A meta-analysis of genetic correlations between plant resistances to multiple enemies

Genetic correlations between plant resistances to multiple natural enemies are important because they have the potential to determine the mode of selection that natural enemies impose on a host plant, the structure of herbivore and pathogen communities, and the success of plant breeding for resistance to multiple diseases and pests. We conducted a meta-analysis of 29 published studies of 16 different plant species reporting a total of 467 genetic correlations between resistances to multiple herbivores or pathogens. In general, genetic associations between resistances to multiple natural enemies tended to be positive regardless of the breeding design, type of attacker, and type of host plant. Positive genetic correlations between resistances were stronger when both attackers were pathogens or generalist herbivores and when resistance to different enemies was tested independently, suggesting that generalists may be affected by the same plant resistance traits and that interactions among natural enemies are common. Although the mean associations between resistances were positive, indicating the prevalence of diffuse selection and generalized defenses against multiple enemies, the large variation in both the strength and the direction of the associations suggests a continuum between pairwise and diffuse selection.     

CLONAL VARIATION AND COVARIATION IN APHID RESISTANCE TO PARASITOIDS AND A PATHOGEN

Abstract The potential rate of evolution of resistance to natural enemies depends on the genetic variation present in the population and any trade-offs between resistance and other components of fitness. We measured clonal variation and covariation in pea aphids ( Acyrthosiphon pisum ) for resistance to two parasitoid species ( Aphidius ervi and A. eadyi ) and a fungal pathogen ( Erynia neoaphidis ). We found significant clonal variation in resistance to all three natural enemies. We tested the hypothesis that there might be trade-offs (negative covariation) in defensive ability against different natural enemies, but found no evidence for this. All correlations in defensive ability were positive, that between the two parasitoid species significantly so. Defensive ability was not correlated with fecundity. A number of aphid clones were completely resistant to one parasitoid ( A. eadyi ), but a subset of these failed to reproduce subsequently. We discuss the factors that might maintain clonal variation in natural enemy resistance.     

Does low nutritional quality act as a plant defence? An experimental test of the slow‐growth,high‐mortality hypothesis

Abstract.  1. The slow-growth, high-mortality hypothesis was experimentally tested in this study by investigating the effects of plant quality and natural enemies on leaf-miner growth, performance, and survivorship. Two leaf miners ( Acrocercops albinatella and Brachys tesselatus ) occurring on the turkey oak Quercus laevis were studied using a factorial design that manipulated predation/parasitism pressure and plant nutritional quality.
2. Forty trees were randomly divided into four treatments: (1) control plants (nutrients and natural enemies unaltered); (2) nutrients added, natural enemies unaltered; (3) nutrients unaltered, natural enemies reduced; and (4) nutrients added and natural enemies reduced. Water content, leaf toughness, tannin concentration, and foliar nitrogen were quantified monthly for each plant, and mine growth and survivorship were assessed by tracing mines on a 2–3-day interval and by following the fates of 50 mines per species per treatment combination.
3. Fertilised plants exhibited significantly higher amounts of nitrogen, but no significant differences among treatments were observed for water content, leaf toughness, and tannin concentration. These results only partially support the slow-growth, high-mortality hypothesis, as mines were significantly smaller and developed faster on fertilised plants, but neither fertilisation nor natural enemy exclusion significantly affected mine survivorship or mortality caused by natural enemies.     

Effects of variation among plant species on the interaction between a herbivore and its parasitoid

Abstract.  1. Previous studies have demonstrated that phenotypic traits of plants have the potential to affect interactions between herbivores and their natural enemies. Consequently, the impact of natural enemies on herbivore vital rates and population dynamics may vary among plant species. This study was designed to investigate the potential for density-dependent parasitism of an aphid herbivore feeding on six different host plant species.
2. Population densities of the aphid Aphis nerii B de F (Homoptera: Aphididae) and its parasitoid Lysiphlebus testaceipes Cresson (Hymenoptera: Braconidae) were recorded within a single growing season on six different species of milkweed in the genus Asclepias L. (Asclepiadaceae). Asclepias species are known to vary in their quality as food for herbivores. Although data on plant quality were not available in this study, population data were analysed to determine the effects of different Asclepias species on rates of parasitism and aphid population growth.
3. Parasitism rates of A. nerii varied among Asclepias species but were temporally density dependent over at least some range of aphid density on all plant species. Aphid population growth rates also varied among Asclepias species, and declined with an increase in the maximum parasitism rates among plant species; however, in no case was density-dependent parasitism sufficient to prevent exponential population growth of aphids within the growing season. The results serve to emphasise that, if natural enemies are to regulate herbivore populations, density-dependent mortality is a necessary, but not sufficient, condition for regulation.     

