Abstract
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.
Similar content being viewed by others
References
Abrams PA, Rowe L (1996) The effects of predation on the age and size of maturity of prey. Evolution 50:1052–1061
Anholt BR, Werner EE (1995) Interaction between food availability and predation mortality mediated by adaptive behavior. Ecology 76:2230–2234
Anholt BR, Werner E, Skelly DK (2000) Effect of food and predators on the activity of four larval ranid frogs. Ecology 81:3509–3521
Beketov MA, Liess M (2007) Predation risk perception and food scarcity induce alterations of life-cycle traits of the mosquito Culex pipiens. Ecol Entomol 32:405–410
Benard MF (2004) Predator-induced phenotypic plasticity in organisms with complex life histories. Annu Rev Ecol Evol Syst 35:651–673
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:e82344
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 441–456
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 263–280
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 51:1277–1285
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 142:131–137
Dahl J, Peckarsky BL (2003) Developmental responses to predation risk in morphologically defended mayflies. Oecologia 137:188–194
Day T, Rowe L (2002) Developmental thresholds and the evolution of reaction norms for age and size at life-history transitions. Am Nat 159:338–350
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 23:1103–1113
Higginson AD, Ruxton GD (2010) Adaptive changes in size and age at metamorphosis can qualitatively vary with predator type and available defenses. Ecology 91:2756–2768
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 347–370
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 78:303–314
Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394
Lima SL, Bednekoff PA (1999) Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am Nat 153:649–659
Ludwig D, Rowe L (1990) Life-history strategies for energy gain and predator avoidance under time constraints. Am Nat 135:686–707
Mikolajewski DJ, Joop G, Wohlfahrt B (2007) Coping with predators and food limitation: testing life history theory for sex-specific larval development. Oikos 116:642–649
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 26:355–366
Orizaola G, Brana F (2005) Plasticity in newt metamorphosis: the effect of predation at embryonic and larval stages. Freshw Biol 50:438–446
Pohnert G, Steinke M, Tollrian R (2007) Chemical cues, defence metabolites and the shaping of pelagic interspecific interactions. Trends Ecol Evol 22:198–204
Relyea RA (2007) Getting out alive: how predators affect the decision to metamorphose. Oecologia 152:389–400
Rieger JF, Binckley CA, Resetarits WJ Jr (2004) Larval performance and oviposition site preference along a predation gradient. Ecology 85:2094–2099
Roberts D (2018) Predator feeding vibrations encourage mosquito larvae to shorten their development and so become smaller adults. Ecol Entomol 43:534–537
Roberts D, Kokkinn M (2010) Larval crowding effects on the mosquito Culex quinquefasciatus: physical or chemical? Entomol Exp Appl 135:271–275
Rowe L, Ludwig D (1991) Size and timing of metamorphosis in complex life cycles: time constraints and variation. Ecology 72:413–427
Schindelin J, Rueden CT, Hiner MC, Eliceiri KW (2015) The ImageJ ecosystem: an open platform for biomedical image analysis. Mol Reprod Dev 82:518–529
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
Silberbush A, Abramsky Z, Tsurim I (2015a) Effects of fish cues on mosquito larvae development. Acta Trop 150:196–199
Silberbush A, Abramsky Z, Tsurim I (2015b) Dissolved oxygen levels affect the survival and developmental period of the mosquito Culex pipiens. J Vector Ecol 40:425–427
StataCorp. (2011) Stata statistical software: release 12. StataCorp LP, College Station
Tigreros N, Wang EH, Thaler JS (2018) Prey nutritional state drives divergent behavioural and physiological responses to predation risk. Funct Ecol 32:982–989
Vinogradova EB (2000) Culex pipiens pipiens mosquitoes: taxonomy, distribution, ecology, physiology, genetics, applied importance and control. Pensoft Publishers, Sofia, pp 46–116
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 19–38
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 111–126
Wellborn GA, Skelly DK, Werner EE (1996) Mechanisms creating community structure across a freshwater habitat gradient. Annu Rev Ecol Syst 27:337–363
Werner EE (1986) Amphibian metamorphosis: growth rate, predation risk, and the optimal size at transformation. Am Nat 128:319–341
Werner EE, Anholt BR (1993) Ecological consequences of the trade-off between growth and mortality rates mediated by foraging activity. Am Nat 142:242–272
Wilbur HM, Collins JP (1973) Ecological aspects of amphibian metamorphosis. Science 182:1305–1314
Acknowledgements
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Silberbush, A., Gertler, N., Ovadia, O. et al. Kairomone-induced changes in mosquito life history: effects across a food gradient. Aquat Sci 81, 53 (2019). https://doi.org/10.1007/s00027-019-0649-9
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00027-019-0649-9