Impacts of climate, land use, and biological invasion on the ecology of immature aedes mosquitoes: implications for la crosse emergence

Arthropod-borne viruses (arboviruses) cause many diseases worldwide and their transmission is likely to change with land use and climate changes. La Crosse virus (LACV) is historically transmitted by the native mosquito Aedes triseriatus (Say) in the upper Midwestern US, but the invasive congeners Aedes albopictus (Skuse) and A. japonicus (Theobald), which co-occur with A. triseriatus in water-holding containers, may be important accessory vectors in the Appalachian region where La Crosse encephalitis is an emerging disease. This review focuses on evidence for how climate, land use, and biological invasions may have direct abiotic and indirect community-level impacts on immature developmental stages (eggs and larvae) of Aedes mosquitoes. Because vector-borne diseases usually vary in space and time and are related to the ecology of the vector species, we propose that the ecology of its mosquito vectors, particularly at their immature stages, has played an important role in the emergence of La Crosse encephalitis in the Appalachian region and represents a model for investigating the effects of environmental changes on other vector-borne diseases. We summarize the health effects of LACV and associated socioeconomic costs that make it the most important native mosquito-borne disease in the US. We review of the transmission of LACV, and present evidence for the impacts of climate, land use, and biological invasions on Aedes mosquito communities. Finally, we discuss important questions about the ecology of LACV mosquito vectors that may improve our understanding of the impacts of environmental changes on LACV and other arboviruses.     

Stage-dependent predation on competitors: consequences for the outcome of a mosquito invasion

1. Predator-mediated coexistence occurs when predation allows competitors to coexist, due to preferential consumption of a superior competitor relative to an inferior competitor. Differences between the native treehole mosquito ( Aedes triseriatus ) and the co-occurring Asian tiger mosquito ( Aedes albopictus ) in anti-predatory larval behaviours account, in part, for the greater vulnerability of this invasive species to native predatory midge ( Corethrella appendiculata ). We test the hypothesis that stage-dependent differences in the sizes of A. albopictus and A. triseriatus larvae, relative to the size-limited C. appendiculata , contribute to differential consumption and the likelihood of predator-mediated coexistence of these competitors.
2. In all instars, larvae of A. triseriatus were larger than A. albopictus of the same stage. Third and fourth instar C. appendiculata selectively consumed late-stage A. albopictus in preference to same-stage A. triseriatus . Small, early-stage prey larvae did not differ in vulnerability to predation, but large, late-stage larvae differed significantly in vulnerability to predation, probably owing to size-limited predation by fourth instar C. appendiculata. This effect was less pronounced for third instar C. appendiculata .
3. Prey size, in conjunction with anti-predatory behavioural responses, alters the probability of predator-mediated coexistence. A stage-structured predation model showed that equally vulnerable early stages reduce the range of environmental conditions (productivities) in which predator-mediated coexistence is possible, increasing the likelihood of both competitive exclusion of the resident species or failure of the invasive to establish. These results underscore the importance of stage-dependent interspecific differences in predator–prey interactions for determining how predators may affect community composition.     

Roles of spatial partitioning,competition, and predation in the North American invasion of an exotic mosquito

Invasion success and species coexistence are often mediated by species interactions across patchily distributed habitats and resources. The invasive mosquito Aedes japonicus japonicus has established in the North American range of the competitively superior resident congener, Aedes albopictus, and the predatory native mosquito Toxorhynchites rutilus. We tested predictions for two hypotheses of invasion success and species coexistence: keystone predation and spatial partitioning. We tested competition between A. japonicus japonicus and A. albopictus with or without T. rutilus in laboratory microcosms, and measured abundances of A. japonicus japonicus, A. albopictus, other resident competing mosquito species, and the presence of T. rutilus among tree holes and tires in metropolitan Washington, DC. In laboratory microcosms, A. albopictus was competitively dominant over A. japonicus japonicus, which is consistent with the few prior studies of competition between these two Aedes species. T. rutilus predation severely lowered performances of both Aedes species but more severely lowered A. japonicus japonicus performance than A. albopictus performance when all three species co-occurred, thus yielding no evidence for keystone predation. Consistent with the spatial partitioning hypothesis, A. japonicus japonicus was negatively correlated and independently aggregated with A. albopictus and all combined resident mosquito competitors and was not associated with T. rutilus among field containers. These results suggest that predation from T. rutilus and competition from A. albopictus are barriers to the spread of A. japonicus japonicus, but that A. japonicus japonicus may escape these interspecific effects by utilizing spatially partitioned container habitats.     