生境异质度对稻田捕食性天敌及水稻害虫的生态调节有效性

【目的】探索生境高异质度对稻田捕食性天敌及水稻害虫的生态调节有效性,了解这种策略是否会引起其他植食性昆虫成为水稻重要害虫的风险。【方法】2017-2018年连续2年种植单季稻,在稻田边缘种植花生与大豆,构建高异质性边缘生境稻田(rice paddy with high heterogeneous marginal habitats, HHR),调查HHR稻田与简单低异质性边缘生境稻田(rice paddy with low heterogeneous marginal habitats, LHR)中捕食性天敌与水稻害虫功能团的发生规律与相关性,计算益害比。【结果】2017年在HHR稻田中采集到捕食性天敌40种,1 667头;在LHR稻田中采集到捕食性天敌30种,991头。2018年在HHR稻田中采集到捕食性天敌33种,1 384头;在LHR稻田中采集到捕食性天敌34种,1 031头。HHR与LHR两类稻田中获得的捕食性天敌群落重要值P_i≥0.01的物种相似度很高,优势种相似。2017年HHR稻田的捕食性天敌物种丰富度明显高于LHR稻田,这种差异主要由群落重要值P_i<0.01的种类引起。2018年两类稻田的捕食性天敌物种丰富度没有差异。单位样方面积内的捕食性天敌个体数量,HHR中明显高于LHR,这种差异在2017年的分蘖期与成熟期达显著水平(P<0.05),在2018年的开花期极显著(P<0.01)。2017年在HHR中采集到水稻害虫22种,637头;在LHR中采集到水稻害虫19种,743头;物种相似性系数0.88。2018年在HHR中采集到水稻害虫16种,1 011头;在LHR中采集到水稻害虫16种,2 014头;物种相似性系数0.75;主要害虫物种组成结构相同。水稻害虫数量发生的时间动态分析表明,在分蘖期,虽然HHR稻田中的水稻害虫数量明显高于LHR(P<0.05),但此期害虫的数量不多,发生较轻。在孕穗期、开花期与成熟期,HHR稻田中的水稻害虫数量明显低于LHR稻田,这种差异在2017年的成熟期与2018年的孕穗期极显著(P<0.01),在2018年的成熟期差异显著(P<0.05)。2017年HHR和LHR中个体数量益害比N_pi值分别为2.62和1.33;2018年分别为1.37和0.51。【结论】具有高异质性边缘生境的稻田,能提高系统对捕食性天敌物种的涵养潜力,显著提高稻田捕食性天敌个体数量,提高益害比,具有更好的控制害虫的物质基础,促进捕食性天敌对水稻害虫的生态控制效能,不会引起其他植食性昆虫演变为水稻重要害虫风险,可为保护稻田生态系统天敌发挥生态效能提供可借鉴的策略与方法。     

Fouling mediates grazing: intertwining of resistances to multiple enemies in the brown alga Fucus vesiculosus

