Herbivore species, infestation time, and herbivore density affect induced volatiles in tea plants

In response to insect herbivory, plants emit volatiles that are used by the herbivores’ natural enemies to locate their host or prey. Herbivore attack also enhances tea aroma. Herbivore-induced plant volatiles (HIPVs) vary both quantitatively and qualitatively with infestation duration and herbivore density. Thus, whether HIPVs can reliably communicate the identities of herbivores is of interest. Here, we studied the tea plant volatiles induced by the tea leafhopper (Empoasca vitis, a piercing–sucking insect), the tea geometrid (Ectropis oblique, a chewing insect), and methyl jasmonate (MeJA, a plant hormone). Geometrid feeding induced more complex volatile blends than did leafhopper infestation. The volatiles induced by both herbivores significantly increased in quality and quantity with time during the first 16 h of infestation, after which the profiles of induced volatile blends and the emission of induced compounds varied diurnally. (E)-β-Ocimene displayed a unique rhythm in which emission peaked at night. The amount of HIPVs significantly increased, while their profiles changed little, with herbivore density. Overall, the leafhoppers and geometrids induced significantly different volatiles from tea plants, while the HIPV profiles varied with a circadian rhythm and were similar at different herbivore densities. Our findings also suggest a new method of enhancing tea flavor using exogenously applied plant hormones, because the volatiles induced by leafhoppers and MeJA were similar in general composition.     

Induced defenses in herbivores and plants differentially modulate a trophic cascade

Inducible defenses are dynamic traits that modulate the strength of both plant-herbivore and herbivore-carnivore interactions. Surprisingly few studies have considered the relative contributions of induced plant and herbivore defenses to the overall balance of bottom-up and top-down control. Here we compare trophic cascade strengths using replicated two-level and three-level plankton communities in which we systematically varied the presence or absence of induced defenses at the plant and/or herbivore levels. Our results show that a trophic cascade, i.e., significantly higher plant biomass in three-level than in two-level food chains, occurred whenever herbivores were undefended against carnivores. Trophic cascades did not occur when herbivores exhibited an induced defense. This pattern was obtained irrespective of the presence or absence of induced defenses at the plant level. We thus found that herbivore defenses, not plant defenses, had an overriding effect on cascade strength. We discuss these results in relation to variation in cascade strengths in natural communities.     

Parasitic wasps orient to green leaf volatiles

Summary Undamaged plants emit low levels of green leaf volatiles (GLVs), while caterpillar-damaged and artificially damaged plants emit relatively higher levels of certain GLVs. Female braconid parasitoids,Microplitis croceipes, oriented to both damaged plants and to individual GLVs in no-choice tests in a wind tunnel, but seldom oriented to undamaged plants. Female ichneumonid parasitoids,Netelia heroica, also oriented to individual GLVs in a wind tunnel. Males of both wasp species failed to orient to the GLVs. These data show that leaf-feeding caterpillars can cause the release of GLVs, and that parasitic wasps can respond to these odors by flying upwind (chemoanemotactic response), which brings the wasps to their caterpillar hosts. This supports the hypothesis that plants communicate with members of the third trophic level,i.e., plants under herbivore attack emit chemical signals that guide natural enemies of herbivores to sites of plant damage. In this interaction, the GLVs serve as tritrophic plant-to-parasitoid synomones. That parasitoids from two different wasp families oriented to GLVs suggests that the response may be widespread among the Hymenoptera.Mention of a commercial or proprietary product does not constitute an endorsement by the U.S. Department of Agriculture     

Additive effects of aboveground polyphagous herbivores and soil feedback in native and range-expanding exotic plants

