Behavioral Ecology and Sociobiology

, Volume 62, Issue 7, pp 1079–1083 | Cite as

Threat-sensitive learning of predators by larval mosquitoes Culex restuans

  • Maud C. O. Ferrari
  • François Messier
  • Douglas P. Chivers
Original Paper

Abstract

A prerequisite for prey to show adaptive behavioural responses to predators is that the prey has the ability to recognise predators as threats. While predator recognition can be innate in many situations, learning is often essential. For many aquatic species, one common way to learn about predators is through the pairing of a novel predator odour with alarm cues released from injured conspecifics. One study with fish demonstrated that this mode of learning not only allows the prey to recognise the predatory cues as a threat, but also mediates the level of threat associated with the predator cues (i.e. threat-sensitive learning). When the prey is exposed to the novel predator with a high concentration of alarm cues, they subsequently show a high intensity of antipredator response to the predator cues alone. When exposed to the predator with a low concentration of alarm cues, they subsequently show a low-intensity response to the predator cues. Here, we investigated whether larval mosquitoes Culex restuans have the ability to learn to recognise salamanders as a threat through a single pairing of alarm cues and salamander odour and also whether they would learn to respond to salamander cues in a threat-sensitive manner. We conditioned individual mosquitoes with water or a low, medium or high concentration of crushed conspecific cues (alarm cues) paired with salamander odour. Mosquitoes exposed to salamander odour paired with alarm cues and subsequently exposed to salamander odour alone responded to the salamander as a threat. Moreover, the intensity of antipredator response displayed during the conditioning phase matched the response intensity during the testing phase. This is the first demonstration of threat-sensitive learning in an aquatic invertebrate.

Keywords

Culex restuans Predator cues Threat-sensitive learning Alarm cues Novel predators 

References

  1. Berejikian BA, Tezaka EP, LaRaeb AL (2003) Innate and enhanced predator recognition in hatchery-reared chinook salmon. Environ Biol Fishes 67:241–251CrossRefGoogle Scholar
  2. Chivers DP, Smith RJF (1994) Fathead minnows, Pimephales promelas, acquire predator recognition when alarm substance is associated with the sight of unfamiliar fish. Anim Behav 48:597–605CrossRefGoogle Scholar
  3. Chivers DP, Smith RJF (1998) Chemical alarm signalling in aquatic predator–prey systems: a review and prospectus. Ecoscience 5:338–352Google Scholar
  4. Curio E, Ernst U, Vieth W (1978) Cultural transmission of enemy recognition: one function of mobbing. Science 202:899–901PubMedCrossRefGoogle Scholar
  5. Fendt M (2006) Exposure to urine of canids and felids, but not of herbivores, induces defensive behavior in laboratory rats. J Chem Ecol 32:2617–2627PubMedCrossRefGoogle Scholar
  6. Ferrari MCO, Trowell JJ, Brown GE, Chivers DP (2005) The role of learning in the development of threat-sensitive predator avoidance in fathead minnows. Anim Behav 70:777–784CrossRefGoogle Scholar
  7. Ferrari MCO, Gonzalo A, Messier F, Chivers DP (2007a) Generalization of learned predator recognition: an experimental test and framework for future studies. Proc R Soc B 274:1853–1859PubMedCrossRefGoogle Scholar
  8. Ferrari MCO, Messier F, Chivers DP (2007b) Variable predation risk and the dynamic nature of mosquito antipredator responses. Chemoecology, DOI 10.1007/s00049-007-0380-1
  9. Ferrari MCO, Messier F, Chivers DP (2007c) Degradation of alarm cues under natural conditions: risk assessment by larval amphibians. Chemoecology, DOI 10.1007/s00049-007-0381-0
  10. Goth A (2001) Innate predator-recognition in Australian brush-turkey (Alectura lathami, Megapodiidae) hatchlings. Behaviour 138:117–136CrossRefGoogle Scholar
  11. Griffin AS, Evans CS, Blumstein DT (2001) Learning specificity in acquired predator recognition. Anim Behav 62:577–589CrossRefGoogle Scholar
  12. Hazlett BA (2003) Predator recognition and learned irrelevance in the crayfish Orconectes virilis. Ethology 109:765–780CrossRefGoogle Scholar
  13. Helfman GS (1989) Threat-sensitive predator avoidance in damselfish–trumpetfish interactions. Behav Ecol Sociobiol 24:47–58CrossRefGoogle Scholar
  14. Kesavaraju B, Damal K, Juliano SA (2007) Threat-sensitive behavioral responses to concentrations of water-borne cues from predation. Ethology 113:199–206PubMedCrossRefGoogle Scholar
  15. Lima SL, Bednekoff PA (1999) Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am Nat 153:649–659CrossRefGoogle Scholar
  16. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640CrossRefGoogle Scholar
  17. Mathis A, Chivers DP, Smith RJF (1993) Population differences in responses of fathead minnows (Pimephales promelas) to visual and chemical stimuli from predators. Ethology 93:31–40CrossRefGoogle Scholar
  18. Mirza RS, Ferrari MCO, Kiesecker JM, Chivers DP (2006) Responses of American toad tadpoles to predation cues: behavioural response thresholds, threat-sensitivity and acquired predation recognition. Behaviour 143:887–889CrossRefGoogle Scholar
  19. Rochette R, Arsenault DJ, Justome B, Himmelman JH (1998) Chemically-mediated predator recognition learning in a marine gastropod. Ecoscience 5:353–360Google Scholar
  20. Sih A, Ziemba R, Harding KC (2000) New insights on how temporal variation in predation risk shapes prey behavior. Trends Ecol Evol 15:3–4PubMedCrossRefGoogle Scholar
  21. Wiebe KL (2004) Innate and learned components of defence by flickers against a novel nest competitor, the European starling. Ethology 110:779–791CrossRefGoogle Scholar
  22. Wisenden BD, Millard MC (2001) Aquatic flatworms use chemical cues from injured conspecifics to assess predation risk and to associate risk with novel cues. Anim Behav 62:761–766CrossRefGoogle Scholar
  23. Wisenden BD, Chivers DP, Smith RJF (1997) Learned recognition of predation risk by Enallagma damselfly larvae (Odonata, Zygoptera) on the basis of chemical cues. J Chem Ecol 23:137–151CrossRefGoogle Scholar
  24. Woody DR, Mathis A (1998) Acquired recognition of chemical stimuli from an unfamiliar predator: associative learning by adult newts, Notophthalmus viridescens. Copeia 1998:1027–1031CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Maud C. O. Ferrari
    • 1
  • François Messier
    • 1
  • Douglas P. Chivers
    • 1
  1. 1.Department of BiologyUniversity of SaskatchewanSaskatoonCanada

Personalised recommendations