When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses

Two venerable hypotheses, widely cited as explanations for either the success or failure of introduced species in recipient communities, are the natural enemies hypothesis and the biotic resistance hypothesis. The natural enemies hypothesis posits that introduced organisms spread rapidly because they are liberated from their co‐evolved predators, pathogens and herbivores. The biotic resistance hypothesis asserts that introduced species often fail to invade communities because strong biotic interactions with native species hinder their establishment and spread. We reviewed the evidence for both of these hypotheses as they relate to the importance of non‐domesticated herbivores in affecting the success or failure of plant invasion.
To evaluate the natural enemies hypothesis, one must determine how commonly native herbivores have population‐level impacts on native plants. If native herbivores seldom limit native plant abundance, then there is little reason to think that introduced plants benefit from escape from these enemies. Studies of native herbivore‐native plant interactions reveal that plant life‐history greatly mediates the strength with which specialist herbivores suppress plant abundance. Relatively short‐lived plants that rely on current seed production for regeneration are most vulnerable to herbivory that reduces seed production. As such, these plants may gain the greatest advantage from escaping their specialist enemies in recipient communities. In contrast, native plants that are long lived or that possess long‐lived seedbanks may not be kept “in check” by native herbivores. For these species, escape from native enemies may have little to do with their success as exotics; they are abundant both where they are native and introduced.
Evidence for native herbivores providing biotic resistance to invasion by exotics is conflicting. Our review reveals that: 1) introduced plants can attract a diverse assemblage of native herbivores and that 2) native herbivores can reduce introduced plant growth, seed set and survival. However, the generality of these impacts is unclear, and evidence that herbivory actually limits or reduces introduced plant spread is scarce. The degree to which native herbivores provide biotic resistance to either exotic plant establishment or spread may be greatly determined by their functional and numerical responses to exotic plants, which we know little about. Generalist herbivores, through their direct effects on seed dispersal and their indirect effects in altering the outcome of native–non‐native plant competitive interactions, may have more of a facilitative than negative effect on exotic plant abundance.     

Host plant manipulation of natural enemies: leaf domatia protect beneficial mites from insect predators

Acarodomatia are small tufts of hair or invaginations in the leaf surface and are frequently inhabited by several taxa of non-plant-feeding mites. For many years, ecologists have hypothesized that these structures represent a mutualistic association between mites and plants where the mites benefit the plant by reducing densities of phytophagous arthropods and epiphytic microorganisms, and domatia benefit the mite by providing protection from stressful environmental conditions, other predaceous arthropods, or both. We tested these hypothesized benefits of domatia to domatia-inhabiting mites in laboratory and growth chamber experiments. In separate experiments we examined whether domatia on the wild grape, Vitis riparia, provided protection against drying humidity conditions or predaceous arthropods to two species of beneficial mite: the mycophagous species Orthotydeus lambi, and the predaceous species Amblyseius andersoni. For both taxa of beneficial mite, domatia significantly increased mite survivorship in the presence of the predatory bug, Orius insidiosus and the coccinellids Coccinella septempunctata and Harmonia varigata. There was no evidence for a protective effect of domatia with a third species of predatory arthropod, lacewing larvae Chrysoperla rufilabris. In contrast, there was no evidence for either species of beneficial mite that domatia provided any protection against low humidity. Thus in this system the primary mechanism by which domatia benefit beneficial mites is by protecting these organisms from other predatory arthropods on the leaf surface.     

Airborne interactions between undamaged plants of different cultivars affect insect herbivores and natural enemies

This study investigated the effects of airborne interaction between different barley cultivars on the behaviour of bird cherry-oat aphid Rhopalosiphum padi, the ladybird Coccinella septempunctata and the parasitoid Aphidius colemani. In certain cultivar combinations, exposure of one cultivar to air passed over a different cultivar caused barley to have reduced aphid acceptance and increased attraction of ladybirds and parasitoids. Parasitoids attacked aphids that had developed on plants under exposure more often than those from unexposed plants, leading to a higher parasitisation rate. Ladybirds, but not parasitoids, were more attracted to combined odours from certain barley cultivars than either cultivar alone. The results show that airborne interactions between undamaged plants can affect higher trophic levels, and that odour differences between different genotypes of the same plant species may be sufficient to affect natural enemy behaviour.     

