Asymmetric effects of native and exotic invasive shrubs on ecology of the West Nile virus vector Culex pipiens (Diptera: Culicidae)
© Gardner et al. 2015
Received: 20 January 2015
Accepted: 5 June 2015
Published: 16 June 2015
Exotic invasive plants alter the structure and function of native ecosystems and may influence the distribution and abundance of arthropod disease vectors by modifying habitat quality. This study investigated how invasive plants alter the ecology of Culex pipiens, an important vector of West Nile virus (WNV) in northeastern and midwestern regions of the United States.
Field and laboratory experiments were conducted to test the hypothesis that three native leaf species (Rubus allegheniensis, blackberry; Sambucus canadensis, elderberry; and Amelanchier laevis, serviceberry), and three exotic invasive leaf species (Lonicera maackii, Amur honeysuckle; Elaeagnus umbellata, autumn olive; and Rosa multiflora, multiflora rose) alter Cx. pipiens oviposition site selection, emergence rates, development time, and adult body size. The relative abundance of seven bacterial phyla in infusions of the six leaf species also was determined using quantitative real-time polymerase chain reaction to test the hypothesis that variation in emergence, development, and oviposition site selection is correlated to differences in the diversity and abundance of bacteria associated with different leaf species, important determinants of nutrient quality and availability for mosquito larvae.
Leaf detritus from invasive honeysuckle and autumn olive yielded significantly higher adult emergence rates compared to detritus from the remaining leaf species and honeysuckle alleviated the negative effects of intraspecific competition on adult emergence. Conversely, leaves of native blackberry acted as an ecological trap, generating high oviposition but low emergence rates. Variation in bacterial flora associated with different leaf species may explain this asymmetrical production of mosquitoes: emergence rates and oviposition rates were positively correlated to bacterial abundance and diversity, respectively.
We conclude that the displacement of native understory plant species by certain invasive shrubs may increase production of Cx. pipiens with potential negative repercussions for human and wildlife health. These findings may be relevant to mosquito control and invasive plant management practices in the geographic range of Cx. pipiens. Further, our discovery of a previously unknown ecological trap for an important vector of WNV has the potential to lead to novel alternatives to conventional insecticides in mosquito control by exploiting the apparent “attract-kill” properties of this native plant species.
Exotic shrubs, aided mostly by human activities, have become dominant features of urban and suburban landscapes in North America [1, 2]. Deliberate introduction of non-native turf grass lawns and ornamental plants remains a common practice in residential neighborhoods despite the well-documented potential for these species to become invasive in their introduced ranges . On a broader scale, the disturbed structure of urban communities has given rise to an altered natural selection process that often functions to the competitive detriment of native species . As a consequence, propagation of exotic invasive plants (hereafter “invasive plants”) may reduce the ecosystem services typically provided by native plant communities, including nutrient cycling, prevention of stream erosion, air filtration, and preservation of wildlife diversity [5–9].
There is also recent evidence that invasive plants can cause ecological cascades that alter human risk of exposure to diseases vectored by arthropods. For example, invasive plants may enhance the risk of exposure to tick-borne pathogens by increasing the abundance and encounter frequency of ticks and their vertebrate hosts [10–12]. In mosquito-borne disease systems, changes in habitat complexity resulting from plant invasions may alter oviposition site selection by some vector species , and inputs of fruits and leaves of some terrestrial invasive plant species into aquatic larval habitats may provide a high-quality nutritional base for mosquito larvae . Yet despite the strong potential for vectors to interact with invasive plants, we have limited understanding of the diversity of potential mechanisms by which these plants alter vector ecology and the consequences for human health.