Does differential predation permit invasive and native mosquito larvae to coexist in Florida?

Abstract.  1. The hypothesis that selective predation on larvae of the invasive Aedes albopictus (Skuse) could account for its stable coexistence with the native mosquito species and inferior competitor Ochlerotatus triseriatus (Say) in Florida treeholes and container systems was tested experimentally.
2. Functional responses of the two dipteran predators Toxorhynchites rutilus (Coquillett) and Corethrella appendiculata (Grabham) were evaluated separately for A. albopictus and O. triseriatus prey. Both predators exhibited type II functional responses and consistently consumed more of the invasive species. Handling time of T. rutilus feeding upon O. triseriatus was significantly longer than when preying upon the invasive species.
3. When either predator species was offered varying ratios of the two prey species, A. albopictus was consumed preferentially. The absence of a prey ratio effect on preference indicated that switching probably does not occur.
4. The higher maximum feeding rate upon, and preference for, A. albopictus suggests that differential predation may foster coexistence of the invasive and native mosquito prey species in Florida.     

A survey of mosquitoes breeding in used tires in Spain for the detection of imported potential vector species.

The used tire trade has facilitated the introduction, spread, and establishment of the Asian tiger mosquito, Aedes albopictus, and other mosquito species in several countries of America, Africa, Oceania, and Europe. A strategy for detecting these imported mosquito vectors was developed in Spain during 2003-2004 by EVITAR (multidisciplinary network for the study of viruses transmitted by arthropods and rodents). A survey in 45 locations found no invasive species. Eight autochthonous species of mosquitoes were detected in used tires, including Culex pipiens, Cx. hortensis, Cx. modestus, Anopheles atroparvus, An. claviger, Culiseta longiareolata, Cs. annulata, and Aedes caspius. Dominant species were Cx. pipiens and Cs. longiareolata. Aedes caspius was found in only once, near its natural breeding habitat. Considering the recent discovery of an established population of Ae. albopictus in Catalonia, the increasing commerce of used tires in Spain for recycling, storage, and recapping might greatly contribute to the rapid spread of this species across the Iberian Peninsula.     

Larval competition alters susceptibility of adult Aedes mosquitoes to dengue infection

Dengue, the most important human arboviral disease, is transmitted primarily by Aedes aegypti and, to a lesser extent, by Aedes albopictus. The current distributions of these invasive species overlap and are affected by interspecific larval competition in their container habitats. Here we report that competition also enhances dengue infection and dissemination rates in one of these two vector species. We determined the effects of competition on adult A. aegypti and A. albopictus, comparing their susceptibility to infection with a Southeast Asian strain of dengue-2 virus. High levels of intra- or interspecific competition among larvae enhanced the susceptibility of A. albopictus to dengue virus infection and potential for transmission, as indicated by disseminated infections. Doubling the number of competing larvae (A. albopictus or A. aegypti), led to a significant (more than 60%) increase in the proportion of A. albopictus with disseminated dengue-2 infection. Competition-enhanced vector competence appears to result from a reduction in 'barriers' (morphological or physiological) to virus infection and dissemination and may contribute to the importance of A. albopictus in dengue transmission. Similar results for other unrelated arboviruses suggest that larval competition, common in mosquitoes, should be considered in estimates of vector competence for pathogens that infect humans.     