Influence of native flowering plant strips on natural enemies and herbivores in adjacent blueberry fields

Conservation plantings of native wildflowers were established adjacent to highbush blueberry (Vaccinium corymbosum L.) fields to test the hypothesis that provision of resources for natural enemies increases their abundance in adjacent crop fields without increasing the abundance of pest insects. For two growing seasons, natural enemies and herbivorous insects were sampled in fields with flowering borders and in control fields where growers maintained standard mown grass perimeters. Insects were categorized according to their trophic level and their potential pest status, and their abundance was compared between years and between treatments. Syrphid flies (Diptera: Syrphidae) were significantly more abundant in fields with conservation strips, as were plant bugs (Hemiptera: Miridae), thrips (Thysanoptera: Thripidae), and hoppers (Hemiptera: Auchenorrhyncha). Aphids (Hemiptera: Aphididae), thrips, fruit flies (Diptera: Tephritidae), and pirate bugs (Hemiptera: Anthocoridae) decreased significantly in abundance from 2007 to 2008. Beneficial insect abundance in crop fields increased in the latter half of the season in both years and this increase was more pronounced in fields adjacent to conservation plantings. We discuss the implications of these findings for pest management and conservation of biodiversity in farmland.     

Jasmonate-mediated induced plant resistance affects a community of herbivores

1. The negative effect of induced plant resistance on the preference and performance of herbivores is a well‐documented ecological phenomenon that is thought to be important for both plants and herbivores. This study links the well‐developed mechanistic understanding of the biochemistry of induced plant resistance in the tomato system with an examination of how these mechanisms affect the community of herbivores in the field. 2. Several proteins that are induced in tomato foliage following herbivore damage have been linked causally to reductions in herbivore performance under laboratory conditions. Application of jasmonic acid, a natural elicitor of these defensive proteins, to tomato foliage stimulates induced responses to herbivory. 3. Jasmonic acid was sprayed on plants in three doses to generate plants with varying levels of induced responses, which were measured as increases in the activities of proteinase inhibitors and polyphenol oxidase. 4. Field experiments conducted over 3 years indicated that induction of these defensive proteins is associated with decreases in the abundance of all four naturally abundant herbivores, including insects in three feeding guilds, caterpillars, flea beetles, aphids, and thrips. Induced resistance killed early instars of noctuid caterpillars. Adult flea beetles strongly preferred control plants over induced plants, and this effect on host plant preference probably contributed to differences in the natural abundance of flea beetles. 5. The general nature of the effects observed in this study suggests that induced resistance will suppress many members of the herbivore community. By linking plant biochemistry, insect preference, performance, and abundance, tools can be developed to manipulate plant resistance sensibly and to predict its outcome under field conditions.     

Chemical interaction between undamaged plants--effects on herbivores and natural enemies

Most research on plant-plant chemical interactions has focussed on events following herbivore or pathogen attack. However, undamaged plants also interact chemically as a natural facet of their behaviour, and this may have consequences for insects that use the plants as hosts. In this review, the links between allelopathy and insect behaviour are outlined. Findings on how chemical interactions between different plant species and genotypes affect aphid herbivores and their natural enemies are reviewed, and the role of plant diversity and chemical interaction for trophic interactions in crops is discussed.     

The tri-trophic interactions hypothesis: interactive effects of host plant quality, diet breadth and natural enemies on herbivores

Several influential hypotheses in plant-herbivore and herbivore-predator interactions consider the interactive effects of plant quality, herbivore diet breadth, and predation on herbivore performance. Yet individually and collectively, these hypotheses fail to address the simultaneous influence of all three factors. Here we review existing hypotheses, and propose the tri-trophic interactions (TTI) hypothesis to consolidate and integrate their predictions. The TTI hypothesis predicts that dietary specialist herbivores (as compared to generalists) should escape predators and be competitively dominant due to faster growth rates, and that such differences should be greater on low quality (as compared to high quality) host plants. To provide a preliminary test of these predictions, we conducted an empirical study comparing the effects of plant (Baccharis salicifolia) quality and predators between a specialist (Uroleucon macolai) and a generalist (Aphis gossypii) aphid herbivore. Consistent with predictions, these three factors interactively determine herbivore performance in ways not addressed by existing hypotheses. Compared to the specialist, the generalist was less fecund, competitively inferior, and more sensitive to low plant quality. Correspondingly, predator effects were contingent upon plant quality only for the generalist. Contrary to predictions, predator effects were weaker for the generalist and on low-quality plants, likely due to density-dependent benefits provided to the generalist by mutualist ants. Because the TTI hypothesis predicts the superior performance of specialists, mutualist ants may be critical to A. gossypii persistence under competition from U. macolai. In summary, the integrative nature of the TTI hypothesis offers novel insight into the determinants of plant-herbivore and herbivore-predator interactions and the coexistence of specialist and generalist herbivores.     

