Increased resistance to generalist herbivores in invasive populations of the California poppy (Eschscholzia californica)

Escape from enemies in the native range is often assumed to contribute to the successful invasion of exotic species. Following optimal defence theory, which assumes a trade‐off between herbivore resistance and plant growth, some have predicted that the success of invasive species could be the result of the evolution of lower resistance to herbivores and increased allocation of resources to growth and reproduction. Lack of evidence for ubiquitous costs of producing plant toxins, and the recognition that invasive species may escape specialist, but not generalist enemies, has led to a new prediction: invasive species may escape ecological trade‐offs associated with specialist herbivores, and evolve increased, rather than decreased, production of defensive compounds that are effective at deterring generalist herbivores in the introduced range. We tested the performance of two generalist lepidopteran herbivores, Trichoplusia ni and Orgyia vetusta, when raised on diets of native and invasive populations of the California poppy, Eschscholzia californica. Pupae of T. ni were significantly larger when reared on native populations. Similarly, caterpillars of O. vetusta performed significantly better when raised on native populations, indicating that invasive populations of the California poppy are more resistant to herbivores than native populations. The chance of successful establishment of some non‐indigenous plant species may be increased by retaining resistance to generalist herbivores, and in some cases, invasive species may be able to escape ecological trade‐offs in their new range and evolve, as we observed, even greater resistance to generalist herbivores than native plants.     

Resistance to herbicide and susceptibility to herbivores: environmental variation in the magnitude of an ecological trade-off

Trade-offs can maintain genetic diversity and constrain adaptation; however, their magnitude may depend on ecological factors. I considered whether resistance to the herbicide triazine in Amaranthus hybridus (Amaranthaceae) imposed the trade-off of increasing susceptibility to herbivorous insects. I grew triazine-resistant and triazine-susceptible plants under contrasting levels of light and fertilization, and quantified susceptibility to herbivores using the specialist Disonycha glabrata (Coleoptera: Chrysomelidae) and the generalist Trichoplusia ni (Lepidoptera: Noctuidae). Resistance to triazine increased susceptibility to both species of herbivorous insects, as manifested by greater feeding preference, growth, and survival of herbivores. However, these effects were more pronounced with T. ni and for plants grown under high light. My results demonstrate the presence of a trade-off between resistance to triazine and susceptibility to herbivorous insects that may in turn impose an ecologically based fitness cost, and illustrate the potential for this cost to vary across environments.     

Second and third trophic level effects of differences in plant species reflect dietary specialisation of herbivores and their endoparasitoids

In natural populations, plants demonstrate an array of indirect and direct defence strategies that help to protect them from their herbivores and pathogens. Indirect defences include the release of odours that attract the natural enemies of herbivores, whereas direct defences may include the production of secondary compounds, allelochemicals that impair herbivore development or repel herbivore attack. Although both strategies have been well studied independently, comparatively little attention has been paid to examining the conflict that may arise between indirect and direct defences, such as when the performance of ‘recruited’ parasitoids or predators is negatively affected by plant allelochemicals. Here, we examine the growth and development of polyphagous and oligophagous folivores and their respective endoparasitoids on three crucifer species. One of the species, Brassica oleracea, was recently cultivated, whereas populations of B. nigra and Barbarea vulgaris occur naturally. Additionally, these species possess contrasting life‐history patterns and are also known to exhibit differences in secondary chemistry. The development of the generalist herbivore–parasitoid system was much more variable over the three crucifers than that exhibited by the specialists. Moreover, generalist herbivore and/or parasitoid fitness‐related traits (survival, development time, pupal, or adult size) were much more negatively affected on the wild crucifers than in the specialist association. Our results suggest that the relative importance of direct and indirect defences in plants may rest on the degree of dietary specialisation exhibited by herbivores and their natural enemies, and on the level of toxicity in the plant species under investigation.     

