Log in

Predation resistance does not trade off with competitive ability in early-colonizing mosquitoes

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

Abstract

The tradeoff between colonization and competitive ability has been proposed as a mechanism for ecological succession, and this tradeoff has been demonstrated in multiple successional communities. The tradeoff between competitive ability and predation resistance is also a widely-described phenomenon; however, this tradeoff is not usually postulated as a cause of ecological succession. Early successional species that arrive before predator colonization could be either (1) less vulnerable to predation than their successors, by virtue of being poor competitors (direct competition-predation tradeoff); or (2) equally or more vulnerable to predation, because they normally colonize ahead of predators in succession and therefore are not evolutionarily adapted to avoid predators that they rarely encounter (no competition–predation tradeoff). To test these alternative hypotheses, we established water-filled containers in an oak–hickory forest. We allowed half of the containers to be naturally colonized by early-successional Culex mosquitoes, mid-successional Aedes mosquitoes, and the mosquito predator Toxorhynchites rutilus. In the other half of the containers, we prevented Aedes colonization via systematic removal of Aedes eggs, but allowed Culex and T. rutilus to colonize. The numbers of mature Culex larvae and pupae, and later the total number of Culex, were significantly greater in containers where Aedes had been removed, which suggests that Culex are competitively suppressed by Aedes. Toxorhynchites rutilus abundance and colonization rate were unaffected by the removal of Aedes, and densities of both Culex and Aedes decreased significantly with T. rutilus abundance in both treatments. In-laboratory bioassays showed that Culex were significantly more vulnerable to predation by T. rutilus than were Aedes. These data are consistent with the hypothesis that Culex and Aedes demonstrate a direct colonization–competition tradeoff, and are inconsistent with the hypothesis of a direct competition–predation tradeoff.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alto BW, Kesavaraju B, Juliano SA, Lounibos LP (2009) Stage-dependent predation on competitors: consequences for the outcome of a mosquito invasion. J Anim Ecol 78:928–936

    Article  PubMed  Google Scholar 

  • Amalraj DD, Das PK (1996) Frequency-dependent prey selection by larvae of Toxorhynchites splendens (Diptera: Culicidae). Bull Entomol Res 86:633–639

    Article  Google Scholar 

  • Angelon KA, Petranka JW (2002) Chemicals of predatory mosquitofish (Gambusia affinis) influence selection of oviposition site by Culex mosquitoes. J Chem Ecol 28:797–806

    Article  PubMed  CAS  Google Scholar 

  • Bates M (1949) The natural history of mosquitoes. The MacMillan Company, New York

    Google Scholar 

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

    Google Scholar 

  • Bergelson JM (1985) A mechanistic interpretation of prey selection by Anax junius larvae (Odonata: Aeschnidae). Ecology 66:1699–1705

    Article  Google Scholar 

  • Blaustein L, Kiflawi M, Eitam A, Mangel M, Cohen J (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

    Article  PubMed  Google Scholar 

  • Bradshaw WE, Holzapfel CM (1983) Predator-mediated, non-equilibrium coexistence of tree-hole mosquitoes in southeastern North America. Oecologia 57:239–256

    Article  Google Scholar 

  • Bradshaw WE, Holzapfel CM (1988) Drought and the organization of tree-hole mosquito communities. Oecologia 74:507–514

    Article  Google Scholar 

  • Cadotte MC, Mai DV, Jantz S, Collins MD, Keele M, Drake JA (2006) On testing the competition-colonization trade-off in a multispecies assemblage. Am Nat 168:704–709

    Article  PubMed  Google Scholar 

  • Carrieri M, Bacchi M, Bellini R, Maini S (2003) On the competition occurring between Aedes albopictus and Culex pipiens (Diptera: Culicidae) in Italy. Environ Entomol 32:1313–1321

    Article  Google Scholar 

  • Chase JM, Leibold MA (2003) Ecological niches: linking classical and contemporary approaches, 1st edn. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Connell JH, Slayter RO (1977) Mechanisms of succession in natural communities and their role in community stability and organization. Am Nat 111:1119–1144