The effects of leaf quality on herbivore performance and attack from natural enemies

A diverse array of sublethal plant secondary compounds are commonly found in the foliage of temperate deciduous trees. These traits are thought to defend a plant in two principal ways, either directly by reducing insect oviposition, feeding, or biomass gain, or indirectly, through digestive inhibition. Such inhibition is hypothesized to slow the rate of herbivore development, thereby increasing their susceptibility to natural enemies (the slow-growth-high-mortality hypothesis). To clarify the defensive role of these compounds, field experiments were conducted to examine the relationships among oak leaf quality, herbivore family, and three herbivore performance measures: survivorship, development time, and pupal mass, for a bivoltine leaf-tying caterpillar, Psilocorsis quercicella (Lepidoptera: Oecophoridae). Two experiments, one for each generation of the insect, were conducted to examine the effects of intraspecific variation in leaf chemistry of its host, white oak trees (Quercus alba). In each experiment, full-sib neonate larvae were placed in experimental leaf ties on high- versus low-quality trees and allowed to feed for 2 weeks under field conditions. To determine the effect of the third trophic level, a portion of each family in each leaf-quality treatment was bagged to prevent attack from natural enemies. This treatment also allowed us to test a prediction of the slow-growth-high-mortality hypothesis, i.e., that development time, as measured for full sibs in the bagged treatment, should be positively correlated with mortality of their full sibs exposed to natural enemies. Low leaf quality significantly reduced survivorship of the caterpillars in the first generation but not the second. The third trophic level decreased survivorship in both generations. Larval development time was not affected by leaf quality in either generation, but varied significantly among insect families in both generations. In turn, larvae from slower-developing families did not suffer increased predation and parasitism, as predicted by the slow-growth-high mortality hypothesis. In contrast to development time, pupal mass showed a greater response to intraspecific variation in leaf quality, although the effect was only significant in generation 1. Concentrations of both total phenolics and hydrolyzable tannins in Q. alba foliage appear to be important negative predictors of pupal mass in P. quercicella. In marked contrast to development time, no main family effect was found for pupal mass in either experiment; however, significant family2environment interactions were found for the effects of the bagging treatment (generation 1) and the leaf-quality treatment (generation 2). Overall, the first trophic level had a greater influence on pupal mass (a fecundity correlate), while larval development time was determined more by the insect's family (genotype+maternal environment). The third trophic level was a consistently strong source of mortality in both experiments, but as a whole did not respond to familial differences in development time. Thus, from the perspective of P. quercicella, plant quality appears to serve as a defense more through its direct effect on herbivore survivorship and fecundity than through an indirect effect on predation via changes in development time.     

Nutrient presses and pulses differentially impact plants, herbivores, detritivores and their natural enemies

Anthropogenic nutrient inputs into native ecosystems cause fluctuations in resources that normally limit plant growth, which has important consequences for associated food webs. Such inputs from agricultural and urban habitats into nearby natural systems are increasing globally and can be highly variable, spanning the range from sporadic to continuous. Despite the global increase in anthropogenically-derived nutrient inputs into native ecosystems, the consequences of variation in subsidy duration on native plants and their associated food webs are poorly known. Specifically, while some studies have examined the effects of nutrient subsidies on native ecosystems for a single year (a nutrient pulse), repeated introductions of nutrients across multiple years (a nutrient press) better reflect the persistent nature of anthropogenic nutrient enrichment. We therefore contrasted the effects of a one-year nutrient pulse with a four-year nutrient press on arthropod consumers in two salt marshes. Salt marshes represent an ideal system to address the differential impacts of nutrient pulses and presses on ecosystem and community dynamics because human development and other anthropogenic activities lead to recurrent introductions of nutrients into these natural systems. We found that plant biomass and %N as well as arthropod density fell after the nutrient pulse ended but remained elevated throughout the nutrient press. Notably, higher trophic levels responded more strongly than lower trophic levels to fertilization, and the predator/prey ratio increased each year of the nutrient press, demonstrating that food web responses to anthropogenic nutrient enrichment can take years to fully manifest themselves. Vegetation at the two marshes also exhibited an apparent tradeoff between increasing %N and biomass in response to fertilization. Our research emphasizes the need for long-term, spatially diverse studies of nutrient enrichment in order to understand how variation in the duration of anthropogenic nutrient subsidies affects native ecosystems.     

