Abstract
Intraguild predation (IGP) is a type of biological interaction involving the killing and consuming of competing species that exploit similar and often limited resources. This phenomenon is widespread among a great variety of taxonomic groups and has already been reported for mosquito (Diptera: Culicidae) larvae. Moreover, the larvae of certain mosquito species of the tribe Sabethini have evolved modified mouthparts ending in rigid apical structures signaling their capacity to be effective intraguild predators. We assumed that IGP confers a selective advantage under severe competitive conditions by both providing an immediate energetic gain and reducing potential competition. Because potential competition is likely to increase with decreasing habitat size, we hypothesized that the proportion of species with modified mouthparts would increase in smaller aquatic habitats. We tested this hypothesis by examining the mosquito species naturally associated with phytotelmata of decreasing sizes in French Guiana. We show that the degree of specialization in mosquito-phytotelm associations is high, suggesting a long coevolutive process. Indeed, short-term interaction experiments confirmed that species with modified mouthparts are able to prey upon similarly-sized intraguild prey and are, thus, effective intraguild predators. In addition, these species are larger and associated with smaller phytotelmata than those with typical mouthparts. Moreover, below a certain threshold of phytotelm size, only species with modified mouthparts were present. These results show that IGP confers a selective advantage under severe competitive conditions and results from the coadaptation of mosquito species to their specific phytotelm habitat. The presence of functionally analogous structures in different mosquito genera also implies that IGP has emerged from convergent evolution in small phytotelmata.
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References
Arim M, Marquet PA (2004) Intraguild predation: a widespread interaction related to species biology. Ecol Lett 7(7):557–564
Blüthgen N, Menzel F, Blüthgen N (2006) Measuring specialization in species interaction networks. BMC Ecol 6(1):9
Brown JL, Twomey E, Morales V, Summers K (2008) Phytotelm size in relation to parental care and mating strategies in two species of Peruvian poison frogs. Behaviour 145(9):1139–1165
Church SC, Sherratt TN (1996) The selective advantages of cannibalism in a Neotropical mosquito. Behav Ecol Sociobiol 39(2):117–123
Clements AN (1990) The biology of mosquitoes: development, nutrition and reproduction, vol 1. Chapman & Hall, London
Dézerald O, Céréghino R, Corbara B, Dejean A, Leroy C (2015) Temperature: diet interactions affect survival through foraging behavior in a bromeliad-dwelling predator. Biotropica 47(5):569–578
Dunne JA, Williams RJ, Martinez ND (2002) Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecol Lett 5(4):558–567
Dyar HG (1928) The mosquitoes of the Americas. Carnegie Institution, Washington
Edgerly JS, Willey MS, Livdahl T (1999) Intraguild predation among larval treehole mosquitoes, Aedes albopictus, Ae. aegypti, and Ae. triseriatus (Diptera: Culicidae), in laboratory microcosms. J Med Entomol 36(3):394–399
Fisher RA, Corbet AS, Williams CB (1943) The relation between the number of species and the number of individuals in a random sample of an animal population. J Anim Ecol 12(1):42–58
Funk V, Hollowell T, Berry P, Kelloff C, Alexander SN (2007) Checklist of the plants of the Guiana Shield (Venezuela: Amazonas, Bolivar, Delta Amacuro; Guyana, Surinam, French Guiana). Smithsonian Institution, Contr US Natl Herb, vol 55, pp 1–584
Gaffigan T, Pecor J (1997) Collecting, rearing, mounting and shipping mosquitoes. http://wrbu.si.edu/techniques.html
Harbach RE, Peyton EL (1993) Morphology and evolution of the larval maxilla and its importance in the classification of the Sabethini (Diptera: Culicidae). Mosq Syst 25(1):1–17
