Abstract
Mosquito and predatory larvae often share the same habitat. Predators may influence mosquito prey populations through both lethal effect and non-lethal pathways. A series of experimental manipulations were used to distinguish between lethal (density-mediated interaction) and non-lethal (trait-mediated interaction) effects in a model system comprised of invasive prey mosquito, Aedes aegypti, and a predatory mosquito Toxorhynchites rutilus. Treatments with predators present or manipulations mimicking daily mortality (density reduction) reduced developmental time and recruitment to the adult stage. Daily records of adult survival of A. aegypti showed that exposure to predators during the juvenile stage shortened the lifespan of adults. This was also observed in treatments, where A. aegypti were replaced at the rate of consumption by T. rutilus. In contrast, numerical reductions in A. aegypti that mimicked daily rate of predation led to adults with the longest lifespan. These observations suggest strong effects of density and trait-mediated interactions in the influence of predators on mosquito biology relevant to their ability to transmit pathogens. These results have potentially important implications for disease control strategies. The primary approach to reduce risk of mosquito-borne diseases is through population reduction of the vectors. We show an unanticipated benefit of biological control by predation for the control of juvenile stages of mosquitoes. Specifically, mosquitoes that are exposed to predators but survive to adulthood will have compromised life expectancy, a key parameter in determining risk of disease transmission.
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References
Abrams PA (2007) Defining and measuring the impact of dynamic traits on interspecific interactions. Ecology 88(10):2555–2562. https://doi.org/10.1890/06-1381.1
Alto BW, Griswold MW, Lounibos LP (2005) Habitat complexity and sex-dependent predation of mosquito larvae in containers. Oecologia 146:300–310. https://doi.org/10.1007/s00442-005-0198-x
Alto BW, Malicoate J, Elliott SM, Taylor J (2012) Demographic consequences of predators on prey: trait and density mediated effects on mosquito larvae in containers. PLoS One 7(11):e45785. https://doi.org/10.1371/journal.pone.0045785
Babbitt KJ, Tanner GW (1998) Effects of cover and predator size on survival and development of Rana utricularia tadpoles. Oecologia 114:258–262. https://doi.org/10.1007/s004420050444
Ball SL, Baker RL (1996) Predator-induced life-history changes: anti-predator behavior costs or facultative life history shifts. Ecology 77:1116–1124. https://doi.org/10.2307/2265580
Barrera R, Amador M, Clark GC (2006) Ecological factors influencing Aedes aegypti (Diptera: Culicidae) productivity in artificial containers in Salinas, Puerto Rico. J Med Entomol 43:484–492
Bedhomme S, Agnew P, Sidobre C, Michalakis Y (2003) Sex-specific reaction norms to intraspecific larval competition in the mosquito Aedes aegypti. J Evol Biol 16:721–730
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(4):405–410. https://doi.org/10.1111/j.1365-2311.2007.00889.x
Benard MF (2004) Predator-induced phenotypic plasticity in organisms with complex life histories. Annu Rev Ecol Evol Syst 35:651–673. https://doi.org/10.1146/annurev.ecolsys.35.021004.112426
Briegel H, Knüsel I, Timmermann SE (2000) Aedes aegypti: size, reserves, survival, and flight potential. J Vector Ecol 26(1):21–31
Cain AJ, Sheppard PM (1952) The effects of natural selection on body colour in the land snail Cepaea nemoralis. Heredity 6(2):217–231. https://doi.org/10.1038/hdy.1952.22
Caltagirone LE (1981) Landmark examples in classical biological control. Annu Rev Entomol 26(1):213–232. https://doi.org/10.1146/annurev.en.26.010181.001241
Cook PE, McMeniman CJ, O’Neill SL (2008) Modifying insect population age structure to control vector-borne disease. In: Aksoy S (ed) Transgenesis and the management of vector-borne disease. Springer, New York, pp 126–140
Corbet PS, Griffiths A (1963) Observations on the aquatic stages of two species of Toxorhynchites in Uganda. Proc R Entomol Soc A 38:125–135. https://doi.org/10.1111/j.1365-3032.1963.tb00767.x
Costanzo S, Muturi EJ, Alto BW (2011) Trait-mediated effects of predation across life-history stages in container mosquitoes. Ecol Entomol 36:605–615. https://doi.org/10.1111/j.1365-2311.2011.01302.x
