Skip to main content

Escape from Gregarine Parasites Affects the Competitive Interactions of an Invasive Mosquito

Biological Invasions volume 4, pages 283–297 (2002)Cite this article

Abstract

When a species is introduced into a new location, it may escape, at least temporarily, from its natural enemies. In field surveys, we found that when the exotic, invasive mosquito, Aedes albopictus, invades new sites, it initially experiences reduced infection by its gut parasite, Ascogregarina taiwanensis. To determine the effect of this escape from parasitism on the competitive ability of A. albopictus, we performed a laboratory competition experiment in which infected and uninfected A. albopictus larvae were reared in microcosms alone and in competition with larvae of the native mosquito, Ochlerotatus triseriatus. We analyzed the effect of parasitism by A. taiwanensis on A. albopictus performance when subjected to intra- and interspecific competition across a range of larval densities, as well as the effect of A. albopictus parasitism by A. taiwanensis on the competitive impact of A. albopictus on O. triseriatus. At a density of 30 O. triseriatus larvae, O. triseriatus survivorship was significantly reduced by the addition of 30 unifected A. albopictus, but not by addition of 30 infected A. albopictus, and not by addition of 15 A. albopictus whether infected or uninfected. Although estimated finite rate of population increase (λ') showed similar trends, and was significantly affected by treatments, no pairwise differences in rate of increase were significant. Infection by A. taiwanensis also significantly prolonged A. albopictus female development time and reduced the intraspecific competitive effect of increased density of A. albopictus, but did not affect A. albopictus survivorship, mass, or estimated finite rate of population increase. Thus, when A. albopictus escapes from this parasite as it colonizes new sites, this escape may give it a small, but significant, added competitive advantage over O. triseriatus, which may facilitate range expansion of A. albopictus and enhance A. albopictus's initial impact on resident species.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

  • Ball SL and Baker RL (1996) Predator-induced life history changes: antipredator behavior costs or facultative life history shifts? Ecology 77: 1116–1124

    Google Scholar 

  • Barrera R (1996) Competition and resistance to starvation in larvae of container-inhabiting Aedes mosquitoes. Ecological Entomology 21: 117–127

    Google Scholar 

  • Beier JC and Craig GB, Jr (1985) Gregarine parasites of mosquitoes. In: Laird M and Miles JW (eds) Integrated Mosquito Control Methodologies, Vol 2, pp 167–184. Academic Press, London

    Google Scholar 

  • Blackmore MS, Scoles GA and Craig GB, Jr (1995) Parasitism of Aedes aegypti and Ae. albopictus (Diptera: Culicidae) by Ascogregarina spp. (Apicomplexa: Lecudinidae) in Florida. Journal of Medical Entomology 32: 847–852

    PubMed  Google Scholar 

  • Centers for Disease Control (1999) US: distribution of Aedes albopictus. Available at http://www.cdc.gov./ncidod/dvbid/arbor/ albopic new.htm

  • Chen WJ and Kuo HC (1990) An investigation of Aedes albopictus infected with Ascogregarina taiwanensis. Chinese Journal of Parasitology 3: 122

    Google Scholar 

  • Chen W and Yang C (1996) Developmental synchrony of Ascogregarina taiwanensis (Apicomplexa: Lecudinidae) within Aedes albopictus (Diptera: Culicidae). Journal of Medical Entomology 33: 212–215

    PubMed  Google Scholar 

  • Clark GG, Pretula HL, Langkop CW, Martin RJ and Calisher CH (1983a) Occurrence of La Crosse (California serogroup) encephalitis viral infections in Illinois. American Journal of Tropical Medicine and Hygene 32: 838–843

    Google Scholar 

  • Clark GG, Pretula HL, Rohrer WH, Harnoff RN and Jakubowski T (1983b) Persistence of La Crosse virus (California encephalitis serogroup) in north-central Illinois. American Journal of Tropical Medicine and Hygene 32: 175–184

    Google Scholar 

  • Clausen CP (ed) (1978) Introduced Parasites and Predators of Arthropod Pests and Weeds: a World Review. Agricultural Handbook 480. US Department of Agriculture, Washington, DC

    Google Scholar 

  • Comiskey NM, Lowrie RC, Jr and Wesson DM (1999) Role of habitat components on the dynamics of Aedes albopictus (Diptera: Culicidae) fromNewOrleans. Journal of Medical Entomology 36: 313–320

    PubMed  Google Scholar 

  • Copeland RS and Craig GB, Jr (1992) Interspecific competition, parasitism, and predation affect development of Aedes hendersoni and A. triseriatus (Diptera: Culicidae) in artificial treeholes. Annals of the Entomological Society of America 85: 154–163