Plant biomass and plant abundance can be controlled by aboveground and belowground natural enemies. However, little is known about how the aboveground and belowground enemy effects may add up. We exposed 15 plant species to aboveground polyphagous insect herbivores and feedback effects from the soil community alone, as well as in combination. We envisaged three possibilities: additive, synergistic, or antagonistic effects of the aboveground and belowground enemies on plant biomass. In our analysis, we included native and phylogenetically related range-expanding exotic plant species, because exotic plants on average are less sensitive to aboveground herbivores and soil feedback than related natives. Thus, we examined if lower sensitivity of exotic plant species to enemies also alters aboveground-belowground interactions. In a greenhouse experiment, we exposed six exotic and nine native plant species to feedback from their own soil communities, aboveground herbivory by polyphagous insects, or a combination of soil feedback and aboveground insects and compared shoot and root biomass to control plants without aboveground and belowground enemies. We observed that for both native and range-expanding exotic plant species effects of insect herbivory aboveground and soil feedback added up linearly, instead of enforcing or counteracting each other. However, there was no correlation between the strength of aboveground herbivory and soil feedback. We conclude that effects of polyphagous aboveground herbivorous insects and soil feedback add up both in the case of native and related range-expanding exotic plant species, but that aboveground herbivory effects may not necessarily predict the strengths of soil feedback effects.     

Why do plants ‘talk’?

Summary Plant defence can be induced by herbivory. This is true for both direct and indirect plant defence. Induced direct defence has been the most studied of the two. However, in most cases induced direct defence does not appear to be a water-tight defence option. In contrast, induced indirect defence through the production of herbivore-induced carnivore attractants can be a decisive factor in the extermination of herbivore populations. In this paper the main characteristics of induced attraction of carnivores by plants are reviewed. This includes the similarities and dissimilarities among tritrophic systems. There are two main patterns of induced carnivore attraction. (1) Through the emission of the same bouquet as that emitted by mechanically damaged plants, but in larger quantities and for a longer period of time after damage. (2) Through emission of large amounts of new volatiles that are synthesizedde novo in response to herbivore feeding andnot in response to mechanical wounding.Herbivore populations may be decimated by carnivores. Therefore it should be realized that herbivoreinduced carnivore attractants are essential in an important step in carnivore foraging,i.e. long-distance herbivore location. Once herbivores have started feeding on a plant and direct defence is not effective, induced indirect defence may be decisive for plant survival. Therefore, it is concluded that indirect defence is an essential aspect of induced plant defence directed at herbivorous arthropods.     

Bottom-up effects of plant genotype on aphids, ants, and predators

Theory predicts that bottom-up ecological forces can affect community dynamics, but whether this extends to the effects of heritable plant variation on tritrophic communities is poorly understood. In a field experiment, I contrasted the effects of plant genotype (28 genotypes; 1064 plants), aphid density, and the presence/absence of mutualistic ants in affecting the per capita population growth of a specialist aphid herbivore, as well as the effects of plant genotype on the third trophic level. Plant genotype strongly affected aphid population growth rate, explaining 29% of the total variation in growth rate, whereas aphid density and ant-aphid interactions explained substantially less variation (< 2%) in aphid population growth rate. Plant genotype also had direct and indirect effects on the third trophic level, affecting the abundance of aphid-tending ants and the richness of predators. Multiple regression identified several heritable plant traits that explained 49% of the variation in aphid growth rate and 30% of the variation in ant abundance among plant genotypes. These bottom-up effects of plant genotype on tritrophic interactions were independent of the effects of either initial aphid density or the presence/absence of mutualistic ants. This study shows that plant genotype can be one of the most important ecological factors shaping tritrophic communities.     

Effects of combining an intraguild predator with a cannibalistic intermediate predator on a species-level trophic cascade

A greater diversity of natural enemies can in some cases disrupt prey suppression, particularly when natural enemies engage in intraguild predation, where natural enemies compete with and prey upon each other. However, empirical studies have often demonstrated enhanced prey suppression despite intraguild predation. A recent theoretical study proposed the hypothesis that, when the intermediate predator is cannibalistic, intraguild predation can reduce cannibalism within the intermediate predator population, leading to little change in intermediate predator mortality and thus enhanced prey suppression. The goal of this study was to examine this hypothesis empirically. Two summer-long field enclosure experiments were conducted in cotton fields. We investigated the effects of adding an intraguild predator, Zelus renardii, on (1) the abundance of a cannibalistic intermediate predator, Geocoris pallens, (2) the abundance of a herbivore, Lygus hesperus, and (3) cotton plant performance. G. pallens adult abundance did not increase, even when food availability was high and natural enemies were absent, suggesting that density-dependent cannibalism imposes an upper limit on its densities. Furthermore, although Z. renardii is an intraguild predator of G. pallens, G. pallens long-term densities were unaffected by Z. renardii. In the presence of the intermediate predator, the addition of the intraguild predator Z. renardii enhanced suppression of L. hesperus, and there were suggestions that Z. renardii and G. pallens partitioned the L. hesperus population. Effects of herbivore suppression cascaded to the plant level, improving plant performance. In conclusion, we provide empirical support for the hypothesis that the addition of an intraguild predator may enhance prey suppression if the intermediate predator expresses density-dependent cannibalism. Intraguild predation and cannibalism co-occur in many communities; thus their joint effects may be broadly important in shaping predator effects on herbivores and plant performance.     