Creel S, Christianson D, Liley S, Winnie JA (2007) Predation risk affects reproductive physiology and demography of elk. Science 315(5814):960. https://doi.org/10.1126/science.1135918
Daugherty MP, Alto BW, Juliano SA (2000) Invertebrate carcasses as a resource for competing Aedes albopictus and Aedes aegypti (Diptera: Culicidae). J Med Entomol 37(3):364–372
Fox LR (1975) Cannibalism in natural populations. Ann Rev Ecol Syst 6(1):87–106. https://doi.org/10.1146/annurev.es.06.110175.000511
Gerling D (1992) Approaches to the biological control of whiteflies. Fla Entomol 75:446–456. https://doi.org/10.2307/3496126
Gerling D, Alomar Ò, Arnò J (2001) Biological control of Bemisia tabaci using predators and parasitoids. Crop Prot 20(9):779–799. https://doi.org/10.1016/S0261-2194(01)00111-9
Grill CP, Juliano SA (1996) Predicting species interactions based on behavior: predation and competition in container-dwelling mosquitoes. J Anim Ecol 65:63–76. https://doi.org/10.2307/5700
Gurevitch J, Morrison JA, Hedges LV (2000) The interaction between competition and predation: a meta-analysis of field experiments. Am Nat 155:435–453. https://doi.org/10.1086/303337
Iturbe-Ormaetxe I, WalkerT O’Neill SL (2011) Wolbachia and the biological control of mosquito-borne disease. EMBO Rep 12(6):508–518. https://doi.org/10.1038/embor.2011.84
Juliano SA, Gravel ME (2002) Predation and the evolution of prey behavior: an experiment with tree hole mosquitoes. Behav Ecol 13:301–311. https://doi.org/10.1093/beheco/13.3.301
Kohler SL, McPeek MA (1989) Predation risk and the foraging behavior of competing stream insects. Ecology 70:1811–1825. https://doi.org/10.2307/1938114
Laurila A, Kujasalo J, Ranta E (1998) Predator-induced changes in life history in two anuran tadpoles: effects of predator diet. Oikos. https://doi.org/10.2307/3546842
Lounibos LP (1985) Interactions influencing production of treehole mosquitoes in south Florida. In: Lounibos LP, Rey J, Frank JH (eds) Ecology of mosquitoes: Proceedings of a workshop Florida Medical Entomology Laboratory, Vero Beach, Florida, USA, pp 65–77
Lounibos LP, Nishimura N, Escher RL (1993) Fitness of a treehole mosquito: influences of food type and predation. Oikos 66:114–118
Matz C, Kjelleberg S (2005) Off the hook—how bacteria survive protozoan grazing. Trends Microbiol 13:302–307. https://doi.org/10.1016/j.tim.2005.05.009
Mayntz D, Toft S (2006) Nutritional value of cannibalism and the role of starvation and nutrient imbalance for cannibalistic tendencies in a generalist predator. J Anim Ecol 75(1):288–297. https://doi.org/10.1111/j.1365-2656.2006.01046.x
McCauley SJ, Rowe L, Fortin MJ (2011) The deadly effects of “nonlethal” predators. Ecology 92:2043–2048. https://doi.org/10.1890/11-0455.1
McCollum SA, Leimberger JD (1997) Predator-induced morphological changes in an amphibian: predation by dragonflies affects tadpole shape and color. Oecologia 109(4):615–621. https://doi.org/10.1007/s004420050124
Merritt RW, Dadd RH, Walker ED (1992) Feeding behavior, natural food, and nutritional relationships of larval mosquitoes. Ann Rev Entomol 37:349–376
Morin PJ (1983) Predation, competition, and the composition of larval anuran guilds. Ecol Monogr 53(2):119–138. https://doi.org/10.2307/1942491
Nicieza AG (2000) Interacting effects of predation risk and food availability on larval anuran behaviour and development. Oecologia 123(4):497–505. https://doi.org/10.1007/s004420000343
Nylin S, Gotthard K (1998) Plasticity in life-history traits. Annu Rev Entomol 43(1):63–83
Pechenik JA (2006) Larval experience and latent effects—metamorphosis is not a new beginning. Integr Comp Biol 46(3):323–333. https://doi.org/10.1093/icb/icj028
Peckarsky BL (1982) Aquatic insect predator–prey relations. Bioscience 32(4):261–266. https://doi.org/10.2307/1308532
Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology 86(2):501–509. https://doi.org/10.1890/04-0719
Rasgon JL, Styer LM, Scott TW (2003) Wolbachia-induced mortality as a mechanism to modulate pathogen transmission by vector arthropods. J Med Entomol 40:125–132. https://doi.org/10.1603/0022-2585-40.2.125
Relyea RA (2000) Trait-mediated indirect effects in larval anurans: reversing competition with the threat of predation. Ecology 81(8):2278–2289. https://doi.org/10.1890/0012-9658(2000)081[2278:TMIEIL]2.0.CO;2