    Article  Google Scholar 

  • Costanzo KS, Mormann K, Juliano SA (2005a) Asymmetrical competition and patterns of abundance of Aedes albopictus and Culex pipiens (Diptera: Culicidae). J Med Entomol 42:559–570

    Article  PubMed  Google Scholar 

  • Costanzo KS, Kesavaraju B, Juliano SA (2005b) Condition-specific competition in container mosquitoes: the role of non-competing life-history stages. Ecology 86:3289–3295

    Article  PubMed  Google Scholar 

  • Dodge HR (1964) Larval chaetotaxy and notes on the biology of Toxorhynchites rutilus septentrionalis. Ann Entomol Soc Am 57:46–53

    Google Scholar 

  • Elliot JM (2004) Prey switching in four species of carnivorous stoneflies. Freshw Biol 49:709–720

    Article  Google Scholar 

  • Farajollahi A, Kesavaraju B, Nelder MP, Crans SC, Gaugler R (2009) An unusual larval collection and survival of Orthopodomyia signifera in the presence of the predator Toxorhynchites rutilus septentrionalis. J Am Mosq Control Assoc 25:370–373

    Article  PubMed  Google Scholar 

  • Gleeson SK, Tilman D (1994) Plant allocation, growth rate, and successional status. Funct Ecol 8:543–550

    Article  Google Scholar 

  • Godoy O, Valladares F, Castro-Diez P (2011) Multispecies comparison reveals that invasive and native plants differ in their traits but not in their plasticity. Funct Ecol 25:1248–1259

    Article  Google Scholar 

  • Griswold MW, Lounibos LP (2006) Predator identity and additive effects in a treehole community. Ecology 87:987–995

    Article  PubMed  Google Scholar 

  • Higgs P, Fox BJ (1993) Interspecific competition: a mechanism for rodent succession after fire heathland. Aust J Ecol 18:193–201

    Article  Google Scholar 

  • Jones CJ, Schreiber ET (1994a) Color and height affects oviposition site preferences of in wet Toxorhynchites splendens and Toxorhynchites rutilus rutilus (Diptera: Culicidae) in the laboratory. Environ Entomol 23:130–135

    CAS  Google Scholar 

  • Jones CJ, Schreiber ET (1994b) The carnivores, Toxorhynchites. Wing Beats 5:4

    Google Scholar 

  • Juliano SA (2007) Population dynamics. J Am Mosq Control Assoc 23(2 Suppl):265–275

    Article  PubMed  Google Scholar 

  • Juliano SA (2009) Species interactions among larval mosquitoes: Context dependence across habitat gradients. Annu Rev Entomol 54:37–56

    Article  PubMed  CAS  Google Scholar 

  • Kennedy PG, Higgins LM, Rogers RH, Weber MG (2011) Colonization-competition tradeoffs as a mechanism driving successional dynamics in ectomycorrhizal fungal communities. PLoS ONE 6:1–10

    Google Scholar 

  • Kesavaraju B, Damal K, Juliano SA (2008) Do natural container habitats impede invader dominance? Predator-mediated coexistence of invasive and native container-dwelling mosquitoes. Oecologia 155:631–639

    Article  PubMed  Google Scholar 

  • Leibold MA (1996) A graphical model of keystone predators in food webs: trophic regulation of abundance, incidence, and diversity patterns in communities. Am Nat 147:784–812

    Article  Google Scholar 

  • Linley JR (1995) Behavior on approach to surface prey by larvae of Toxorhynchites amboinensis and T. brevipalpis (Diptera: Culicidae). J Med Entomol 32:53–65

    PubMed  CAS  Google Scholar 

  • Linley JR, Darling K (1993) Search behavior associated with egg cannibalism in Toxorhynchites amboinensis and Toxorhynchites rutilus rutilus (Diptera: Culicidae). J Med Entomol 30:561–570

    PubMed  CAS  Google Scholar 

  • McCook LJ (1994) Understanding ecological community succession—casual-models and theories, a review. Vegetatio 110:115–147

