Skip to main content
SpringerLink
Log in

Interactive effects of salinity and a predator on mosquito oviposition and larval performance

  • Population ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Oviposition habitat selection (OHS) is increasingly being recognized as playing a large role in explaining mosquito distributions and community assemblages. Most studies have assessed the role of single factors affecting OHS, while in nature, oviposition patterns are most likely explained by multiple, interacting biotic and abiotic factors. Determining how various factors interact to affect OHS is important for understanding metapopulation and metacommunity dynamics. We investigated the individual and interactive effects of three water salinities (0, 15 and 30 p.p.t. NaCl added) and the aquatic predator Anisops debilis Perplexa (Hemiptera: Notonectidae) on OHS and larval performance of the mosquitoes Ochlerotatus caspius Pallas and Culiseta longiareolata Macquart (Diptera: Culicidae) in outdoor-artificial-pool and laboratory experiments. C. longiareolata inhabited only freshwater pools, strongly avoided pools containing A. debilis, and larvae experienced lower survival in the presence of A. debilis. Salinity concentration interacted strongly with the predator in affecting OHS and larval survival of O. caspius; oviposition increased with increasing salinity in the absence of the predator and decreased with increasing salinity in the presence of the predator. O. caspius larval survival in predator-free pools was lowest in freshwater and highest at intermediate salinity. In predator pools, survival was highest at high salinity, where predation rate was shown to be lowest in the laboratory. Our results highlight that assessing the role of single factors in affecting mosquito distributions can be misleading. Instead, multiple factors may interact to affect oviposition patterns and larval performance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Al Saadi M, Mohsen ZH (1988) Predatory and cannibalistic behavior of Culiseta longiareolata (Macquart) (Diptera: Culicidae) in Iraq. J Biol Sci Res 19:339–351

    Google Scholar 

  • Arav DL (2007) Oviposition and development responses of temporary pool dipterans to risks of predation and desiccation. Master’s thesis, Department of Evolutionary and Environmental Biology, University of Haifa, Haifa

  • Bentley MD, Day JF (1989) Chemical ecology and behavioral aspects of mosquito oviposition. Annu Rev Entomol 34:401–421. doi:10.1146/annurev.ento.34.1.401

    Article  CAS  PubMed  Google Scholar 

  • Binckley CA, Resetarits WJ (2005) Habitat selection determines abundance, richness and species composition of beetles in aquatic communities. Biol Lett 1:370–374. doi:10.1098/rsbl.2005.0310

    Article  PubMed Central  PubMed  Google Scholar 

  • Blaustein L (1999) Oviposition site selection in response to risk of predation: evidence from aquatic habitats and consequences for population dynamics and community structure. In: Wasser SP (ed) Evolutionary theory and processes: modern perspectives. Kluwer, Dordrecht, pp 441–456

    Chapter  Google Scholar 

  • Blaustein L, Kotler BP (1993) Oviposition habitat selection by Culiseta longiareolata: effects of immature conspecifics, tadpoles and food levels. Ecol Entomol 18:104–108. doi:10.1111/j.1365-2311.1993.tb01190.x

    Article  Google Scholar 

  • Blaustein L, Margalit J (1994) Mosquito larvae (Culiseta longiareolata) compete with and prey upon toad (Bufo viridis) immatures. J Anim Ecol 63:841–850. doi:10.2307/5261

    Article  Google Scholar 

  • Blaustein L, Whitman DW (2009) Behavioral plasticity in response to risk of predation: oviposition habitat selection by a mosquito. In: Whitman D, Ananthakrishnan TN (eds) Phenotypic plasticity in insects: mechanisms and consequences. Science Publishers, London, pp 263–280

    Google Scholar 

  • Blaustein L, Kotler B, Ward D (1995) Direct and indirect effects of a predatory backswimmer (Notonecta maculata) on community structure of desert temporary pools. Ecol Entomol 20:311–318. doi:10.1111/j.1365-2311.1995.tb00462.x

    Article  Google Scholar 

  • 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 138:300–305. doi:10.1007/s00442-003-1398-x

    Article  PubMed  Google Scholar 

  • Blaustein L, Blaustein J, Chase J (2005) Chemical detection of the predator Notonecta irrorata by ovipositing Culex mosquitoes. J Vector Ecol 30:299–301