Reznick DN, Ghalambor CK (2001) The population ecology of contemporary adaptations: what empirical studies reveal about the conditions that promote adaptive evolution. Genetica 112(1):183–198. https://doi.org/10.1023/A:1013352109042
Reznick DN, Butler MJ IV, Rodd FH, Ross P (1996) Life-history evolution in guppies (Poecilia reticulate) 6. Differential mortality as a mechanism for natural selection. Evolution 50:1651–1660. https://doi.org/10.2307/2410901
Reznick DN, Butler MJ IV, Rodd H (2001) Life-history evolution in guppies. VII. The comparative ecology of high- and low-predation environments. Am Nat 157:126–140. https://doi.org/10.1086/318627
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43(1):223–225. https://doi.org/10.2307/2409177
Roux O, Vantaux A, Roche B, Yameogo KB, Dabiré KR, Diabaté A, Simard F, Lefevre T (2015) Evidence for carry-over effects of predator exposure on pathogen transmission potential. Proc R Soc B 282(1821):20152430. https://doi.org/10.1098/rspb.2015.2430
Sailer RI (1971) Invertebrate predators. USDA Forest Service, Res. Paper NE-195:32-44
Scheiner SM (2001) MANOVA: multiple response variables and multispecies interactions. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments, 2nd edn. Oxford University Press, Oxford, pp 99–115
Skelly DK, Werner EE (1990) Behavioral and life-historical responses of larval American toads to an odonate predator. Ecology 71(6):2313–2322. https://doi.org/10.2307/1938642
Steffan WA, Evenhuis NL (1981) Biology of Toxorhynchites. Annu Rev Entomol 26(1):159–181
Stoks R, De Block M, Slos S, Doorslaer WV, Rolff J (2006) Time constraints mediate predator-induced plasticity in immune function, condition, and life history. Ecology 87:809–815. https://doi.org/10.1890/0012-9658(2006)87[809:TCMPPI]2.0.CO;2
Tonn WM, Paszkowski CA, Holopainen IJ (1992) Piscivory and recruitment: mechanisms structuring prey populations in small lakes. Ecology 73(3):951–958. https://doi.org/10.2307/1940171
Tun-Lin W, Burkot TR, Kay BH (2000) Effects of temperature and larval diet on development rates and survival of the dengue vector Aedes aegypti in north Queensland, Australia. Med Vet Entomol 14:31–37
van den Bosch R (1975) Biological control of insects by predators and parasites. Environ Lett 8(1):5–21. https://doi.org/10.1080/00139307509435833
van Uitregt VO, Hurst TP, Wilson RS (2012) Reduced size and starvation resistance in adult mosquitoes, Aedes notoscriptus, exposed to predation cures as larvae. J Anim Biol 81:108–115. https://doi.org/10.1111/j.1365-2656.2011.01880.x
Walsh MR, Reznick DN (2009) Phenotypic diversification across an environmental gradient: a role for predators and resource availability on the evolution of life histories. Evolution 63(12):3201–3213. https://doi.org/10.1111/j.1558-5646.2009.00785.x
Werner EE (1991) Nonlethal effects of a predator on competitive interactions between two anuran larvae. Ecology 72(5):1709–1720. https://doi.org/10.2307/1940970
Werner EE, Gilliam JF, Hall DJ, Mittelbach GG (1983) An experimental test of the effects of predation risk on habitat use in fish. Ecology 64:1540–1548. https://doi.org/10.2307/1937508
Yee DA, Kesavaraju B, Juliano SA (2007) Direct and indirect effects of animal detritus on growth, survival, and mass of invasive container mosquito Aedes albopictus (Diptera: Culicidae). J Med Entomol 44(4):580–588
Acknowledgements
We thank Sheila O’Connell for assistance in establishing a colony of Toxorhynchites rutilus at the Florida Medical Entomology Laboratory and Steven Juliano for useful communications about the experimental protocols used in the treatment manipulations.
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BWA conceived and designed the experiments. SB performed the experiments. SB and BWA analyzed the data. SB and BWA wrote the manuscript.
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Communicated by Jill Lancaster.
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Bellamy, S.K., Alto, B.W. Mosquito responses to trait- and density-mediated interactions of predation. Oecologia 187, 233–243 (2018). https://doi.org/10.1007/s00442-018-4107-5
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DOI: https://doi.org/10.1007/s00442-018-4107-5