Competitor‐free space mediates non‐target impact of an introduced biological control agent

Abstract 1. Enemy‐free space has been shown to mediate host shifts in herbivores, but this has not previously been documented in parasitoids. Also, natural enemies shown to maintain host shifts have always been from higher trophic levels, rather than competitors. 2. In Hawaii, an Australian parasitoid (Diachasmimorpha tryoni) of medflies that loses competition contests to a subsequently introduced Asian parasitoid (Fopius arisanus) has shifted its realised host range to attack non‐target gall flies on lantana. 3. The present study demonstrates experimentally that D. tryoni reproduction is: (i) lower on medflies in coffee when F. arisanus is present than when it is absent; (ii) higher in gall flies on lantana than on medflies in coffee, when F. arisanus is present; and (iii) higher in medflies on coffee than in gall flies on lantana, when F. arisanus is absent. This meets Berdegue et al.’s (Ecological Entomology, 21 , 203–217, 1996) three conditions to confirm the importance of enemy‐free space. 4. In the field, F. arisanus is abundant on medflies, whereas D. tryoni is rare on medflies, but is the dominant parasitoid of lantana gall flies. 5. Competitor‐free space is thus shown to be a key mechanism maintaining an apparent host shift by an introduced biocontrol agent onto a non‐target species.     

Phenology in a warming world: differences between native and non‐native plant species

Phenology is a harbinger of climate change, with many species advancing flowering in response to rising temperatures. However, there is tremendous variation among species in phenological response to warming, and any phenological differences between native and non‐native species may influence invasion outcomes under global warming. We simulated global warming in the field and found that non‐native species flowered earlier and were more phenologically plastic to temperature than natives, which did not accelerate flowering in response to warming. Non‐native species' flowering also became more synchronous with other community members under warming. Earlier flowering was associated with greater geographic spread of non‐native species, implicating phenology as a potential trait associated with the successful establishment of non‐native species across large geographic regions. Such phenological differences in both timing and plasticity between native and non‐natives are hypothesised to promote invasion success and population persistence, potentially benefiting non‐native over native species under climate change.     

Detecting impacts of non‐native species on associated invertebrate assemblages depends on microhabitat

Invasive plants that displace native floral communities can cause changes to associated invertebrate species assemblages. Using a mini‐review of the literature and our own data we add to the still considerable debate about the most effective methods for testing community‐level impacts by invasive species. In endangered saltmarshes of southeast Australia, the non‐native rush Juncus acutus L. is displacing its native congener J. kraussii Hochst., with concurrent changes to floral and faunal assemblages. In two coastal saltmarshes, we tested the hypothesis that the ability to detect differences in the invertebrate assemblage associated with these congeneric rushes depends on the microhabitat of the plant sampled. We used three sampling methods, each targeting specific microhabitats: sweep netting of the plant stems, vacuum sampling of the plant tussock, and vacuum sampling of the ground directly below the plants. Over 3800 individuals and 92 morphospecies were collected across four main taxa: gastropods, crustaceans, hexapods and arachnids. Detection of differences in invertebrate density, richness and composition associated with native compared with non‐native rushes was dependent on the microhabitat sampled and these differences were spatially variable. For example, at one saltmarsh the stems and tussock of J. acutus had a lower density and richness of total invertebrates and hexapods than those of the native J. kraussii. In contrast, crustaceans on the ground were in greater abundance below J. acutus than J. kraussii. This study demonstrates that on occasions where overall differences in the assemblage are not detected between species, differences may become apparent when targeting different microhabitats of the plant. In addition, separately targeting multiple microhabitats likely leads to a greater probability of detecting impacts of invasion. Comparing the invertebrate assemblage without differentiating between or sampling an array of microhabitats can fail to determine the impact of invasive species. These results highlight that a combination of methods targeting different microhabitats is important for detecting differences within the invertebrate community, even for phylogenetically related species.     

