POPULATION AND COMMUNITY ECOLOGY Asymmetrical Competition and Patterns of Abundance of Aedes albopictus and Culex pipiens (Diptera: Culicidae) 1 KATIE S. COSTANZO, KIMBERLY MORMANN, AND STEVEN A. JULIANO Department of Biological Sciences, Illinois State University, Normal, IL 61790-4120 J. Med. Entomol. 42(4): 559Ð570 (2005) ABSTRACT We tested for competitive advantage among larvae of Aedes albopictus (Skuse) and Culex pipiens L. in a laboratory experiment and determined the frequency and spatial and temporal patterns of co-occurrence in the Þeld in East St. Louis, IL. In a laboratory competition experiment at multiple combined densities of Ae. albopictus and Cx. pipiens larvae, Ae. albopictus survivorship and developmental times were signiÞcantly affected by conspeciÞc densities but not by Cx. pipiens densities. In contrast, Cx. pipiens survivorship and developmental times were signiÞcantly affected by both conspeciÞc and Ae. albopictus densities. Per capita rate of increase (rЈ) for Ae. albopictus cohorts declined signiÞcantly due to density of conspeciÞcs, but not density of Cx. pipiens. InterspeciÞc competition between Ae. albopictus and Cx. pipiens under these laboratory conditions was strong and asymmetrical, with the effect of Ae. albopictus on Cx. pipiens much stronger than the reverse. In monthly samples from tire sites in East St. Louis, Ae. albopictus was highly seasonal, occurring in relatively low abundance from early May to July and increasing in abundance in August and Sep- tember. Co-occurrence corresponded to the seasonality of Ae. albopictus, with Cx. pipiens encoun- tering Ae. albopictus in more tires and at higher numbers within a tire, in August and September. Abundance of both species was high in residential areas and was unrelated to overstory cover, total nitrogen, and total phosphorus. Abundance of Ae. albopictus, but not of Cx. pipiens, was positively associated with conductivity. We expect Cx. pipiens to suffer from the effects of interspeciÞc com- petition in tires in which it encounters Ae. albopictus. InterspeciÞc competition between these species may be of both ecological and medical importance. COMPETITIVE INTERACTIONS BETWEEN two species are of- been associated with declines in abundance and local ten asymmetrical, so that the effect of one of the extinction of other North American mosquitoes species on the other is much more prominent than the (Hobbs et al. 1991, McHugh 1993, Hornby et al. 1994, reverse (Lawton and Hassell 1981). Competitive Mekuria and Hyatt 1995, OÕMeara et al. 1995). asymmetry has important consequences for compet- There have been numerous studies on the compet- itors. With high competitive asymmetry, the compet- itive interactions of larval Ae. albopictus with contain- itively superior species is expected to eliminate the er-dwelling aedine mosquitoes, particularly Ochlero- competitively weaker species unless other processes tatus triseriatus (Say) and Aedes aegypti L. In most (e.g., disturbance and predation) intervene to facili- instances, Ae. albopictus proves the superior compet- tate coexistence (Lawton and Hassell 1981, Connell itor, notably when resources are limiting (Livdahl and 1983). Willey 1991, Edgerly et al. 1993, Barrera 1996, Juliano The Asian tiger mosquito, Aedes albopictus (Skuse), 1998, Daugherty et al. 2000, Teng and Apperson 2000, was introduced into the United States in the mid-1980s Braks et al. 2004). through tire shipments from Asia (Sprenger and Culex pipiens L., the northern house mosquito, is Wuithranyagool 1986). It has become the most abun- established throughout the northern United States dant container-dwelling mosquito in many regions of and southern Canada (Darsie and Ward 1981). Re- the country (Moore and Mitchell 1997). Ae. albopictus cently, interest in the ecology of Cx. pipiens has in- is medically important because it is a vector of arbo- creased because laboratory and Þeld studies implicate viruses, including dengue, La Crosse encephalitis, it as an important vector of WNV (Kulasekera et al. eastern equine encephalitis, and West Nile virus 2001; Spielman 2001; Turell et al. 2001, 2005; Fonseca (WNV) (Iban˜ ez-Bern˜ al et al. 1997; Mitchell et al. 1992; et al. 2004). There have been relatively few studies of Gerhardt et al. 2001; Turell et al. 2001, 2005). Invasion competitive interactions of larvae of this species (but by Ae. albopictus also had an ecological impact and has see Carrieri et al. 2003). The distribution of Cx. pipiens is largely associated 1 Current address: Department of Biological Sciences, University at with development and urbanization (Vinogradova Buffalo, Buffalo, NY 14260. 