Evolution of plant volatile production in insect-plant relationships

Summary The production of volatile secondary plant substances during the evolution of terrestrial plants is reviewed in regard to the defensive systems of plants to microorganisms and herbivores. Plant volatiles can be produced by both anabolic and catabolic processes. Although attraction of pollinators is a well-studied phenomenon, functions of volatiles range from excretion of waste products to the production of compounds attracting natural enemies of herbivores. During the evolution of the angiosperms a diversity of volatiles were selected to defend generative parts against microorganisms. Many of these allomones were related to or even identical with sex pheromones of insects. As a result flowers of angiosperms became utilized as a mating site. Consequently insects visiting flowers became involved in pollination, facilitating the steps from anemophily to entomophily. The efficiency of entomophily was increased because of nutritional rewards.An evolutionary scenario for the impact of plant volatiles on insects is presented and the role of volatile allomones in the establishment of plant-insect relationships is emphasized by (1) their strong antimicrobial properties, (2) strategies to protect symbiotic microorganisms, (3) their function as repellents and deterrents, (4) the use of volatile allomones as kairomones. These facts speak for an adaptation of insects to plant physiology and a limited importance of phytophagous insects in selection pressure upon plants. Herbivorous insects have realized specific adaptations to be able to discriminate between complex odour blends, but the utilization of chemical groups among insect taxa is different.The main theories on plant chemical defence do not discuss the impact of volatiles on host plant selection and may be apt to revision when pheromones, allomones, kairomones and synomones are not taken into account.     

Herbivory by an introduced Asian weevil negatively affects population growth of an invasive Brazilian shrub in Florida

The enemy release hypothesis (ERH) is often cited to explain why some plants successfully invade natural communities while others do not. This hypothesis maintains that plant populations are regulated by coevolved enemies in their native range but are relieved of this pressure where their enemies have not been co-introduced. Some studies have shown that invasive plants sustain lower levels of herbivore damage when compared to native species, but how damage affects fitness and population dynamics remains unclear. We used a system of co-occurring native and invasive Eugenia congeners in south Florida (USA) to experimentally test the ERH, addressing deficiencies in our understanding of the role of natural enemies in plant invasion at the population level. Insecticide was used to experimentally exclude insect herbivores from invasive Eugenia uniflora and its native co-occurring congeners in the field for two years. Herbivore damage, plant growth, survival, and population growth rates for the three species were then compared for control and insecticide-treated plants. Our results contradict the ERH, indicating that E. uniflora sustains more herbivore damage than its native congeners and that this damage negatively impacts stem height, survival, and population growth. In addition, most damage to E. uniflora, a native of Brazil, is carried out by Myllocerus undatus, a recently introduced weevil from Sri Lanka, and M. undatus attacks a significantly greater proportion of E. uniflora leaves than those of its native congeners. This interaction is particularly interesting because M. undatus and E. uniflora share no coevolutionary history, having arisen on two separate continents and come into contact on a third. Our study is the first to document negative population-level effects for an invasive plant as a result of the introduction of a novel herbivore. Such inhibitory interactions are likely to become more prevalent as suites of previously noninteracting species continue to accumulate and new communities assemble worldwide.     

Foliar fungal pathogens and grassland biodiversity

By attacking plants, herbivorous mammals, insects, and belowground pathogens are known to play an important role in maintaining biodiversity in grasslands. Foliar fungal pathogens are ubiquitous in grassland ecosystems, but little is known about their role as drivers of community composition and diversity. Here we excluded foliar fungal pathogens from perennial grassland by using fungicide to determine the effect of natural levels of disease on an otherwise undisturbed plant community. Importantly, we excluded foliar fungal pathogens along with rabbits, insects, and mollusks in a full factorial design, which allowed a comparison of pathogen effects along with those of better studied plant enemies. This revealed that fungal pathogens substantially reduced aboveground plant biomass and promoted plant diversity and that this especially benefited legumes. The scale of pathogen effects on productivity and biodiversity was similar to that of rabbits and insects, but different plant species responded to the exclusion of the three plant enemies. These results suggest that theories of plant coexistence and management of biodiversity in grasslands should consider foliar fungal pathogens as potentially important drivers of community composition.     