    PubMed  Google Scholar 

  • Bond JG, Arredondo-Jimenez JI, Rodriguez MH, Quiroz-Martinez H, Williams T (2005) Oviposition habitat selection for a predator refuge and food source in a mosquito. Ecol Entomol 30:255–263. doi:10.1111/j.0307-6946.2005.00704.x

    Article  Google Scholar 

  • Bradshaw WE, Holzapfel CM (2010) Light, time and the physiology of biotic response to rapid climate change in animals. Annu Rev Physiol 72:147–166. doi:10.1146/annurev-physiol-021909-135837

    Article  CAS  PubMed  Google Scholar 

  • Carver S, Spafford H, Storey A, Weinstein P (2009) Colonization of ephemeral water bodies in the wheat belt of Western Australia by assemblages of mosquitoes (Diptera: Culicidae): role of environmental factors, habitat, and disturbance. Environ Entomol 38: 1585–1594. doi:http://dx.doi.org/10.1603/022.038.0609

    Google Scholar 

  • Carver S, Spafford H, Storey A, Weinstein P (2010) The roles of predators, competitors, and secondary salinization in structuring mosquito (Diptera: Culicidae) assemblages in ephemeral water bodies of the wheat belt of Western Australia. Environ Entomol 39:798–810. doi:10.1603/EN09235

    Article  PubMed  Google Scholar 

  • Clark TM, Flis BJ, Remold SK (2004) Differences in the effects of salinity on larval growth and developmental programs of a freshwater and a euryhaline mosquito species (Insecta: Diptera, Culicidae). J Exp Biol 207:2289–2295. doi:10.1242/jeb.01018

    Article  PubMed  Google Scholar 

  • Dimentman CH, Margalit J (1981) Rainpools as breeding and dispersal sites of mosquitoes and other aquatic insects in the Central Negev Desert. J Arid Environ 4:123–129

    Google Scholar 

  • Duquesne S, Kroeger I, Kutyniok M, Liess M (2011) The potential of cladocerans as controphic competitors of the mosquito Culex pipiens. J Med Entomol 48:554–560. doi:10.1603/ME09282

    Article  PubMed  Google Scholar 

  • Eitam A, Blaustein L (2004) Oviposition habitat selection by mosquitoes in response to predator (Notonecta maculata) density. Physiol Entomol 29:188–191. doi:10.1111/j.0307-6962.2004.0372.x

    Article  Google Scholar 

  • 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 485:183–189. doi:10.1023/A:1021315309758

    Article  Google Scholar 

  • Foley DH, Bryan JH (1999) Oviposition preference for freshwater in coastal malaria vector, Anopheles farauti. J Am Mosq Contr 15:291–294. doi:10.2987/8756-971X(2006)22[42:OPAEEI]2.0.CO;2

    CAS  Google Scholar 

  • Greenhouse SW, Geisser S (1959) On methods in the analysis of profile data. Psychometrika 24:95–112

    Article  Google Scholar 

  • Hampton SE, Gilbert JJ, Burns CW (2000) Direct and indirect effects of juvenile Buenoa macrotibialis (Hemiptera: Notonectidae) on the zooplankton of a shallow pond. Limnol Oceanogr 45:1006–1012

    Article  Google Scholar 

  • Hein AM, Gillooly JF (2011) Predators, prey, and transient states in the assembly of spatially structured communities. Ecology 92:549–555. doi:10.1890/10-1922.1

    Article  PubMed  Google Scholar 

  • Juliano SA (2009) Species interactions among larvae mosquitoes: context dependence across habitat gradients. Annu Rev Entomol 54:37–56. doi:10.1146/annurev.ento.54.110807.090611

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kershenbaum A, Stone L, Ostfeld RS, Blaustein L (2012) Modeling transmission of vector-borne pathogens when vector-feeding sites are limited: a departure from frequency-dependence. PLoS One 7:e36730. doi:10.1371/journal.pone.0036730

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kotler BP, Blaustein L (1995) Titrating food and safety in a heterogeneous environment: when is the risky patch of equal value? Oikos 74:251–258

    Article  Google Scholar 

  • Larsen E, Blaustein L (2005) New backswimmer (Heteroptera: Notonectidae) records for Israel. Zool Middle East 36:114–116. doi:10.1080/09397140.2005.10638137

