Evolutionary Ecology

, Volume 26, Issue 4, pp 955–974 | Cite as

Modelling evolutionarily stable strategies in oviposition site selection, with varying risks of predation and intraspecific competition

  • Arik Kershenbaum
  • Matthew Spencer
  • Leon Blaustein
  • Joel E. Cohen
Research Article

Abstract

Many ovipositing mosquitoes, as well as other species, can detect biotic factors that affect fitness. However, a female mosquito seeking a high quality oviposition site (e.g. one with low risk of predation and competition to her progeny) must often balance the competing risk of increasing probability of mortality to herself while she continues to search, against increased probability of finding a high quality site. Such oviposition site selection may affect adult population size. We examined a female mosquito’s expected strategy of oviposition site selection under conditions of varying predator prevalence and adult mortality risk, by combining a detailed structured population model with a Markov chain implementation of the adult behavioural process. We used parameter values from the specific mosquito-predator system, Culiseta longiareolata-Notonecta maculata, although the overall results can be generalised to many mosquito species. Our model finds the evolutionarily stable strategy of oviposition site selection for different parameter combinations. Our model predicts that oviposition strategy does not vary smoothly with varying environmental risk of adult mortality, but that certain oviposition strategies become unstable at some parameter values. Mosquitoes will distribute their reproductive effort between breeding sites of varying predation risk only when adult mortality is low or larval competition high. Our model predicts that females will continue searching for predator-free pools, rather than oviposit in the first site encountered, regardless of the risk of mortality to the adult. The ecological basis for a reproductive strategy with alternative behaviours is important for understanding the effect of biotic factors on the population dynamics of mosquitoes, and for the development of biological control strategies, such as the dissemination of predator-cue chemicals.

Keywords

Culiseta longiareolata Evolutionarily stable strategy Notonecta maculata Oviposition site selection Reproductive strategy 

Supplementary material

10682_2011_9548_MOESM1_ESM.doc (178 kb)
Supplementary material 1 (DOC 178 kb)

