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Juliano, S.A., & Lounibos, L.P. 2005. Ecology of Invasive Mosquitoes

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Juliano, S.A., & Lounibos, L.P. 2005. Ecology of Invasive Mosquitoes Ecology Letters, (2005) 8: 558–574 doi: 10.1111/j.1461-0248.2005.00755.x REVIEWS AND SYNTHESES Ecology of invasive mosquitoes: effects on resident species and on human health Abstract Steven A. Juliano1* and Investigations of biological invasions focus on patterns and processes that are related to L. Philip Lounibos2 introduction, establishment, spread and impacts of introduced species. This review 1Department of Biological focuses on the ecological interactions operating during invasions by the most prominent Sciences, Behavior, Ecology, group of insect vectors of disease, mosquitoes. First, we review characteristics of non- Evolution and Systematics native mosquito species that have established viable populations, and those invasive Section, Illinois State University, species that have spread widely and had major impacts, testing whether biotic Normal, IL 61790-4120, USA characteristics are associated with the transition from established non-native to invasive. 2Florida Medical Entomology Second, we review the roles of interspecific competition, apparent competition, Laboratory, University of Florida, 200 9th St, SE, Vero predation, intraguild predation and climatic limitation as causes of impacts on residents Beach, FL 32962, USA or as barriers to invasion. We concentrate on the best-studied invasive mosquito, Aedes *Correspondence: E-mail: albopictus, evaluating the application of basic ecological theory to invasions by Aedes [email protected] albopictus. We develop a model based on observations of Aedes albopictus for effects of resource competition and predation as barriers to invasion, evaluating which community and ecosystem characteristics favour invasion. Third, we evaluate the ways in which invasive mosquitoes have contributed to outbreaks of human and animal disease, considering specifically whether invasive mosquitoes create novel health threats, or modify disease transmission for existing pathogen–host systems. Keywords Aedes albopictus, apparent competition, Culicidae, disease ecology, disease vectors, interspecific competition, intraguild predation, invasion, local adaptation, predation. Ecology Letters (2005) 8: 558–574 may alter the transmission cycles of native or non-native INTRODUCTION pathogens (McMichael & Bouma 2000). This review focuses Invasion biology focuses on patterns and processes related on the ecological interactions that produce impacts to introduction, establishment, spread and impacts of non- associated with invasions by the most prominent group of native species (Williamson 1996; Davis & Thompson 2000; insect vectors of disease, mosquitoes (Diptera, Culicidae). Lounibos 2002). We will apply the term ÔinvasiveÕ to We are specifically interested in two kinds of impacts of introduced species that have increased and spread, creating invasive mosquitoes: effects – usually detrimental – on the potential for impacts on native species and ecosystems, (i) resident species or ecosystems and (ii) human or vertebrate or on human activities (agriculture, conservation). We refer animal health. The first represents a class of effects that could to species that have become established, but have neither apply to any invasive species, so that what we learn from spread widely nor had important impacts as Ônon-nativeÕ. investigations of impacts of mosquitoes may serve as a Invasive species produce impacts on other species and paradigm for investigations of any invasion. The second ecosystems primarily via their biotic interactions, including represents a class of impacts relevant primarily to vectors. predation and parasitism, interspecific competition, or For mosquitoes, different life cycle stages are likely to be ecosystem engineering (Williamson 1996). Also among the central to the two kinds of impacts. The aquatic larval phase potential biotic impacts of some invasive species are effects is most likely to interact with and to impact other species, on human and animal health (Lounibos 2002). Invasive whereas the terrestrial adult phase is the cause of threats to pathogens may affect health directly, and invasive vectors human health. In examining both kinds of effects, we wish to Ó2005 Blackwell Publishing Ltd/CNRS Invasive mosquitoes 559 identify the characteristics of the invasive species and the about species characteristics, but they are questions deemed biological interactions that are associated with these impacts. generally important by those working in the field of invasion For mosquitoes, there is one well studied invasive species biology (e.g. Sakai et al. 2001). First, we can ask what (Asian tiger mosquito, Aedes albopictus Skuse) for which characteristics are associated with becoming an