The effect of plant chemistry on the acceptability of caterpillar prey to the argentine antIridomyrmex humilils (Hymenoptera: Formicidae)

Experiments were performed to test the acceptability of two palatable, cryptic caterpillars, the tobacco hornworm,Manduca sexta, and the cabbage looper,Trichoplusia ni, reared on different diets, to the Argentine ant,Iridomyrmex humilis. Ants preferred larvae reared on artificial diet, groundcherry, or cowpea to tobacco-reared larvae. Ants also preferred larvae reared on artificial diet without nicotine to larvae reared on diet containing nicotine (5% dry wt). Experiments were also performed to test the response of ants to larval extracts and chemicals applied to the surface of palatable prey. Ants did not respond differently to larvae of the potato tuber moth,Phthorimaea operculella, treated with larval extracts or regurgitate from tobacco-reared larvae compared to artificialdiet-reared larvae, but ants were deterred byP. operculella larvae treated with nicotine compared to untreated larvae. The results of this study indicate that caterpillars can derive at least some degree of chemical protection from their food plant without sequestering and storing plant compounds and without the development of elaborate aposematic characteristics.     

Nutritional suitability and ecological relevance of <Emphasis Type="Italic">Arabidopsis thaliana</Emphasis> and <Emphasis Type="Italic">Brassica oleracea</Emphasis> as foodplants for the cabbage butterfly, <Emphasis Type="Italic">Pieris rapae</Emphasis>

The thale cress, Arabidopsis thaliana, is considered to be an important model species in studying a suite of evolutionary processes. However, the species has been criticized on the basis of its comparatively small size at maturity (and consequent limitations in the amount of available biomass for herbivores) and on the duration and timing of its life cycle in nature. In the laboratory, we studied interactions between A. thaliana and the cabbage butterfly, Pieris rapae, in order to determine if plants are able to support the complete development of the herbivore. Plants were grown in pots from seedlings in densities of one, two, or four per pot. In each treatment, one, two, or five newly hatched larvae of P. rapae were placed on fully developed rosettes of A. thaliana. In a separate experiment, the same densities of P. rapae larvae were reared from hatching on single mature cabbage (Brassica oleracea) plants. Pupal fresh mass and survival of P. rapae declined with larval density when reared on A. thaliana but not on B. oleracea. However, irrespective of larval density and plant number, some P. rapae were always able to complete development on A. thaliana plants. A comparison of the dry mass of plants in different treatments with controls (= no larvae) revealed that A. thaliana partially compensated for plant damage when larval densities of P. rapae were low. By contrast, single cress plants with 5 larvae generally suffered extensive damage, whereas damage to B. oleracea plants was negligible. Rosettes of plants that were monitored in spring, when A. thaliana naturally grows, were not attacked by any insect herbivores, but there was often extensive damage from pulmonates (slugs and snails). Heavily damaged plants flowered less successfully than lightly damaged plants. Small numbers of generalist plant-parasitic nematodes were also recovered in roots and root soil. By contrast, plants monitored in a sewn summer plot were heavily attacked by insect herbivores, primarily flea beetles (Phyllotreta spp.). These results reveal that, in natural populations of A. thaliana, there is a strong phenological mismatch between the plant and most of its potential specialist insect herbivores (and their natural enemies). However, as the plant is clearly susceptible to attack from non-insect generalist invertebrate herbivores early in the season, these may be much more suitable for studies on direct defense strategies in A. thaliana.     

Decreased Response to Feeding Deterrents Following Prolonged Exposure in the Larvae of a Generalist Herbivore, Trichoplusia ni (Lepidoptera: Noctuidae)

We investigated the role of experience with several antifeedants on the feeding behavior of a generalist herbivore, Trichoplusia ni. Second-, third-, and fifth-instar larvae of T. ni were examined for their feeding responses to plant extracts (Melia volkensii, Origanum vulgare) and individual plant allelochemicals (cymarin, digitoxin, xanthotoxin, toosendanin, and thymol), after being exposed to them continually beginning as neonates. All tested instars of T. ni were capable of showing a decreased antifeedant response following prolonged exposure to most of the antifeedants tested compared with their naive conspecifics. Cardenolides (digitoxin and cymarin) were the exceptions. The response to oregano was affected as a result of previous exposure to different concentrations of oregano, unlike M. volkensii, leading us to conclude that T. ni sensitivity varies between stimuli and cannot be generalized. To demonstrate that decreased deterrence following prolonged exposure to M. volkensii was the result of learned habituation, three aversive stimuli were used. A high concentration of the particular antifeedant, xanthotoxin, acted as a noxious stimulus and dishabituated (reversed) the decrement in the antifeedant response to M. volkensii. Cold shock or CO₂ was marginally effective in dishabituating the response. The fact that the decrease in antifeedant response can be dishabituated has implications for pest management.     

