz der Waldameise (Formica polyctena) in einem Eichenwald. Insectes Soc 29:402–421

    Article  Google Scholar 

  • Hughes NK, Price CJ, Banks PB (2010) Predators are attracted to the olfactory signals of prey. PLoS One 5:5–8

    Google Scholar 

  • Hunter JS, Durant SM, Caro TM (2007) To flee or not to flee: predator avoidance by cheetahs at kills. Behav Ecol Sociobiol 61:1033–1042

    Article  Google Scholar 

  • Jędrzejewski W, Rychlik L, Jędrzejewska B (1993) Responses of bank voles to odours of seven species of predators: experimental data and their relevance to natural data and their experimental relationships. Oikos 68:251–257

    Article  Google Scholar 

  • Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394

    Google Scholar 

  • Labonte D, Federle W (2015) Rate-dependence of ‘wet’ biological adhesives and the function of the pad secretion in insects. Soft Matter 11:8661–8673

    Article  CAS  PubMed  Google Scholar 

  • Lang C, Menzel F (2011) Lasius niger ants discriminate aphids based on their cuticular hydrocarbons. Anim Behav 82:1245–1254

    Article  Google Scholar 

  • Leonhardt SD, Menzel F, Nehring V, Schmitt T (2016) Ecology and evolution of communication in social insects. Cell 164:1277–1287

    Article  CAS  PubMed  Google Scholar 

  • Martin S, Drijfhout F (2009) A review of ant cuticular hydrocarbons. J Chem Ecol 35:1151–1161

    Article  CAS  PubMed  Google Scholar 

  • McCormick AC, Unsicker SB, Gershenzon J (2012) The specificity of herbivore-induced plant volatiles in attracting herbivore enemies. Trends Plant Sci 17:303–310

    Article  Google Scholar 

  • McDougall P, Milne H (1968) The anti-predator function of defecation on their own eggs by female Eiders. Wildfowl 29:55–59

    Google Scholar 

  • Menzel F, Blüthgen N, Tolasch T et al (2013) Crematoenones—a novel substance class exhibited by ants functions as appeasement signal. Front Zool 10:32

    Article  PubMed  PubMed Central  Google Scholar 

  • Mestre L, Bucher R, Entling MH (2014) Trait-mediated effects between predators: ant chemical cues induce spider dispersal. J Zool 293:119–125

    Article  Google Scholar 

  • Morgan ED (2009) Trail pheromones of ants. Physiol Entomol 34:1–17

    Article  CAS  Google Scholar 

  • Pearce-Duvet JMC, Feener DHJ (2010) Resource discovery in ant communities: do food type and quantity matter? Ecol Entomol 35:549–556

    Article  Google Scholar 

  • Peattie AM, Dirks JH, Henriques S, Federle W (2011) Arachnids secrete a fluid over their adhesive pads. PLoS ONE 6:e20485

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Persons MH, Rypstra AL (2001) Wolf spiders show graded antipredator behavior in the presence of chemical cues from different sized predators. J Chem Ecol 27:2493–2504

    Article  CAS  PubMed  Google Scholar 

  • Persons MH, Walker SE, Rypstra AL, Marshall SD (2001) Wolf spider predator avoidance tactics and survival in the presence of diet-associated predator cues (Araneae: Lycosidae). Anim Behav 61:43–51

    Article  PubMed  Google Scholar 

  • Persons MH, Walker SE, Rypstra AL (2002) Fitness costs and benefits of antipredator behavior mediated by chemotactile cues in the wolf spider Pardosa milvina (Araneae: Lycosidae). Behav Ecol 13:386–392

    Article  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S et al (2012) nlme: Linear and nonlinear mixed effects models, Version 3.1-110. http://cran.r-project.org/web/packages/nlme/index.html

  • Roberts MJ (1996) Collins field guide to the spiders of Britain and Northern Europe. HarperCollins, London

    Google Scholar 

  • Rosengren R, Fortelius W (1986) Ortstreue in foraging ants of the Formica rufa group—hierarchy of orienting cues and long-term memory. Insectes Soc 33:306–337