From a non‐target to a target: identification of a fermentation volatile blend attractive to Zaprionus indianus

The African fig fly, Zaprionus indianus Gupta, is rapidly spreading through the New World and is a new potential pest for numerous fruit crops. Methods are needed to detect and monitor Z. indianus. A recent study shows that Z. indianus can be attracted with a mixture of wine and vinegar, but there are no chemical attractants yet identified. This fly was captured incidentally as a non‐target insect in experiments to develop chemical lures, based on wine and vinegar fermentation volatiles, for Drosophila suzukii Matsumura and Drosophila melanogaster Meigen. We then generated testable hypotheses on what combination of these volatiles was involved in Z. indianus attraction to wine and vinegar. We determined through a series of trapping experiments that the blend of ethanol, acetic acid, acetoin, isoamyl acetate, methionol and ethyl hexanoate constitutes a strong attractant for Z. indianus and accounts for its attraction to the combination of wine and vinegar. These results and findings provide the first opportunity to develop a long‐lasting and consistent chemical lure for trapping of Z. indianus. Such a lure in a suitable trap should provide a good means to document the spread of the fly and determine its seasonality and abundance in new areas and crops.     

Retention of gene diversity during the spread of a non‐native plant species

Spatial expansion, which is a crucial stage in the process to successful biological invasion, is anticipated to profoundly affect the magnitude and spatial distribution of genetic diversity in novel colonized areas. Here, we show that, contrasting common expectations, Pyrenean rocket (Sisymbrium austriacum), retained SNP diversity as this introduced plant species descended in the Meuse River Basin. Allele frequencies did not mirror between‐population distances along the predominant expansion axis. Reconstruction of invasion history based on the genotypes of historical herbarium specimens indicated no influence of additional introductions or multiple points of entry on this nongradual pattern. Assignment analysis suggested the admixture of distant upstream sources in recently founded downstream populations. River dynamics seem to have facilitated occasional long‐distance dispersal which brought diversity to the expansion front and so maintained evolutionary potential. Our findings highlight the merit of a historical framework in interpreting extant patterns of genetic diversity in introduced species and underscore the need to integrate long‐distance dispersal events in theoretical work on the genetic consequences of range expansion.     

Climate warming affects biological invasions by shifting interactions of plants and herbivores

Plants and herbivorous insects can each be dramatically affected by temperature. Climate warming may impact plant invasion success directly but also indirectly through changes in their natural enemies. To date, however, there are no tests of how climate warming shifts the interactions among invasive plants and their natural enemies to affect invasion success. Field surveys covering the full latitudinal range of invasive Alternanthera philoxeroides in China showed that a beetle introduced for biocontrol was rare or absent at higher latitudes. In contrast, plant cover and mass increased with latitude. In a 2‐year field experiment near the northern limit of beetle distribution, we found the beetle sustained populations across years under elevated temperature, dramatically decreasing A. philoxeroides growth, but it failed to overwinter in ambient temperature. Together, these results suggest that warming will allow the natural enemy to expand its range, potentially benefiting biocontrol in regions that are currently too cold for the natural enemy. However, the invader may also expand its range further north in response to warming. In such cases where plants tolerate cold better than their natural enemies, the geographical gap between plant and herbivorous insect ranges may not disappear but will shift to higher latitudes, leading to a new zone of enemy release. Therefore, warming will not only affect plant invasions directly but also drive either enemy release or increase that will result in contrasting effects on invasive plants. The findings are also critical for future management of invasive species under climate change.     

Increased activity and growth rate in the non‐dispersive aquatic larval stage of a damselfly at an expanding range edge

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Climate change,boundary increase and elongation of a pre‐existing cline: A case study in Drosophila ananassae

During the past two to three decades, Drosophila ananassae, a warm adapted tropical species, has invaded low to mid altitude localities in the western Himalayas. Due to its cold sensitivity, this species had never been recorded from higher latitudes as well as altitudes in India to the 1960s. A latitudinal cline in this desiccation‐sensitive species corresponds with southern humid tropical localities rather than northern drier subtropical localities. An extension of its cline into lowland to midland montane localities has resulted due to global climatic change as well as local thermal effects through anthropogenic impact. However, D. ananassae populations at species borders are characterized by lower genetic variability for body melanization as well as for desiccation resistance. There is a lack of thermal plastic effects for body melanization, and the observed extended cline might represent evolutionary (genetic) response due to selection pressure imposed by drier habitats. A comparison of fecundity, hatchability and viability at three growth temperatures (17, 20 and 25°C) showed significant reduction in trait values at 17°C in D. ananassae. Thus, its recent range expansion into northern montane localities might involve genetic effects on stress‐related traits and plastic effects on life history traits. We suggest that D. ananassae could serve as an indicator species for analyzing range expansion under changing climatic conditions.     