An ecological genomic approach challenging the paradigm of differential plant responses to specialist versus generalist insect herbivores

A general prediction of the specialist/generalist paradigm indicates that plant responses to insect herbivores may depend on the degree of ecological specialization of the insect attacker. However, results from a single greenhouse experiment evaluating the responses of the model plant Arabidopsis thaliana to three specialist (Plutella xylostella, Pieris rapae, and Brevicoryne brassicae) and three generalist (Trichoplusia ni, Spodoptera exigua, and Myzus persicae) insect species did not support the previous prediction. Using an ecological genomic approach, we assessed plant responses in terms of herbivore-induced changes in genome-wide gene expression, defense-related pathways, and concentrations of glucosinolates (i.e., secondary metabolites that are ubiquitously present in cruciferous plants). Our results showed that plant responses were not influenced by the degree of specialization of insect herbivores. In contrast, responses were more strongly shaped by insect taxa (i.e., aphid vs. lepidopteran species), likely due to their different feeding modes. Interestingly, similar patterns of plant responses were induced by the same insect herbivore species in terms of defense signaling (jasmonic acid pathway), aliphatic glucosinolate metabolism (at both the gene expression and phenotypic levels) and genome-wide responses. Furthermore, plant responses to insect herbivores belonging to the same taxon (i.e., four lepidopteran species) were not explained by herbivore specialization or phylogenetic history. Overall, this study suggests that different feeding modes of insect taxa as well as herbivore-specific plant responses, which may result from distinct ecological/evolutionary interactions between A. thaliana (or a close relative) and each of the lepidopteran species, may explain why observed responses deviate from those predicted by the specialist/generalist paradigm.     

Effects of chlorogenic acid-and tomatine-fed caterpillars on the behavior of an insect predator

If generalist insect predators are a selective force contributing to patterns of feeding specialization by insect herbivores, then predators should be deterred from eating allelochemical-fed prey. The attack and feeding behaviors of naive predators (Podisus maculiventris stinkbugs) reared on control caterpillars (Manduca sexta) fed plain diet were compared to experienced predators reared on caterpillars fed tomato allelochemicals. Tomatine-fed prey were found more quickly by both naive and tomatine-experienced predators, and chlorogenic acid-experienced predators were more stimulated to begin searching for prey. However, experienced predators were less likely to attack both chlorogenic acidfed and tomatine-fed caterpillars than were naive predators. These results indicate that allelochemical-fed prey were easier for predators to locate, but allelochemical-containing prey often deterred predation by experienced predtors.     

The nutritional landscape of host plants for a specialist insect herbivore

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Larval feeding induced defensive responses in tobacco: comparison of two sibling species of <Emphasis Type="Italic">Helicoverpa</Emphasis> with different diet breadths

Plants respond differently to damage by different herbivorous insects. We speculated that sibling herbivorous species with different host ranges might also influence plant responses differently. Such differences may be associated with the diet breadth (specialization) of herbivores within a feeding guild, and the specialist may cause less intensive plant responses than the generalist. The tobacco Nicotinana tabacum L. is the common host plant of a generalist Helicoverpa armigera (Hübner) and a specialist H. assulta Guenée (Lepidoptera, Noctuidae). The induced responses of tobacco to feeding of these two noctuid herbivores and mechanical wounding were compared. The results showed that the feeding of the specialist H. assulta and the generalist H. armigera resulted in the same inducible defensive system, but response intensity of plants was different to these two species. Inductions of jasmonic acid (JA), lipoxygenase (LOX), and proteinase inhibitors (PIs) were not significantly different concerning these two species, but H. assulta caused the less intensive foliar polyphenol oxidase (PPO) increase, more intensive nicotine and peroxidase (POD) increases in tobacco than H. armigera. The defensive response of plant to herbivores with different diet breadth seems to be more complicated than we expected, and the specialist does not necessarily cause less intensive plant responses than the generalist.     