Container-dwelling mosquitoes provide an ideal model system for understanding the effects of native and invasive plants on mosquito ecology and the risk of human exposure to vector-borne pathogens. Culex pipiens pipiens Linnaeus (Diptera: Culicidae), an important vector for West Nile virus in urban landscapes throughout the northeastern and midwestern United States , oviposits in a variety of natural and artificial containers such as small ponds, discarded tires, and storm water catch basins [16, 17]. These habitats are mainly fueled by plant-based detritus from the surrounding terrestrial vegetation. This often includes leaves of non-native understory plant species (Gardner, pers. obs.), which commonly are introduced to residential environments for home landscaping and often become invasive in small urban forest fragments . Detritus type and quantity determine the composition and abundance of microbial communities that form in container habitats as microbes break down terrestrial leaf litter [19–23]. In turn, these bacteria and fungi provide a direct food source for mosquito larvae [24, 25] and influence oviposition behavior of gravid female mosquitoes through emission of oviposition attractants and stimulants [26, 27]. Thus, detritus from terrestrial plants and its associated microbes play a critical role in determining vector distribution, relative abundance, and life history traits that are important for vector-borne pathogen transmission including adult body size, longevity, biting rates, and vector competence [28–31].
It has been proposed that detritus from invasive plants benefits mosquito vectors and enhances vector-borne disease transmission potential because these leaves decompose faster and facilitate more rapid microbial growth compared to native plants [32–34]. In this study, we test the hypotheses that A) leaf detritus of three native and three invasive shrubs asymmetrically affects the emergence rates, development, and oviposition site selection by Cx.pipiens, and B) variation in emergence, development, and oviposition site selection is correlated with differences in the diversity and abundance of bacterial flora among leaf detritus types.
Selection of plant species
Six focal plant species were selected among shrubs common within the geographic range of Cx. pipiens . The invasive shrubs were Lonicera maackii (Dipsacales: Caprifoliaceae; Amur honeysuckle), Elaeagnus umbellata (Rosales: Elaeagnaceae; autumn olive), and Rosa multiflora (Rosales: Rosaceae; multiflora rose). Found in both natural and domestic environments – including forest fragments, landscaped parks, and residential neighborhoods – these three exotics are highly invasive throughout much of the United States, and in some areas of the northeast and Midwest dominate over 80 % of land cover [36, 37]. The native shrubs were Rubus allegheniensis (Rosales: Rosaceae; blackberry), Sambucus canadensis (Dipsacales: Adoxaceae; elderberry), and Amelanchier laevis (Rosales: Rosaceae; serviceberry), all three of which are common understory species in mixed deciduous forests and residential landscapes.
Attractiveness of leaf species forCx. pipiens oviposition
Six oviposition traps  each containing 4 L of tap water and 80 g of fresh whole leaves of one of the six shrub species were placed 1 m apart from each other in partial shade at five sites located within a 5 km radius in residential Champaign-Urbana, Illinois. The 30 oviposition traps were monitored for egg rafts daily and the number of egg rafts collected in each substrate from June 24 to August 5, 2013 (39 days) was recorded. This design, which was informed by a smaller pilot study performed in 2012, tested for temporal variation in the attractiveness of the leaf species to gravid females based on the number of egg rafts collected, which may vary as the microbial and chemical composition of the infusion changes with decomposition of the leaves [32, 33].
Day was the repeated variable, and an autoregressive-1 covariance structure with restricted maximum likelihood (REML) was used for estimation of covariance parameters. Orthogonal contrasts were used to test the linear and quadratic components of the quantitative day variable. Tukey’s mean separation test was used for comparisons of leaf detritus species treatment means. Number of egg rafts was log (x + 0.1)-transformed to meet the assumptions of normally, identically, and independently distributed residuals.
Effect of leaf detritus species on Cx. pipiens emergence and development
Culex pipiens larvae were obtained by collecting egg rafts from five sites using standard grass infusion-baited oviposition traps. Egg rafts were individually hatched in petri dishes containing deionized water and first instar larvae of Cx. pipiens were distinguished from those of Culex restuans Theobald based on the presence or absence of a clear area anterior to the sclerotized egg-breaker which is present in Cx. restuans and absent in Cx. pipiens . Culex pipiens larvae collected from different sites were pooled prior to their random allocation to experimental treatments.
