Skip to main content
Log in

Adaptive growth reduction in response to fish kairomones allows mosquito larvae (Culex pipiens) to reduce predation risk

  • Research Article
  • Published:
Aquatic Sciences Aims and scope Submit manuscript

Abstract

Phenotypic plasticity is predicted to evolve when subsequent generations are likely to experience alternating selection pressures; e.g., piscine predation on mosquitoes (Culex pipiens) varies strongly depending on habitat type. A prey-choice experiment (exp. 1) detected a predilection of common mosquito predators (sticklebacks, Gasterosteus aculeatus) for large-bodied mosquito larvae, suggesting that larvae could benefit from suppressing growth under predation risk, and experiment 2 confirmed reduced pupa size and weight when we exposed larvae to stickleback kairomones. In experiment 3, we measured adult (imago) size instead to test if altered larval growth-patterns affect adult life-history traits. We further asked how specific life-history responses are, and thus, also used kairomones from introduced Eastern mosquitofish (Gambusia holbrooki), and from algivorous, non-native catfish (Ancistrus sp.). Adult body mass was equally reduced in all three kairomone treatments, suggesting that a non-specific anti-predator response (e.g., reduced activity) results in reduced food uptake. However, imagines were distinctly smaller only in the stickleback treatment, pointing towards a specific, adaptive life-history shift in response to the presence of a coevolved predator: mosquito larvae appear to suppress growth when exposed to their native predator, which presumably reduces predation risk, but also affects body size after pupation. Our study suggests that (1) not all antipredator responses are necessarily predator-specific, and (2) fluctuation in the cost-benefit ratio of suppressing larval growth has selected for phenotypic plasticity in C. pipiens larval life histories. This implies costs associated with suppressed growth, for example, in the form of lower lifetime reproductive success.

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
Fig. 4

Similar content being viewed by others

References

  • Afify A, Galizia CG (2015) Chemosensory cues for mosquito oviposition site selection. J Med Entomol. doi:10.1093/jme/tju024

    PubMed  Google Scholar 

  • Agrawal AA (2001) Phenotypic plasticity in the interactions and evolution of species. Science 294:321–326

    Article  CAS  PubMed  Google Scholar 

  • Allan JD (1978) Trout predation and the size composition of stream drift. Limnol Oceanogr 23:1231–1237

    Article  Google Scholar 

  • Alvarez M, Landeira-Dabarca A, Peckarsky B (2014) Origin and specificity of predatory fish cues detected by Baetis larvae (Ephemeroptera; Insecta). Anim Behav 96:141–149

    Article  Google Scholar 

  • Auld JR, Agrawal AA, Relyea RA (2009) Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proc R Soc Lond B Biol Sci 277:503–511

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Beklioglu M, Telli M, Gozen AG (2006) Fish and mucus-dwelling bacteria interact to produce a kairomone that induces diel vertical migration in Daphnia. Freshw Biol 51:2200–2206

    Article  Google Scholar 

  • Beldade P, Mateus ARA, Keller RA (2011) Evolution and molecular mechanisms of adaptive developmental plasticity. Mol Ecol 20:1347–1363

    Article  PubMed  Google Scholar 

  • Benard MF (2004) Predator-induced phenotypic plasticity in organisms with complex life histories. Annu Rev Ecol Syst 35:651–673

    Article  Google Scholar 

  • Betancur-R R et al (2013) The tree of life and a new classification of bony fishes. PLoS Curr 2013:5. doi:10.1371/currents.tol.53ba26640df0ccaee75bb165c8c26288

    Google Scholar 

  • Bradshaw WE, Holzapfel CM (1992) Reproductive consequences of density-dependent size variation in the pitcherplant mosquito, Wyeomyia smithii (Diptera: Culicidae). Ann Entomol Soc Am 85:274–281

    Article  Google Scholar 

  • Briegel H (1990) Metabolic relationship between female body size, reserves, and fecundity of Aedes aegypti. J Insect Physiol 36:165–172