    Article  Google Scholar 

  • McCall PJ (2002) Chemoecology of oviposition in insects of medical and veterinary importance. In: Hikler M, Meiners T (eds) Chemoecology of insect eggs and egg deposition. Blackwell, Berlin, pp 265–289

    Google Scholar 

  • Morris DW, Clark RG, Boyce MS (2008) Habitat and habitat selection: theory, tests, and implication. Isr J Ecol Evol 54:287–294. doi:10.1560/IJEE.54.3-4.287

    Article  Google Scholar 

  • Nguyen AT, Williams-Newkirk AJ, Kitron UD, Chaves LF (2012) Seasonal weather, nutrients, and conspecific presence impacts on the southern house mosquito oviposition dynamics in combined sewage overflows. J Med Entomol 49:1328–1338. doi:10.1603/ME12090

    Article  PubMed  Google Scholar 

  • Osborn FR, Diaz S, Gomez CJ, Moreno M, Hernandez G (2006) Oviposition preference and egg eclosion in different salt concentrations in the coastal malaria vector Anopheles aquasalis curry. J Am Mosq Contr 22:42–46. doi:10.2987/8756971X(2006)22[42:OPAEEI]2.0.CO;2

    Article  Google Scholar 

  • Osborn FR, Herrera MJ, Gomez CJ, Salazar A (2007) Comparison of two commercial formulations of Bacillus thuringiensis var. israelensis for the control of Anopheles aquasalis (Diptera: Culicidae) at three salt concentrations. Mem I Oswaldo Cruz 102: 69–72. doi:http://dx.doi.org/10.1590/S0074-02762007000100011

    Google Scholar 

  • Refsnider JM, Janzen FJ (2010) Putting eggs in one basket: ecological and evolutionary hypotheses for variation in oviposition-site choice. Annu Rev Ecol Evol Syst 41:39–57. doi:10.1146/annurev-ecolsys-102209-144712

    Article  Google Scholar 

  • Reiskind MH, Wilson ML (2004) Culex restuans (Diptera: Culicidae) oviposition behavior determined by larval habitat quality and quantity in southeastern Michigan. J Med Entomol 41:179–186. doi:10.1603/0022-2585-41.2.179

    Article  PubMed  Google Scholar 

  • Resetarits WJ (2001) Colonization under threat of predation: avoidance of fish by an aquatic beetle, Tropisternus lateralis (Coleoptera: Hydrophilidae). Oecologia 129:155–160. doi:10.1007/s004420100704

    Article  Google Scholar 

  • Rieger JF, Binckley CA, Resetarits WJ (2004) Larval performance and oviposition site preference along a predation gradient. Ecology 85:2094–2099. doi:10.1890/04-0156

    Article  Google Scholar 

  • Roberts D (1996) Mosquitoes breeding in brackish water: female ovipositional preference or larval survival? J Med Entomol 33:525–530

    CAS  PubMed  Google Scholar 

  • Rosenzweig ML, Abramsky Z (1997) Two gerbils of the Negev: a long-term investigation of optimal habitat selection and its consequences. Evol Ecol 11:733–756

    Article  Google Scholar 

  • Sadeh A, Mangel M, Blaustein L (2009) Context-dependent reproductive habitat selection: the interactive roles of structural complexity and cannibalistic conspecifics. Ecol Lett 12:1158–1164. doi:10.1111/j.1461-0248.2009.01371.x

    Article  PubMed  Google Scholar 

  • Schemske DW, Mittelbach GG, Cornell HV, Sobel JM, Kaustuv R (2009) Is there a latitudinal gradient in the importance of biotic interactions? Annu Rev Ecol Evol Syst 40:245–269. doi:10.1146/annurev.ecolsys.39.110707.173430

    Article  Google Scholar 

  • Service MW (1986) The biologies of Aedes caspius (Pallas) and Culex quinquefasciatus Say (Diptera: Culicidae) in Dubai. Insect Sci Appl 7:11–18

    Google Scholar 

  • Sih A (1980) Optimal behavior: can foragers balance two conflicting demands. Science 210:1041–1043