Effects of agroecosystem diversification on natural enemies of soybean herbivores

This study evaluated the effects of agroecosystem diversification through no-tillage and strip intercropping on the abundance of natural enemies of soybean (Glycine max Merrill) herbivores. Twenty-four plots (289 m² each) were arranged in a randomized complete block design for a 3 by 2 factorial experiment. Factors were cropping systems (corn monoculture, soybean monoculture, and strip intercropping of corn and soybean) and tillage systems (no-tillage and conventional tillage). Natural enemies were sampled during 1988, 1989 and 1990 by sweep net, suction net (D-Vac), pitfall traps and quadrat samples. Analyses of variance indicated that of 15 taxa analyzed, most foliage-inhabiting natural enemies were significantly more abundant in intercropping than in monoculture plots, whereas soil-inhabiting natural enemies had higher numbers in no-tillage plots than conventional tillage plots. Therefore, the results support the theory of greater abundance of natural enemies in more complex agroecosystems. Better environmental conditions in diversified treatments was the possible reason for these results. Corn in intercropping plots provided shade, reduced wind speed, alternate food, and possibly higher humidity and lower temperatures for soybean natural enemies. A similar effect was likely cuased by the stubble and weeds, in no-tillage plots.     

Attractiveness of Michigan native plants to arthropod natural enemies and herbivores

The use of plants to provide nectar and pollen resources to natural enemies through habitat management is a growing focus of conservation biological control. Current guidelines frequently recommend use of annual plants exotic to the management area, but native perennial plants are likely to provide similar resources and may have several advantages over exotics. We compared a set of 43 native Michigan perennial plants and 5 frequently recommended exotic annual plants for their attractiveness to natural enemies and herbivores for 2 yr. Plant species differed significantly in their attractiveness to natural enemies. In year 1, the exotic annual plants outperformed many of the newly established native perennial plants. In year 2, however, many native perennial plants attracted higher numbers of natural enemies than exotic plants. In year 2, we compared each flowering plant against the background vegetation (grass) for their attractiveness to natural enemies and herbivores. Screening individual plant species allowed rapid assessment of attractiveness to natural enemies. We identified 24 native perennial plants that attracted high numbers of natural enemies with promise for habitat management. Among the most attractive are Eupatorium perfoliatum L., Monarda punctata L., Silphium perfoliatum L., Potentilla fruticosa auct. non L., Coreopsis lanceolata L., Spiraea alba Duroi, Agastache nepetoides (L.) Kuntze, Anemone canadensis L., and Angelica atropurpurea L. Subsets of these plants can now be tested to develop a community of native plant species that attracts diverse natural enemy taxa and provides nectar and pollen throughout the growing season.     

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.     

An ecological cost of plant defence: attractiveness of bitter cucumber plants to natural enemies of herbivores

Plants produce defences that act directly on herbivores and indirectly via the attraction of natural enemies of herbivores. We examined the pleiotropic effects of direct chemical defence production on indirect defence employing near‐isogenic varieties of cucumber plants (Cucumis sativus) that differ qualitatively in the production of terpenoid cucurbitacins, the most bitter compounds known. In release–recapture experiments conducted in greenhouse common gardens, blind predatory mites were attracted to plants infested by herbivorous mites. Infested sweet plants (lacking cucurbitacins), however, attracted 37% more predatory mites than infested bitter plants (that produce constitutive and inducible cucurbitacins). Analysis of the headspace of plants revealed that production of cucurbitacins was genetically correlated with large increases in the qualitative and quantitative spectrum of volatile compounds produced by plants, including induced production of (E )‐β‐ocimene (3E )‐4,8‐dimethyl‐1,3,7‐nonatriene, (E,E)‐α‐farnesene, and methyl salicylate, all known to be attractants of predators. Nevertheless, plants that produced cucurbitacins were less attractive to predatory mites than plants that lacked cucurbitacins and predators were also half as fecund on these bitter plants. Thus, we provide novel evidence for an ecological trade‐off between direct and indirect plant defence. This cost of defence is mediated by the effects of cucurbitacins on predator fecundity and potentially by the production of volatile compounds that may be repellent to predators.     