    Article  Google Scholar 

  • Brooks JL, Dodson SI (1965) Predation, body size, and composition of plankton. Science 150:28–35

    Article  CAS  PubMed  Google Scholar 

  • Caudill CC, Peckarsky BL (2003) Lack of appropriate behavioral or developmental responses by mayfly larvae to trout predators. Ecology 84:2133–2144

    Article  Google Scholar 

  • Crowl TA, Covich AP (1990) Predator-induced life-history shifts in a freshwater snail. Science 247:949–951

    Article  CAS  PubMed  Google Scholar 

  • DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81

    Article  CAS  PubMed  Google Scholar 

  • Dixon S, Baker R (1988) Effects of size on predation risk, behavioural response to fish, and cost of reduced feeding in larval Ischnura verticalis (Coenagrionidae: Odonata). Oecologia 76:200–205

    Article  Google Scholar 

  • Dodson S (1989) Predator-induced reaction norms. Bioscience 39:447–452

    Article  Google Scholar 

  • Dodson SI, Crowl TA, Peckarsky BL, Kats LB, Covich AP, Culp JM (1994) Non-visual communication in freshwater benthos: an overview. J North Am Benthol Soc 13:268–282. doi:10.2307/1467245

    Article  Google Scholar 

  • Ferrari MC, 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 

  • Flecker AS (1992) Fish predation and the evolution of invertebrate drift periodicity: evidence from neotropical streams. Ecology 73:438–448

    Article  Google Scholar 

  • Forward RB, Rittschof D (2000) Alteration of photoresponses involved in diel vertical migration of a crab larva by fish mucus and degradation products of mucopolysaccharides. J Exp Mar Biol Ecol 245:277–292

    Article  CAS  PubMed  Google Scholar 

  • Gilbert SF, Epel D (2009) Ecological developmental biology: integrating epigenetics, medicine, and evolution. Sinauer Associates, Sunderland

    Google Scholar 

  • Harbach RE, Harrison BA, Gad AM (1984) Culex (culex) molestus Forskal (Diptera: Culicidae): neotype designation, description, variation, and taxonomic status. Proc Entomol Soc Wash 86:521–542

    Google Scholar 

  • Hebert PD, Grewe PM (1985) Chaoborus-induced shifts in the morphology of Daphnia ambigua. Limnol Oceanogr 30:1291–1297

    Article  Google Scholar 

  • Heulett ST, Weeks SC, Meffe GK (1995) Lipid dynamics and growth relative to resource level in juvenile eastern mosquitofish (Gambusia holbrooki: Poeciliidae). Copeia 1995:97–104

    Article  Google Scholar 

  • Huryn AD, Chivers DP (1999) Contrasting behavioral responses by detritivorous and predatory mayflies to chemicals released by injured conspecifics and their predators. J Chem Ecol 25:2729–2740

    Article  CAS  Google Scholar 

  • Hynes H (1950) The food of fresh-water sticklebacks (Gasterosteus aculeatus and Pygosteus pungitius), with a review of methods used in studies of the food of fishes. J Anim Ecol 19:36–58

    Article  Google Scholar 

  • Iyengar EV, Harvell CD (2002) Specificity of cues inducing defensive spines in the bryozoan Membranipora membranacea. Mar Ecol Prog Ser 225:205–218

    Article  Google Scholar 

  • Kaufmann C, Reim C, Blanckenhorn WU (2013) Size-dependent insect flight energetics at different sugar supplies. Biol J Linn Soc 108:565–578. doi:10.1111/j.1095-8312.2012.02042.x

    Article  Google Scholar 

  • Kesavaraju B, Juliano S (2004) Differential behavioral responses to water-borne cues to predation in two container-dwelling mosquitoes. Ann Entomol Soc Am 97:194