References

  1. Abrams PA, Cressman R, Křivan V (2007) The role of behavioral dynamics in determining the patch distributions of interacting species. Am Nat 169:505–518PubMedCrossRefGoogle Scholar
  2. Angelon KA, Petranka JW (2002) Chemicals of predatory mosquitofish (Gambusia affinis) influence selection of oviposition site by Culex mosquitoes. J Chem Ecol 28:797–806Google Scholar
  3. Austad SN (1984) A classification of alternative reproductive behaviors and methods for field-testing ESS models. Am Zool 24:309Google Scholar
  4. Binckley CA, Resetarits WJ (2002) Reproductive decisions under threat of predation: squirrel treefrog (Hyla squirella) responses to banded sunfish (Enneacanthus obesus). Oecologia 130:157–161Google Scholar
  5. Bishop D, Cannings C (1978) A generalized war of attrition. J Theor Biol 70:85–124PubMedCrossRefGoogle Scholar
  6. Black AR, Dodson SI (1990) Demographic costs of Chaoborus-induced phenotypic plasticity in Daphnia pulex. Oecologia 83:117–122CrossRefGoogle Scholar
  7. Blaustein L (1998) Influence of the predatory backswimmer, Notonecta maculata, on invertebrate community structure. Ecol Entomol 23:246–252CrossRefGoogle Scholar
  8. 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, pp 441–456Google Scholar
  9. Blaustein L, Kotler BP (1993) Oviposition habitat selection by Culiseta longiareolata: effects of immature conspecifics, tadpoles and food levels. Ecol Entomol 18:104–108Google Scholar
  10. Blaustein L, Margalit J (1995) Spatial distributions of Culiseta longiareolata (Culicidae: Diptera) and Bufo viridis (Amphibia: Bufonidae) among and within desert pools. J Arid Environ 29:199–211CrossRefGoogle Scholar
  11. Blaustein L, Margalit J (1996) Priority effects in temporary pools: nature and outcome of mosquito larva-toad tadpole interactions depend on order of entrance. J Anim Ecol 65:77–84CrossRefGoogle Scholar
  12. Blaustein L, Whitman DW (2009) Behavioral plasticity to risk of predation: oviposition site selection by a mosquito in response to its predators. In: Whitman D, Ananthakrishnan TN (eds) Phenotypic plasticity of insects: mechanisms and consequences. Science Pub Inc, Plymouth, pp 263–280Google Scholar
  13. Blaustein L, Kotler BP, Ward D (1995) Direct and indirect effects of a predatory backswimmer (Notonecta maculata) on community structure of desert temporary pools. Ecol Entomol 20:311–318CrossRefGoogle Scholar
  14. Blaustein L, Kiflawi M, Eitam A, Mangel M, Cohen JE (2004) Oviposition habitat selection in response to risk of predation in temporary pools: mode of detection and consistency across experimental venue. Oecologia 138:300–305PubMedCrossRefGoogle Scholar
  15. Chesson J (1984) Effect of notonectids (Hemiptera: Notonectidae) on mosquitoes (Diptera: Culicidae): predation or selective oviposition. Environ Entomol 13:531–538Google Scholar
  16. Choh Y, Takabayashi J (2010) Predator avoidance by phytophagous mites is affected by the presence of herbivores in a neighboring patch. J Chem Ecol 36:614–619PubMedCrossRefGoogle Scholar
  17. Cushing J (1996) Nonlinear matrix equations and population dynamics. In: Structured-population models in marine, terrestrial, and freshwater systems. Kluwer Academic Publishers, pp 205–243 Google Scholar
  18. Dawkins R (1980) Good strategy or evolutionarily stable strategy? In: Barlow GW, Silverberg J (eds) Sociobiology: beyond nature/nurture?Google Scholar
  19. Eitam A, Blaustein L (2004) Oviposition habitat selection by mosquitoes in response to predator (Notonecta maculata) density. Physiol Entomol 29:188–191CrossRefGoogle Scholar
  20. Eitam A, Blaustein L, Mangel M (2002) Effects of Anisops sardea (Hemiptera: Notonectidae) on oviposition habitat selection by mosquitoes and other dipterans and on community structure in artificial pools. Hydrobiologia 485:183–189CrossRefGoogle Scholar
  21. Eitam A, Norena C, Blaustein L (2004) Microturbellarian species richness and community similarity among temporary pools: relationships with habitat properties. Biodivers Conserv 13:2107–2117CrossRefGoogle Scholar
