Asymmetric effects of native and exotic invasive shrubs on ecology of the West Nile virus vector Culex pipiens (Diptera: Culicidae)

Particle and Fibre Toxicology

Ephantus J. Muturi²  Lauren A. Frisbie¹  Brian F. Allan¹  Allison M. Gardner³ 

[1] School of Integrative Biology, University of Illinois at Urbana-Champaign, 505 S. Goodwin Ave., Urbana 61801, IL, USA;Illinois Natural History Survey, 1816 S. Oak St., Champaign 61820, IL, USA;Department of Entomology, University of Illinois at Urbana-Champaign, 505 S. Goodwin Ave., Urbana 61801, IL, USA

关键词: Mosquito ecology;    Ecological trap;    Habitat selection;    Invasive plants;    Culex pipiens;   

Others  :  1224192
DOI  :  10.1186/s13071-015-0941-z

 received in 2015-01-20, accepted in 2015-06-05,  发布年份 2015

【 摘 要 】

Background

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.

Methods

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.

Results

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.

Conclusions

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.

【 授权许可】

   
2015 Gardner et al.

【 图 表 】

Fig. 1.

Fig. 2.

Fig. 3.

Fig. 4.

【 参考文献 】

• [1]Bertin RI. Losses of native plant species from Worcester, Massachusetts. Rhodora. 2002; 104:325-49.
• [2]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.
• [3]Mack RN, Lonsdale WM. Humans as global plant dispersers: getting more than we bargained for. Bioscience. 2001; 51:95-102.
• [4]Byers JE. Impact of non-indigenous species on natives enhanced by anthropogenic alteration of selection regimes. Oikos. 2002; 97:449-58.
• [5]Kareiva P, Watts S, McDonald R, Boucher T. Domesticated nature: shaping landscapes and ecosystems for human welfare. Science. 2007; 316:1866-9.
• [6]Masters RA, Sheley RL. Principles and practices for managing rangeland invasive plants. J Range Manage. 2001; 54:502-17.
• [7]Bolund P, Hunhammar S. Ecosystem services in urban areas. Ecol Econ. 1999; 29:293-301.
• [8]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.
• [9]Burghardt KT, Tallamy DW, Shriver WG. Impact of native plants on bird and butterfly biodiversity in suburban landscapes. Cons Biol. 2009; 23:219-24.
• [10]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.
• [11]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.
• [12]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.
• [13]Conley AK, Watling JI, Orrock JL. Invasive plant alters ability to predict disease vector distribution. Ecol Appl. 2011; 21:329-34.
• [14]Reiskind MH, Zarrabi AA. The importance of an invasive tree fruit as a resource for mosquito larvae. J Vector Ecol. 2011; 36:197-203.
• [15]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.
• [16]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.
• [17]Yee DA. Tires as habitats for mosquitoes: a review of studies within the eastern United States. J Med Entomol. 2008; 45:581-93.
• [18]Reichard SH, White P. Horticulture as a pathway of invasive plant introductions in the United States. Bioscience. 2001; 51:103-13.
• [19]Fish D, Carpenter SR. Leaf litter and larval mosquito dynamics in tree-hole ecosystems. Ecology. 1982; 63:283-8.
• [20]Walker ED, Merritt RW. The significance of leaf detritus to mosquito (Diptera: Culicidae) productivity from treeholes. Environ Entomol. 1988; 17:199-206.
• [21]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.
• [22]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.
• [23]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: Article ID e71812
• [24]Merritt RW, Dadd RH, Walker ED. Feeding behavior, natural food, and nutritional relationships of larval mosquitos. Annu Rev Entomol. 1992; 37:349-76.
• [25]Kitching RL. Food webs in phytotelmata: “bottom-up” and “top-down” explanations for community structure. Annu Rev Entomol. 2001; 46:729-60.
• [26]Bentley MD, Day JF. Chemical ecology and behavioral aspects of mosquito oviposition. Annu Rev Entomol. 1988; 34:401-21.
• [27]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.
• [28]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.
• [29]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.
• [30]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.
• [31]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.
• [32]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.
• [33]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.
• [34]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.
• [35]Darsie RF, Ward RA. Identification and geographical distribution of the mosquitoes of North America, north of Mexico. University Press of Florida, Gainesville; 2004.
• [36]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.
• [37]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.
• [38]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.
• [39]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.
• [40]Hardy JL, Houk EJ, Kramer LD, Reeves WC. Intrinsic factors affecting vector competence of mosquitoes for arboviruses. Annu Rev Entomol. 1983; 28:229-262.
• [41]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; 31:123-126.
• [42]Alto BW, Reiskind MH, Lounibos LP. Size alters susceptibility of vectors to dengue virus infection and dissemination. Am J Trop Med Hyg. 2009; 79:688-695.
• [43]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; 10:170-172.
• [44]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: Article ID e10165
• [45]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.
• [46]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.
• [47]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. BioMed Central Full Text
• [48]Schlaepfer MA, Runge MC, Sherman PW. Ecological and evolutionary traps. Trends Ecol Evol. 2002; 17:474-80.
• [49]Stiles EW. Expansions of mockingbird and multiflora rose in the northeastern United States and Canada. Am Birds. 1982; 36:358-64.
• [50]Larson BM. The war of the roses: demilitarizing invasion biology. Front Ecol Environ. 2005; 3:495-500.
• [51]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: Article ID e72522
• [52]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.
• [53]Foo LY, Porter LJ. The structure of tannins of some edible fruits. J Sci Food Agr. 1981; 32:711-6.
• [54]Gudej J, Tomczyk M. Determination of flavonoids, tannins, and ellagic acid in leaves from Rubus L. species. Arch Farm Res. 2004; 27:1114-9.
• [55]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.
• [56]Rey D, Cuany A, Pauton MP, Meyran JC. Differential sensitivity of mosquito taxa to vegetable tannins. J Chem Ecol. 1999; 25:537-48.
• [57]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.
• [58]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.
• [59]Yanoviak SP. Effects of leaf litter species on macroinvertebrate community properties and mosquito yield in Neotropical tree hole microcosms. Oecologia. 1999; 120:147-55.