Aquatic Sciences

, 81:53 | Cite as

Kairomone-induced changes in mosquito life history: effects across a food gradient

  • Alon SilberbushEmail author
  • Nofar Gertler
  • Ofer Ovadia
  • Zvika Abramsky
  • Ido Tsurim
Research Article


The aquatic immature stages of species with complex life histories exhibit a range of defense mechanisms in response to predator released kairomones (PRK). Employing these costly mechanisms often results in delayed metamorphosis. Larvae of the house mosquito Culex pipiens (Linnaeus) show a rare exception of accelerated metamorphosis in response to kairomones originated from the mosquitofish Gambusia affinis (Baird and Girard). In a series of lab experiments we examined whether this response is context-dependent with respect to food availability (i.e. applied only when food is abundant and cost is low). We examined life history variables of C. pipiens larvae, reared at different levels of food availability, either with or without PRK. We further examined the effect of PRK on the foraging behavior of the larvae at different instars. We also examined the effect of PRK-induced behavior on larvae survival under actual predation. We showed that the response of C. pipiens larvae to PRK was independent of food availability. Larvae exposed to PRK were less active and survived longer when exposed to direct predation. Exposure to both PRK and small food amounts also resulted in reduced adult size and survival period. The effects of food and PRK were independent of one another. We argue that for organisms with short development time, such as mosquitoes, decreasing time to metamorphosis may be the main feasible refuge from increased predation risk. Hence, Culex larvae exploit their capability for rapid development rate as a main anti-predator mechanism, minimizing the time spent in high-risk environments by accelerating metamorphosis, regardless of available resources, at the expense of other life history traits.


Culex pipiens Food abundance Predator-released kairomones Life history Gambusia affinis Metamorphosis 



We wish to thank Yehonatan Alcalay and Gil Ben-Natan for fruitful discussions. Anat Ben-Natan for technical assistance. This work was supported by the Pratt Foundation, awarded to Alon Silberbush.

Supplementary material

27_2019_649_MOESM1_ESM.xlsx (27 kb)
Supplementary material 1 (XLSX 27 kb)