To test for the effect of leaf substrate on intraspecific competition, 18 treatments were established with five replicates per treatment (90 containers). Each treatment included one of three densities of first instar larvae of Cx. pipiens (10, 20, or 40 per container) and 360 mL infusion of one of the six leaf detritus species in 400 mL tri-pour beakers. Infusions were prepared by fermenting 80 g of fresh leaves of each plant species in 4 L of tap water for 7 days, a standard infusion age used in comparable studies. Fresh leaves constitute a substantial portion of leaf litter inputs in container habitats and are superior food source for mosquito larvae compared to senescent leaves . The containers were monitored daily and pupae were removed from containers and housed individually in cotton-sealed plastic vials with deionized water. The experiment was conducted under ambient conditions of 25 °C, 70 % relative humidity, and a 16:8 (L:D) photoperiod. Adults were sorted by sex and date of eclosion and their wing lengths determined. Time to eclosion and adult body size are important determinants of the potential for disease transmission (i.e., “vectorial capacity”) in mosquitoes [40–43]. Rapid time to eclosion facilitates high emergence rates of mosquitoes even from ephemeral habitats, while adult body size is directly related to longevity and potential to transmit viruses; only a vector that survives the duration of the viral extrinsic incubation period can infect a human or wildlife host .
Separate Multivariate Analysis of Variance (MANOVA) tests were used to test for the fixed effects of leaf detritus species, competition, and their interaction on male and female development time to eclosion and adult wing length. Standardized canonical coefficients (SCCs) were used to describe the relative contributions of development time and wing length to significant treatment effects as well as the relationship between the two variables. A GLMM with a factorial treatment structure was used to test the fixed effects of leaf species, competition, and their interaction on Cx. pipiens emergence rates (male and female combined) with Tukey’s separation of means. Development time and wing length were log (x + 0.1)-transformed and emergence data were arcsine-square root (x)-transformed to meet the assumptions of the analysis.
Relationship between leaf detritus species and microbial composition and abundance
Before adding larvae to treatments as described above, 2 mL aliquots of 7 day old leaf infusions were taken from each container and stored at−80 °C until further processing. Genomic DNA was extracted from the samples using the UltraClean® Soil DNA Isolation Kit (Mo Bio Laboratories Inc., Carlsbad CA, Cat. No. 12800-50) according to the manufacturer’s instructions. Real-time polymerase chain reaction was conducted to detect total bacterial abundance and abundance of seven bacterial phyla (α-proteobacteria, β-proteobacteria, γ-proteobacteria, firmicutes, acidobacteria, actinobacteria, and bacteroidetes) in aliquots of leaf infusions, according to the methods described in .
The Shannon diversity index (H) was used to calculate bacterial diversity at the phylum level associated with each leaf detritus species. Further analysis was carried out in three steps. First, GLMs were used to compare total bacterial abundance and bacterial diversity among leaf species, with Tukey’s separation of treatment means. Second, multiple linear regression models were used to assess the relationship between bacterial abundance, bacterial diversity, larval density, and their interaction and mosquito emergence rates, and the relationship between bacterial abundance, bacterial diversity, and their interaction and oviposition rates. Finally, multiple linear regression models were used to identify specific bacterial phyla that are related to mosquito emergence and oviposition rates with phylum-level abundance of seven bacterial phyla as independent effects. Emergence rates were arcsine-square root (x)-transformed and oviposition rates and bacterial abundance and diversity measures were log (x + 0.1)-transformed to meet the assumptions of all tests.
Attractiveness of leaf species for Cx. pipiens oviposition
Thus, all leaf detritus species initially increased in attractiveness and then declined in attractiveness after the critical point at 19 days.
Effect of leaf detritus species on Cx. pipiens emergence and development
Multivariate Analysis of Variance (MANOVA) for the effect of leaf detritus species and intraspecific competition on Culex pipiens female and male time to eclosion (days) and wing length (mm). Standardized canonical coefficients (SCCs) describe the relative contribution of each life history trait to the multivariate effect
Relationship between leaf detritus species and microbial composition and abundance
Multiple linear regressions for the effect of total bacterial abundance, bacterial diversity, larval density (10, 20, and 40 larvae), and their interaction on Culex pipiens female and male emergence rate and oviposition rates
Multivariate linear regressions for the effect of phylum-level bacterial composition, larval density (10, 20, and 40 larvae), and their interaction on Culex pipiens female and male emergence and oviposition rates
Bacterial diversity but not total bacterial abundance or their interaction was positively correlated to mosquito oviposition rate (Table 2). No particular bacterial phyla were identified that were significantly correlated to oviposition rate (Table 3).