Judd DD (1996) Review of the systematic and phylogenetic relationships of the Sabethini (Diptera: Culicidae). Syst Entomol 21(2):129–150
Juliano SA (2009) Species interactions among larval mosquitoes: context dependence across habitat gradients. Annu Rev Entomol 54(1):37–56
Kitching RL (2000) Food webs and container habitats: the natural history and ecology of phytotelmata. Cambridge University Press, Cambridge
Knight KL, Harbach RE, Chang MCC (1977) Maxillae of fourth stage mosquito larvae (Diptera: Culicidae). Mosq Syst 9(4):455–477
Lounibos LP (1983) Behavioral convergences among fruit-husk mosquitoes. Fla Entomol 66(1):32–41
Merritt RW, Dadd RH, Walker ED (1992) Feeding behavior, natural food, and nutritional relationships of larval mosquitoes. Annu Rev Entomol 37(1):349–374
Mogi M, Sembel DT (1996) Predator-prey system structure in patchy and ephemeral phytotelmata: aquatic communities in small aroid axils. Res Popul Ecol 38(1):95–103
Motta MA, Lourenço-de-Oliveira R (2000) The subgenus Dendromyia Theobald: a review with redescriptions of four species (Diptera: Culicidae). Mem Inst Oswaldo Cruz 95(5):649–683
Muturi EJ, Kim CH, Jacob B, Murphy S, Novak RJ (2010) Interspecies predation between Anopheles gambiae ss and Culex quinquefasciatus larvae. J Med Entomol 47(2):287–290
Navarro JC, Liria J, Pinango H, Barrera R (2007) Biogeographic area relationships in Venezuela: a Parsimony analysis of Culicidae–Phytotelmata distribution in National Parks. Zootaxa 1547(1):1–19
Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of intraguild predation: potential competitors that eat each other. Annu Rev Ecol Syst 20:297–330
R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for statistical computing, Vienna. http://www.R-project.org/
Reichstein B, Schröder A, Persson L, De Roos AM (2013) Habitat complexity does not promote coexistence in a size-structured intraguild predation system. J Anim Ecol 82(1):55–63
Schröder A, Nilsson KA, Persson L, van Kooten T, Reichstein B (2009) Invasion success depends on invader body size in a size-structured mixed predation–competition community. J Anim Ecol 78(6):1152–1162
Summers K, McKeon CS (2004) The evolutionary ecology of phytotelmata use in Neotropical poison frogs. Misc Publ Mus Zool Univ Mich 193:55–73
Sunahara T, Ishizaka K, Mogi M (2002) Habitat size: a factor determining the opportunity for encounters between mosquito larvae and aquatic predators. J Vector Ecol 27(1):8–20
Talaga S, Murienne J, Dejean A, Leroy C (2015a) Online database for mosquito (Diptera, Culicidae) occurrence records in French Guiana. ZooKeys 532:107–115
Talaga S, Dejean A, Carinci R, Gaborit P, Dusfour I, Girod R (2015b) Updated checklist of the mosquitoes (Diptera: Culicidae) of French Guiana. J Med Entomol 52(5):770–782
Wilbur HM (1980) Complex life cycles. Annu Rev Ecol Syst 11:67–93
Zavortink TJ (1979) Mosquito studies (Diptera, Culicidae) XXXV. The new sabethine genus Johnbelkinia and a preliminary reclassification of the composite genus Trichoprosopon. Contrib Am Entomol Inst 17(1):1–61
Acknowledgments
We are grateful to Pascal Petronelli for identifying the phytotelm plant species, as well as to Hector Rodriguez, Marceau Minot and Clémence Mouza for field assistance. We would also like to thank Andrea Yockey-Dejean for proofreading the manuscript. Financial support was provided by the French Agence Nationale de la Recherche through an “Investissement d’Avenir” (Grant ANR-10-LABX-25-01) and the Rainwebs project (Grant ANR-12-BSV7-0022-01). ST was funded by a Ph.D. fellowship from the Université Antilles-Guyane.
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Talaga, S., Leroy, C., Céréghino, R. et al. Convergent evolution of intraguild predation in phytotelm-inhabiting mosquitoes. Evol Ecol 30, 1133–1147 (2016). https://doi.org/10.1007/s10682-016-9862-3
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DOI: https://doi.org/10.1007/s10682-016-9862-3