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Aquatic Sciences

, Volume 78, Issue 2, pp 303–314 | Cite as

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

  • Jonas JourdanEmail author
  • Jasmin Baier
  • Rüdiger Riesch
  • Sven Klimpel
  • Bruno Streit
  • Ruth Müller
  • Martin PlathEmail author
Research Article

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.

Keywords

Chemical cues Inducible defense trait Invasive species Phenotypic plasticity Predator–prey interaction Predator avoidance 

Notes

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.

Supplementary material

27_2015_432_MOESM1_ESM.docx (35 kb)
Supplementary material 1 (DOCX 35 kb)

References

  1. Afify A, Galizia CG (2015) Chemosensory cues for mosquito oviposition site selection. J Med Entomol. doi: 10.1093/jme/tju024 PubMedGoogle Scholar
  2. Agrawal AA (2001) Phenotypic plasticity in the interactions and evolution of species. Science 294:321–326CrossRefPubMedGoogle Scholar
  3. Allan JD (1978) Trout predation and the size composition of stream drift. Limnol Oceanogr 23:1231–1237CrossRefGoogle Scholar
  4. Alvarez M, Landeira-Dabarca A, Peckarsky B (2014) Origin and specificity of predatory fish cues detected by Baetis larvae (Ephemeroptera; Insecta). Anim Behav 96:141–149CrossRefGoogle Scholar
  5. Auld JR, Agrawal AA, Relyea RA (2009) Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proc R Soc Lond B Biol Sci 277:503–511CrossRefGoogle Scholar
  6. 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
  7. 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 51:2200–2206CrossRefGoogle Scholar
  8. Beldade P, Mateus ARA, Keller RA (2011) Evolution and molecular mechanisms of adaptive developmental plasticity. Mol Ecol 20:1347–1363CrossRefPubMedGoogle Scholar
  9. Benard MF (2004) Predator-induced phenotypic plasticity in organisms with complex life histories. Annu Rev Ecol Syst 35:651–673CrossRefGoogle Scholar
  10. 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
  11. Bradshaw WE, Holzapfel CM (1992) Reproductive consequences of density-dependent size variation in the pitcherplant mosquito, Wyeomyia smithii (Diptera: Culicidae). Ann Entomol Soc Am 85:274–281CrossRefGoogle Scholar
  12. Briegel H (1990) Metabolic relationship between female body size, reserves, and fecundity of Aedes aegypti. J Insect Physiol 36:165–172CrossRefGoogle Scholar
  13. Brooks JL, Dodson SI (1965) Predation, body size, and composition of plankton. Science 150:28–35CrossRefPubMedGoogle Scholar
  14. Caudill CC, Peckarsky BL (2003) Lack of appropriate behavioral or developmental responses by mayfly larvae to trout predators. Ecology 84:2133–2144CrossRefGoogle Scholar
  15. Crowl TA, Covich AP (1990) Predator-induced life-history shifts in a freshwater snail. Science 247:949–951CrossRefPubMedGoogle Scholar
  16. DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81CrossRefPubMedGoogle Scholar
  17. 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 76:200–205CrossRefGoogle Scholar
  18. Dodson S (1989) Predator-induced reaction norms. Bioscience 39:447–452CrossRefGoogle Scholar
  19. 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 CrossRefGoogle Scholar
  20. Ferrari MC, Wisenden BD, Chivers DP (2010) Chemical ecology of predator-prey interactions in aquatic ecosystems: a review and prospectus. Can J Zool 88:698–724CrossRefGoogle Scholar
  21. Flecker AS (1992) Fish predation and the evolution of invertebrate drift periodicity: evidence from neotropical streams. Ecology 73:438–448CrossRefGoogle Scholar
  22. 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 245:277–292CrossRefPubMedGoogle Scholar
  23. Gilbert SF, Epel D (2009) Ecological developmental biology: integrating epigenetics, medicine, and evolution. Sinauer Associates, SunderlandGoogle Scholar
  24. Harbach RE, Harrison BA, Gad AM (1984) Culex (culex) molestus Forskal (Diptera: Culicidae): neotype designation, description, variation, and taxonomic status. Proc Entomol Soc Wash 86:521–542Google Scholar
  25. Hebert PD, Grewe PM (1985) Chaoborus-induced shifts in the morphology of Daphnia ambigua. Limnol Oceanogr 30:1291–1297CrossRefGoogle Scholar
