Predator-Induced Shifts in Mosquito Oviposition Site Selection: A Meta-Analysis and Implications for Vector Control

References

• Abjornsson, K., Bronmark, C., Hansson, L.-A. 2002. The relative importance of lethal and non-lethal effects of fish on insect colonization of ponds. Freshwater Biol. 47: 1489-1495.
   Google Scholar
• Angelon, K. A., Petranka, J. W. 2002. Chemicals of predatory mosquitofish (Gambusia affinis) influence selection of oviposition site by Culex mosquitoes. J. Chem. Ecol. 28: 797-806.
   Google Scholar
• Arav, D., Blaustein, L. 2006. Effects of pool depth and risk of predation on oviposition habitat selection by temporary pool dipterans. J. Med. Entomol. 43: 493-497.
   Google Scholar
• Bay, E. C. 1974. Predator-prey relationships among aquatic insects. Annu. Rev. Entomol. 19: 441-453.
   Google Scholar
• Bentley, M. D., Day, J. F. 1989. Chemical ecology and behavioral aspects of mosquito oviposition. Annu. Rev. Entomol. 34: 401-421.
   Google Scholar
• Bernard, M. F., Fordyce, J. A. 2003. Are induced defenses costly? Consequences of predator-induced defenses in western toads, Bufo boreas. Ecology 84: 68-78.
   Google Scholar
• Binckley, C. A., Resetarits, W. J. 2005. Habitat selection determines abundance, richness and species composition of beetles in aquatic communities. Biol. Lett. 1: 370-374.
   Google Scholar
• Binckley, C. A., Resetarits, W. J. 2008. Oviposition behavior partitions aquatic landscapes along predation and nutrient gradients. Behavioral Ecology 19(3): 552-557.
   Google Scholar
• Black, A. R., Dodson, S. I. 1990. Demographic cost of Chaoborus-induced phenotypic plasticity in Daphnia pulex. Oecologia 83: 117-122.
   Google Scholar
• Blaustein, L. 1998. Influence of the predatory backswimmer, Notonecta maculata, on invertebrate community structure. Ecol. Entomol. 23: 246-252.
   Google Scholar
• Blaustein, L., Blaustein, J., Chase, J. 2005. Chemical detection of the predator Notonecta irrorata by ovipositing Culex mosquitoes. J. Vector Ecol. 30(2): 299-301.
   Google Scholar
• Blaustein, L., Dumont, H. J. 1990. Typhloplanid flatworms (Mesostoma and related genera): Mechanisms of predation and evidence that they structure aquatic invertebrate communities. Hydrobiologia 198: 61-77.
   Google Scholar
• Blaustein, L., Kiflawi, M., Eitam, A., Mangel, M., Cohen, J. E. 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.
   Google Scholar
• Blaustein, L., Kolter, B. P. 1993. Oviposition habitat selection by Culiseta longiareolata: effects of immature conspecifics, tadpoles and food levels. Ecol. Entomol. 18: 104-108.
   Google Scholar
• Campos, J., Andrade, C. F. 2003. Larval susceptibility of Aedes aegypti and Culex quinquefasciatus populations to chemical insecticides. Revista Saúde Pública 37: 523-527.
   Google Scholar
• Case, T. J., Washino, R. K. 1979. Flatworm control of mosquito larvae in rice fields. Science 206: 1412-1414.
   Google Scholar
• Chandra, G., Mandal, S. K., Ghosh, A. K., Das, D., Banerjee, S. S., Chakraborty, S. 2008. Biocontrol of larval mosquitoes by Acilius sulcatus (Coleoptera: Dytiscidae). BMC Infect. Dis. 8: 138.
   Google Scholar
• Chesson, J. 1984. Effect of notonectids (Hemiptera: Notonectidae) on mosquitoes (Diptera: Culicidae): predation or selective oviposition? Environ. Entomol. 13: 531-538.
   Google Scholar
• Collins, F. H., Washino, R. K. 1985. Insect predators. In: Chapman, H. C., ed. Biological control of mosquitoes. American Mosquito Control Association Bulletin 6: 26-41.
   Google Scholar
• Corbel, V., Guessan, R. N., Brengues, C., Chandre, F., Djogbenou, L., Martin, T., Akogbeto, M., Hougard, J. M., Rowland, M. 2007. Multiple insecticide resistance mechanisms in Anopheles gambiae and Culex quinquefasciatus from Benin, West Africa. Acta Trop. 101: 207-216.
   Google Scholar
• Delibes, M., Gaona, P., Ferreras, P. 2001. Effects of an attractive sink leading into maladaptive habitat selection. Am. Nat. 158: 277-285.
   Google Scholar
• DeWitt, T. J. 1998. Costs and limits of plasticity: tests with predator-induced morphology and life history in a freshwater snail. J. Evol. Biol. 11: 465-480.