    Google Scholar 

  • Coulson JR and Soper RS (1989) Protocols for the introduction of biological control agents in the US. In: Kahn RP (ed) Plant Protection and Quarantine. Special Topics, Vol III, pp 1–35. CRC Press, Boca Raton, Florida

    Google Scholar 

  • Craven RB, Eliason DA, Francy DB, Reiter P, Campos EG, James WL, Smith GC, Bozzi CJ, Moore CG, Maupin GO and Monath TP (1988) Importation of Aedes albopictus species into the United States in used tires from Asia. Journal of the American Mosquito Control Association 4: 138–142

    PubMed  Google Scholar 

  • Cully JF, Jr, Streit TG and Heard PB (1992) Transmission of La Crosse virus by four strains of Aedes albopictus to and from the eastern chipmunk (Tamias striatus). Journal of the American Mosquito Control Association 8: 237–240

    PubMed  Google Scholar 

  • Drake JA, Mooney HA, di Castri F, Groves RH, Kruger FJ, Rejmánek M and Williamson M (eds) (1989) Biological Invasions: a Global Perspective. John Wiley & Sons, New York, 525 pp

    Google Scholar 

  • Edgerly JS, WilleyMS and Livdahl TP (1993) The community ecology of Aedes egg hatching: implication for a mosquito invasion. Ecological Entomology 17: 28–32

    Google Scholar 

  • Ehrlich PR (1986) Which animal will invade? In: Mooney HA and Drake JA (eds) Ecology of Biological Invasions of North America and Hawaii, pp 79–95. Springer-Verlag, New York

    Google Scholar 

  • Focks DA, Linda SB, Craig GB, Jr, Hawley WA and Pumpuni CB (1994) Aedes albopictus (Diptera: Culicidae): a statistical model of the role of temperature, photoperiod, and geography in the induction of egg diapause. Journal of Medical Entomology 31: 278–286

    PubMed  Google Scholar 

  • Fukuda T, Osborne RW and Barnard DR (1997) Parasites of the Asian tiger mosquito and other container-inhabiting mosquitoes (Diptera: Culicidae) in northern Florida. Journal of Medical Entomology 34: 226–233

    PubMed  Google Scholar 

  • Garcia JJ, Fukuda T and Becnel JJ (1994) Seasonality, prevalence and pathogenicity of the gregarine Ascogregarina taiwanensis (Apicomplexa: Lecudinidae) in mosquitoes from Florida. Journal of the American Mosquito Control Association 10: 413–418

    PubMed  Google Scholar 

  • Grill CP and Juliano SA (1996) Predicting species interactions based on behaviour: predation and competition in container-dwelling mosquitoes. Journal of Animal Ecology 65: 63–76

    Google Scholar 

  • Grimstad PR and Haramis LD (1984) Aedes triseriatus (Diptera: Culicidae) and La Crosse virus, III. Enhanced oral transmission by nutrition-deprived mosquitoes. Journal of Medical Entomology 21: 249–256

    PubMed  Google Scholar 

  • Grimstad PR, Kobayashi J, Zhang M and Craig GB, Jr (1989) Recently introduced Aedes albopictus in the United States: potential vector of La Crosse virus (Bunyaviridae: California serogroup). Journal of the American Mosquito Control Association 5: 422–427

    PubMed  Google Scholar 

  • Hawley WA (1988) The biology of Aedes albopictus. Journal of the American Mosquito Control Association 4 (Suppl): 1–39

    PubMed  Google Scholar 

  • Hawley WA, Reiter P, Copeland RS, Pumpuni CB and Craig GB, Jr (1987) Aedes albopictus in North America: probable introduction in used tires from northern Asia. Science 236: 1114–1116

    PubMed  Google Scholar 

  • Hechtel LJ and Juliano SA (1997) Effects of a predator on prey metamorphosis: plastic responses by prey or selective mortality? Ecology 78: 838–851

    Google Scholar 

  • Ho BC, Ewert A and Chew LM (1989) Interspecific competition among Aedes aegypti, Ae. albopictus, and Ae. triseriatus (Diptera: Culicidae): larval development in mixed cultures. Journal of Medical Entomology 26: 615–623

    PubMed  Google Scholar 

  • Hobbs JH, Hughes EA and Eichold BH, II (1991) Replacement of Aedes aegypti by Aedes albopictus in Mobile, Alabama. Journal of the American Mosquito Control Association 7: 488–489

