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Abstract
Mosquito larvae have developed a variety of responses to reduce the risk of predation, but this requires them to be able to identify the different species of predators and respond accordingly. We investigated the behavioural response of two mosquito species to three chemical signals: kairomones from two predators, and also to alarm semiochemicals from killed mosquito larvae. Culex perexiguus mosquito larvae are primarily surface filter-feeders. In response to all three chemical signals, they significantly reduced feeding by the high-risk active bottom scraping of biofilms in favour of the less active (and so lower predator-detection risk) surface filter feeding. Active escape swimming (instead of feeding) also increased for all three signals, but was much less for dragonfly nymph kairomones. Dragonflies are almost entirely bottom feeders and so are a much lower danger to surface feeding mosquitoes compared with damselfly nymphs, which feed at all depths. Culiseta longiareolata mosquito larvae normally have a high level of bottom-feeding. This was significantly reduced to all three chemical signals, but escape swimming only occurred for dragonfly kairomones (which are natural predators for the bottom-feeding larvae).
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References
- Griffin, L.F. and Knight, J.M. A review of the role of fish as biological control agents of disease vector mosquitoes in mangrove forests; reducing human health risks while reducing environmental risk. Wetlands Ecological Management, 2012, 20, 243-252.
- Roberts, D.M. Mosquito larvae change their feeding behavior in response to kairomones from some predators. Journal of Medical Entomology, 2014, 51, 368-374.
- Chivers, D.P., Wiseden, B.D. and Smith, R.J.F. Damselfly larvae learn to recognise predators from chemical cues in the predator’s diet. Animal Behaviour, 1996, 52, 315-320.
- Hopper, K.R. Flexible antipredator behavior in a dragonfly species that coexists with different predator types. Oikos, 2001, 93, 470-476.
- Stoks, R.M., McPeek, M.A. and Mitchell, J. L. Evolution of prey behavior in response to changes in predation regime: damselflies in fish and dragonfly lakes. Evolution, 2003, 57,
- -585.
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- Kesavaraju, B., and Juliano, S.A. Differential behavioral responses to water-borne cues to predation in two-container-dwelling mosquitoes. Annals of the Entomological Society of America, 2004, 97, 194-201.
- Takahara, T., Kohmatsu, Y., Maruyama, A., Doi, H., Yamanaka, H. and Yamaoka, R. Inducible defense behavior of an anuran tadpole: cue-detection range and cue types used 10 against predators. Behavioural Ecology, 2012, 23, 863-868.
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- Ferrari, M.C.O., Messier, F. and Chivers, D.P. Threat-sensitive learning of predators by larval mosquitoes Culex restuans. Behavioural Ecology and Sociobiology, 2007, 62, 1079-1083.
- Roberts, D.M. Responses of three species of mosquito larvae to the presence of predatory dragonfly and damselfly larvae. Entomologia Experimentalis et Applicata, 2012, 145, 23-29.
- Angelon, K.A. and Petranka, J.W. Chemicals of predatory mosquito fish Gambusia affinis in fluence selection of oviposition site by Culex mosquitoes. Journal of Chemical Ecology, 2002, 28, 797-806.
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- Silberbush, A. and Blaustein, L. Mosquito females quantify risk of predation to their progeny when selecting an oviposition site. Functional Ecology, 2011, 25, 1091-1095.
- Why, A.M., Lara, J.R. and Walton, W.E. Oviposition of Culex tarsalis (Diptera: Culicidae to waters from conspecific larvae subject to crowding, confinement, starvation, or infection. Journal of Medical Entomology, 2016, 53, 1093-1099.
- Werner, E.E. and Anholt, B.R. Ecological consequences of the trade-off between growth and mortality rates mediated by foraging activity. American Naturalist, 1993, 142, 242-11272.
- Ferrari, M.C.O., Messier, F. and Chivers, D.P. Variable predation risk and the dynamic nature of mosquito antipredator responses to chemical alarm cues. Chemoecology, 2008, 17, 223-229.
- Knight, T.M., Chase, J.M., Goss, C.W. and Knight, J.J. Effects of interspecific competition, predation, and their interaction on survival and development time of immature Anopheles quadrimaculatus. Journal of Vector Ecology, 2004, 29, 277-284.
- Beketov, M.A. and Leiss, M. Predation risk perception and food scarcity induce alterations of life cycle traits of the mosquito Culex pipiens. Ecological Entomology, 2007, 32, 405-410.
- Roberts, D.M. Predator feeding vibrations encourage mosquito larvae to shorten their development and so become smaller adults. Ecological Entomology, 2018, 43, 534-537. DOI: 10.1111/een.12519.
- Juliano, S.A. and Gravel, M.E. Predation and the evolution of prey behavior: an experiment with tree hole mosquitoes. Behavioural Ecology, 2002, 13, 301-311.
- Awasthi, A.K., Molinero, J.C., Wu, C.H., Tsai, K.H., King, C.C. and Hwang, J.S. Behavioral changes in mosquito larvae induced by copepod predation. Hydrobiologia, 2015, 749, 113-123.
- Gimonneau, G, Pombi, M., Dabiré, R.K., Diabaté, A., Morand, S. and Simard, F. Behavioural responses of Anopheles gambiae sensu stricto M and S molecular form larvae to an aquatic predator in Burkino Faso. Parasites & Vectors, 2012, 5, 1-11.
