Skip to main content
Log in

Exploratory decisions of Trinidadian guppies when uncertain about predation risk

  • Original Paper
  • Published:
Animal Cognition Aims and scope Submit manuscript

Abstract

Animals can reduce their uncertainty of predation risk by gathering new information via exploration behaviour. However, a decision to explore may also be costly due to increased predator exposure. Here, we found contextual effects of predation risk on the exploratory activity of Trinidadian guppies Poecilia reticulata in a novel environment. First, guppies were exposed to a 3-day period of either high or low background predation risk in the form of repeated exposure to either injured conspecific cues (i.e. alarm cues) or control water, respectively. A day later, guppies were moved into a testing arena with limited visual information due to structural barriers and were then presented with an acute chemical stimulus, either alarm cues (a known and reliable indicator of risk), a novel odour (an ambiguous cue), or control water. In the presence of control water, guppies from high and low background risk showed a similar willingness to explore the arena. However, high-risk individuals significantly reduced their spatial evenness, although not their movement latency, in the presence of both the alarm and novel cues. When these high-risk individuals were a member of a shoal, they became willing to explore the environment more evenly in the presence of alarm cues while remaining cautious toward the novel cue, indicating an effect of the greater uncertainty associated with the novel cue. In contrast, low-risk guppies showed a willingness to explore the arena regardless of acute threat or social context. Such contextual effects of background risk and social context highlight the complexity of exploratory decisions when uncertain.

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

Similar content being viewed by others

Data availability

Data are provided as supplementary information.

References

  • Archard GA, Braithwaite V (2010) The importance of wild populations in studies of animal temperament. J Zool 281:149–160

    Article  Google Scholar 

  • Archard GA, Braithwaite V (2011) Increased exposure to predators increases both exploration and activity level in Brachyrhaphis episcopi. J Fish Biol 78:593–601

    Article  CAS  PubMed  Google Scholar 

  • Berdahl A, Torney CJ, Ioannou CC, Faria JJ, Couzin ID (2013) Emergent sensing of complex environments by mobile animal groups. Science 339:574–576

    Article  CAS  PubMed  Google Scholar 

  • Brown GE, Godin JGJ (1999) Chemical alarm signals in wild Trinidadian guppies (Poecilia reticulata). Can J Zool 77:562–570

    Article  CAS  Google Scholar 

  • Brown C, Jones F, Braithwaite V (2005) In situ examination of boldness–shyness traits in the tropical poeciliid, Brachyraphis episcopi. Anim Behav 70:1003–1009

    Article  Google Scholar 

  • Brown GE, Macnaughton CJ, Elvidge CK, Ramnarine I, Godin JGJ (2009) Provenance and threat-sensitive predator avoidance patterns in wild-caught Trinidadian guppies. Behav Ecol Sociobiol 63:699–706

    Article  Google Scholar 

  • Brown GE, Elvidge CK, Macnaughton CJ, Ramnarine I, Godin JGJ (2010) Cross-population responses to conspecific chemical alarm cues in wild Trinidadian guppies, Poecilia reticulata: evidence for local conservation of cue production. Can J Zool 88:139–147

    Article  Google Scholar 

  • Brown GE, Ferrari MC, Elvidge CK, Ramnarine I, Chivers DP (2013) Phenotypically plastic neophobia: a response to variable predation risk. Proc Roy Soc B 280:20122712

    Article  Google Scholar 

  • Crane AL, Ferrari MCO (2017) Patterns of predator neophobia: a meta-analytic review. Proc Roy Soc B 284:20170583

    Article  Google Scholar 

  • Crane AL, Brown GE, Chivers DP, Ferrari MCO (2020a) An ecological framework of neophobia: from cells to organisms to populations. Biol Rev 95:218–231

    Article  Google Scholar 

  • Crane AL, Feyten LE, Ramnarine IW, Brown GE (2020b) The propensity for re-triggered predation fear in a prey fish. Sci Rep 10:1–8

    Article  CAS  Google Scholar 

  • Dall SR (2010) Managing risk: the perils of uncertainty. In: Westneat DF, Fox CW (eds) Evolutionary behavioral ecology. Oxford University Press, New York, pp 194–206

    Google Scholar 

  • Deacon AE, Jones FA, Magurran AE (2018) Gradients in predation risk in a tropical river system. Curr Zool 64:213–221

    Article  PubMed  PubMed Central  Google Scholar 

  • Elvidge C, Macnaughton C, Brown G (2013) Sensory complementation and antipredator behavioural compensation in acid-impacted juvenile Atlantic salmon. Oecologia 172:69–78