Do top-down or bottom-up forces determine Stephanitis pyrioides abundance in urban landscapes?

This study examined the influence of habitat structural complexity on the collective effects of top-down and bottom-up forces on herbivore abundance in urban landscapes. The persistence and varying complexity of urban landscapes set them apart from ephemeral agroecosystems and natural habitats where the majority of studies have been conducted. Using surveys and manipulative experiments. We explicitly tested the effect of natural enemies (enemies hypothesis), host plant quality, and herbivore movement on the abundance of the specialist insect herbivore, Stephanitis pyrioides, in landscapes of varying structural complexity. This herbivore was extremely abundant in simple landscapes and rare in complex ones. Natural enemies were the major force influencing abundance of S. pyrioides across habitat types. Generalist predators, particularly the spider Anyphaena celer, were more abundant in complex landscapes. Predator abundance was related to greater abundance of alternative prey in those landscapes. Stephanitis pyrioides survival was lower in complex habitats when exposed to endemic natural enemy populations. Laboratory feeding trials confirmed the more abundant predators consumed S. pyrioides. Host plant quality was not a strong force influencing patterns of S. pyrioides abundance. When predators were excluded, adult S. pyrioides survival was greater on azaleas grown in complex habitats, in opposition to the observed pattern of abundance. Similarly, complexity did not affect S. pyrioides immigration and emigration rates. The complexity of urban landscapes affects the strength of top-down forces on herbivorous insect populations by influencing alternative prey and generalist predator abundance. It is possible that habitats can be manipulated to promote the suppressive effects of generalist predators.     

GC-EAG-analysis of volatiles from Brussels sprouts plants damaged by two species of Pieris caterpillars: olfactory receptive range of a specialist and a generalist parasitoid wasp species

Summary. Feeding by Pieris brassicae or P. rapae caterpillars on Brussels sprouts plants induces the emission of synomones that attract natural enemies of the caterpillars, Cotesia glomerata, a generalist parasitoid, and C. rubecula, a specialist on P. rapae. Previous research on this tritrophic system has identified a large number of volatiles in the headspace of herbivore-damaged Brussels sprouts plants, and this paper addresses the question which of these volatiles are perceived by the two parasitoid species. Headspace odors from both P. brassicae- and P. rapae-damaged Brussels sprouts plants were analyzed by coupled gas chromatography electro- antennogram (GC-EAG) detection. Twenty volatiles evoked consistent EAG reactions in the antennae of both species and nineteen of these volatiles could be identified with GC-MS. One component that could not be identified due to its low concentration, evoked EAG responses in antennae of C. rubecula only. Possible consequences for searching behavior of the two parasitoid species are discussed.     

The effects of seston food quality on planktonic food web patterns

In planktonic food webs, the conversion rate of plant material to herbivore biomass is determined by a variety of factors such as seston biochemical/elemental composition, phytoplankton cell morphology, and colony architecture. Despite the overwhelming heterogeneity characterizing the plant–animal interface, plankton population models usually misrepresent the food quality constraints imposed on zooplankton growth. In this study, we reformulate the zooplankton grazing term to include seston food quality effects on zooplankton assimilation efficiency and examine its ramifications on system stability. Using different phytoplankton parameterizations with regards to growth strategies, light requirements, sinking rates, and food quality, we examined the dynamics induced in planktonic systems under varying zooplankton mortality/fish predation, light conditions, nutrient availability, and detritus food quality levels. In general, our analysis suggests that high food quality tends to stabilize the planktonic systems, whereas unforced oscillations (limit cycles) emerge with lower seston food quality. For a given phytoplankton specification and resource availability, the amplitude of the plankton oscillations is primarily modulated from zooplankton mortality and secondarily from the nutritional quality of the alternative food source (i.e., detritus). When the phytoplankton community is parameterized as a cyanobacterium-like species, conditions of high nutrient availability combined with high zooplankton mortality led to phytoplankton biomass accumulation, whereas a diatom-like parameterization resulted in relatively low phytoplankton to zooplankton biomass ratios highlighting the notion that high phytoplankton food quality allows the zooplankton community to sustain relatively high biomass and to suppress phytoplankton biomass to low levels. During nutrient and light enrichment conditions, both phytoplankton and detritus food quality determine the extent of the limit cycle region, whereas high algal food quality increases system resilience by shifting the oscillatory region towards lower light attenuation levels. Detritus food quality seems to regulate the amplitude of the dynamic oscillations following enrichment, when algal food quality is low. These results highlight the profitability of the alternative food sources for the grazer as an important predictor for the dynamic behavior of primary producer–grazer interactions in nature.     