Macroalgae have to cope with multiple natural enemies, such as herbivores and epibionts. As these are harmful for the host, the host is expected to show resistance to them. Evolution of resistance is complicated by the interactions among the enemies and the genetic correlations among resistances to different enemies. Here, we explored genetic variation in resistance to epibiosis and herbivory in the brown alga Fucus vesiculosus, both under conditions where the enemies coexisted and where they were isolated. F. vesiculosus showed substantial genetic variation in the resistance to both epibiosis and grazing. Grazing pressure on the alga was generally lower in the presence than in the absence of epibiota. Furthermore, epibiosis modified the susceptibility of different algal genotypes to grazing. Resistances to epibiosis and grazing were independent when measured separately for both enemies but positively correlated when both these enemies coexisted. Thus, when the enemies coexisted, the fate of genotypes with respect to these enemies was intertwined. Genotypic correlation between phlorotannins, brown-algal phenolic secondary metabolites, and the amount of epibiota was negative, indicating that these compounds contribute to resistance to epibiosis. In addition, phlorotannins correlated also with the resistance to grazing, but this correlation disappeared when grazing occurred in the absence of epibiota. This indicates that the patterns of selection for the type of the resistance as well as for the resistance traits vary with the occurrence patterns of the enemies.     

Indirect cost of a defensive trait: variation in trichome type affects the natural enemies of herbivorous insects on <Emphasis Type="Italic">Datura wrightii</Emphasis>

The costs and benefits of defensive traits in plants can have an ecological component that arises from the effect of defenses on the natural enemies of herbivores. We tested if glandular trichomes in Datura wrightii, a trait that confers resistance to several species of herbivorous insects, impose an ecological cost by decreasing rates of predation by the natural enemies of herbivores. For two common herbivores of D. wrightii, Lema daturaphila and Tupiocoris notatus, several generalized species of natural enemies exhibited lower rates of predation on glandular compared to non-glandular plants. Lower rates of predation were associated with reductions in the residence time and foraging efficiency of natural enemies on plants with glandular trichomes, but not with direct toxic effects of glandular exudate. Our results suggest that the benefit of resistance to herbivores conferred by glandular trichomes might be offset by the detrimental effect of this trait on the natural enemies of herbivores, and that the fitness consequences of this trichome defense might depend on the composition and abundance of the natural-enemy community.     

枣粮间作系统节肢动物群落组成与时序动态

为揭示枣粮间作系统中枣园和农田两个亚系统节肢动物群落的关系,将枣粮间作系统区分为枣园亚系统和农田亚系统进行节肢动物生态调查并分析时序动态.调查共发现节肢动物14 936头,分属3纲、14目、96科,其中枣园亚系统个体5 992头,分属3纲、14目、82科,农田亚系统个体8 971头,分属3纲、14目、80科,且枣园、农田两个亚系统节肢动物群落的结构存在一定差异.对系统进行时间序列的最优分割可将其划分为4个不同的时期,即麦田亚系统衰落期、系统物种增长期、系统发展稳定期、系统动荡衰落期.系统主要天敌物种在4个阶段中表现出相互迁移的特性,且两个亚系统寄生性天敌物种对另一系统的害虫存在着制约作用.枣粮间作系统中枣园和农田两个亚系统节肢动物群落间的物种迁移和相互作用对提高系统的稳定性和控害能力有积极意义.     

Plant sex and induced responses independently influence herbivore performance, natural enemies and aphid-tending ants

Sex is an ecologically important form of genetic variation in dioecious plants, with males and females generally differing in constitutive resistance to herbivores. Yet little is known about sexual dimorphism with respect to induced or indirect defense, or whether sex-based differences are underlain by trade-offs among modes of defense. We compared male and female Valeriana edulis plants for constitutive and induced direct resistance to two herbivores, an early-season caterpillar and a late-season aphid, and for constitutive and induced indirect resistance in terms of abundance of natural enemies and aphid-tending ants. No sexual dimorphism was found in constitutive direct plant resistance, yet the sexes differed for constitutive indirect resistance, with 78?% more natural enemies and 117?% more ants present on females than males. Past feeding damage by caterpillars induced direct and indirect resistance in both males and females, increasing caterpillar development time by 26?% and the abundance of natural enemies by 147?%. Caterpillar feeding did not induce direct resistance with respect to caterpillar final mass or aphid performance. In all cases, there were no interactions between the effects of caterpillar damage and plant sex. In summary, plant sexual dimorphism and induced responses to herbivore damage independently influenced herbivore performance and the composition of arthropod communities at higher trophic levels.     