    Article  CAS  PubMed  Google Scholar 

  • Elvidge CK, Ramnarine I, Brown GE (2014) Compensatory foraging in Trinidadian guppies: effects of acute and chronic predation threats. Curr Zool 60:323–332

    Article  Google Scholar 

  • Elvidge CK, Chuard PJ, Brown GE (2016) Local predation risk shapes spatial and foraging neophobia patterns in Trinidadian guppies. Curr Zool 62:457–462

    Article  PubMed  PubMed Central  Google Scholar 

  • Endler J (1986) Defense against predators. In: Feder ME, Lauder GV (eds) Predator-prey relationships: perspectives and approaches from the study of lower vertebrates. University of Chicago Press, Chicago, pp 169–202

    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 

  • Feyten LEA, Crane AL, Ramnarine I, Brown GE (in press) Predation risk shapes the use of conflicting personal risk and social social information in guppies

  • Godin J-G (1995) Predation risk and alternative mating tactics in male Trinidadian guppies (Poecilia reticulata). Oecologia 103:224–229

    Article  PubMed  Google Scholar 

  • Goldman JA, Feyten LE, Ramnarine IW, Brown GE (2020) Sender and receiver experience alters the response of fish to disturbance cues. Curr Zool 66:255–261

    Article  PubMed  Google Scholar 

  • Goldman JA, Crane AL, Feyten LEA, Collins E, Brown GE (in press) Disturbance cue communication is shaped by emitter diet and receiver background risk in Trinidadian guppies. Curr Zool

  • Hartman EJ, Abrahams MV (2000) Sensory compensation and the detection of predators: the interaction between chemical and visual information. Proc Roy Soc B 267:571–575

    Article  CAS  Google Scholar 

  • Hasenjager MJ, Dugatkin LA (2017) Fear of predation shapes social network structure and the acquisition of foraging information in guppy shoals. Proc Roy Soc B 284:20172020

    Article  Google Scholar 

  • Hills JM, Thomason JC, Davis H, Köhler J, Millett E (2000) Exploratory behaviour of barnacle larvae in field conditions. Biofouling 16:171–179

    Article  Google Scholar 

  • Johnson DD, Blumstein DT, Fowler JH, Haselton MG (2013) The evolution of error: error management, cognitive constraints, and adaptive decision-making biases. Trends Ecol Evol 28:474–481

    Article  PubMed  Google Scholar 

  • Kelley JL, Phillips SC, Evans JP (2013) Individual consistency in exploratory behaviour and mating tactics in male guppies. Naturwissenschaften 100:965–974

    Article  CAS  PubMed  Google Scholar 

  • Krause J, Godin J-GJ (1995) Predator preferences for attacking particular prey group sizes: consequences for predator hunting success and prey predation risk. Anim Behav 50:465–473

    Article  Google Scholar 

  • Leduc A, Kim JW, Macnaughton CJ, Brown GE (2010) Sensory complement model helps to predict diel alarm response patterns in juvenile Atlantic salmon (Salmo salar) under natural conditions. Can J Zool 88:398–403

    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 

  • Lima SL, Dill LM (1990) Behavioral decision made under the risk of predation - a review and prospectus. Can J Zool 68:619–640

    Article  Google Scholar 

  • Magurran AE, Seghers BH (1990a) Population differences in predator recognition and attack cone avoidance in the guppy Poecilia reticulata. Anim Behav 40:443–452

    Article  Google Scholar 

  • Magurran AE, Seghers BH (1990b) Risk sensitive courtship in the guppy (Poecilia reticulata). Behaviour 112:194–201

    Article  Google Scholar 

  • Mathis A, Crane AL (2017) Chemoreception. In: Call J (ed) APA handbook of comparative psychology, vol 2. APA Books, Washington, pp 69–87

    Google Scholar 

  • Mettke-Hofmann C (2017) Neophobia. In: Vonk J, Shackelford T (eds) Encyclopedia of animal cognition and behavior. Springer International Publishing, Cham, pp 1–8

    Google Scholar 

  • Money DA, Ingley SJ, Johnson JB (2017) Divergent predation environment between two sister species of livebearing fishes (Cyprinodontiformes: Poeciliidae) predicts boldness, activity, and exploration behavior. Rev Biol Trop 65:267–277

    Article  PubMed  Google Scholar 

  • Munoz NE, Blumstein DT (2012) Multisensory perception in uncertain environments. Behav Ecol 23:457–462