    PubMed  Google Scholar 

  • Hornby JA, Moore DE, and Miller TW, Jr (1994) Aedes albopictus distribution, abundance, and colonization in Lee county, Florida, and its effect on Aedes aegypti. Journal of the American Mosquito Control Association 10: 397–402

    PubMed  Google Scholar 

  • Juliano SA (1998) Species introduction and replacement among mosquitoes: interspecific resource competition or apparent competition? Ecology 79: 255–268

    Google Scholar 

  • Juliano SA and Stoffregen TL (1994) Effects of habitat drying on size at and time to metamorphosis in the tree hole mosquito Aedes triseriatus. Oecologia 97: 369–376

    Google Scholar 

  • Kitron U, Swanson J, Crandell M, Sullivan PJ, Anderson J, Garro R, Haramis LD and Grimstad PR (1998) Introduction of Aedes albopictus into a La Crosse virus-enzootic site in Illinois. Emerging Infectious Diseases 4: 627–630

    PubMed  Google Scholar 

  • Léonard PM and Juliano SA (1995) Effect of leaf litter and density on fitness and population performance of the hole mosquito Aedes triseriatus. Ecological Entomology 20: 125–136

    Google Scholar 

  • Lien S and Levine ND (1980) Three new species of Ascocystis (Apicomplexa, Lecudinidae) from mosquitoes. Journal of Protozoology 27: 147–151

    Google Scholar 

  • Livdahl TP and Sugihara G (1984) Non-linear interactions of populations and the importance of estimating per capita rates of change. Journal of Animal Ecology 53: 573–580

    Google Scholar 

  • Livdahl TP and Willey MS (1991) Prospects for an invasion: competition between Aedes albopictus and native Aedes triseriatus. Science 253: 189–191

    PubMed  Google Scholar 

  • Lounibos LP, Nishimura N and Escher RL (1993) Fitness of a treehole mosquito: influences of food type and predation. Oikos 66: 114–118

    Google Scholar 

  • Lugo AE (1994) Maintaining an open mind on exotic species. In: Meffe GK and Carroll CR (eds) Principles of Conservation Biology, pp 218–220. Sinauer Associates, Sunderland, Massachusetts

    Google Scholar 

  • Munstermann LE and Wesson DW (1990) First record of Ascogregarina taiwanensis (Apicomplexa: Lecudinidae) in North American Aedes albopictus. Journal of the American Mosquito Control Association 6: 235–242

    PubMed  Google Scholar 

  • Nannini MA and Juliano SA(1998) Effects of the facultative predator Anopheles barberi on population performance of its prey Aedes triseriatus (Diptera Culicidae). Annals of the Entomological Society of America 91: 33–42

    Google Scholar 

  • Novak MG, Higley LG, Christianssen CA and Rowley WA (1993) Evaluating larval competition between Aedes albopictus and A. triseriatus (Diptera: Culicidae) through replacement series experiments. Environmental Entomology 22: 311–318

    Google Scholar 

  • Novak RJ and Shroyer DA (1978) Eggs of Aedes triseriatus and Ae. hendersoni: a method to stimulate optimal hatch. Mosquito News 38: 515–521

    Google Scholar 

  • O'Meara GF, Gettman AD, Evans LF, Jr and Scheel FD (1992) Invasion of cemeteries in Florida and association with Aedes aegypti. Journal of the American Mosquito Control Association 5: 1–5

    Google Scholar 

  • O'Meara GF, Evans LF, Gettman AD and Cuda JP (1995) Spread of Aedes albopictus and decline of Aedes aegypti (Diptera: Culicidae) in Florida. Journal of Medical Entomology 32: 554–562

    PubMed  Google Scholar 

  • Paulson SL and Hawley WA (1991) Effect of body size on the vector competence of field and laboratory populations of Aedes triseriatus for La Crosse virus. Journal of the American Mosquito Control Association 7: 170–175

    PubMed  Google Scholar 

  • Peacock BE, Smith JP, Gregory PG, Loyless TM, Mulrennen JA, Jr, Simmonds PR, Padgett L, Jr, Cook EK and Eddins TR (1988) Aedes albopictus in Florida. Journal of the American Mosquito Control Association 4: 362–365

    PubMed  Google Scholar 

  • Rai KS (1991) Aedes albopictus in the Americas. Annual Review of Entomology 36: 459–484

    PubMed  Google Scholar 

  • Reiter P (1998) Aedes albopictus and the world trade in used tires, 1988–1995: the shape of things to come? Journal of the American Mosquito Control Association 14: 83–94

    PubMed  Google Scholar 

  • Rosen D (1991) Forum. Newsletter, Nearctic Region, Section, International Organization of Biological Control, Summer, No. 37: 14–15