Using a combination of laboratory and field experiments, we identified two invasive shrubs that may promote growth and emergence of an important mosquito vector relative to native shrub species by improving the nutritional quality of the larval environment via leaf detritus inputs. Culex pipiens emergence rates were significantly higher in leaf infusions of honeysuckle and autumn olive compared to the other shrub species. We also noted that the deleterious effects of intraspecific larval competition were mitigated in honeysuckle treatments. The reduction of this important constraint on mosquito population carrying capacity  indicates that this invasive leaf species may support higher mosquito densities in heavily invaded areas. Similarly, mosquitoes reared in honeysuckle and autumn olive infusion had the shortest development time to eclosion and the longest adult wing lengths in both females and males compared to the other leaf detritus species. These life history characteristics are positively associated with efficiency of mosquito-borne pathogen transmission (i.e., “vectorial capacity”) [40, 43]. Therefore, the widespread distribution of these two invasive shrubs in North America raises concerns regarding their impact on the transmission of several mosquito-borne viruses such as West Nile virus and St. Louis encephalitis.
Although not the most attractive leaf detritus species observed in the experiment, honeysuckle and autumn olive were by far the most favorable leaf detritus species for development and emergence of laboratory-reared mosquitoes. These results complement a growing body of field studies that suggest landscaping with exotic – and potentially invasive – plants has the potential to influence local larval and adult mosquito abundance and distribution . For instance, the presence of ornamental lawn shrubs, including many invasive species, is positively associated with abundance of Cx. pipiens and Cx. restuans larvae in roadside storm water catch basins . However, it is noteworthy that our experiments also identified a third invasive plant, multiflora rose, that is lethal to Cx. pipiens, suggesting that the effect of displacement of native plants by invasive species has neither uniformly positive nor negative impacts on the abundance and distribution of mosquitoes.
Our comparisons of native and invasive leaf detritus species on larval development and oviposition facilitated the discovery of a naturally-occurring ecological trap for Cx. pipiens. Ecological traps occur due to a mismatch between the attractiveness of a habitat and its quality for reproduction . The greatest number of egg rafts was collected in water containing leaves of blackberry, a native plant species found throughout the geographic range of Cx. pipiens. However, in laboratory assays, exceptionally low mosquito emergence rates were observed in blackberry infusions, with fewer than 20 % of larvae surviving to eclosion even at the lowest larval density. Blackberry-reared mosquitoes also exhibited significantly longer development times to eclosion and the shortest adult wing lengths compared to those exposed to other leaf detritus species. Infusion of multiflora rose, an exotic shrub of limited importance in the Midwest but highly invasive in the northeastern United States [49, 50], similarly yielded lower emergence with no mosquitoes developing to eclosion across all density treatments. However, gravid females were better able to discriminate against this leaf detritus species and consequently water containing multiflora rose leaves collected fewer egg rafts than water containing blackberry leaves. Future research will determine whether exploitation of this ecological trap may yield a novel “attract-kill” approach to control mosquito larvae in closed aquatic environments, such as rain barrels, buckets, and storm water catch basins.
A potential mechanism to explain both asymmetrical oviposition rates and emergence and development rates of mosquitoes with respect to leaf detritus species and differences in the associated microbial flora. Honeysuckle, autumn olive, and elderberry infusions contained greater abundances of bacterial flora than multiflora rose, serviceberry, and blackberry infusion, an observation that likely reflects more rapid leaf decomposition rates among the former species [32, 33], yielding larger amounts of bacteria. For the most part, mosquito emergence reflected this pattern; the notable exception was serviceberry infusion, in which a moderate proportion of mosquitoes developed to eclosion despite low bacterial abundance. This result suggests total bacterial abundance may be a good indicator of habitat quality under most but not all conditions . Microbial abundance also varied significantly between different phyla across leaf detritus species, and was statistically correlated to mosquito emergence. In particular, β-proteobacteria was negatively correlated with emergence rates while bacteroidetes and acidobacteria were positively correlated with emergence rates. This result is consistent with studies of other mosquitoes; for example, Aedes triseriatus Say and Culex tarsalis Coquillett appear to feed preferentially on bacteroidetes [51, 52].