    Article  PubMed  PubMed Central  Google Scholar 

  • Kesavaraju B, Alto BW, Lounibos LP, Juliano SA (2007) Behavioural responses of larval container mosquitoes to a size-selective predator. Ecol Entomol 32:262–272

    Article  PubMed  PubMed Central  Google Scholar 

  • Kreß A, Oehlmann J, Kuch U, Müller R (2014) Impact of temperature and nutrition on the toxicity of the insecticide λ-cyhalothrin in fulllifecycle tests with the target mosquito species Aedes albopictus and Culex pipiens. J Pest Sci 87:739–750. doi:10.1007/s10340-014-0620-4

    Article  Google Scholar 

  • Krueger DA, Dodson SI (1981) Embryological induction and predation ecology in Daphnia pulex. Limnol Oceanogr 26:219–223

    Article  Google Scholar 

  • Krumholz LA (1948) Reproduction in the Western Mosquitofish, Gambusia affinis affinis (Baird & Girard) and its use in mosquito control. Ecol Monogr 18:1–43. doi:10.2307/1948627

    Article  Google Scholar 

  • Kumar R, Hwang JS (2006) Larvicidal efficiency of aquatic predators: a perspective for mosquito biocontrol. Zool Stud 45:447–466

    Google Scholar 

  • Langerhans RB, Layman CA, Shokrollahi A, DeWitt TJ (2004) Predator-driven phenotypic diversification in Gambusia affinis. Evolution 58:2305–2318

    Article  PubMed  Google Scholar 

  • Lass S, Spaak P (2003) Chemically induced anti-predator defences in plankton: a review. Hydrobiologia 491:221–239

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Lyimo EO, Takken W (1993) Effects of adult body size on fecundity and the pre-gravid rate of Anopheles gambiae females in Tanzania. Med Vet Entomol 7:328–332

    Article  CAS  PubMed  Google Scholar 

  • Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710. doi:10.2307/2641039

    Article  Google Scholar 

  • McCann S, Day JF, Allan S, Lord CC (2009) Age modifies the effect of body size on fecundity in Culex quinquefasciatus Say (Diptera: Culicidae). J Vector Ecol 34:174–181

    Article  PubMed  PubMed Central  Google Scholar 

  • Medlock J, Snow K (2008) Natural predators and parasites of British mosquitoes—a review. European Mosquito Bulletin 25:1–11

    Google Scholar 

  • Miyakawa H et al (2010) Gene up-regulation in response to predator kairomones in the water flea, Daphnia pulex. BMC Dev Biol 10:45

    Article  PubMed  PubMed Central  Google Scholar 

  • Müller R, Knautz T, Völker J, Kreß A, Kuch U, Oehlmann J (2013) Appropriate larval food quality and quantity for Aedes albopictus (Diptera: Culicidae). J Med Entomol 50:668–673

    Article  PubMed  Google Scholar 

  • Neems R, McLachlan A, Chambers R (1990) Body size and lifetime mating success of male midges (Diptera: Chironomidae). Anim Behav 40:648–652

    Article  Google Scholar 

  • Nijhout H, Wheeler D (1996) Growth models of complex allometries in holometabolous insects. Am Nat 148:40–56

    Article  Google Scholar 

  • Nilsson PA, Brönmark C (2000) Prey vulnerability to a gape-size limited predator: behavioural and morphological impacts on northern pike piscivory. Oikos 88:539–546

    Article  Google Scholar 

  • OECD (2004) OECD guideline for testing chemicals: Test No. 219: Sediment-water chironomid toxicity using 474 spiked water. Organization for Economic Cooperation and Development, Paris

  • Offill Y, Walton W (1999) Comparative efficacy of the threespine stickleback (Gasterosteus aculeatus) and the mosquitofish (Gambusia affinis) for mosquito control. J Am Mosq Control Assoc 15:380–390