    Article  Google Scholar 

  • Newar SL, Careau V (2018) The fast and the curious: locomotor performance and exploratory behaviour in eastern chipmunks. Behav Ecol Sociobiol 72:27. https://doi.org/10.1007/s00265-018-2445-2

    Article  Google Scholar 

  • Nordell SE (1998) The response of female guppies, Poecilia reticulata, to chemical stimuli from injured conspecifics. Environ Biol Fishes 51:331–338

    Article  Google Scholar 

  • Preisser EL, Bolnick DI (2008) When predators don’t eat their prey: nonconsumptive predator effects on prey dynamics. Ecology 89:2414–2415

    Article  PubMed  Google Scholar 

  • Reader SM, Kendal JR, Laland KN (2003) Social learning of foraging sites and escape routes in wild Trinidadian guppies. Anim Behav 66:729–739

    Article  Google Scholar 

  • Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318

    Article  PubMed  Google Scholar 

  • Rojas-Ferrer I, Thompson MJ, Morand-Ferron J (2020) Is exploration a metric for information gathering? Attraction to novelty and plasticity in black-capped chickadees. Ethology 126:383–392

    Article  Google Scholar 

  • Salena MG, Turko AJ, Singh A, Pathak A, Hughes E, Brown C, Balshine S (2021) Understanding fish cognition: a review and appraisal of current practices. Anim Cogn 24:395–406

    Article  PubMed  Google Scholar 

  • Seghers BH (1974) Schooling behavior in the guppy (Poecilia reticulata): an evolutionary response to predation. Evolution 28:486–489

    PubMed  Google Scholar 

  • Sih A (1992) Prey uncertainty and the balancing of antipredator and feeding needs. Am Nat 139:1052–1069

    Article  Google Scholar 

  • Swaney W, Kendal J, Capon H, Brown C, Laland KN (2001) Familiarity facilitates social learning of foraging behaviour in the guppy. Anim Behav 62:591–598

    Article  Google Scholar 

  • Trimmer PC, Houston AI, Marshall JA, Mendl MT, Paul ES, McNamara JM (2011) Decision-making under uncertainty: biases and Bayesians. Anim Cogn 14:465–476

    Article  PubMed  Google Scholar 

  • Wade AS, Ramnarine IW, Ioannou CC (2020) The effect of group size on the speed of decision making depends on compromise and predation risk across populations in the guppy Poecilia reticulata. Behaviour 1:1–20

    Google Scholar 

  • Wang Y, Fu S-J, Fu C (2019) Behavioral adjustments to prior predation experience and food deprivation of a common cyprinid fish species vary between singletons and a group. PeerJ 7:e7236

    Article  PubMed  PubMed Central  Google Scholar 

  • Ward AJ, Herbert-Read JE, Sumpter DJ, Krause J (2011) Fast and accurate decisions through collective vigilance in fish shoals. P Nat Acad Sci 108:2312–2315

    Article  CAS  Google Scholar 

  • Wilson AD et al (2014) Dynamic social networks in guppies (Poecilia reticulata). Behav Ecol Sociobiol 68:915–925

    Article  Google Scholar 

  • Wirsing AJ, Heithaus MR, Brown JS, Kotler BP, Schmitz OJ (2020) The context dependence of non-consumptive predator effects. Ecol Lett 24:113–129

    Article  PubMed  Google Scholar 

  • Zanette LY, Clinchy M (2017) Predator-prey interactions: integrating fear effects. In: Call J (ed) APA handbook of comparative psychology, vol 1. APA Books, Washington D.C., pp 815–831

    Google Scholar 

Download references

Acknowledgements

We thank Kharran Deonarinesingh for assistance in the laboratory.

Funding

Funding for this work was provided by the Natural Sciences and Engineering Research Council of Canada in the form of a Discovery Grant to GEB and as NSERC PGS-D to EED.

Author information

Authors and Affiliations

Authors

Contributions

EED, IWR, and GEB conceived the study. EED and LEAF collected the data. GEB and ALC conducted the analyses, and ALC wrote the first draft of the manuscript. All authors contributed to the final version of the manuscript.

Corresponding author

Correspondence to Adam L. Crane.

Ethics declarations

Conflict of interest

We declare no conflicts of interest.

Ethical approval

This research was approved by Concordia University’s Animal Research Ethics Board (protocol #30000255).

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 17 KB)

Supplementary file2 (DOCX 420 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Crane, A.L., Demers, E.E., Feyten, L.E.A. et al. Exploratory decisions of Trinidadian guppies when uncertain about predation risk. Anim Cogn 25, 581–587 (2022). https://doi.org/10.1007/s10071-021-01575-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10071-021-01575-4

Keywords

Navigation