Further, irrespective of bacterial abundance, phylum-level bacterial diversity was positively correlated with oviposition rates. This result supports previous research which indicates that mosquito oviposition site discovery and selection may be mediated by the odors produced by a higher diversity of bacteria [22, 27]. Thus, we propose that optimal habitats for mosquito production may contain both higher bacterial abundance and higher bacterial diversity, which jointly facilitate discovery of the habitat and the emergence and development of larvae within. Meanwhile, high-diversity and low-abundance habitats such as blackberry-infused water may constitute ecological traps, while low-diversity and high-abundance habitats such as honeysuckle-infused water appear to attract fewer gravid females but promote higher rates of mosquito emergence. It is possible that observed differences in oviposition and emergence rates were not driven by bacterial diversity per se, but rather variation in bacterial community composition between leaf species. It also is noteworthy that oviposition and emergence rates associated with different leaf species may be influenced by phytochemicals unrelated to microbial flora; for example, tannins are abundant in blackberry leaves [53, 54] and are known to be toxic to mosquitoes in other systems [55, 56]. However, these hypotheses were not tested thoroughly in our current experiment.
Our understanding of the mechanistic role potentially played by variation in microbial growth is limited by our focus on a higher taxonomic level of bacteria (i.e., phylum) and at the exclusion of fungi and other microbes that may be consumed by mosquito larvae. Additional studies are required to identify the particular microbial taxa that may be involved in determining mosquito emergence and oviposition site selection. Further, our molecular approach is subject to limitations such as potential underestimation of bacterial abundance due to DNA extraction bias and PCR bias [57, 58]. However, important conclusions can still be made; our findings corroborate previous research which has demonstrated that resource type and availability may influence emergence and oviposition. For example, variation in microbial communities among leaf detritus treatments have been shown to be related to Culex mollis Dyar life history traits , and binary choice laboratory assays revealed that Aedes aegypti Linnaeus oviposition site selection may be related to extracts released by the microbes present in infusions of different leaf species .
In summary, we observed elevated emergence rates and more rapid development among Cx. pipiens mosquitoes reared in infusions of honeysuckle and autumn olive leaves, two exotic, invasive shrubs that occur throughout much of the northeastern and midwestern United States. In contrast, we discovered mosquito emergence was significantly reduced among mosquitoes reared in infusions of native blackberry and exotic multiflora rose leaves compared to those exposed to other leaf detritus species. Our results have applications in two areas. First, our findings that some exotic, invasive shrubs are favorable for mosquito production may be relevant to mosquito control and invasive plant management practices in the geographic range of Cx. pipiens. Second, our discovery of a previously unknown ecological trap for an important vector of West Nile virus has the potential to lead to novel alternatives to conventional insecticides in mosquito control, exploiting the apparent “attract-kill” properties of this native plant species.
We thank Nina Krasavin, Millon Blackshear, Chang-Hyun Kim, Matthew Edinger, Audrey Killarney, and William LeGare for their technical assistance, Andrew Mackay and Richard Lampman for their advice on the experimental design, and the Muturi and Allan lab groups for their comments on the manuscript. We also thank homeowners in the City of Urbana and the City of Champaign, Illinois, for land use permission. This study was supported by the Used Tire Fund and Emergency Public Health Act from the State of Illinois to EJM. Summer salary for AMG was supported by the University of Illinois at Urbana-Champaign (UIUC) School of Integrative Biology, and research assistant support for AMG for fall 2013 was provided by a UIUC Center for a Sustainable Environment Sustainability Fellowship to BFA.