  26. Heulett ST, Weeks SC, Meffe GK (1995) Lipid dynamics and growth relative to resource level in juvenile eastern mosquitofish (Gambusia holbrooki: Poeciliidae). Copeia 1995:97–104CrossRefGoogle Scholar
  27. 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 25:2729–2740CrossRefGoogle Scholar
  28. 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 19:36–58CrossRefGoogle Scholar
  29. Iyengar EV, Harvell CD (2002) Specificity of cues inducing defensive spines in the bryozoan Membranipora membranacea. Mar Ecol Prog Ser 225:205–218CrossRefGoogle Scholar
  30. 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 CrossRefGoogle Scholar
  31. Kesavaraju B, Juliano S (2004) Differential behavioral responses to water-borne cues to predation in two container-dwelling mosquitoes. Ann Entomol Soc Am 97:194CrossRefPubMedPubMedCentralGoogle Scholar
  32. Kesavaraju B, Alto BW, Lounibos LP, Juliano SA (2007) Behavioural responses of larval container mosquitoes to a size-selective predator. Ecol Entomol 32:262–272CrossRefPubMedPubMedCentralGoogle Scholar
  33. 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 CrossRefGoogle Scholar
  34. Krueger DA, Dodson SI (1981) Embryological induction and predation ecology in Daphnia pulex. Limnol Oceanogr 26:219–223CrossRefGoogle Scholar
  35. 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 CrossRefGoogle Scholar
  36. Kumar R, Hwang JS (2006) Larvicidal efficiency of aquatic predators: a perspective for mosquito biocontrol. Zool Stud 45:447–466Google Scholar
  37. Langerhans RB, Layman CA, Shokrollahi A, DeWitt TJ (2004) Predator-driven phenotypic diversification in Gambusia affinis. Evolution 58:2305–2318CrossRefPubMedGoogle Scholar
  38. Lass S, Spaak P (2003) Chemically induced anti-predator defences in plankton: a review. Hydrobiologia 491:221–239CrossRefGoogle Scholar
  39. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640CrossRefGoogle Scholar
  40. 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 7:328–332CrossRefPubMedGoogle Scholar
  41. 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 CrossRefGoogle Scholar
  42. 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 34:174–181CrossRefPubMedPubMedCentralGoogle Scholar
  43. Medlock J, Snow K (2008) Natural predators and parasites of British mosquitoes—a review. European Mosquito Bulletin 25:1–11Google Scholar
  44. Miyakawa H et al (2010) Gene up-regulation in response to predator kairomones in the water flea, Daphnia pulex. BMC Dev Biol 10:45CrossRefPubMedPubMedCentralGoogle Scholar
  45. 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 50:668–673CrossRefPubMedGoogle Scholar
  46. Neems R, McLachlan A, Chambers R (1990) Body size and lifetime mating success of male midges (Diptera: Chironomidae). Anim Behav 40:648–652CrossRefGoogle Scholar
  47. Nijhout H, Wheeler D (1996) Growth models of complex allometries in holometabolous insects. Am Nat 148:40–56CrossRefGoogle Scholar
  48. Nilsson PA, Brönmark C (2000) Prey vulnerability to a gape-size limited predator: behavioural and morphological impacts on northern pike piscivory. Oikos 88:539–546CrossRefGoogle Scholar
  49. OECD (2004) OECD guideline for testing chemicals: Test No. 219: Sediment-water chironomid toxicity using 474 spiked water. Organization for Economic Cooperation and Development, ParisGoogle Scholar
  50. 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 15:380–390PubMedGoogle Scholar
  51. 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 37:410–418CrossRefGoogle Scholar
  52. Palmer MA, Poff NL (1997) The influence of environmental heterogeneity on patterns and processes in streams. J North Am Benthol Soc 16:169–173CrossRefGoogle Scholar
  53. 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 CrossRefPubMedGoogle Scholar
  54. 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 82:740–757CrossRefGoogle Scholar
  55. 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 54:303–309CrossRefGoogle Scholar
  56. Relyea RA (2001) Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology 82:523–540CrossRefGoogle Scholar
  57. Relyea RA (2003) How prey respond to combined predators: a review and an empirical test. Ecology 84:1827–1839CrossRefGoogle Scholar