  22. Fretwell SD, Lucas HL (1969) On territorial behavior and other factors influencing habitat distribution in birds. Acta Biotheor 19:16–36CrossRefGoogle Scholar
  23. Holt RD (1985) Population dynamics in two-patch environments: some anomalous consequences of an optimal habitat distribution. Theor Popul Biol 28:181–208CrossRefGoogle Scholar
  24. Kiflawi M, Blaustein L, Mangel M (2003a) Oviposition habitat selection by the mosquito Culiseta longiareolata in response to risk of predation and conspecific larval density. Ecol Entomol 28:168–173CrossRefGoogle Scholar
  25. Kiflawi M, Blaustein L, Mangel M (2003b) Predation-dependent oviposition habitat selection by the mosquito Culiseta longiareolata: a test of competing hypotheses. Ecol Letters 6:35–40Google Scholar
  26. Kiflawi M, Eitam A, Blaustein L (2003c) The relative impact of local and regional processes on macro-invertebrate species richness in temporary pools. J Anim Ecol 72:447–452CrossRefGoogle Scholar
  27. Kiszewski A, Mellinger A, Spielman A, Malaney P, Sachs SE, Sachs J (2004) A global index representing the stability of malaria transmission. Am J Trop Med Hyg 70:486–498PubMedGoogle Scholar
  28. Maciá A (2009) Effects of larval crowding on development time, survival and weight at metamorphosis in Aedes aegypti (Diptera: Culicidae). Revista de la Sociedad Entomológica Argentina 68:107–114Google Scholar
  29. Manda H, Gouagna LC, Foster WA, Jackson RR, Beier JC, Githure JI, Hassanali A (2007) Effect of discriminative plant-sugar feeding on the survival and fecundity of Anopheles gambiae. Malar J 6:113PubMedCrossRefGoogle Scholar
  30. Mangel M, Clark CW (1988) Dynamic modeling in behavioral ecology. Princeton University Press, PrincetonGoogle Scholar
  31. Manoukis NC, Touré MB, Sissoko I, Doumbia S, Traoré SF, Diuk-Wasser MA, Taylor CE (2006) Is vector body size the key to reduced malaria transmission in the irrigated region of Niono, Mali? J Med Entomol 43:820PubMedCrossRefGoogle Scholar
  32. Mayhew PJ (1997) Adaptive patterns of host-plant selection by phytophagous insects. Oikos 79:417–428CrossRefGoogle Scholar
  33. Maynard Smith J, Price GR (1973) The logic of animal conflict. Nature 246:15–18CrossRefGoogle Scholar
  34. Munga S, Minakawa N, Zhou G, Barrack OOJ, Githeko AK, Yan G (2006) Effects of larval competitors and predators on oviposition site selection of Anopheles gambiae sensu stricto. J Med Entomol 43:221–224PubMedCrossRefGoogle Scholar
  35. Murdoch WW, Scott MA, Ebsworth P (1984) Effects of the general predator, Notonecta (Hemiptera) upon a freshwater community. J Anim Ecol 53:791–808CrossRefGoogle Scholar
  36. Murdoch WW, Chesson J, Chesson PL (1985) Biological control in theory and practice. Am Nat 125:344–366CrossRefGoogle Scholar
  37. Nakajima Y, Fujisaki K (2010) Fitness trade-offs associated with oviposition strategy in the winter cherry bug, Acanthocoris sordidus. Entomol Exp Appl 137:280–289CrossRefGoogle Scholar
  38. Reguera P, Gomendio M (2002) Flexible oviposition behavior in the golden egg bug (Phyllomorpha laciniata) and its implications for offspring survival. Behav Ecol 13:70–74CrossRefGoogle Scholar
  39. Reiskind M, Lounibos L (2009) Effects of intraspecific larval competition on adult longevity in the mosquitoes Aedes aegypti and Aedes albopictus. Med Vet Entomol 23:62–68PubMedCrossRefGoogle Scholar
  40. Reiskind MH, Wund MA (2009) Experimental assessment of the impacts of northern long-eared bats on ovipositing Culex (Diptera: Culicidae) mosquitoes. J Med Entomol 46:1037–1044PubMedCrossRefGoogle Scholar
  41. Resetarits WJ, Rieger JF, Binckley CA (2004) Threat of predation negates density effects in larval gray treefrogs. Oecologia 138:532–538PubMedCrossRefGoogle Scholar
  42. Rieger JF, Binckley CA, Resetarits WJ (2004) Larval performance and oviposition site preference along a predation gradient. Ecology 85:2094–2099CrossRefGoogle Scholar