- Bertin RI. Losses of native plant species from Worcester, Massachusetts. Rhodora. 2002;104:325–49.Google Scholar
- DeCandido R, Muir AA, Gargiullo MB. First approximation of the historial and extant vascular flora of New York City: implications for native plant species conservation. J Torrey Bot Soc. 2004;131:243–51.View ArticleGoogle Scholar
- Mack RN, Lonsdale WM. Humans as global plant dispersers: getting more than we bargained for. Bioscience. 2001;51:95–102.View ArticleGoogle Scholar
- Byers JE. Impact of non-indigenous species on natives enhanced by anthropogenic alteration of selection regimes. Oikos. 2002;97:449–58.View ArticleGoogle Scholar
- Kareiva P, Watts S, McDonald R, Boucher T. Domesticated nature: shaping landscapes and ecosystems for human welfare. Science. 2007;316:1866–9.PubMedView ArticleGoogle Scholar
- Masters RA, Sheley RL. Principles and practices for managing rangeland invasive plants. J Range Manage. 2001;54:502–17.View ArticleGoogle Scholar
- Bolund P, Hunhammar S. Ecosystem services in urban areas. Ecol Econ. 1999;29:293–301.View ArticleGoogle Scholar
- Smith RM, Thompson K, Hodgson JG, Warren PH, Gaston KJ. Urban domestic gardens (IX): composition and richness of the vascular plant flora, and implications for native biodiversity. Biol Cons. 2006;129:312–22.View ArticleGoogle Scholar
- Burghardt KT, Tallamy DW, Shriver WG. Impact of native plants on bird and butterfly biodiversity in suburban landscapes. Cons Biol. 2009;23:219–24.View ArticleGoogle Scholar
- Williams SC, Ward JS, Worthley TE, Stafford KC. Managing Japanese barberry (Ranunculales: Berberidaceae) infestations reduces blacklegged tick (Acari: Ixodidae) abundance and infection prevalence with Borrelia burgdorferi (Spirochaetales: Spirochaetaceae). Environ Entomol. 2009;38:977–84.PubMedView ArticleGoogle Scholar
- Williams SC, Ward JS. Effects of Japanese barberry (Ranunculales: Berberidaceae) removal and resulting microclimatic changes on Ixodes scapularis (Acari: Ixodidae) abundances in Connecticut, USA. Environ Entomol. 2010;39:1911–21.PubMedView ArticleGoogle Scholar
- Allan BF, Dutra HP, Goessling LS, Barnett K, Chase JM, Marquis RJ, et al. Invasive honeysuckle eradication reduces tick-borne disease risk by altering host dynamics. Proc Natl Acad Sci U S A. 2010;107:18523–7.PubMed CentralPubMedView ArticleGoogle Scholar
- Conley AK, Watling JI, Orrock JL. Invasive plant alters ability to predict disease vector distribution. Ecol Appl. 2011;21:329–34.PubMedView ArticleGoogle Scholar
- Reiskind MH, Zarrabi AA. The importance of an invasive tree fruit as a resource for mosquito larvae. J Vector Ecol. 2011;36:197–203.PubMedView ArticleGoogle Scholar
- Turell MJ, Dohm DJ, Sardelis MR, O’Guinn ML, Andreadis TG, Blow JA. An update on the potential of North American mosquitoes (Diptera: Culicidae) to transmit West Nile virus. J Med Entomol. 2005;42:57–62.PubMedView ArticleGoogle Scholar
- Geery PR, Holub RE. Seasonal abundance and control of Culex spp in catch basins in Illinois. J Am Mosq Control Assoc. 1989;5:537–40.PubMedGoogle Scholar
- Yee DA. Tires as habitats for mosquitoes: a review of studies within the eastern United States. J Med Entomol. 2008;45:581–93.PubMedView ArticleGoogle Scholar
- Reichard SH, White P. Horticulture as a pathway of invasive plant introductions in the United States. Bioscience. 2001;51:103–13.View ArticleGoogle Scholar
- Fish D, Carpenter SR. Leaf litter and larval mosquito dynamics in tree-hole ecosystems. Ecology. 1982;63:283–8.View ArticleGoogle Scholar
- Walker ED, Merritt RW. The significance of leaf detritus to mosquito (Diptera: Culicidae) productivity from treeholes. Environ Entomol. 1988;17:199–206.View ArticleGoogle Scholar