Evolutionary history predicts high‐impact invasions by herbivorous insects

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Comparing the effects of GM and non‐GM soybean varieties on non‐target arthropods

In order to guarantee the safety of genetically modified (GM) soybean crops, it is important to assess the potential toxicity of their expressed insecticidal proteins to non‐target organisms. In the present study, the effects of the GM soybean Insulin‐like Growth Factor (IGF), which is tolerant to the herbicide glufosinate, on plant‐dwelling non‐target insects and arachnids were evaluated in soybean agroecosystems. For comparison, the non‐GM parental cultivar of soybean Gwangan‐kong was used as a control. Data were collected in 2016 and 2017 via surveying at Ochang and Jeonju, Korea. In total, 13,031 individual insects and arachnids, representing 64 families in 11 orders, were captured during the study. Firstly, the results indicate that the GM soybean IGF did not negatively affect plant‐dwelling non‐target insects and arachnids. However, the numbers of captured individuals on both IGF and Gwangan‐kong were higher at Ochang in 2017. The occurrence of insect pests, natural enemies, and other insects differed significantly according to region, region and survey year, and survey year, respectively. In addition, the dominance, diversity, evenness, and richness indices for the collected insects varied significantly among the regions and survey years regardless of soybean variety. The score from PROXSCAL multidimensional scaling using combined data showed that insects and arachnids in different natural environments were separated by their cultivation regions and years irrespective of soybean cultivars.     

Experimental warming disrupts reproduction and dung burial by a ball‐rolling dung beetle

1. Insects are sensitive to climate change. Consequently, insect‐mediated ecosystem functions and services may be altered by changing climates. 2. Dung beetles provide multiple services by burying manure. Using climate‐controlled chambers, the effects of warming on dung burial and reproduction by the dung beetle Sisyphus rubrus Paschalidis, 1974 were investigated. Sisyphus rubrus break up dung by forming and rolling away balls of manure for burial and egg deposition. 3. To simulate warming in the chambers, 0, 2 or 4 °C offsets were added to field‐recorded, diurnally fluctuating temperatures. We measured dung ball production and burial, egg laying, survival and residence times of beetles. 4. Temperature did not affect the size or number of dung balls produced; however warming reduced dung ball burial by S. rubrus. Because buried balls were more likely to contain eggs, warming could reduce egg laying via a reduction in ball burial. Warming reduced the humidity inside the chambers, and a positive relationship was found between the number of dung balls produced and humidity in two temperature treatments. Temperature did not affect survival, or whether or not a beetle left a chamber. Beetles that did leave the chambers took longer to do so in the warmest treatment. 5. This study demonstrates that climate warming could reduce reproduction and dung burial by S. rubrus, and is an important first step to understanding warming effects on burial services. Future studies should assess warming effects in field situations, both on individual dung beetle species and on aggregate dung burial services.     

Climate warming alters effects of management on population viability of threatened species: results from a 30‐year experimental study on a rare orchid

Climate change is expected to influence the viability of populations both directly and indirectly, via species interactions. The effects of large‐scale climate change are also likely to interact with local habitat conditions. Management actions designed to preserve threatened species therefore need to adapt both to the prevailing climate and local conditions. Yet, few studies have separated the direct and indirect effects of climatic variables on the viability of local populations and discussed the implications for optimal management. We used 30 years of demographic data to estimate the simultaneous effects of management practice and among‐year variation in four climatic variables on individual survival, growth and fecundity in one coastal and one inland population of the perennial orchid Dactylorhiza lapponica in Norway. Current management, mowing, is expected to reduce competitive interactions. Statistical models of how climate and management practice influenced vital rates were incorporated into matrix population models to quantify effects on population growth rate. Effects of climate differed between mown and control plots in both populations. In particular, population growth rate increased more strongly with summer temperature in mown plots than in control plots. Population growth rate declined with spring temperature in the inland population, and with precipitation in the coastal population, and the decline was stronger in control plots in both populations. These results illustrate that both direct and indirect effects of climate change are important for population viability and that net effects depend both on local abiotic conditions and on biotic conditions in terms of management practice and intensity of competition. The results also show that effects of management practices influencing competitive interactions can strongly depend on climatic factors. We conclude that interactions between climate and management should be considered to reliably predict future population viability and optimize conservation actions.     