Ecology of forest insect invasions

Forests in virtually all regions of the world are being affected by invasions of non-native insects. We conducted an in-depth review of the traits of successful invasive forest insects and the ecological processes involved in insect invasions across the universal invasion phases (transport and arrival, establishment, spread and impacts). Most forest insect invasions are accidental consequences of international trade. The dominant invasion ‘pathways’ are live plant imports, shipment of solid wood packaging material, “hitchhiking” on inanimate objects, and intentional introductions of biological control agents. Invading insects exhibit a variety of life histories and include herbivores, detritivores, predators and parasitoids. Herbivores are considered the most damaging and include wood-borers, sap-feeders, foliage-feeders and seed eaters. Most non-native herbivorous forest insects apparently cause little noticeable damage but some species have profoundly altered the composition and ecological functioning of forests. In some cases, non-native herbivorous insects have virtually eliminated their hosts, resulting in major changes in forest composition and ecosystem processes. Invasive predators (e.g., wasps and ants) can have major effects on forest communities. Some parasitoids have caused the decline of native hosts. Key ecological factors during the successive invasion phases are illustrated. Escape from natural enemies explains some of the extreme impacts of forest herbivores but in other cases, severe impacts result from a lack of host defenses due to a lack of evolutionary exposure. Many aspects of forest insect invasions remain poorly understood including indirect impacts via apparent competition and facilitation of other invaders, which are often cryptic and not well studied.     

Generation of a novel Wolbachia infection in Aedes albopictus (Asian tiger mosquito) via embryonic microinjection

Genetic strategies that reduce or block pathogen transmission by mosquitoes are being investigated as a means to augment current control measures. Strategies of vector suppression and replacement are based upon intracellular Wolbachia bacteria, which occur naturally in many insect populations. Maternally inherited Wolbachia have evolved diverse mechanisms to manipulate host insect reproduction and promote infection invasion. One mechanism is cytoplasmic incompatibility (CI) through which Wolbachia promotes infection spread by effectively sterilizing uninfected females. In a prior field test, releases of Wolbachia-infected males were used to suppress a field population of Culex pipiens. An additional strategy would employ Wolbachia as a vehicle to drive desired transgenes into vector populations (population replacement). Wolbachia-based population suppression and population replacement strategies require an ability to generate artificial Wolbachia associations in mosquitoes. Here, we demonstrate a technique for transferring Wolbachia (transfection) in a medically important mosquito species: Aedes albopictus (Asian tiger mosquito). Microinjection was used to transfer embryo cytoplasm from a double-infected Ae. albopictus line into an aposymbiotic line. The resulting mosquito line is single-infected with the wAlbB Wolbachia type. The artificially generated infection type is not known to occur naturally and displays a new CI crossing type and the first known example of bidirectional CI in Aedes mosquitoes. We discuss the results in relation to applied mosquito control strategies and the evolution of Wolbachia infections in Ae. albopictus.     

The role of refuges in biological invasions: A systematic review

Aim

Ecological refuges buffer organisms against stressors and mediate a range of species interactions. However, their role in the context of biological invasions has yet to be synthesized, despite the increasing prevalence and impact of non-native species. To address this, we conducted a systematic review aiming to determine the extent to which refuges are considered explicitly in the invasion literature and to synthesize their function.

Location

Global.

Time period

Present day.

Major taxa studied

All.

Methods

Our search of the literature was conducted using the SCOPUS and Web of Science databases and followed the preferred reporting items for systematic reviews and meta-analyses (PRISMA) protocol. We obtained 315 records of refuge use in biological invasions from 300 studies. From each record, we extracted information relating to the experimental design, species characteristics and refuge type, where available.

Results

Refuges and refuge-mediated processes are widely reported in the invasion literature. Native species commonly use refuges to avoid non-native predation and competition, with spatial complexity and habitat heterogeneity key factors in facilitating their coexistence. Records show that artificial structures safeguard non-natives in their introduced range. However, there were key differences in the use of such structures in marine and terrestrial environments. Moreover, the enhanced structural complexity created by non-native plants and bivalves is often reported to act as a predation refuge for other species.

Main conclusions

The ubiquity of refuge-based processes suggests that refuges can play an important role in affecting the persistence, spread and impacts of non-native species, either through previously described mechanisms (i.e. refuge-mediated apparent competition and the persistent pressure scenario) or through a mechanism we describe (i.e. when non-native species use existing refuges), or both.     

Timing of resource input and larval competition between invasive and native container-inhabiting mosquitoes (Diptera: Culicidae).