    Article  Google Scholar 

  • Rypstra AL, Buddle CM (2013) Spider silk reduces insect herbivory. Biol Lett 9:20120948

    Article  PubMed  PubMed Central  Google Scholar 

  • Schatz B, Hossaert-McKey M (2010) Ants use odour cues to exploit fig–fig wasp interactions. Acta Oecol 36:107–113

    Article  Google Scholar 

  • Schatz B, Anstett M-C, Out W, Hossaert-McKey M (2003) Olfactive detection of fig wasps as prey by the ant Crematogaster scutellaris (Formicidae; Myrmicinae). Naturwissenschaften 90:456–459

    Article  CAS  PubMed  Google Scholar 

  • Seifert B (2007) Die Ameisen Mittel- und Nordeuropas. lutra Verlag, Görlitz

    Google Scholar 

  • Storm JJ, Lima SL (2008) Predator-naïve fall field crickets respond to the chemical cues of wolf spiders. Can J Zool 86:1259–1263

    Article  CAS  Google Scholar 

  • R Development Core Team (2013) R: a language and environment for statistical computing, Version 3.0.2. R Foundation for Statistical Computing. http://www.R-project.org, Vienna, Austria

  • Uhl G (2013) Spider olfaction: attracting, detecting, luring and avoiding. In: Nentwig W (ed) Spider ecophysiology. Springer, Berlin Heidelberg, Germany

    Google Scholar 

  • Van der Aart PJM, De Wit T (1971) A field study on interspecific competition between ants (Formicidae) and hunting spiders (Lycosidae, Gnaphosidae, Ctenidae, Pisauridae, Clubionidae). Neth J Zool 21:117–126

    Article  Google Scholar 

  • Van Zweden JS, D’Ettorre P (2010) Nestmate recognition in social insects and the role of hydrocarbons. In: Blomquist GJ, Bagnères A-G (eds) Insect hydrocarbons: biology, biochemistry, and chemical ecology. Cambridge University Press, Cambridge, pp 222–243

    Chapter  Google Scholar 

  • Vinson SB (1977) Behavioral chemicals in the augmentation of natural enemies. In: Ridgeway SBV (ed) Biological control by augmentation of natural enemies. Plenum, New York, pp 237–279

    Chapter  Google Scholar 

  • Weier JA, Feener DHJ (1995) Foraging in the seed-harvester ant genus Pogonomyrmex: are energy costs important? Behav Ecol Sociobiol 36:291–300

    Article  Google Scholar 

  • Wüst M, Menzel F (in press) I smell where you walked—how chemical cues influence movement decisions in ants. Oikos. doi:10.1111/oik.03332

  • Zhou X, Slone JD, Rokas A et al (2012) Phylogenetic and transcriptomic analysis of chemosensory receptors in a pair of divergent ant species reveals sex-specific signatures of odor coding. PLoS Genet 8:e1002930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank Roman Bucher for sharing his knowledge about arthropod behavior. We are very grateful to Diethelm Freise-Harenberg from the local nature conservation authority, Mainz-Bingen, Germany, and Jürgen Koch from the forestry commission office Rhine-Hesse, Germany, for providing collection permit for Formica polyctena worker groups. The study was supported by the German Research Foundation (DFG) under Grant Number ME3842/2-1 to Florian Menzel. The authors have no conflict of interest.

Author information

Authors and Affiliations

  1. Institute of Zoology, University of Mainz, Johannes-von-Müller-Weg 6, 55128, Mainz, Germany

    Hellena Binz, Elena F. Kraft & Florian Menzel

  2. Institute for Environmental Sciences, University of Koblenz-Landau, Fortstraße 7, 76829, Landau, Germany

    Hellena Binz & Martin H. Entling

Authors
  1. Hellena Binz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elena F. Kraft
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Martin H. Entling
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Florian Menzel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hellena Binz.

Additional information

Handling Editor: Michael Heethoff.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 22 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Binz, H., Kraft, E.F., Entling, M.H. et al. Behavioral response of a generalist predator to chemotactile cues of two taxonomically distinct prey species. Chemoecology 26, 153–162 (2016). https://doi.org/10.1007/s00049-016-0215-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00049-016-0215-z

Keywords

Search

Navigation