Direct and ecological costs of resistance and tolerance in the stinging nettle

Plant resistance and tolerance to herbivores, parasites, pathogens, and abiotic factors may involve two types of costs. First, resistance and tolerance may be costly in terms of plant fitness. Second, resistance and tolerance to multiple enemies may involve ecological trade-offs. Our study species, the stinging nettle ( Urtica dioica L.) has significant variation among seed families in resistance and tolerance as well as costs of resistance and tolerance to the holoparasitic plant Cuscuta europaea L. Here we report on variation among seed families (i.e. genetic) in tolerance to nutrient limitation and in resistance to both mammalian herbivores (i.e. number of stinging trichomes) and an invertebrate herbivore (i.e. inverse of the performance of a generalist snail, Arianta arbustorum). Our results indicate direct fitness costs of snail resistance in terms of host reproduction whereas we did not detect fitness costs of mammalian resistance or tolerance to nutrient limitation. We further tested for ecological trade-offs among tolerance or resistance to the parasitic plant, herbivore resistance, and tolerance to nutrient limitation in the stinging nettle. Tolerance of nettles to nutrient limitation and resistance to mammalian herbivores tended to correlate negatively. However, there were no significant correlations among resistance and tolerance to the different natural enemies (i.e. parasitic plants, snails, and mammals). The results of this greenhouse study thus suggest that resistance and tolerance of nettles to diverse enemies are free to evolve independently of each other but not completely without direct costs in terms of plant fitness.     

Host tolerance does not impose selection on natural enemies

Coevolution between hosts and their natural enemies is believed to operate through the evolution of resistance traits. Although the importance of tolerance to natural enemies as an alternative defensive strategy has been recognized, there is still no consensus about the possible role of host tolerance in the evolutionary outcome of the interaction. Here, using bioassay experiments, we tested the hypothesis that variation in host tolerance among selected plant genotypes could impose a selection pressure upon a specialist herbivore. Tolerance did not affect herbivore larvae survival, weight gain, efficiency of food consumption, total food consumption, developmental time and adult mass. These results therefore do not support the hypothesis that host tolerance could affect natural enemy performance. However, resistance did negatively affect herbivore larva survival. Genetic variation in herbivore larva survival was detected, thus suggesting the potential for a coevolutionary response. Our results indicate that host tolerance would reduce opportunities for a coevolutionary response by the natural enemies of the host. Contrary to predictions from previous models, our results suggest that host tolerance may constitute an evolutionarily unstable defensive strategy.     

Aphid population dynamics: does resistance to parasitism influence population size?

1. Insect population size is regulated by both intrinsic traits of organisms and extrinsic factors. The impacts of natural enemies are typically considered to be extrinsic factors, however insects have traits that affect their vulnerability to attack by natural enemies, and thus intrinsic and extrinsic factors can interact in their effects on population size. 2. Pea aphids Acyrthosiphon pisum Harris (Hemiptera: Aphididae) in New York and Maryland that are specialised on alfalfa are approximately two times more physiologically resistant to parasitism by Aphidius ervi Haliday (Hymenoptera: Braconidae) than pea aphids specialised on clover. To assess the potential influence of this genetically based difference in resistance to parasitism on pea aphid population dynamics, pea aphids, A. ervi, and other natural enemies of aphids in clover and alfalfa fields were sampled. 3. Rates of successful parasitism by A. ervi were higher and pea aphid population sizes were lower in clover, where the aphids are less resistant to parasitism. In contrast, mortality due to a fungal pathogen of pea aphids was higher in alfalfa. Generalist aphid predators did not differ significantly in density between the crops. 4. To explore whether intrinsic resistance to parasitism influences field dynamics, the relationship between resistance and successful field parasitism in 12 populations was analysed. The average level of resistance of a population strongly predicts rates of successful parasitism in the field. The ability of the parasitoid to regulate the aphid may vary among pea aphid populations of different levels of resistance.     