  1. Abrams PA, Rowe L (1996) The effects of predation on the age and size of maturity of prey. Evolution 50:1052–1061CrossRefGoogle Scholar
  2. Anholt BR, Werner EE (1995) Interaction between food availability and predation mortality mediated by adaptive behavior. Ecology 76:2230–2234CrossRefGoogle Scholar
  3. Anholt BR, Werner E, Skelly DK (2000) Effect of food and predators on the activity of four larval ranid frogs. Ecology 81:3509–3521CrossRefGoogle Scholar
  4. Beketov MA, Liess M (2007) Predation risk perception and food scarcity induce alterations of life-cycle traits of the mosquito Culex pipiens. Ecol Entomol 32:405–410CrossRefGoogle Scholar
  5. Benard MF (2004) Predator-induced phenotypic plasticity in organisms with complex life histories. Annu Rev Ecol Evol Syst 35:651–673CrossRefGoogle Scholar
  6. Bennett AM, Pereira D, Murray DL (2013) Investment into defensive traits by anuran prey (Lithobates pipiens) is mediated by the starvation-predation risk trade-off. PLoS ONE 8:e82344CrossRefGoogle Scholar
  7. Blaustein L (1999) Oviposition habitat selection in response to risk of predation: consequences for populations and community structure. In: Wasser SP (ed) Evolutionary processes and theory: modern perspectives. Kluwer Academic Publishers, Amsterdam, pp 441–456CrossRefGoogle Scholar
  8. Blaustein L, Whitman D (2009) Behavioral plasticity in response to risk of predation: oviposition habitat selection by a mosquito. In: Whitman D, Ananthakrishnan TN (eds) Phenotypic plasticity of insects: mechanisms and consequences. Science, Enfield, pp 263–280Google Scholar
  9. Brodin T, Johansson F, Bergsten J (2006) Predator related oviposition site selection of aquatic beetles (Hydroporus spp.) and effects on offspring life-history. Freshw Biol 51:1277–1285CrossRefGoogle Scholar
  10. Chobu M, Nkwengulila G, Mahande AM, Mwang’onde BJ, Kweka EJ (2015) Direct and indirect effect of predators on Anopheles gambiae sensu stricto. Acta Trop 142:131–137CrossRefGoogle Scholar
  11. Dahl J, Peckarsky BL (2003) Developmental responses to predation risk in morphologically defended mayflies. Oecologia 137:188–194CrossRefGoogle Scholar
  12. Day T, Rowe L (2002) Developmental thresholds and the evolution of reaction norms for age and size at life-history transitions. Am Nat 159:338–350CrossRefGoogle Scholar
  13. Higginson AD, Ruxton GD (2009) Dynamic models allowing for flexibility in complex life histories accurately predict timing of metamorphosis and antipredator strategies of prey. Funct Ecol 23:1103–1113CrossRefGoogle Scholar
  14. Higginson AD, Ruxton GD (2010) Adaptive changes in size and age at metamorphosis can qualitatively vary with predator type and available defenses. Ecology 91:2756–2768CrossRefGoogle Scholar
  15. Johansson F, Stoks R (2005) Adaptive plasticity in response to predators in dragonfly larvae and other aquatic insects. In: Fellows MDE, Holloway GJ, Rolff J (eds) Insect evolutionary ecology. CABI Publishing, Walford, pp 347–370Google Scholar
  16. Jourdan J, Baier J, Riesch R, Klimpel S, Streit B, Müller R, Plath M (2016) Adaptive growth reduction in response to fish kairomones allows mosquito larvae (Culex pipiens) to reduce predation risk. Aquat Sci 78:303–314CrossRefGoogle Scholar
  17. Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394CrossRefGoogle Scholar
  18. Lima SL, Bednekoff PA (1999) Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am Nat 153:649–659CrossRefGoogle Scholar
  19. Ludwig D, Rowe L (1990) Life-history strategies for energy gain and predator avoidance under time constraints. Am Nat 135:686–707CrossRefGoogle Scholar
  20. Mikolajewski DJ, Joop G, Wohlfahrt B (2007) Coping with predators and food limitation: testing life history theory for sex-specific larval development. Oikos 116:642–649Google Scholar
  21. Op de Beeck L, Janssens L, Stoks R (2016) Synthetic predator cues impair immune function and make the biological pesticide Bti more lethal for vector mosquitoes. Ecol Appl 26:355–366CrossRefGoogle Scholar
  22. Orizaola G, Brana F (2005) Plasticity in newt metamorphosis: the effect of predation at embryonic and larval stages. Freshw Biol 50:438–446CrossRefGoogle Scholar
  23. Pohnert G, Steinke M, Tollrian R (2007) Chemical cues, defence metabolites and the shaping of pelagic interspecific interactions. Trends Ecol Evol 22:198–204CrossRefGoogle Scholar
  24. Relyea RA (2007) Getting out alive: how predators affect the decision to metamorphose. Oecologia 152:389–400CrossRefGoogle Scholar
  25. Rieger JF, Binckley CA, Resetarits WJ Jr (2004) Larval performance and oviposition site preference along a predation gradient. Ecology 85:2094–2099CrossRefGoogle Scholar
  26. Roberts D (2018) Predator feeding vibrations encourage mosquito larvae to shorten their development and so become smaller adults. Ecol Entomol 43:534–537CrossRefGoogle Scholar
  27. Roberts D, Kokkinn M (2010) Larval crowding effects on the mosquito Culex quinquefasciatus: physical or chemical? Entomol Exp Appl 135:271–275CrossRefGoogle Scholar
  28. Rowe L, Ludwig D (1991) Size and timing of metamorphosis in complex life cycles: time constraints and variation. Ecology 72:413–427CrossRefGoogle Scholar
  29. Schindelin J, Rueden CT, Hiner MC, Eliceiri KW (2015) The ImageJ ecosystem: an open platform for biomedical image analysis. Mol Reprod Dev 82:518–529CrossRefGoogle Scholar
  30. Silberbush A, Markman S, Lewinsohn E, Bar E, Cohen JE, Blaustein L (2010) Predator-released hydrocarbons repel oviposition by a mosquito. Ecol Lett 13:1129–1138CrossRefGoogle Scholar
  31. Silberbush A, Abramsky Z, Tsurim I (2015a) Effects of fish cues on mosquito larvae development. Acta Trop 150:196–199CrossRefGoogle Scholar
  32. Silberbush A, Abramsky Z, Tsurim I (2015b) Dissolved oxygen levels affect the survival and developmental period of the mosquito Culex pipiens. J Vector Ecol 40:425–427CrossRefGoogle Scholar
  33. StataCorp. (2011) Stata statistical software: release 12. StataCorp LP, College StationGoogle Scholar
  34. Tigreros N, Wang EH, Thaler JS (2018) Prey nutritional state drives divergent behavioural and physiological responses to predation risk. Funct Ecol 32:982–989CrossRefGoogle Scholar
  35. Vinogradova EB (2000) Culex pipiens pipiens mosquitoes: taxonomy, distribution, ecology, physiology, genetics, applied importance and control. Pensoft Publishers, Sofia, pp 46–116Google Scholar
  36. von Elert E, Brönmark C, Hansson L (2012) Information conveyed by chemical cues. In: Brönmark C, Hansson L (eds) Chemical ecology in aquatic systems. Oxford University Press, New York, pp 19–38CrossRefGoogle Scholar
  37. Weiss L, Laforsch C, Tollrian R (2012) The taste of predation and the defences of prey. In: Brönmark C, Hansson L (eds) Chemical ecology in aquatic systems. Oxford University Press, New York, pp 111–126CrossRefGoogle Scholar
  38. Wellborn GA, Skelly DK, Werner EE (1996) Mechanisms creating community structure across a freshwater habitat gradient. Annu Rev Ecol Syst 27:337–363CrossRefGoogle Scholar
  39. Werner EE (1986) Amphibian metamorphosis: growth rate, predation risk, and the optimal size at transformation. Am Nat 128:319–341CrossRefGoogle Scholar
  40. Werner EE, Anholt BR (1993) Ecological consequences of the trade-off between growth and mortality rates mediated by foraging activity. Am Nat 142:242–272CrossRefGoogle Scholar
  41. Wilbur HM, Collins JP (1973) Ecological aspects of amphibian metamorphosis. Science 182:1305–1314CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Life SciencesBen-Gurion University of the NegevBeer-ShevaIsrael
  2. 2.Department of Biology and the EnvironmentUniversity of Haifa-OranimKiryat TivonIsrael
  3. 3.Department of Life SciencesAchva Academic CollegeArugotIsrael

Personalised recommendations