Container-inhabiting mosquito species are subject to both intraspecific and interspecific competition during larval development in resource-limited habitats. The arrival of an invasive species, Aedes albopictus, in the U.S. has altered competitive interactions among container-inhabiting mosquito species and, in some cases, has led to displacement of these species. Resource enrichment of container habitats has been shown to alleviate competitive interactions and to promote species co-existence; however, the importance of the timing of enrichment has yet to be explored. Larval competition between Ae. albopictus and a native species, Ochlerotatus triseriatus, was explored when resources were added either gradually or in a single pulse. Replacement series experiments revealed that Ae. albopictus was able to outcompete and displace Oc. triseriatus via resource monopolization when all resources were made available simultaneously; however, when the same resource amount was added over time, survival was high for both species, leading to co-existence. Timing of resource input also had an effect in monospecific treatments, indicating that intraspecific competition impacts survival as well. Duration of larval development was influenced by both species presence and by timing of resource input for Oc. triseriatus. These results indicate competitive outcome is condition-specific and that timing of resource input can determine whether a dominant invasive competitor displaces a native species, or if the two species are able to co-exist. Both intraspecific and interspecific competition occur at different temporal scales due to species-specific differences in larval developmental time. Timing of resource availability in container habitats can impact mosquito survival via competitive interactions, which can ultimately influence vector population size and behavior, possibly influencing vector-borne disease transmission.     

A review of ecological interactions between native frogs and invasive cane toads in Australia

Translocated from their native range in the Americas in 1935, cane toads (Rhinella marina, Bufonidae) have now spread through much of tropical and subtropical Australia. The toad's invasion and impact have attracted detailed study. In this paper, I review information on ecological interactions between cane toads and Australian anurans. The phylogenetic relatedness and ecological similarity between frogs and toads creates opportunities for diverse interactions, ranging from predation to competition to parasite transfer, plus a host of indirect effects mediated via impacts of toads on other species, and by people's attempts to control toads. The most clear‐cut effect of toads on frogs is a positive one: reducing predator pressure by fatally poisoning anuran‐eating varanid lizards. However, toads also have a wide range of other effects on frogs, some positive (e.g. taking up parasites that would otherwise infect native frogs) and others negative (e.g. eating frogs, poisoning frogs, competing with tadpoles). Although information on such mechanisms predicts intense interactions between toads and frogs, field surveys show that cane toad invasion has negligible overall impacts on frog abundance. That counter‐intuitive result is because of a broad balancing of negative and positive impacts, coupled with stochastic (weather‐induced) fluctuations in anuran abundance that overwhelm any impacts of toads. Also, the impacts of toads on frogs differ among frog species and life‐history stages, and depend upon local environmental conditions. The impacts of native frogs on cane toads have attracted much less study, but may well be important: frogs may impose biotic resistance to cane toad colonization, especially via competition in the larval phase. Overall, the interactions between native frogs and invasive toads illustrate the diverse ways in which an invader's arrival can perturb the native fauna by both direct and indirect mechanisms, and by which the native species can curtail an invader's success. These studies also offer a cautionary tale about the difficulty of predicting the impact of an invasive species, even with a clear understanding of mechanisms of direct interaction.     

淡水鱼类入侵种的分布、入侵途径、机制与后果

生物入侵已经成为全球面临的三大环境问题之一。鱼类入侵现象也随全球经济一体化的进程日益严重。本文综述了全球淡水鱼类入侵的现状和研究进展, 包括鱼类入侵的定义及分布、入侵途径和机制、产生的生态和社会经济影响以及预防措施等。据统计, 目前全球外来鱼类达624种, 该数量超过30年前的两倍。外来鱼类主要通过水产养殖(51%)、观赏渔业(21%)、休闲垂钓(12%)、渔业捕捞运输(7%)等多种途径被引进。入侵鱼类对本地种产生了捕食、种内种间竞争、杂交和疾病传播等负面影响, 破坏本地生态系统, 但是其正面的生态及社会经济影响也不可忽略。近20年来全球鱼类入侵日益受到重视, 相关论文发表数量翻了8倍。值得提出的是, 近10年来全球鱼类入侵风险评价系统的研究显著增加, 一些鱼类入侵模型已应用于五大洲的多个国家。我国淡水外来鱼类共计439种。然而, 我国关于鱼类入侵的研究起步较晚, 发表文献数仅占全球的3.7%, 且主要研究方向仍集中在入侵物种的分布及生物学特性等基础研究上, 缺乏对于鱼类入侵机制及风险评价预测的研究。因此, 我们建议: (1)开展全国范围的本底调查并建立数据库, 实现数据共享, 明确鱼类入侵的历史与分布现状; (2)联合多个政府部门和机构, 对鱼类入侵进行长期观测, 从整个水生生态系统的角度出发, 深入了解其入侵机制及其产生的正面和负面生态和社会经济影响; (3)加强增殖放流的科学研究和管理; (4)构建区域性外来鱼类入侵风险评价系统, 有效预测鱼类入侵活动, 评价入侵种的危害, 并为相关政府部门的决策提供科学依据。     