Phylogenetic distance can predict susceptibility to attack by natural enemies

If related species share enemies, variation in the damage experienced by species within a community may be predictable based on phylogeny. We examined the hypothesis that plant species more closely related to other community members experience greater herbivory by assessing leaf damage to native and exotic plants in two North American communities: an Eastern hardwood forest and a Rocky Mountain montane community. Pairwise phylogenetic distances between focal species and the hundreds of other native species in each community were calculated. We examined the influence of four measures of relatedness within each community: NND (phylogenetic distance to the nearest native neighbor), MPD (mean phylogenetic distance to the native species in the community), and two new metrics, MIPD (mean inverse phylogenetic distance) and INND (inverse nearest neighbor distance). These new metrics assume a nonlinear increase in interaction strength with relatedness; in the context of natural enemies, they posit that the sharing of enemies between any two species increases nonlinearly with their relatedness. Using regression models, we found that herbivore damage decreased with decreasing phylogenetic similarity of focal species to native species (as measured by MIPD) in both sites, although the pattern was significant only for native focal species in the montane community and exotic focal species in the hardwood forest. Similar decreases in herbivory with decreasing relatedness were detected using INND (montane natives) and MPD (hardwood forest exotics). There was no significant relationship between NND and herbivory for any of the four site by focal plant origin combinations. Our results are the first to support the hypothesis that native species can escape attack as a function of their phylogenetic dissimilarity to the larger community of native species, and to demonstrate that exotic species show these patterns in the wild (as opposed to in common gardens). We suggest that phylogenetic distance metrics assuming a nonlinear increase in interaction strength with relatedness show promise for broader application.     

Interspecific Interactions among Natural Enemies ofBemisiain an Inundative Biological Control Program

Interspecific interactions among insect natural enemies have seldom been investigated experimentally within the context of biological control. Research in this area is needed due to the often contradictory predictions provided by the many theoretical models, the increasing dependence on biological control, and the concern that biological control agents may adversely affect some nontarget organisms. We describe a study whereby the occurrence and dynamics of interspecific interactions among three natural enemies (two parasitoids:Encarsia formosaandEncarsia pergandiella;and one predatorDelphastus pusillus) of the whitefly,Bemisia argentifolii(previously referred to asBemisia tabacistrain “B”), were evaluated in greenhouse cage experiments. Eight populations consisting of all possible combinations of the three natural enemies and one population of whitefly alone were established to test the following hypotheses: (1) Natural enemy introductions are capable of suppressingB. argentifoliipopulations; (2) all interspecific interactions are detrimental to achieving biological control; (3) the likelihood of achieving biological control decreases as the potential number of interspecific interactions increases; and (4) the species composition of biological control agents is of greater consequence than the number of natural enemy species released. In addition, we tested the hypothesis (5) that the frequency of interspecific interactions increases with a decrease in host or prey availability. Our results demonstrate that all combinations of natural enemies provided significant levels of whitefly suppression. While the intensities of interspecific interactions among natural enemy species were frequently positively and significantly correlated with the densities of parasitized whitefly, interspecific interactions among natural enemies were not detrimental to achieving higher levels of biological control. The composition of species released, rather than the number of species released, was of greater importance to accomplishing biological control. Releases ofD. pusillusin combination with one or both of the parasitoids provided the greatest levels of whitefly suppression. These results suggest that the types of interspecific interactions rather than the numbers of interspecific interactions among natural enemies may be important to the outcome of inundative biological control programs.     

Phytophagy on phylogenetically isolated trees: why hosts should escape their relatives

Hosts belonging to the same species suffer dramatically different impacts from their natural enemies. This has been explained by host neighbourhood, that is, by surrounding host-species diversity or spatial separation between hosts. However, even spatially neighbouring hosts may be separated by many million years of evolutionary history, potentially reducing the establishment of natural enemies and their impact. We tested whether phylogenetic isolation of oak hosts from neighbouring trees within a forest canopy reduces phytophagy. We found that an increase in phylogenetic isolation by 100 million years corresponded to a 10-fold decline in phytophagy. This was not due to poorer living conditions for phytophages on phylogenetically isolated oaks. Neither species diversity of neighbouring trees nor spatial distance to the closest oak affected phytophagy. We suggest that reduced pressure by natural enemies is a major advantage for individuals within a host species that leave their ancestral niche and grow among distantly related species.     