established multiple hypotheses concerning the ecological processes non-native. Desiccation-resistant eggs, which enhance sur- operating during its invasions have been tested in several vival in inhospitable environments, occur in 14 of 31 locations. For other species there is very little information invasive or non-native species (Table 1). Across the on the processes that operated during invasions. Although a Culicidae, strongly desiccation-resistant eggs are confined broad review of the processes involved in invasions by to members of the genera Aedes, Ochlerotatus, Psorophora, mosquitoes would be desirable, relevant data are not Haemagogus and Opifex (Clements 1992), totalling some 1012 available. In some cases (e.g. Ochlerotatus japonicus)the species, or about 29% of c. 3491 mosquito species (Walter invasions are recent and research on ecological processes is Reed Biosystematics Unit 2005). Thus, desiccation-resistant ongoing. In other cases the invasions occurred sufficiently eggs are strongly associated with becoming an introduced far in the past that the potential to investigate establishment non-native species (Fisher’s exact test, P ¼ 0.0024), perhaps and spread is long gone. We therefore begin with a simple because they increase probability of successful transport. A review of the characteristics of the major invasive mosqui- second question we can ask is what characteristics are toes, evaluating which traits are associated with invasive associated with making the transition from non-native to potential. We then concentrate our review of processes invasive (Sakai et al. 2001). Desiccation resistance (yes, no) primarily on Aedes albopictus, with a summary of what little is and status (invasive, non-invasive) are not significantly known or postulated about ecological processes involved in associated (Fisher’s exact test, P ¼ 0.693), indicating that other invasions by mosquitoes. This portion of our review species with desiccation-resistant eggs are not more likely to will enable us to test basic ecological theory as it applies to become invasive. Development in small man-made con- mosquitoes, and may thus improve our understanding of tainers, tree holes, bromeliads, or rock pools is also not only invasive mosquitoes, but of invasive species in common among invasive and non-native mosquitoes (17 general, and of the roles of biotic interactions that may apply of 31 total species; Table 1), but again, larval habitat to any invasive species. (container, non-container) and status (invasive, non-native) We divide the ecological processes into: (i) species are not significantly associated (Fisher’s exact test, P ¼ interactions that may influence invasions, either by affecting 0.132). Occupying human-dominated habitats (i.e. urban, resident species, or by serving as barriers to invasions and suburban, domestic) is significantly (Fisher’s exact test, P ¼ (ii) effects of climate that may foster invasion success, act as 0.028) more common among invasive (six of nine) than barriers to invasion, alter the impacts of invasions, or act as among non-native (three of 14) mosquitoes (Table 1). agents of natural selection on invasive mosquitoes. Inter- Association of invasion with human disturbance in some specific competition, predation and apparent competition form (e.g. Moyle & Light 1996; Richardson et al. 2000) has via shared pathogens are the species interactions that have been observed in other groups. There are at least two broad been best studied. We will review some models of these hypotheses explaining this association: human commensals interactions and empirical data on the roles of these may have traits (e.g. a high maximum rate of population processes in invasions by Aedes albopictus. We also review increase) that make them more likely to become invasive; or data on known effects of climate on invasions by Aedes expanding human population and urbanization may create albopictus. new, relatively under exploited, macrohabitat suitable for There are data on the health impacts of most invasions human commensal specialists. Autogeny and diapause are (Lounibos 2002), and we finish with a review of the disease not significantly associated with invasive status, but data are ecology of invasive mosquitoes. We do this by posing absent for many species (Table 1). Mode of introduction questions about the origins of disease organisms (e.g. non- (natural dispersal vs. human transport) is uncertain for many native, resident), and whether introduction of a new vector of these mosquitoes, but hitchhiking on ships is probably initiates or alters outbreaks of important diseases. We hope common (Lounibos 2002). that this portion of our review will provide a paradigm for investigations necessary to understand which non-native ECOLOGICAL PROCESSES species constitute the greatest hazard to human health. In the context of invasions,
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