    Article  CAS  PubMed  Google Scholar 

  • Silberbush A (2004) Effects of salinity and predation on community structure in temporary pools: behavioral and physiological mechanisms. Master’s thesis, Department of Life Sciences, Ben Gurion University, Beer-Sheva

  • Silberbush A, Blaustein L (2011) Mosquito female quantify risk of predation to their progeny when selecting an oviposition site. Funct Ecol 25:1091–1095. doi:10.1111/j.1365-2435.2011.01873.x

    Article  Google Scholar 

  • Silberbush A, Blaustein L, Margalith Y (2005) Influence of salinity concentration on insect community structure: a mesocosm experiment in the Dead Sea basin region. Hydrobiologia 548:1–10. doi:10.1007/s10750-004-8336-8

    Article  Google Scholar 

  • 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. doi:10.1111/j.1461-0248.2010.01501.x

    Article  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. doi:10.2307/3071872

    Article  Google Scholar 

  • Stav G, Blaustein L, Margalith Y (1999) Experimental evidence for predation sensitive oviposition by a mosquito, Culiseta longiareolata. Ecol Entomol 24:202–207. doi:10.1046/j.1365-2311.1999.00183.x

    Article  Google Scholar 

  • Stav G, Blaustein L, Margalit Y (2005) Individual and interactive effects of a predator and controphic species on mosquito populations. Ecol Appl 15:587–598. doi:10.1890/03-5191

    Article  Google Scholar 

  • Tsurim I, Silberbush A, Ovadia O, Blaustein L, Margalith Y (2013) Inter- and intra-specific density-dependent effects on life history and development strategies of larval mosquitoes. PLoS ONE 8:e57875. doi:10.1371/journal.pone.0057875

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Van den Bosch R, Messenger PS, Gutierrez AP (1982) An introduction to biological control. Plenum, New York

    Book  Google Scholar 

  • Van Pletzen R, Van Der Linde TCDK (1981) Studies on the biology of Culiseta longiareolata (Macquart) (Diptera: Culicidae). Bull Entomol Res 71:71–79

    Article  Google Scholar 

  • Van Schie C, Spafford H, Carver S, Weinstein P (2009) Salinity tolerance of Aedes camptorhynchus (Diptera: Culicidae) from two regions in southwestern Australia. Aust J Entomol 48:293–299. doi:10.1111/j.1440-6055.2009.00719.x

    Article  Google Scholar 

  • 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 56:263–279. doi:10.1560/IJEE.56.3-4.263

    Article  Google Scholar 

  • Yamamura K (1999) Transformation using (x + 0.5) to stabilize the variance of populations. Res Popul Ecol 41:229–234

    Article  Google Scholar 

  • Young KA (2004) Asymmetric competition, habitat selection, and niche overlap in juvenile salmonids. Ecology 85:134–149

    Article  Google Scholar 

Download references

Acknowledgments

We thank William J. Resetarits for fruitful conversations, Bert Schneider for his assistance in the field and statistical support. This work was partially supported by a United States–Israel Binational Science Foundation grant (98-305) awarded to Leon Blaustein and Marc Mangel, and funds from the Tamar Regional Council awarded to Yoel Margalith.

Author information

Authors and Affiliations

  1. Department of Life Sciences, Center for Biological Control, Ben-Gurion University of the Negev, P.O. Box 653, 8410501, Beer-Sheva, Israel

    Alon Silberbush, Ido Tsurim & Yoel Margalith

  2. Community Ecology Laboratory, Institute of Evolution and Department of Evolutionary and Environmental Biology, Faculty of Natural Sciences, University of Haifa, 3498838, Haifa, Israel

    Alon Silberbush & Leon Blaustein

Authors
  1. Alon Silberbush
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ido Tsurim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yoel Margalith
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Leon Blaustein
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alon Silberbush.

Additional information

Communicated by Steven Kohler.

Y. Margalith: deceased.

Electronic supplementary material

Below is the link to the ESM.

Supplementary material 1 (DOCX 382 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Silberbush, A., Tsurim, I., Margalith, Y. et al. Interactive effects of salinity and a predator on mosquito oviposition and larval performance. Oecologia 175, 565–575 (2014). https://doi.org/10.1007/s00442-014-2930-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-014-2930-x

Keywords

Search

Navigation