大豆蚜自然天敌种群动态及其控蚜作用研究

2008-2010年间,分别在辽东山区和辽西半干旱丘陵地区设置试验田,采用系统调查的方法,对大豆蚜Aphis glycines Matsumura自然天敌种群动态及控蚜作用进行研究。共鉴定辽宁地区大豆蚜天敌7目、16科、44种,其中优势天敌异色瓢虫Leis axyridis(Pallas)居首位。田间试验结果表明,大豆蚜天敌田间消长表现连续6个阶段,即初见期、波动期、上升期、盛期、下降期和消退期;田间3年平均大豆蚜数量与天敌(天敌单位)总体呈极显著的相关关系,各年度百株蚜量与天敌单位也均呈极显著相关关系。辽东地区天敌跟随紧密并随蚜虫数量变化波动,具有明显的自然控蚜作用。其中,7月11-21日天敌发生盛期与蚜虫高峰期吻合,蚜虫急剧下降;7月下旬后,受高温、多雨、蚜霉菌作用、植株老化等影响,蚜虫种群逐步下降、消退,天敌也陆续迁出豆田。辽西地区天敌迁入豆田比蚜虫晚10～15d,对前期蚜虫控制弱,且天敌峰期滞后蚜虫5d左右,一般年份蚜虫发生较重。     

Influence of meteorological factors on the quantitative following relationship between Empoasca onukii Matsuda (Hemiptera: Cicadellidae) and its natural enemies in tea plantations

Our aim was to study the close relationship between the number of Empoasca onukii and its natural enemies in tea plantations to provide a scientific basis for the control of E. onukii. The relationship between the number of E. onukii and its main natural enemies in tea plantations in Hefei, China, were compared by gray relational analysis, and then the relationships between seven meteorological factors and the populations of E. onukii were analyzed by the method of path analysis. The results showed that among the top six natural enemies most closely related to the population of E. onukii, two natural enemies were the same in the three years of study and four natural enemies were the same in any two years of the study, and that the natural enemy species closely related to the population of E. onukii varied greatly among years. The direct effect of monthly average relative humidity was the greatest effect in 2020 and the direct effect of monthly average temperature was the greatest effect in 2021, with both being negative in terms of their effect on the population size of E. onukii. The direct effect of the number of days of rainfall was the greatest effect in both 2021 and 2022, and the indirect effect of monthly sunshine hours through rainfall days was the greatest effect on the population of E. onukii. The highest temperatures in early and mid-August 2022 were higher than in previous years, which had an impact on the growth and development of subsequent E. onukii.     

Invading from the garden? A comparison of leaf herbivory for exotic and native plants in natural and ornamental settings

Abstract The enemies release hypothesis proposes that exotic species can become invasive by escaping from predators and parasites in their novel environment. Agrawal et al. (Enemy release? An experiment with congeneric plant pairs and diverse above‐ and below‐ground enemies. Ecology, 86, 2979–2989) proposed that areas or times in which damage to introduced species is low provide opportunities for the invasion of native habitat. We tested whether ornamental settings may provide areas with low levels of herbivory for trees and shrubs, potentially facilitating invasion success. First, we compared levels of leaf herbivory among native and exotic species in ornamental and natural settings in Cincinnati, Ohio, United States. In the second study, we compared levels of herbivory for invasive and noninvasive exotic species between natural and ornamental settings. We found lower levels of leaf damage for exotic species than for native species; however, we found no differences in the amount of leaf damage suffered in ornamental or natural settings. Our results do not provide any evidence that ornamental settings afford additional release from herbivory for exotic plant species.     

麦田天敌种群动态及主要天敌对麦蚜捕食效能的研究

查明麦田害虫天敌有98种,其中捕食性天敌80种,寄生性天敌18种,对天敌种群动态作了系统观察,分析了影响天敌种群数量的环境因素,对大灰食蚜蝇,黑带食蚜蝇,七星瓢虫捕食麦蚜效能进行了探讨。     

夏大豆田主要害虫及天敌生态位研究

研究了7—8月份夏大豆田主要食叶性害虫及其天敌的生态位宽度和生态位重叠度。分析了各昆虫种间的竞争动态,害虫与其天敌在时间上的同步性和空间上的同域性均较强,为保护利用自然天敌控制夏大豆害虫提供了科学依据。