Ecological costs on local adaptation of an insect herbivore imposed by host plants and enemies

Herbivore populations may become adapted to the defenses of their local hosts, but the traits that maximize host exploitation may also carry ecological costs. We investigated the patterns and costs of local adaptation in the pine processionary moth, Thaumetopoea pityocampa, to its host plants, Pinus nigra and P. sylvestris. The two hosts differ in needle toughness, a major feeding impediment for leaf-eating insects. We observed a west-to-east gradient of increasing progeny size in the Italian Alps, matching the pattern in toughness of their respective local host plant. Eastern populations that feed on the native P. nigra with tough needles had larger eggs, and neonate larvae with larger head capsules, than western populations that feed on the native P. sylvestris and the introduced P. nigra with softer foliage. In a reciprocal transfer experiment that involved the eastern-most and the western-most populations of T. pityocampa from this region, and excluded natural enemies, we found evidence for local adaptation to the host plant. Specifically, larvae from the western population only performed well when raised on their local hosts with soft needles, and they suffered near-complete mortality on the tough foliage at the eastern site. In contrast, larvae from the eastern population survived equally well at both sites. Local adaptation involved a trade-off between progeny size and the number of offspring. We hypothesized that an additional cost, imposed by natural enemies, may be associated with increased egg size: we also observed a west-to-east gradient of increased egg parasitism. We tested this hypothesis in a common garden by exposing eggs of both populations to parasitism by two native egg parasitoids, Ooencyrtus pityocampae and Baryscapus servadeii. The eastern population suffered a higher level of parasitoid attack by O. pityocampae than the western population, and performance of hatched adults of both parasitoids was enhanced in large eggs. Thus, increased neonate quality (larger eggs yielding larger larvae) confers an advantage on tough foliage but incurs the ecological cost of increased parasitism, which may constrain further adaptation by this herbivore.     

Plant-mediated and nonadditive effects of two global change drivers on an insect herbivore community

Warmer temperatures can alter the phenology and distribution of individual species. However, differences across species may blur community-level phenological responses to climate or cause biotic homogenization by consistently favoring certain taxa. Additionally, the response of insect communities to climate will be subject to plant-mediated effects, which may or may not overshadow the direct effect of rising temperatures on insects. Finally, recent evidence for the importance of interaction effects between global change drivers suggests that phenological responses of communities to climate may be altered by other drivers. We used a natural temperature gradient (generated by elevation and topology), combined with experimental nitrogen fertilization, to investigate the effects of elevated temperature and globally increasing anthropogenic nitrogen deposition on the structure and phenology of a seminatural grassland herbivore assemblage (lepidopteran insects). We found that both drivers, alone and in combination, severely altered how the relative abundance and composition of species changed through time. Importantly, warmer temperatures were associated with biotic homogenization, such that herbivore assemblages in the warmest plots had more similar species composition than those in intermediate or cool plots. Changes in herbivore composition and abundance were largely mediated by changes in the plant community, with increased nonnative grass cover under high treatment levels being the strongest determinant of herbivore abundance. In addition to compositional changes, total herbivore biomass more than doubled under elevated nitrogen and increased more than fourfold with temperature, bearing important functional implications for herbivores as consumers and as a prey resource. The crucial role of nonnative plant dominance in mediating responses of herbivores to change, combined with the frequent nonadditive (positive and negative) effects of the two drivers, and the differential responses of species, highlight that understanding complex ecosystem responses will benefit from multifactor, multitrophic experiments at community scales or larger.     