   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.
   Google Scholar
• Eitam, A., Blaustein, L. 2004. Oviposition habitat selection by mosquitoes in response to predator (Notonecta maculata) density. Physiol. Entomol. 29: 188-191.
   Google Scholar
• Epstein, P. R., Diaz, H. F., Elias, S., Grabherr, G., Graham, N. E., Martens, W. J. M., Mosley-Thompson, E., Susskind, J. 1998. Biological and physical signs of climate change: focus on mosquito-borne diseases. Bull. Am. Meteorol. Soc. 79: 409-417.
   Google Scholar
• Garcia, E. A. 2006. Regional coexistence and local dominance in Chaoborus: species sorting along a predation gradient. Dissertation. Michigan State University, East Lansing, Michigan, USA.
   Google Scholar
• Garcia, E. A., Mittelbach, G. G. 2008. Regional coexistence and local dominance in Chaoborus: Species sorting along a predation gradient. Ecology 89: 1703-1713.
   Google Scholar
• Gerberich, J. B., Laird, M. 1985. Larvacious fish in the biological control of mosquitoes, with a selected bibliography of recent literature. In: Laird, M., Miles, J. W., eds. Integrated mosquito control methodologies. Academic Press, London, pp. 47-58.
   Google Scholar
• Gould, E. A., Higgs, S. 2009. Impact of climate change and other factors on emerging arbovirus diseases. Trans. R. Soc. Trop. Med. Hyg. 103: 109-121.
   Google Scholar
• Gratz, N. G. 1999. Emerging and resurging vector-borne diseases. Annu. Rev. Entomol. 44: 51-75.
   Google Scholar
• Gubler, D. J. 1998. Resurgent vector-borne diseases as a global health problem. Emerging Infect. Dis. 4: 442-449.
   Google Scholar
• Hedges, L. V., Gurevitch, J., Curtis, P. 1999. The meta-analysis of response ratios in experimental ecology. Ecology 80: 1150-1156.
   Google Scholar
• Hedges, L. V., Olkin, I. 1985. Statistical methods for meta-analysis. Academic Press, New York.
   Google Scholar
• Howard, A. F. V., Omlin, F. X. 2008. Abandoning small-scale fish farming in western Kenya leads to higher malaria vector abundance. Acta Trop. 105: 67-73.
   Google Scholar
• Juliano, S. A. Coexistence, exclusion, or neutrality? A meta-analysis of competition between Aedes albopictus and resident mosquitoes. Isr. J. Ecol. Evol. 58: 325-351, this issue.
   Google Scholar
• Juliano, S. A., Lounibos, L. P., Nishimura, N., Greene, K. 2009. Your worst enemy could be your best friend: predator contributions to invasion resistance and persistence of natives. Oecologia 164: 221-230.
   Google Scholar
• Kay, B. H., Nam, V. S., Van Tien, T., Yen, N. T., Phong, T. V., Diep, V. T. B., Ninh, T. U., Bektas, A., Aaskov, J. G. 2002. Control of Aedes vectors of dengue in three provinces of Vietnam by use of Mesocyclops (Copepoda) and community-based methods validated by entomologic, clinical, and serological surveillance. Am. J. Trop. Med. Hyg. 66: 40-48.
   Google Scholar
• Kiflawi, M., Blaustein, L., Mangel, M. 2003a. Predation-dependent oviposition habitat selection by the mosquito Culiseta longiareolata: a test of competing hypotheses. Ecol. Lett. 6: 35-40.
   Google Scholar
• Kiflawi, M., Blaustein, L., Mangel, M. 2003b. Oviposition habitat selection by the mosquito Culiseta longiareolata in response to risk of predation and conspecifics larval density. Ecol. Entomol. 28: 168-173.
   Google Scholar
• Kraus, J. M., Vonesh, J. R. 2010. Feedbacks between community assembly and top predator effects on habitat selection shape variation in colonization rates. J. Anim. Ecol. 79: 795-802.
   Google Scholar
• Kristan, W. B. 2003. The role of habitat selection behavior in population dynamics: source-sink systems and ecological traps. Oikos 103: 457-468.
   Google Scholar
• Kumar, L., Hwang, J.-S. 2006. Larvicidal efficiency of aquatic predators: a perspective for mosquito biocontrol. Zool. Stud. 45: 447-466.
   Google Scholar
• Lacey, L. A., Orr, B. K. 1994. The role of biological control of mosquitoes in integrated vector control. Am. J. Trop. Med. Hyg. 50: 97-115.
   Google Scholar
• Le Menach, A., Mckenzie, F. E., Flahault, A., Smith, D. L. 2005. The unexpected importance of mosquito oviposition behavior for malaria: non-productive larval habitats can be sources for malaria transmission. Malar. J. 4: 23-33.