    Article  Google Scholar 

  • Menge BA (1976) Organization of the New England rocky intertidal community: role of predation, competition, and environmental heterogeneity. Ecol Monogr 46:355–393

    Article  Google Scholar 

  • Murrell EG, Juliano SA (2012) Competitive abilities in experimental microcosms are accurately predicted by a demographic index for R*. PLoS ONE 7(9):e43458. doi:10.1371/journal.pone.0043458

    Article  PubMed  CAS  Google Scholar 

  • Pinder JE III (1975) Effects of species removal on an old-field plant community. Ecology 56:747–751

    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

    Article  PubMed  Google Scholar 

  • Rey JR, Nishimura N, Wagner B, Braks MAH, O’Connell SM (2006) Habitat segregation of mosquito arbovirus vectors in south Florida. J Med Entomol 43:1134–1141

    Article  PubMed  Google Scholar 

  • Rueda LM, Patel KJ, Axtell RC, Stinner RE (1990) Temperature-dependent development and survival rates of Culex quinquefasciatus and Aedes aegypti (Diptera: Culicidae). J Med Entomol 25:892–898

    Google Scholar 

  • SAS Institute (1990) SAS/Stat User’s Guide. Version 6, 4th edn. SAS Institute, Cary, NC

  • Tilman D (1994) Competition and biodiversity in spatially structured habitats. Ecology 75:2–16

    Google Scholar 

  • Tirok K, Gaedke U (2010) Internally driven alternation of functional traits in a multispecies predator-prey system. Ecology 91:1748–1762

    Article  PubMed  Google Scholar 

  • Van Dam AR, Walton WE (2008) The effects of predatory fish exudates on the ovipositional behavior of three mosquito species: Culex quinquefaciatus, Aedes aegypti and Culex tarsalis. Med Vet Entomol 22:399–404

    Article  PubMed  Google Scholar 

  • Viola DV, Mordecai EA, Jaramillo AG, Sistla SA, Albertson LK, Gosnell JS, Carinale BJ, Levine JM (2010) Competition-defense tradeoffs and the maintenance of plant diversity. Proc Natl Acad Sci USA 107:17217–17222

    Article  PubMed  CAS  Google Scholar 

  • Wellborn GA, Skelly DK, Werner EE (1996) Mechanisms creating community structure across a freshwater habitat gradient. Annu Rev Ecol Syst 27:337–363

    Article  Google Scholar 

  • Wissinger SA, Whiteman HH, Sparks GB, Rouse GL, Brown WS (1999) Foraging trade-offs along a predator-permanence gradient in subalpine wetlands. Ecology 80:2102–2116

    Google Scholar 

  • Yee DA (2008) Tires as habitats for mosquitoes: a review of studies within the eastern United States. J Med Entomol 45:581–593

    Article  PubMed  Google Scholar 

  • Yee DA, Kneitel JM, Juliano SA (2010) Environmental correlates of abundances of mosquito species and stages in discarded vehicle tires. J Med Entomol 47:53–62

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank J.A. Breaux, J.M. Chase, T.L. Dickson, D. Kovcic, C.R. Stephens, and C.S. Tillman for their assistance in the field, J.M. Chase and the Tyson Research Center staff for the use of their research facilities, N. Vick for her assistance in the laboratory, A.R. Ives for his assistance with statistics, and R.C. Anderson, V.A. Borowicz, T.E. Miller, W.L. Perry, J. Shurin, and three anonymous reviewers for their comments on the manuscript. This research was funded by the Beta Lambda chapter of Phi Sigma Society, and by NIAID grant R15 AI075306-01.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ebony G. Murrell.

Additional information

Communicated by Jonathan Shurin.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 1314 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Murrell, E.G., Juliano, S.A. Predation resistance does not trade off with competitive ability in early-colonizing mosquitoes. Oecologia 173, 1033–1042 (2013). https://doi.org/10.1007/s00442-013-2674-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-013-2674-z

Keywords

Navigation