- Murrell EG, Juliano SA. Detritus type alters the outcome of interspecific competition between Aedes aegypti and Aedes albopictus (Diptera: Culicidae). J Med Entomol. 2008;45:375–83.PubMed CentralPubMedView ArticleGoogle Scholar
- Ponnusamy L, Wesson DM, Arellano C, Schal C, Apperson CS. Species composition of bacterial communities influences attraction of mosquitoes to experimental plant infusions. Microb Ecol. 2010;59:158–73.PubMedView ArticleGoogle Scholar
- Muturi EJ, Orindi BO, Kim CH. Effect of leaf type and pesticide exposure on abundance of bacterial taxa in mosquito larval habitats. PLoS One. 2013;8, e71812.PubMed CentralPubMedView ArticleGoogle Scholar
- Merritt RW, Dadd RH, Walker ED. Feeding behavior, natural food, and nutritional relationships of larval mosquitos. Annu Rev Entomol. 1992;37:349–76.PubMedView ArticleGoogle Scholar
- Kitching RL. Food webs in phytotelmata: “bottom-up” and “top-down” explanations for community structure. Annu Rev Entomol. 2001;46:729–60.PubMedView ArticleGoogle Scholar
- Bentley MD, Day JF. Chemical ecology and behavioral aspects of mosquito oviposition. Annu Rev Entomol. 1988;34:401–21.View ArticleGoogle Scholar
- Ponnusamy L, Xu N, Nojima S, Wesson DM, Schal C, Apperson CS. Identificiation of bacteria and bacteria-associated chemical cues that mediate oviposition site preferences by Aedes aegypti. Proc Natl Acad Sci U S A. 2008;105:9262–7.PubMed CentralPubMedView ArticleGoogle Scholar
- Leonard PM, Juliano SA. Effect of leaf litter and density on fitness and population performance of the hole mosquito Aedes triseriatus. Ecol Entomol. 1995;20:125–36.View ArticleGoogle Scholar
- Walker ED, Kaufman MG, Ayres MP, Riedel MH, Merritt RW. Effects of variation in quality of leaf detritus on growth of the eastern tree-hole mosquito, Aedes triseriatus(Diptera: Culicidae). Can Rev Zool. 1997;75:706–18.View ArticleGoogle Scholar
- Bevins SN. Invasive mosquitoes, larval competition, and indirect effects on the vector competence of native mosquito species (Diptera: Culicidae). Biol Invasions. 2008;10:1109–17.View ArticleGoogle Scholar
- Muturi EJ, Allan BF, Ricci J. Influence of leaf detritus type on production and longevity of container-breeding mosquitoes. Environ Entomol. 2012;41:1062–8.PubMedView ArticleGoogle Scholar
- Blair BC, Stowasser A. Impact of Lonicera maackii on decomposition rates of native leaf litter in a southwestern Ohio woodland. Ohio J Sci. 2009;109:43–7.Google Scholar
- Poulette MM, Arthur MA. The impact of the invasive shrub Lonicera maackii on the decomposition dynamics of a native plant community. Ecol Appl. 2012;22:412–24.PubMedView ArticleGoogle Scholar
- Watling JL, Hickman CR, Lee E, Wang K, Orrock JL. Extracts of the invasive shrub Lonicera maackii increase mortality and alter behavior of amphibian larvae. Oecologia. 2011;165:153–9.PubMedView ArticleGoogle Scholar
- Darsie RF, Ward RA. Identification and geographical distribution of the mosquitoes of North America, north of Mexico. Gainesville: University Press of Florida; 2004.Google Scholar
- Luken JO. Population structure and biomass allocation of the naturalized shrub Lonicera maackii (Rupr.) Maxim. in forest and open habitats. Am Midl Nat. 1988;119:258–67.View ArticleGoogle Scholar
- Meiners SJ, Pickett ST, Cadenasso ML. Exotic plant invasions over 40 years of old field successions: community patterns and associations. Ecography. 2002;25:215–23.View ArticleGoogle Scholar
- Reiter P. A standardized procedure for the quantitative surveillance of certain Culexmosquitoes by egg raft collection. J Am Mosq Control Assoc. 1986;2:219–21.PubMedGoogle Scholar
- Dodge HR. Studies on mosquito larvae III. The first instar larvae of North American Culicidae and of world Anophelinae. Can Entomol. 1966;98:337–93.View ArticleGoogle Scholar