   Google Scholar
• Lowenberger, C. A., Rau, M. E. 1994. Selective oviposition by Aedes aegypti (Diptera: Culicidae) in response to a larval parasite, Plagiorchis elegans (Trematoda: Plagiorchiidae). Environ. Entomol. 23(5): 1269-1276.
   Google Scholar
• Marten, G. G. 1990. Evaluation of cyclopoid copepods for Aedes albopictus in tires. J. Am. Mosq. Control Assoc. 6: 681-688.
   Google Scholar
• Mokany, A., Shine, R. 2003. Oviposition site selection by mosquitoes in affected by cues from conspecifics larvae and anuran tadpoles. Austral. Ecol. 28: 33-37.
   Google Scholar
• Munga, S., Minakawa, N., Zhou, G., Barrack, O.-O. J., Githeko, A., Yan, G. 2006. Effects of larval competitors and predators on oviposition site selection of Anopheles gambiae sensu stricto. J. Med. Entomol. 43(2): 221-224.
   Google Scholar
• Nam, V. S., Yen, N. T., Phong, T. V., Ninh, T. U., Mai, L. Q., Lo, L. V., Nghia, L. T., Bektas, A., Briscombe, A., Aaskov, J. G., Ryan, P. A., Kay, B. H. 2005. Elimination of dengue by community programs using Mesocyclops (copepoda) against Aedes aegypti in central Vietnam. Am. J. Trop. Med. Hyg. 72: 67-73.
   Google Scholar
• Osenberg C. W., Shima, J. S., St. Mary, C. M. 2006. Habitat degradation and settlement behaviour: effects on fish settlement, survival, and recruitment. In: Suzuki, Y., Nakamori, T., Hidaka, M., Kayanne, H., Casareto, B. E., Nadaoka, K., Yamano, H., Tsuchiya, M., eds. Proceedings of the 10th International Coral Reef Symposium, Okinawa, Japan. Japanese Coral Reef Society, Tokyo, pp. 257-263.
   Google Scholar
• Pangle, K. L., Peacor, S. D., Johannsson, O. E. 2007. Large nonlethal effects of an invasive invertebrate predator on zooplankton population growth rate. Ecology 88: 402-412.
   Google Scholar
• Pates, H., Curtis, C. 2005. Mosquito behavior and vector control. Ann, Rev. Entomol. 50: 53-70.
   Google Scholar
• Peacor, S. D., Werner, E. E. 2004. How dependent are species-pair interaction strengths on other species in the food web? Ecology 85: 2754-2763.
   Google Scholar
• Peckarsky, B. L., Abrams, P. A., Bolnick, D. I., Dill, L. M., Grabowski, J. H., Luttbeg, B., Orrock, J. L., Peacor, S. D., Preisser, E. L., Schmitz, O. J., Trussell, G. C. 2008. Revisiting the classics: considering nonconsumptive effects in textbook examples of predator-prey interactions. Ecology 89: 2416-2425.
   Google Scholar
• Petranka, J. W., Fakhoury, K. 1991. Evidence of a chemically-mediated avoidance response of ovipositiong insects to blue gills and green frog tadpoles. Copeia 1991.: 234-239.
   Google Scholar
• Preisser, E. L., Bolnick, D. I. 2008. When predators don't eat their prey: nonconsumptive predator effects on prey dynamics. Ecology 89: 2414-2415.
   Google Scholar
• Preisser, E. L., Bolnick, D. I., Benard, M. F. 2005. Scared to death? The effects of intimidation and consumption in predator-prey interactions. Ecology 86: 501-509.
   Google Scholar
• Resetarits, W. J., Binckley, C. A., Chalcraft, D. R. 2005. Habitat selection, species interactions, and processes of community assembly in complex landscapes: a metacommunity perspective. In: Holyoak, M., Leibold, M., Holt, R. D. eds. Metacommunities: spatial dynamics and ecological communities. The University of Chicago Press, Chicago, pp. 374-398.
   Google Scholar
• Resetarits, W. J., Wilbur, H. M. 1989. Choice of oviposition site by Hyla chrysoscelis: role of predators and competitors. Ecology 70: 220-228.
   Google Scholar
• Rieger, J. F., Binckley, C. A., Resetarits, W. J. 2004. Larval performance and oviposition site preference along a predation gradient. Ecology 85: 2094-2099.
   Google Scholar
• Ritchie, S. A., Laidlaw-Bell, C. 1984. Do fish repel oviposition by Aedes taeniorhynchus? J. Am. Mosq. Control Assoc. 10: 380-384.
   Google Scholar
• Ritchie, S. A., Montague, C. L. 1995. Simulated populations of the black salt marsh mosquito (Aedes taeniorhynchus) in a Florida mangrove forest. Ecol. Modell. 77: 123-141.