- Dalesman, S., Rundle, S.D., Coleman, R.A. and Cotton, P.A. Cue association and antipredator behaviour in a pulmonate snail, Lymnaea stagnalis. Animal Behaviour, 2006, 71,789-797.
References
Griffin, L.F. and Knight, J.M. A review of the role of fish as biological control agents of disease vector mosquitoes in mangrove forests; reducing human health risks while reducing environmental risk. Wetlands Ecological Management, 2012, 20, 243-252.
Roberts, D.M. Mosquito larvae change their feeding behavior in response to kairomones from some predators. Journal of Medical Entomology, 2014, 51, 368-374.
Chivers, D.P., Wiseden, B.D. and Smith, R.J.F. Damselfly larvae learn to recognise predators from chemical cues in the predator’s diet. Animal Behaviour, 1996, 52, 315-320.
Hopper, K.R. Flexible antipredator behavior in a dragonfly species that coexists with different predator types. Oikos, 2001, 93, 470-476.
Stoks, R.M., McPeek, M.A. and Mitchell, J. L. Evolution of prey behavior in response to changes in predation regime: damselflies in fish and dragonfly lakes. Evolution, 2003, 57,
-585.
Sih, A. Antipredator responses and the perception of danger by mosquito larvae. Ecology, 1986, 67, 434-441.
Kesavaraju, B., and Juliano, S.A. Differential behavioral responses to water-borne cues to predation in two-container-dwelling mosquitoes. Annals of the Entomological Society of America, 2004, 97, 194-201.
Takahara, T., Kohmatsu, Y., Maruyama, A., Doi, H., Yamanaka, H. and Yamaoka, R. Inducible defense behavior of an anuran tadpole: cue-detection range and cue types used 10 against predators. Behavioural Ecology, 2012, 23, 863-868.
Ferrari, M.C.O., Wisenden, B.D. and Chivers, D.P. Chemical ecology of predator-prey interactions in aquatic ecosystems: a review and prospectus. Canadian Journal of Zoology, 2010, 88, 698-724.
Ferrari, M.C.O., Messier, F. and Chivers, D.P. Threat-sensitive learning of predators by larval mosquitoes Culex restuans. Behavioural Ecology and Sociobiology, 2007, 62, 1079-1083.
Roberts, D.M. Responses of three species of mosquito larvae to the presence of predatory dragonfly and damselfly larvae. Entomologia Experimentalis et Applicata, 2012, 145, 23-29.
Angelon, K.A. and Petranka, J.W. Chemicals of predatory mosquito fish Gambusia affinis in fluence selection of oviposition site by Culex mosquitoes. Journal of Chemical Ecology, 2002, 28, 797-806.
Walton, W.E., Van Dam, R.A. and Popko, D.A. Ovipositional responses of two Culex (Diptera: Culicidae) species to larvivorous fish. Journal of Medical Entomology, 2009, 46, 1338-1343.
Silberbush, A. and Blaustein, L. Mosquito females quantify risk of predation to their progeny when selecting an oviposition site. Functional Ecology, 2011, 25, 1091-1095.
Why, A.M., Lara, J.R. and Walton, W.E. Oviposition of Culex tarsalis (Diptera: Culicidae to waters from conspecific larvae subject to crowding, confinement, starvation, or infection. Journal of Medical Entomology, 2016, 53, 1093-1099.
Werner, E.E. and Anholt, B.R. Ecological consequences of the trade-off between growth and mortality rates mediated by foraging activity. American Naturalist, 1993, 142, 242-11272.
Ferrari, M.C.O., Messier, F. and Chivers, D.P. Variable predation risk and the dynamic nature of mosquito antipredator responses to chemical alarm cues. Chemoecology, 2008, 17, 223-229.
Knight, T.M., Chase, J.M., Goss, C.W. and Knight, J.J. Effects of interspecific competition, predation, and their interaction on survival and development time of immature Anopheles quadrimaculatus. Journal of Vector Ecology, 2004, 29, 277-284.
Beketov, M.A. and Leiss, M. Predation risk perception and food scarcity induce alterations of life cycle traits of the mosquito Culex pipiens. Ecological Entomology, 2007, 32, 405-410.
Roberts, D.M. Predator feeding vibrations encourage mosquito larvae to shorten their development and so become smaller adults. Ecological Entomology, 2018, 43, 534-537. DOI: 10.1111/een.12519.
Juliano, S.A. and Gravel, M.E. Predation and the evolution of prey behavior: an experiment with tree hole mosquitoes. Behavioural Ecology, 2002, 13, 301-311.
Awasthi, A.K., Molinero, J.C., Wu, C.H., Tsai, K.H., King, C.C. and Hwang, J.S. Behavioral changes in mosquito larvae induced by copepod predation. Hydrobiologia, 2015, 749, 113-123.
Gimonneau, G, Pombi, M., Dabiré, R.K., Diabaté, A., Morand, S. and Simard, F. Behavioural responses of Anopheles gambiae sensu stricto M and S molecular form larvae to an aquatic predator in Burkino Faso. Parasites & Vectors, 2012, 5, 1-11.
Dalesman, S., Rundle, S.D., Coleman, R.A. and Cotton, P.A. Cue association and antipredator behaviour in a pulmonate snail, Lymnaea stagnalis. Animal Behaviour, 2006, 71,789-797.