- Hardy JL, Houk EJ, Kramer LD, Reeves WC. Intrinsic factors affecting vector competence of mosquitoes for arboviruses. Annu Rev Entomol. 1983;28:229–62.PubMedView ArticleGoogle Scholar
- Nasci RS, Mitchell CJ. Larval diet, adult size, and susceptibility of Aedes aegypti (Diptera: Culicidae) to infection with Ross River virus. J Med Entomol. 1994;31:123–6.PubMedView ArticleGoogle Scholar
- Alto BW, Reiskind MH, Lounibos LP. Size alters susceptibility of vectors to dengue virus infection and dissemination. Am J Trop Med Hyg. 2009;79:688–95.Google Scholar
- Ameneshewa B, Service MW. The relationship between female body size and survival rate of the malaria vector Anopheles arabiensis in Ethiopia. Med Vet Entomol. 1996;10:170–2.PubMedView ArticleGoogle Scholar
- Bellan SE. The importance of age dependent mortality and the extrinsic incubation period in models of mosquito-borne disease transmission and control. PLoS One. 2010;5, e10165.PubMed CentralPubMedView ArticleGoogle Scholar
- Reiskind MH, Zarrabi AA, Lounibos LP. Effects of combination of leaf resources on competition in container mosquito larvae. Bull Entomol Res. 2012;7:1–11.Google Scholar
- Shewart L, McEwan RW, Benbow ME. Evidence for facilitation of Culex pipiens (Diptera: Culicidae) life history traits by the nonnative invasive shrub Amur honeysuckle (Lonicera maackii). Environ Entomol. 2014;43:1584–93.View ArticleGoogle Scholar
- Gardner AM, Anderson TK, Hamer GL, Johnson DE, Varela KE, Walker ED, et al. Terrestrial vegetation and aquatic chemistry influence larval mosquito abundance in catch basins, Chicago, USA. Parasites Vectors. 2013;6:e9.View ArticleGoogle Scholar
- Schlaepfer MA, Runge MC, Sherman PW. Ecological and evolutionary traps. Trends Ecol Evol. 2002;17:474–80.View ArticleGoogle Scholar
- Stiles EW. Expansions of mockingbird and multiflora rose in the northeastern United States and Canada. Am Birds. 1982;36:358–64.Google Scholar
- Larson BM. The war of the roses: demilitarizing invasion biology. Front Ecol Environ. 2005;3:495–500.View ArticleGoogle Scholar
- Duguma D, Rugman-Jones P, Kaufman MG, Hall MW, Neufeld JD, Stouthamer R, et al. Bacterial communities associated with Culex mosquito larvae and two emergent aquatic plants of bioremediation importance. PLoS One. 2013;8, e72522.PubMed CentralPubMedView ArticleGoogle Scholar
- Kaufman MG, Chen S, Walker ED. Leaf-associated bacterial and fungal taxa shifts in response to larvae of the tree hole mosquito, Ochlerotatus triseriatus. Microb Ecol. 2008;55:673–84.PubMed CentralPubMedView ArticleGoogle Scholar
- Foo LY, Porter LJ. The structure of tannins of some edible fruits. J Sci Food Agr. 1981;32:711–6.View ArticleGoogle Scholar
- Gudej J, Tomczyk M. Determination of flavonoids, tannins, and ellagic acid in leaves from Rubus L. species. Arch Farm Res. 2004;27:1114–9.View ArticleGoogle Scholar
- Mercer DR. Effect of tannic acid concentration on development of the western treehole mosquito, Aedes sierrensis (Diptera: Culicidae). J Chem Ecol. 1993;19:1119–27.PubMedView ArticleGoogle Scholar
- Rey D, Cuany A, Pauton MP, Meyran JC. Differential sensitivity of mosquito taxa to vegetable tannins. J Chem Ecol. 1999;25:537–48.View ArticleGoogle Scholar
- Kirk JL, Beaudette LA, Hart M, Moutoglis P, Kilronomos JN, Lee H, et al. Methods of studying soil microbial diversity. J Microb Meth. 2004;2:169–88.View ArticleGoogle Scholar
- Martin-Laurent F, Philippot L, Hallet S, Chaussod R, Germon JC, Soulas G, et al. DNA extraction from soils: old bias for new microbial diversity analysis methods. Appl Environ Microb. 2001;67:2354–9.View ArticleGoogle Scholar
- Yanoviak SP. Effects of leaf litter species on macroinvertebrate community properties and mosquito yield in Neotropical tree hole microcosms. Oecologia. 1999;120:147–55.View ArticleGoogle Scholar
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.