   Google Scholar
• Reiskind, M. H., Wund, M. A. 2009. Experimental Assessment of the Impacts of Northern Long-Eared Bats on Ovipositing Culex (Diptera: Culicidae) Mosquitoes. J. Med. Entomol. 46: 1037-1044.
   Google Scholar
• Rosenberg, M. S., Adams, D. C., Gurevitch, J. 2000. Meta Win: statistical software for meta-analysis. Sinauer, Sunderland, MA.
   Google Scholar
• Rosenthal, R. 1979. The "file drawer problem" and tolerance for null results. Psychol. Bull. 86: 638-641.
   Google Scholar
• Service, M. W. 1993. Mosquito ecology: field sampling methods. Elsevier, London.
   Google Scholar
• Sherrat, T. N., Church, S. C. 1994. Ovipositional preferences and larval cannibalism in the Neotropical mosquito Trichoprosopon digitatum (Diptera: Cuclidae). Anim. Behav. 48(3): 645-652.
   Google Scholar
• Silberbush, A., Blaustein, L. 2008. Oviposition habitat selection by a mosquito in response to a predator: are predator-released kairomones air-borne cues? J. Vector Ecol. 33: 208-211.
   Google Scholar
• Siberbush, A., Markman, S, Lewinsohn, E., Bar, E., Cohen, J. 2010. Predator-released hydrocarbons repel oviposition by a mosquito. Ecol. Lett. 13: 1129-1138.
   Google Scholar
• Spencer, M., Blaustein, L., Cohen, J. E. 2002. Oviposition habitat selection by mosquitoes (Culiseta longiareolata) and consequences for population size. Ecology 83: 669-679.
   Google Scholar
• Spielman, A., Sullivan, J. J. 1974. Predation on peridomestic mosquitoes by hylid tadpoles on Grand Bahama Island. American Journal of Tropical Medicine and Hygiene 23: 704-709.
   Google Scholar
• Stav, G., Blaustein, L., Margalith, J. 1999. Experimental evidence for predation risk sensitive oviposition by a mosquito, Culiseta longiareolata. Ecol. Entomol. 24: 202-207.
   Google Scholar
• Stav, G., Blaustein, L., Margalit, Y. 2000. Influence of nymphal Anax imperator (Odonata: Aeshindae) on oviposition by the mosquito Culiseta longiareolata (Diptera: Culicidae) and community structure in temporary pools. J. Vector Ecol. 25: 190-202.
   Google Scholar
• Tietze, N. S., Mulla, M. S. 1991. Biological control of Culex mosquitoes (Diptera, Culcidae) by the tadpole shrimp, Triops longicaudatus (Notostraca, Triopsidae). J. Med. Entomol. 28(1): 24-31.
   Google Scholar
• Tollrian, R., Harvell, C. D. 1999. The ecology and evolution of inducible defenses. Princeton University Press, Princeton, NJ.
   Google Scholar
• Torres-Estrada, J. L., Rodriguez, M. H., Cruz-Lopez, L., Arredondo-Jimenez, J. I. 2001. Selective oviposition by Aedes aegypti (Diptera: Culcidae) in response to Mesocyclops longisetus (Copepoda: Cyclopoidea) under laboratory and field conditions. J. Med. Entomol. 38: 188-192.
   Google Scholar
• Van Dam, A. R., Walton, W. E. 2008. The effect of predatory fish exudates on the ovipositional behavior of three mosquito species: Culex quinquefasciatus, Aedes aegypti and Culex tarsalis. Medical and Veterinary Entomology 22: 399-404.
   Google Scholar
• Vonesh, J. R., Buck, J. 2007. Pesticide alters oviposition site selection in gray treefrogs. Oecologia 154: 219-226.
   Google Scholar
• Vonesh, J. R., Kraus, J. M., Rosenberg, J. S., Chase, J. 2009. Predator effects on aquatic community assembly: disentangling the roles of habitat selection and post-colonization processes. Oikos 118: 1219-1229.
   Google Scholar
• Walton, W. E. 2007. Larvivorous fish including gambusia. J. Am. Mosq. Control Assoc. 23: 184-220.
   Google Scholar
• Whalon, M. E., Mota-Sanchez, D., Hollingworth, R. M., eds. 2008. Global pesticide resistance in arthropods. CAB International, Cambridge, MA, USA, 208 pp.
   Google Scholar
• Xue, R. D., Ali, A., Barnard, D. R. 2005. Effects of forced egg-retention in Aedes albopictus on adult survival and reproduction following application of DEET as an oviposition deterrent. J. Vector Ecol. 30: 45-48.
   Google Scholar
• Xue, R. D., Barnard, D. R., Ali. A. 2006. Laboratory evaluation of 21 insect repellents as larvicides and as oviposition deterrents of Aedes albopictus (Diptera: Culicidae). J. Am. Mosq. Control Assoc. 22: 126-130.
   Google Scholar