Localized outbreak of a willow leaf beetle: plant vigor or natural enemies?

The possible roles of plant quality (vigor) and natural enemies in the development of a localized out-break of the leaf beetle Galerucella lineola (Coleoptera: Chrysomelidae) in a stand of Salix cinerea were investigated. Caged and uncaged larvae on six bushes in the outbreak area were compared with caged and uncaged larvae on six bushes in an adjacent nonoutbreak area in terms of performance. In 1997, when the studies were performed, the natural density of the insect (beetles plus eggs) was six times higher in the outbreak area compared with the nonoutbreak area. Even though the vigor (measured as shoot length) of bushes in the outbreak was 72% higher than that of bushes in the nonoutbreak area, we found no difference between areas in the performance (survival, developmental time, pupal weight) of caged larvae or in the willingness of caged females to lay eggs. Among larvae exposed to natural enemies, the disappearance rate was significantly higher in the nonoutbreak area. The density of generalist predators was significantly higher in the nonoutbreak than in the outbreak area. We conclude that differences in plant quality, despite the observed difference in plant vigor, could not explain the observed difference in beetle density between areas. Lower predation pressure in the outbreak area could, however, not be excluded as a possible reason for the higher density of leaf beetles in this area. Received: October 18, 1999 / Accepted: February 4, 2000     

Associational resistance mediated by natural enemies

Abstract.  1. Associational resistance theory suggests that the association of herbivore-susceptible plant species with herbivore-resistant plant species can reduce herbivore density on the susceptible plant species. Several casual mechanisms are possible but none has so far invoked natural enemies. Associational resistance mediated by natural enemies was tested for by examining densities of a gall fly, Asphondylia borrichiae (Diptera: Cecidomyiidae), and levels of parasitism on two closely related seaside plants, Borrichia frutescens and Iva frutescens , when alone and when co-occurring.
2. Both Borrichia and Iva grow alone or together on small offshore islands in Florida. Each host plant species has its own associated race of fly, but both races of fly are attacked by the same four species of parasitoids. Borrichia normally has a higher density of galls than Iva , and galls are larger on Borrichia than on Iva .
3. Gall size, gall abundance, parasitism levels, and parasitoid community composition were quantified on both Borrichia and Iva on islands where each species grew alone or together. Some islands were then manipulated by adding Borrichia to islands supporting only Iva , and by adding Iva to islands supporting only Borrichia . Subsequent gall densities and gall parasitism levels on the original native species were then examined.
4. On both natural and experimentally manipulated islands, gall densities on Iva were significantly lowered by the presence of Borrichia . This is because bigger parasitoid species that were common on Borrichia galls, which are bigger, spilled over and attacked the smaller Iva galls. Thus, parasitism rates on Iva were higher on islands where Borrichia co-occurred than on islands where Borrichia were absent. Most parasitoids from Iva were too small to successfully attack the large Borrichia galls and so gall density on Borrichia was unaffected by the presence of Iva .     

Biotic interactions of mites, plants and leaf domatia

Leaf domatia, minute structures that typically house mites and other small arthropods, are produced by an impressive number of plants; however, their role in mediating plant-mite mutualism has only recently been elucidated. New evidence indicates that domatia function primarily as refuges for beneficial mites against predators. The presence of domatia therefore results in more beneficial mites on leaves, fewer pathogen attacks and reduced leaf herbivory. Unexpectedly, herbivorous mites are specialized domatia inhabitants of some plants. By providing refuges for herbivores, however, domatia may stabilize interactions between predator and their mite prey and thereby reduce the chances of herbivore outbreaks. Understanding the ecological mechanisms that promote beneficial interactions between mites and plants could have important implications for pest management.     

植物干旱胁迫对植食性昆虫及其天敌的影响

全球正经历以变暖为主要特征的气候变化,由此带来的干旱将对农业生态系统造成重要影响。本文综述了干旱胁迫下寄主植物对植食性昆虫及其天敌影响的国内外最新研究进展。在干旱胁迫下,寄主植物物理性状、营养状况和次生代谢物质等均发生变化,这些变化导致植食性昆虫的生存环境和营养物质的获取等方面发生改变,从而影响了害虫生长发育和种群动态。干旱胁迫还导致寄主物候变化与昆虫发生不同步,使害虫缺乏食物。另外干旱也会引起植食性害虫天敌的种群发生变化,从而对植食性昆虫种群数量产生间接的影响。