    CAS  PubMed  Google Scholar 

  • Ohba S-Y, Ohtsuka M, Sunahara T, Sonoda Y, Kawashima E, Takagi M (2012) Differential responses to predator cues between two mosquito species breeding in different habitats. Ecol Entomol 37:410–418

    Article  Google Scholar 

  • Palmer MA, Poff NL (1997) The influence of environmental heterogeneity on patterns and processes in streams. J North Am Benthol Soc 16:169–173

    Article  Google Scholar 

  • Pease KM, Wayne RK (2014) Divergent responses of exposed and naive Pacific tree frog tadpoles to invasive predatory crayfish. Oecologia 174:241–252. doi:10.1007/s00442-013-2745-1

    Article  PubMed  Google Scholar 

  • Peckarsky BL, Taylor BW, McIntosh AR, McPeek MA, Lytle DA (2001) Variation in mayfly size at metamorphosis as a developmental response to risk of predation. Ecology 82:740–757

    Article  Google Scholar 

  • Plath M, Parzefall J, Schlupp I (2003) The role of sexual harassment in cave and surface dwelling populations of the Atlantic molly, Poecilia mexicana (Poeciliidae, Teleostei). Behav Ecol Sociobiol 54:303–309

    Article  Google Scholar 

  • Relyea RA (2001) Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology 82:523–540

    Article  Google Scholar 

  • Relyea RA (2003) How prey respond to combined predators: a review and an empirical test. Ecology 84:1827–1839

    Article  Google Scholar 

  • Reznick D (1982) The impact of predation on life history evolution in Trinidadian guppies: genetic basis of observed life history patterns. Evolution 36:1236–1250

    Article  Google Scholar 

  • Reznick D, Endler JA (1982) The impact of predation on life history evolution in Trinidadian guppies (Poecilia reticulata). Evolution 36:160–177. doi:10.2307/2407978

    Article  Google Scholar 

  • Riesch R, Plath M, Schlupp I (2010) Toxic hydrogen sulfide and dark caves: life-history adaptations in a livebearing fish (Poecilia mexicana, Poeciliidae). Ecology 91:1494–1505. doi:10.1890/09-1008.1

    Article  PubMed  Google Scholar 

  • Riesch R, Martin RA, Langerhans RB (2013) Predation’s role in life-history evolution of a livebearing fish and a test of the Trexler-DeAngelis model of maternal provisioning. Am Nat 181:78–93

    Article  PubMed  Google Scholar 

  • Rosenheim JA, Kaya H, Ehler L, Marois JJ, Jaffee B (1995) Intraguild predation among biological-control agents: theory and evidence. Biol Control 5:303–335

    Article  Google Scholar 

  • Sakai AK et al (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332. doi:10.1146/annurev.ecolsys.32.081501.114037

    Article  Google Scholar 

  • Salo P, Korpimäki E, Banks PB, Nordström M, Dickman CR (2007) Alien predators are more dangerous than native predators to prey populations. Proc R Soc Lond B Biol Sci 274:1237–1243

    Article  Google Scholar 

  • Schneider RF, Li Y, Meyer A, Gunter HM (2014) Regulatory gene networks that shape the development of adaptive phenotypic plasticity in a cichlid fish. Mol Ecol 23:4511–4526. doi:10.1111/mec.12851

    Article  PubMed  Google Scholar 

  • Sih A (1986) Antipredator responses and the perception of danger by mosquito larvae. Ecology 67:434–441

    Article  Google Scholar 

  • Snell-Rood EC, Van Dyken JD, Cruickshank T, Wade MJ, Moczek AP (2010) Toward a population genetic framework of developmental evolution: the costs, limits, and consequences of phenotypic plasticity. BioEssays 32:71–81

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sommer RJ, Ogawa A (2011) Hormone signaling and phenotypic plasticity in nematode development and evolution. Curr Biol 21:R758–R766

    Article  CAS  PubMed  Google Scholar 

  • Spencer M, Blaustein L, Cohen JE (2002) Oviposition habitat selection by mosquitoes (Culiseta longiareolata) and consequences for population size. Ecology 83:669–679