Climate controls the distribution of a widespread invasive species: implications for future range expansion

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Lethal ovitrap deployment for Aedes aegypti control: potential implications for non‐target organisms

In Australia, dengue control combines source reduction with lethal ovitraps to reduce Aedes aegypti populations during outbreaks. Lethal ovitraps are considered a sustainable and environmentally friendly method of controlling container‐inhabiting mosquitoes, however, to‐date, this claim has not been quantified. This study assesses the potential impact of lethal ovitraps on non‐target organisms when used to control Ae. aegypti in tropical Australia. For retention of specimens, we substituted standard sticky ovitraps for lethal ovitraps. We collected 988 Ae. aegypti and 44,132 non‐target specimens over 13 months from 16 sites. Although Ae. aegypti comprised only 2.2% of the total collection, they were were the eighth most dominant taxa collected, on the 93^rd percentile. Of the non‐target organisms, Collembola were the dominant taxa, 44.2%, with 36.8% and 10.5% Diptera and Hymenoptera, respectively. Of the Dipterans, 61% were family Phoridae. Lethal ovitraps were visited by 90 insect or invertebrate families in total. Ovitraps are attractive to Collembola, Phoridae, Sciaridae, Formicidae, and Culicidae, with minimal attraction by Apidae and other commonly monitored non‐target organisms. For container‐inhabiting mosquitoes, LOs are cost effective operationally, requiring minimal staff resources for placement and retrieval.     

Effect of elevated CO2 on tropical soda apple and its biological control agent Gratiana boliviana (Coleoptera: Chrysomelidae)

Rising atmospheric CO₂ levels could have drastic effects on the performance of invasive weeds and their insect herbivores. Despite the importance of biological control as an effective management tool for environmental weeds, there have been few studies on the potential impact of climate change on the future efficacy of biological control. The objective of the present study was to evaluate the effect of elevated CO₂ on the performance of tropical soda apple Solanum viarum (Solanaceae) and its biological control agent Gratiana boliviana (Coleoptera: Chrysomelidae). We established three levels of CO₂ in environmental growth chambers: ambient (400 ppm), medium (580 ppm) and high (780 ppm). Plants growing at the high level had greater biomass compared to those growing at the ambient and medium levels of CO₂. Leaf water content and the amount of leaf nitrogen were reduced at high compared to ambient or medium CO₂ levels. G. boliviana immature survival and developmental time were negatively affected at high CO₂ but not at medium or ambient levels. Adults were lighter and smaller when reared at the high CO₂ level compared to ambient and medium treatments, while adult fecundity was higher at the medium CO₂ level. Leaf area consumed by fifth instars was lower when feeding on plants grown at the high CO₂ level either inside a Petri dish or on potted plants. These results suggest that beetle performance may be diminished under future climate. However, further studies should incorporate other factors such as temperature and precipitation as well as the evolutionary potential of herbivores and plants to adapt to a changing climate.     

Climate warming is predicted to reduce omega‐3, long‐chain,polyunsaturated fatty acid production in phytoplankton

Phytoplankton are the main source of energy and omega‐3 (n‐3) long‐chain essential fatty acids (EFA) in aquatic ecosystems. Their growth and biochemical composition are affected by surrounding environmental conditions, including temperature, which continues to increase as a result of climate warming. Increasing water temperatures may negatively impact the production of EFA by phytoplankton through the process of homeoviscous adaptation. To investigate this, we conducted an exploratory data synthesis with 952 fatty acid (FA) profiles from six major groups of marine and freshwater phytoplankton. Temperature was strongly correlated with a decrease in the proportion of n‐3 long‐chain polyunsaturated FA (LC‐PUFA) and an increase in omega‐6 FA and saturated FA. Based on linear regression models, we predict that global n‐3 LC‐PUFA production will be reduced by 8.2% for eicosapentaenoic acid (EPA) and 27.8% for docosahexaenoic acid (DHA) with an increase in water temperature of 2.5 °C. Using a previously published estimate of the global production of EPA by diatoms, which contribute to most of the world's supply of EPA, we predict a loss of 14.2 Mt of EPA annually as a result of ocean warming. The n‐3 LC‐PUFA are vitally important for an array of key physiological functions in aquatic and terrestrial organisms, and these FA are mainly produced by phytoplankton. Therefore, reduced production of these EFA, as a consequence of climate warming, is predicted to negatively affect species that depend on these compounds for optimum physiological function. Such profound changes in the biochemical composition of phytoplankton cell membranes can lead to cascading effects throughout the world's ecosystems.     

Effects of climate‐induced increases in summer drought on riparian plant species: a meta‐analysis

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