On the risk of extinction of a wild plant species through spillover of a biological control agent: Analysis of an ecosystem compartment model

Invasive plant species can be controlled by introducing natural enemies (insect herbivores) from their native range. However, such introduction entails the risk that the introduced herbivores attack indigenous plant species in the area of introduction. Here, we study the effect of spillover of a herbivore from a managed ecosystem compartment (agriculture) to a natural compartment (non-managed) and vice versa. In the natural compartment, an indigenous plant species is attacked by the introduced herbivores, whereas another indigenous plant species, which competes with the first, is not attacked. The combination of competition and herbivory may result in extinction of the attacked wild plant species. Using a modelling approach, we determine model parameters that characterize the risk of extinction for a wild plant species. Risk factors include: (1) a high attack rate of the herbivores on the wild non-target species, (2) niche overlap expressed as strong competition between the attacked non-target species and its competitor(s), and (3) factors favouring large spillover from the managed ecosystem compartment to the natural compartment; these include (3a) a high dispersal ability, and (3b) a moderate attack rate of the introduced herbivore on the target species, enabling large resident populations of the insect herbivore in the managed compartment. The analysis thus indicates that a high attack rate on the target species, which is a selection criterion for biocontrol agents with respect to their effectiveness, also mitigates risks resulting from spillover and non-target effects. While total eradication of an invasive plant species is not possible in the one-compartment-one-plant-one-herbivore system, natural enemy spillover from a natural to a managed compartment can make the invasive weed go extinct.     

Systemically-induced response of cabbage plants against a specialist herbivore, Pieris brassicae

Summary. Plant responses to herbivory might directly affect the herbivore (“direct” defences) or might benefit the plant by promoting the effectiveness of natural antagonists of the herbivores (“indirect” defences). Brussels sprouts attacked by Pieris brassicae larvae release volatiles that attract a natural antagonist of the herbivores, the parasitoid Cotesia glomerata, to the damaged plant. In a previous study, we observed that feeding by caterpillars on the lower leaves of the plant triggers the systemic release of volatiles detectable by the parasitoids from upper leaves of the same plant.?The role of these systemically induced volatiles as indirect defence and the dynamics of their emission were investigated in wind-tunnel dual choice tests with C. glomerata. The systemically induced emission of volatiles varied depending on leaf age and on plant age. Systemic induction affected parasitoid effectiveness, as induced plants could be more easily located by parasitoids than non-induced ones.?The role of the systemic induction as a direct defence was investigated through behavioural and feeding tests with P. brassicae. In dual choice assays, 1st instar larvae preferred to feed and fed more on systemically induced than on non-induced leaves. In single choice assays, the leaf area consumed by caterpillars was larger on systemically induced leaves than on non-induced control leaves. However, caterpillars fed on systemically induced leaves attained the same weight as those feeding on non-induced controls. In addition, P. brassicae pupae whose larvae were fed on systemically induced leaves had longer developmental times than those of larvae fed on non-induced leaves. Adult oviposition behavior was not influenced by systemic induction.?We conclude that systemically induced responses in cabbage might reduce P. brassicae fitness both directly, by affecting their development and feeding behavior and indirectly by making caterpillars and pupae more vulnerable to attack by carnivores. The occurrence of a possible relationship between direct and indirect defence is discussed. Received 24 January 2001; accepted 3 May 2001.     

When there is no escape: the effects of natural enemies on native, invasive, and noninvasive plants