    Google Scholar 

  • SAS Institute (1995) SAS/STAT® User's Guide, Version 6, 4th edition, Vols 1 and 2. SAS Institute Inc. Cary, North Carolina

    Google Scholar 

  • Siegel JP, Novak RJ and Maddox JP (1992) Effects of Ascogregarina barretti (Eugregarinida: Lecudinidae) infection on Aedes triseriatus (Diptera: Culicidae) in Illinois. Journal of Medical Entomology 29: 968–973

    PubMed  Google Scholar 

  • Spencer JP and Olson JK (1982) Evaluation of the combined effects of methoprene and the protozoan parasite Ascogregarina culicis (Eugregarinida, Diplocystidae) on Aedes mosquitoes. Mosquito News 42: 384–390

    Google Scholar 

  • Sprenger D and Wuithiranyagool T (1986) The discovery and distribution of Aedes albopictus in Harris County, Texas. Journal of the American Mosquito Control Association 2: 217–219

    PubMed  Google Scholar 

  • Swanson J, Lancaster M, Anderson J, Crandell M, Haramis L, Grimstad P and Kitron U (2000) Overwintering and establishment of Aedes albopictus (Diptera: Culicidae) in an urban La Crosse virus enzootic site in Illinois. Journal of Medical Entomology 37: 454–460

    PubMed  Google Scholar 

  • Teng H-J and Apperson CS (2000) Development and survival of immature Aedes albopictus and Aedes triseriatus (Diptera: Culicidae) in the laboratory: effects of density, food, and competition on response to temperature. Journal of Medical Entomology 37: 40–52

    PubMed  Google Scholar 

  • Tilman D (1999) The ecological consequences of changes in biodiversity: a search for general principles. Ecology 80: 1455–1474

    Google Scholar 

  • Van Rhein SL (1999) Parasitism by Ascogregarina barretti, habitat drying, and host reproductive success in Aedes triseriatus. MS thesis, Department of Biological Sciences, Illinois State University

    Google Scholar 

  • Van Rhein SL, Flanary BE and Juliano SA (2000) Effects of habitat type and drying on Ascogregarina barretti (Eugregarinida: Lecudinidae) infection in Aedes triseriatus (Diptera: Culicidae). Journal of Medical Entomology 37: 950–956

    PubMed  Google Scholar 

  • Vavra J (1969) Lankesteria barretti n. sp. (Eugregarinida, Diplocystidae), a parasite of the mosquito Aedes triseriatus (Say) and a review of the genus Lankesteria Mingazzini. Journal of Protozoology 16: 546–570

    PubMed  Google Scholar 

  • Vitousek PM, Antonio MD, Loope LL and Westbrooks R (1996) Biological invasions as global environmental change. American Scientist 84: 468–478

    Google Scholar 

  • Walker ED, Poirier SJ and Veldman WT (1987) Effects of Ascogregarina barretti (Eugregarinida: Lecudinidae) infection on emergence success, development time, and size of Aedes triseriatus (Diptera: Culicidae) in microcosms and tires. Journal of Medical Entomology 24: 303–309

    PubMed  Google Scholar 

  • Walsh RD and Olson JK (1976) Observations on the susceptibility of certain mosquito species to infection by Lankesteria culicis (Ross). Mosquito News 36: 154–160

    Google Scholar 

  • Werner EE (1994) Ontogenetic scaling of competitive relations: sizedependent effects and responses in two anuran larvae. Ecology 75: 197–213

    Google Scholar 

  • Yeh ML, Chen CS and Liu KC (1994) Experimental infection of mosquitoes with two Ascogregarina species (Eugregarinida: Lecudinidae). Bulletin of Tung Hai University 35: 87–106

    Google Scholar 

Download references

Author information

Affiliations

  1. Behavior, Ecology, Evolution, & Systematics Section, Department of Biological Sciences, Illinois State University, Normal, IL, 61790-4120, USA

    Brianna W. Aliabadi & Steven A. Juliano

Authors
  1. Brianna W. Aliabadi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Steven A. Juliano
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Steven A. Juliano.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Aliabadi, B.W., Juliano, S.A. Escape from Gregarine Parasites Affects the Competitive Interactions of an Invasive Mosquito. Biological Invasions 4, 283–297 (2002). https://doi.org/10.1023/A:1020933705556

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1020933705556

  • Aedes albopictus
  • Ascogregarina taiwanensis
  • competition
  • escape from enemies
  • invasive
  • Ochlerotatus triseriatus
  • species