  58. Reznick D (1982) The impact of predation on life history evolution in Trinidadian guppies: genetic basis of observed life history patterns. Evolution 36:1236–1250CrossRefGoogle Scholar
  59. 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 CrossRefGoogle Scholar
  60. 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 CrossRefPubMedGoogle Scholar
  61. 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 181:78–93CrossRefPubMedGoogle Scholar
  62. Rosenheim JA, Kaya H, Ehler L, Marois JJ, Jaffee B (1995) Intraguild predation among biological-control agents: theory and evidence. Biol Control 5:303–335CrossRefGoogle Scholar
  63. 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 CrossRefGoogle Scholar
  64. 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 274:1237–1243CrossRefGoogle Scholar
  65. 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 CrossRefPubMedGoogle Scholar
  66. Sih A (1986) Antipredator responses and the perception of danger by mosquito larvae. Ecology 67:434–441CrossRefGoogle Scholar
  67. 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 32:71–81CrossRefPubMedPubMedCentralGoogle Scholar
  68. Sommer RJ, Ogawa A (2011) Hormone signaling and phenotypic plasticity in nematode development and evolution. Curr Biol 21:R758–R766CrossRefPubMedGoogle Scholar
  69. Spencer M, Blaustein L, Cohen JE (2002) Oviposition habitat selection by mosquitoes (Culiseta longiareolata) and consequences for population size. Ecology 83:669–679CrossRefGoogle Scholar
  70. Stearns SC (1989) Trade-offs in life-history evolution. Funct Ecol 3:259–268CrossRefGoogle Scholar
  71. 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 266:1049–1054CrossRefGoogle Scholar
  72. 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 CrossRefGoogle Scholar
  73. Twohy DW, Rozeboom LE (1957) A comparison of food reserves in autogenous and anautogenous Culex pipiens populations. Am J Epidemiol 65:316–324Google Scholar
  74. 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 CrossRefPubMedGoogle Scholar
  75. 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 CrossRefGoogle Scholar
  76. Vinogradova EB (2000) Culex pipiens pipiens mosquitoes: taxonomy, distribution, ecology, physiology, genetic, applied importance and control. Pensoft Publishers, Sofia, BulgariaGoogle Scholar
  77. Walker JA (1997) Ecological morphology of lacustrine threespine stickleback Gasterosteus aculeatus L. (Gasterosteidae) body shape. Biol J Linn Soc 61:3–50Google Scholar
  78. Wellborn GA (1994) Size-biased predation and prey life histories: a comparative study of freshwater amphipod populations. Ecology 75:2104–2117CrossRefGoogle Scholar
  79. Wellborn GA, Bartholf SE (2005) Ecological context and the importance of body and gnathopod size for pairing success in two amphipod ecomorphs. Oecologia 143:308–316CrossRefPubMedGoogle Scholar
  80. Werner EE (1974) The fish size, prey size, handling time relation in several sunfishes and some implications. J Fish Res Bd Can 31:1531–1536CrossRefGoogle Scholar
  81. Wilbur HM (1980) Complex life cycles. Annu Rev Ecol Syst 11:67–93CrossRefGoogle Scholar

Copyright information

© Springer Basel 2015

Authors and Affiliations

  • Jonas Jourdan
    • 1
    • 2
    Email author
  • Jasmin Baier
    • 2
    • 3
  • Rüdiger Riesch
    • 4
  • Sven Klimpel
    • 5
  • Bruno Streit
    • 1
    • 2
  • Ruth Müller
    • 6
  • Martin Plath
    • 7
    Email author
  1. 1.Biodiversity and Climate Research Centre (BiK-F)Frankfurt am MainGermany
  2. 2.Department of Ecology and EvolutionGoethe University of FrankfurtFrankfurt am MainGermany
  3. 3.Master Study Program “Ecology and Evolution” at Goethe University of FrankfurtFrankfurt am MainGermany
  4. 4.School of Biological SciencesRoyal Holloway University of LondonEghamUK
  5. 5.Department of Integrative Parasitology and ZoophysiologyGoethe University of FrankfurtFrankfurt am MainGermany
  6. 6.Department Environmental Toxicology and Medical Entomology, Institute of Occupational, Social and Environmental MedicineGoethe UniversityFrankfurt am MainGermany
  7. 7.College of Animal Science and TechnologyNorthwest A&F UniversityYanglingPeople’s Republic of China

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