An important question in the study of biological invasions is the degree to which successful invasion can be explained by release from control by natural enemies. Natural enemies dominate explanations of two alternate phenomena: that most introduced plants fail to establish viable populations (biotic resistance hypothesis) and that some introduced plants become noxious invaders (natural enemies hypothesis). We used a suite of 18 phylogenetically related native and nonnative clovers (Trifolium and Medicago) and the foliar pathogens and invertebrate herbivores that attack them to answer two questions. Do native species suffer greater attack by natural enemies relative to introduced species at the same site? Are some introduced species excluded from native plant communities because they are susceptible to local natural enemies? We address these questions using three lines of evidence: (1) the frequency of attack and composition of fungal pathogens and herbivores for each clover species in four years of common garden experiments, as well as susceptibility to inoculation with a common pathogen; (2) the degree of leaf damage suffered by each species in common garden experiments; and (3) fitness effects estimated using correlative approaches and pathogen removal experiments. Introduced species showed no evidence of escape from pathogens, being equivalent to native species as a group in terms of infection levels, susceptibility, disease prevalence, disease severity (with more severe damage on introduced species in one year), the influence of disease on mortality, and the effect of fungicide treatment on mortality and biomass. In contrast, invertebrate herbivores caused more damage on native species in two years, although the influence of herbivore attack on mortality did not differ between native and introduced species. Within introduced species, the predictions of the biotic resistance hypothesis were not supported: the most invasive species showed greater infection, greater prevalence and severity of disease, greater prevalence of herbivory, and greater effects of fungicide on biomass and were indistinguishable from noninvasive introduced species in all other respects. Therefore, although herbivores preferred native over introduced species, escape from pest pressure cannot be used to explain why some introduced clovers are common invaders in coastal prairie while others are not.     

Bottom-up and top-down effects on insect herbivores do not vary among sites of different salinity

It has been suggested, but rarely tested, that the relative strength of top-down and bottom-up factors in communities varies along an environmental stress gradient. We compared the strength of bottom-up and top-down effects on the densities of insect herbivores along a range of sites of different salinities in west-central Florida. We used a 2 x 2 factorial design with plots divided into four treatments: (1) bottom-up manipulation, where fertilizer was applied to increase plant quality; (2) top-down manipulation, where sticky traps were used to reduce the effects of natural enemies (parasitoids); (3) bottom-up and top-down manipulation, where fertilizer was applied and sticky traps were used; and (4) control plots. These plots were established along a range of salinities among seven different sites containing the salt marsh plant Borrichia frutescens. In each plot, we determined the parasitism levels and abundances of the sap sucker Pissonotus quadripustulatus, the gall maker Asphondylia borrichiae, and the lepidopteran stem borer Argyresthia spp. Gall density, Pissonotus density, and stem borer density were significantly higher in lower salinity sites, suggesting a strong effect of environmental stress. There was a significant increase of galls and Pissonotus and a marginally significant increase of bored stems on fertilized plots but not on trapped plots. There was a significant interaction of site and fertilizer on gall parasitism. There were no interactions of either treatment with salinity on herbivore densities. The general lack of interaction between salinity level and other treatments on herbivore densities contrasts with our previous result where treatment effects did vary with salinity level on a large experimentally generated salinity gradient at one site. Thus, the results of the present paper suggest that, while environmental stress can modify top-down and bottom-up effects on herbivores at single sites, variation in site-to-site factors, possibly including clonal identity of plant, affects herbivore densities so much as to swamp out any observable interaction between environmental stress and top-down or bottom-up factors.     

Weak defence in a tritrophic system: olfactory response to salicylaldehyde reflects prey specialization of potter wasps

Predatory arthropods are attracted to infochemicals emitted by their herbivore prey or by the prey’s host plants. We studied such a tritrophic system measuring the olfactory responses of three potter wasp species (Symmorphus murarius, Symmorphus gracilis, Discoelius zonalis, Hymenoptera: Eumeninae) to salicylaldehyde, sequestered as a defence compound by Chrysomela leaf beetle larvae when feeding on Salicaceae, and volatile organic compounds (VOCs) emitted by aspen (Populus tremula, Salicaceae). In electroantennographic recordings (EAG), the highly specialized S. murarius that almost exclusively feeds on larvae of Salicaceae-feeding Chrysomela species was more sensitive to salicylaldehyde than the less specialized S. gracilis, feeding on such Chrysomela species but also weevil larvae. In contrast the related D. zonalis, foraging for microlepidoptera caterpillars on various host plants, did not respond at all. Furthermore, the three wasp species responded differently to aspen VOCs in GC–MS/EAD measurements. These results indicate that the sense of smell of predatory potter wasps differs for prey and plant volatiles among related wasp species according to their degree of host specialization. The considerable differences in salicylaldehyde perception suggest that its originally defensive function has backfired as it is used by specialist potter wasps for prey location. This is an important clue on adaptive mechanisms of the highest trophic level of the well-studied evolutionary arms race among Chrysomela leaf beetles, their host plants and their enemies.