Global distribution,entry routes,mechanisms and consequences of invasive freshwater fish

Biological invasion is now considered one of the three major environmental issues worldwide. Freshwater fish invasion becomes more serious with globalization of the world economy. We reviewed the current status of global freshwater fish invasions and discussed the definitions, distributions, introduction pathways, mechanisms, ecological and economic impacts, and risk assessments of freshwater fish invasions. Non-native fish are mainly introduced through food aquaculture (51%), as ornamental fish (21%), or for sport fishing (12%) and fisheries (7%). The number of introduced fish has reached 624 species, doubled the number found thirty years ago. Successful invasions may bring many negative ecological consequences, such as predation, hybridization, structure and function alteration of local freshwater ecosystems, as well as diseases transmission. However, it also brings positive biological and economic values. The number of fish invasion studies has increased eight times over the last 20 years, with studies mainly focusing on biology and the biological impact of invasive fish species. Risk assessments of freshwater fish invasions were studied over the last 10 years, and fish invasiveness screening models have been applied in countries of five continents. The number of non-native freshwater fish in China totaled 439. However, research papers on freshwater fish invasions in China was only 3.7% of the global total, and these researches were mainly on the distribution and biology of invasive fish species, and very few studies included risk assessments. Therefore, we suggest investigating the history, distribution, and mechanisms of invasive species at the national level, evaluating both the positive and negative effects of freshwater fish invasions, and also reinforcing studies of risk assessments in China.     

Effects of invasive cane toads on Australian mosquitoes: Does the dark cloud have a silver lining?

Research on the ecological impacts of invasive organisms typically looks only for negative impacts, ignoring the possibility that the wider community might see benefits in some of these effects. To truly understand the impact of invasive species, we need to look as broadly as possible, and incorporate studies on a diversity of variables. The spread of the South American cane toad (Bufo marinus) through tropical Australia is widely viewed as an ecological catastrophe, but anecdotal reports suggest that the invasion of toads may reduce the numbers of mosquitoes (and thus, potentially, the risk they pose to human health). We conducted experiments to determine whether the presence of toad tadpoles affects survival rates, adult body sizes and/or rates of oviposition of four species of disease-carrying mosquitoes. In the laboratory, the presence of toad tadpoles significantly reduced the sizes of adult mosquitoes at emergence, and also reduced survival rates of the larvae of one mosquito species. In field trials, mosquitoes were less likely to oviposit in waterbodies containing toad tadpoles. Accordingly, these data suggest (but do not prove) that toad invasion may reduce mosquito abundance. More generally, any overall evaluation of the impact of an invasive species needs to consider possible benefits (e.g. to human health) as well as negative effects (e.g. to native species). Both types of information are essential to inform community decisions about the management of feral taxa such as the cane toad in Australia.     

入侵植物的繁殖策略以及对本土植物繁殖的影响

理解入侵生物的繁殖策略是阐明生物入侵机制的一个重要方面。入侵植物常表现出一些共同的繁殖特征, 如以两性花为主的性系统、自动自交为主的繁育系统或不依赖传粉媒介的无融合生殖和无性繁殖以及高生殖投资的资源配置策略等。成功入侵的外来植物通过影响本土的传粉者, 在种群和群落水平上影响本土植物的有性繁殖, 甚至促使某些本土植物在繁殖对策和表型性状上发生快速转变。目前, 入侵植物繁殖策略及其生态效应的研究多侧重于入侵种的快速演化, 而有关外来植物与本土植物间的相互影响及其可能存在的协同适应研究还较为缺乏。探讨本土植物在外来种入侵压力下的繁殖对策和响应机制, 将丰富人们对物种间竞争、共存及群落构建等机制的深入了解。从繁殖和适应的角度探求入侵植物与本土植物之间的复杂关系, 将有助于解析生物入侵的机制及人类干扰下的物种演化规律, 也为预测和防控入侵植物提供科学依据。     