    Article  Google Scholar 

  • Stearns SC (1989) Trade-offs in life-history evolution. Funct Ecol 3:259–268

    Article  Google Scholar 

  • Stevens DJ, Hansell MH, Freel JA, Monaghan P (1999) Developmental trade–offs in caddis flies: increased investment in larval defence alters adult resource allocation. Proc R Soc Lond B Biol Sci 266:1049–1054

    Article  Google Scholar 

  • Stoks R, Block MD, Van De Meutter F, Johansson F (2005) Predation cost of rapid growth: behavioural coupling and physiological decoupling. J Anim Ecol 74:708–715. doi:10.1111/j.1365-2656.2005.00969.x

    Article  Google Scholar 

  • Twohy DW, Rozeboom LE (1957) A comparison of food reserves in autogenous and anautogenous Culex pipiens populations. Am J Epidemiol 65:316–324

    CAS  Google Scholar 

  • van Uitregt VO, Hurst TP, Wilson RS (2012) Reduced size and starvation resistance in adult mosquitoes, Aedes notoscriptus, exposed to predation cues as larvae. J Anim Ecol 81:108–115. doi:10.1111/j.1365-2656.2011.01880.x

    Article  PubMed  Google Scholar 

  • Vidal O, Garcia-Berthou E, Tedesco PA, Garcia-Marin J-L (2010) Origin and genetic diversity of mosquitofish (Gambusia holbrooki) introduced to Europe. Biol Invasions 12:841–851. doi:10.1007/s10530-009-9505-5

    Article  Google Scholar 

  • Vinogradova EB (2000) Culex pipiens pipiens mosquitoes: taxonomy, distribution, ecology, physiology, genetic, applied importance and control. Pensoft Publishers, Sofia, Bulgaria

    Google Scholar 

  • Walker JA (1997) Ecological morphology of lacustrine threespine stickleback Gasterosteus aculeatus L. (Gasterosteidae) body shape. Biol J Linn Soc 61:3–50

    Google Scholar 

  • Wellborn GA (1994) Size-biased predation and prey life histories: a comparative study of freshwater amphipod populations. Ecology 75:2104–2117

    Article  Google Scholar 

  • Wellborn GA, Bartholf SE (2005) Ecological context and the importance of body and gnathopod size for pairing success in two amphipod ecomorphs. Oecologia 143:308–316

    Article  PubMed  Google Scholar 

  • Werner EE (1974) The fish size, prey size, handling time relation in several sunfishes and some implications. J Fish Res Bd Can 31:1531–1536

    Article  Google Scholar 

  • Wilbur HM (1980) Complex life cycles. Annu Rev Ecol Syst 11:67–93

    Article  Google Scholar 

Download references

Acknowledgments

We thank H. Geupel and E. Wörner, who kindly helped with animal care. We also thank J. Kirchgesser for help with data assessment. Artworks (drawings of C. pipiens larvae and pupae, as well as G. aculeatus) were provided by V. Achenbach (ink-theater.com). The present study was prepared at the Biodiversity and Climate Research Centre (BiK-F), Frankfurt am Main, and financially supported by the research funding program “LOEWE—Landes-Offensive zur Entwicklung Wissenschaftlich-ökonomischer Exzellenz” of the Hessian Ministry of Higher Education, Research, and the Arts. We further thank two anonymous reviewers for their valuable comments that helped to improve the manuscript. The authors do not have any conflict of interests to declare.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Jonas Jourdan or Martin Plath.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 35 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jourdan, J., Baier, J., Riesch, R. et al. Adaptive growth reduction in response to fish kairomones allows mosquito larvae (Culex pipiens) to reduce predation risk. Aquat Sci 78, 303–314 (2016). https://doi.org/10.1007/s00027-015-0432-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00027-015-0432-5

Keywords

Navigation