2000, Fonseca et al. 2004). Cx. pipiens is ecologically 0022-2585/05/0559Ð0570$04.00/0 ᭧ 2005 Entomological Society of America 560 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 42, no. 4 associated with humans and shows high ecological and what types of macro- and microhabitats, and in what physiological ßexibility, with larvae inhabiting con- season, are these two species are most likely to co- tainers with high levels of organic and industrial pol- occur? Because Cx. pipiens has a high tolerance for lution, drainage canals, and other highly contaminated organic pollution (Vinogradova 2000), we tested bodies of water (Vinogradova 2000). Laboratory and whether variation in dissolved nutrients across tires is Þeld data indicate that the larvae of Cx. pipiens are associated with distribution and abundance of Ae. al- eurytopic, tolerating extreme values of pH, high or- bopictus and Cx. pipiens. We also examined land use ganic material, high temperatures, and high salinity associated with the urban tires occupied by these (Vinogradova 2000). species. Ae. albopictus and Cx. pipiens encounter one an- other in their shared artiÞcial habitats, and their dis- Materials and Methods tributions overlap in much of North America (Hawley 1988, Vinogradova 2000). The larvae of both these Rearing. Individuals used in this experiment were species can occur in natural and artiÞcial containers, Þrst generation progeny of individuals collected from and they share similar feeding habits such as Þltering discarded tires in East St. Louis. Cx. pipiens co-occurs and browsing (Hawley 1988, Vinogradova 2000). In with Cx. quinquefasciatus in East St. Louis, and these Italy, Ae. albopictus and Cx. pipiens commonly co- species produce hybrids in regions of co-occurrence occur in artiÞcial containers in the Þeld, and in com- (Brogdon 1984, Vinogradova 2000, Fonseca et al. petition in the laboratory, Ae. albopictus is more suc- 2004). Field-collected larvae were sorted based on a cessful at high combined densities with low food siphonal index (Brogdon 1984), which can typically availability than is Cx. pipiens (Carrieri et al. 2003). separate pure populations of these species (Brogdon Carrieri et al. (2003) worked with a single strain of 1984, Vinogradova 2000). We cannot, however, sepa- each species from southern Europe, and geographic rate hybrids reliably; hence, our laboratory population variation in larval growth and development is well probably included individuals carrying genes of Cx. known in both species (Vinogradova 2000; P. Arm- quinquefasciatus. Approximately 90% of Þeld-col- bruster and J. Conn, unpublished data). Furthermore, lected individuals from our East St. Louis site were interpretation of the experiment by Carrieri et al. morphologically consistent with Cx. pipiens. We re- (2003) is complicated by their use of highly artiÞcial gard our laboratory population as a representative food substrates (cat biscuits). Outcome of competi- sample of the interbreeding members of the Cx. pipi- tion among mosquito larvae, including Ae. albopictus, ens complex from our Þeld site and therefore the is well known to be sensitive to larval food substrates relevant population for evaluation of effects of com- (Barrera 1996, Daugherty et al. 2000). Thus, results petition from Ae. albopictus. We will refer to them as from Carrieri et al. (2003) cannot be assumed to apply Cx. pipiens for simplicity. to all populations of these species, and more realistic Larvae of both species were reared to adulthood at food substrates may yield very different results. 25ЊC under a photoperiod of 16:8 (L:D) h and then Our overall objective was to test the hypothesis that released into 0.6-m2 cages. Larvae of Ae. albopictus invading North American Ae. albopictus affects Cx. were fed bovine liver powder (ICN Biochemicals, pipiens through interspeciÞc competition. We tested Cleveland, OH), and larvae of Cx. pipiens were fed an this by evaluating two predictions of this hypothesis: artiÞcial diet comprised of bloodmeal, powdered milk, 1) interspeciÞc competition among larvae yields yeast, and wheat ßour (see Copeland 1987 for details). strong effects of Ae. albopictus on Cx. pipiens, and 2) Adult females of both species were housed in an in- co-occurrence of Ae. albopictus and Cx. pipiens within sectary at 22Ð26ЊC under a photoperiod of 16:8 (L:D) containers is common in the Þeld in our study area in h and blood fed on anesthetized laboratory mice to southern Illinois. We tested the Þrst prediction in a obtain eggs used to produce larvae for this study. Adult laboratory experiment testing the effects of increased female Cx. pipiens were provided with a 500-ml black densities of larvae of Ae. albopictus or Cx. pipiens upon cup Þlled with 400 ml of deionized (DI) water and the performance of the other species. We expected several blades of foxtail grass, Setaria faberi Herrmann, that Ae. albopictus