  43. Roitberg BD, Mangel M (2010) Mosquito biting and movement rates as an emergent community property and the implications for malarial interventions. Isr J Ecol Evol 56:297–312Google Scholar
  44. Root RB, Kareiva PM (1984) The search for resources by cabbage butterflies (Pieris rapae): ecological consequences and adaptive significance of Markovian movements in a patchy environment. Ecology 65:147–165CrossRefGoogle Scholar
  45. Sadeh A, Mangel M, Blaustein L (2009) Context-dependent reproductive habitat selection: the interactive roles of structural complexity and cannibalistic conspecifics. Ecol Lett 12:1158–1164PubMedCrossRefGoogle Scholar
  46. Service MW (1976) Mosquito ecology: field sampling methods. Applied ScienceGoogle Scholar
  47. Shaalan EAS, Canyon DV (2009) Aquatic insect predators and mosquito control. Trop Biomed 26:223–261PubMedGoogle Scholar
  48. Silberbush A, Blaustein L (2011) Mosquito females quantify risk of predation to their progeny when selecting an oviposition site. Funct Ecol 25:1091–1095CrossRefGoogle Scholar
  49. Silberbush A, Markman S, Lewinsohn E, Bar E, Cohen JE, Blaustein L (2010) Predator-released hydrocarbons repel oviposition by a mosquito. Ecol Lett 13:1129–1138PubMedCrossRefGoogle Scholar
  50. Singer MC, Vasco D, Parmesan C, Thomas CD, Ng D (1992) Distinguishing between ‘preference’ and ‘motivation’ in food choice: an example from insect oviposition. Anim Behav 44:463–471CrossRefGoogle Scholar
  51. Smith C, Reynolds JD, Sutherland WJ (2000) Population consequences of reproductive decisions. Proc R Soc Lond B Biol Sci 267:1327CrossRefGoogle Scholar
  52. Spencer M, Blaustein L, Cohen JE (2002a) Oviposition habitat selection by mosquitoes (Culiseta longiareolata) and consequences for population size. Ecology 83:669–679CrossRefGoogle Scholar
  53. Spencer M, Schwartz SS, Blaustein L (2002b) Are there fine-scale spatial patterns in community similarity among temporary freshwater pools? Global Ecol Biogeogr 11:71–78CrossRefGoogle Scholar
  54. Spielman A, D’Antonio M, Wallace B (2001) Mosquito: a natural history of our most persistent and deadly foe. Faber and Faber, LondonGoogle Scholar
  55. Stav G, Kotler BP, Blaustein L (2010) Foraging Response to Risks of Predation and Competition in Artificial Pools. Isr J Ecol Evol 56:9–20CrossRefGoogle Scholar
  56. Stone C, Taylor R, Roitberg B, Foster W (2009) Sugar deprivation reduces insemination of Anopheles gambiae (Diptera: Culicidae), despite daily recruitment of adults, and predicts decline in model populations. J Med Entomol 46:1327PubMedCrossRefGoogle Scholar
  57. Strogatz SH (1994) Nonlinear dynamics and chaos: with applications to physics, biology, chemistry, and engineering. Westview Press, CambridgeGoogle Scholar
  58. Styer LM, Carey JR, Wang JL, Scott TW (2007) Mosquitoes do senesce: departure from the paradigm of constant mortality. Am J Trop Med Hyg 76:111PubMedGoogle Scholar
  59. Van Pletzen R, Van Der Linde TCDK (1981) Studies on the biology of Culiseta longiareolata (Macquart) (Diptera: Culicidae). Bull Entomol Res 71:71–79CrossRefGoogle Scholar
  60. Vonesh J, Blaustein L (2010) Predator-induced shifts in mosquito oviposition site selection: a meta-analysis and implications for vector control. Isr J Ecol Evol 56:263–279CrossRefGoogle Scholar
  61. Ward SA (1987) Optimal habitat selection in time-limited dispersers. Am Nat 129:568–579CrossRefGoogle Scholar
  62. Warner RR, Wernerus F, Lejeune P, Van Den Berghe E (1995) Dynamics of female choice for parental care in a fish species where care is facultative. Behav Ecol 6:73CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Arik Kershenbaum
    • 1
  • Matthew Spencer
    • 2
  • Leon Blaustein
    • 1
  • Joel E. Cohen
    • 3
  1. 1.Department of Evolutionary and Environmental Biology, Faculty of Natural Sciences, and the Institute of EvolutionUniversity of HaifaHaifaIsrael
  2. 2.School of Environmental SciencesUniversity of LiverpoolLiverpoolEngland, UK
  3. 3.Laboratory of PopulationsRockefeller University and Columbia UniversityNew YorkUSA

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