Competition and resistance to starvation in larvae of container-inhabiting Aedes mosquitoes

Abstract. 1. Hypotheses about declining populations of container-inhabiting Aedes mosquitoes following the invasion by additional species were tested.
2. The larval competition hypothesis was studied experimentally in pure and mixed cultures of Aedes aegypti (L.), A.albopictus (Skuse) and A.triseriatus (Say). The experiments used decomposing leaf litter in the laboratory, as opposed to most previous research which used non-natural food.
3. Resistance to starvation is introduced as a new measure of larval performance and competitiveness. The hypothesis is that more successful larvae store larger energy reserves and resist the lack of food longer.
4. Contrary to previous research showing better performance of A.aegypti in mixed cultures, A.albopictus developed faster and had greater survival when natural food was used.
5. Resistance to starvation was greater in the better performing species (i.e. A.aegypti with non-natural food and A.albopictus with leaf litter). Oxygen consumption by starved larvae was similar in the three container species, and in the ground-water mosquito, A.taeniorhynchus (Wied.), whose resistance to starvation was comparatively very low.     

Effects of predation by the copepod Mesocyclops ogunnus on the sex ratios of mosquito Aedes albopictus

Cyclopoid copepods are important predators in many aquatic ecosystems and have been used as biological agents in successful programs to control mosquito larvae. However, the impacts of this predation on adult mosquito populations are still poorly understood. The present study compared the sex ratios and body sizes (measured as wing length) of Aedes albopictus mosquitoes emerging from recipients containing the copepod predator Mesocyclops ogunnus with control situations without this predator. We found that copepod predation significantly biased mosquito sex ratios toward females, and that both the males and females emerging from copepod-containing recipients were significantly larger than control insects. The ecological and epidemiological consequences of the changes induced by copepod predation on mosquito populations are discussed.     

外来种对生物多样性的影响及其控制

外来种是那些借助自身力量或其它外界力量传播到其未曾分布过的地域 ,并且能进行繁殖传播的生物。外来种入侵已成为一种引人关注的现象。外来种通过竞争、捕食、牧食、改变生境和传播疾病等方式对本地生物产生威胁 ,影响本地生物多样性。外来种入侵成了生物多样性丧失的两个主要影响之一 (另一影响是生境的破坏 )。因此 ,探寻阻止或减少外来种入侵的方法很有必要。目前 ,人们运用机械法、化学法和生物控制法来控制外来种。在外来种入侵的初始阶段或外来种数量不多时 ,运用机械法较好。化学法有带来新环境污染的危险。生物控制法是应用天敌来防治或消灭有害生物。在外来种的控制上 ,生物控制法有一些成功的案例 ,但它并不是万能的。有些生物控制剂可能对非目标种产生影响 ,这要求在释放前对生物控制剂作更严格的检测。     

Optimal barrier zones for stopping the invasion of Aedes aegypti mosquitoes via transgenic or sterile insect techniques

Biological invasions have dramatically altered the natural world by threatening native species and their communities. Moreover, when the invading species is a vector for human disease, there are further substantive public health and economic impacts. The development of transgenic technologies is being explored in relation to new approaches for the biological control of insect pests. We investigate the use of two control strategies, classical sterile insect techniques and transgenic late-acting bisex lethality (Release of Insects carrying a Dominant Lethal), for controlling invasion of the mosquito Aedes aegypti using a spatial stage-structured mathematical model. In particular, we explore the use of a barrier zone of sterile/transgenic insects to prevent or impede the invasion of mosquitoes. We show that the level of control required is not only highly sensitive to the rate at which the sterile/transgenic males are released in the barrier zone but also to the spatial range of release. Our models characterise how the distribution of sterile/transgenic mosquitoes in the barrier zone can be controlled so as to minimise the number of mass-produced insects required for the arrest of species invasion. We predict that, given unknown rates of mosquito dispersal, management strategies should concentrate on larger release areas rather than more intense release rates for optimal control.