Effects of enhanced UV-B radiation on a weedy forb (Plantago lanceolata) and its interactions with a generalist and specialist herbivore

Assessments of potential impacts of global climate change often focus exclusively on plants; however, as the base of most food webs, plants generally experience abiotic stresses concomitantly with biotic stresses. Longleaf plantain, Plantago lanceolata L., is a cosmopolitan temperate perennial weed that experiences a wide range of environmental conditions throughout its range. We examined the impacts of elevated levels of exposure to shortwave (UV-B) radiation on this plant, on two herbivores associated with this plant, and on the plant-herbivore interaction. Plantains were grown at 6 and 12 kJ m^–2 d^–1 BE₃₀₀ UV-B radiation and concentrations of iridoid glycosides (aucubin and catalpol), verbascosides, and nitrogen were measured. In terms of plant impacts, we found that iridoid glycoside concentrations were unchanged by elevated UV-B radiation, whereas, in one experiment, the concentration of verbascosides in young leaves and levels of nitrogen in old leaves increased under elevated UV-B radiation. Variation in plant chemistry due to leaf age and maternal family was greater than variation due to UV-B exposure. When caterpillars were fed excised leaves from plants grown under elevated UV-B, growth and survivorship of the specialist herbivore, Precis coenia Hbn. (Lepidoptera: Nymphalidae), were unaltered and growth of the generalist herbivore, Trichoplusia ni (Hbn.) (Lepidoptera: Noctuidae), was accelerated. When the caterpillars were reared on potted plants at high and low levels of UV-B radiation, growth and survivorship of P. coenia were unchanged while growth of T. ni was significantly depressed by elevated UV-B. Elevated UV-B altered allocation patterns of above-ground biomass in these plants; masses of crowns and reproductive tissue were reduced. UV-B levels, however, did not affect distribution of damage to foliage inflicted by either species. In two additional experiments with artificial diet, designed to test the direct effect of UV-B radiation on caterpillars, growth and survivorship of P. coenia were unaltered while survivorship of T. ni was significantly depressed when caterpillars were exposed to elevated UV-B radiation. These studies collectively demonstrate that higher trophic level impacts of UV-B-induced changes in plants depend on the identity of the herbivore and its degree of adaptation not only to variation in hostplant quality but also variation in its light environment.     

Behavioral responses to host foodplants of two populations of the insect parasitoid Cotesia congregata (Say)

To test the hypothesis that natural enemy populations differ in their behavioral responses to plants or to plant allelochemicals, we compared two populations of the gregarious larval endoparasitoid, Cotesia congregata (Say) (Hymenoptera: Braconidae) that differed in their historical and present exposure to tobacco. The major hosts for both populations were Manduca sexta L. and M. quinquemaculata (Haworth) (Lepidoptera: Sphingidae), but these hosts were typically encountered on tobacco by parasitoids in one population (Upper Marlboro) and on tomato by parasitoids in another population (Wye). Early in the season, Wye parasitoids preferred to oviposit in M. sexta on tomato rather than on tobacco and Upper Marlboro parasitoids showed no preference; neither population showed any preference later in the season. Neither of the strains originating from the two populations showed a landing preference for tobacco or tomato in flight chamber trials, but Upper Marlboro parasitoids searched longer on tobacco than on tomato, and Wye parasitoids searched longer on tomato. When nicotine solutions were applied to tobacco leaf, searching responses of Upper Marlboro parasitoids were enhanced by 0.001–1.0% nicotine, and searching responses of Wye parasitoids were decreased by 0.01–1.0% nicotine. We speculate that population differences in searching responses to tobacco and nicotine may explain the differential parasitism responses found early in the season.     

Detrimental effects of plant compounds on a polyembryonic parasitoid are mediated through its highly polyphagous herbivore host

Plant defensive compounds can have sometimes severe deleterious effects on both herbivores and their natural enemies. Iridoid glycosides (IGs) are defensive compounds that are well established as deterrent to several generalist herbivores and generalist predators. Trichoplusia ni Hübner (Lepidoptera: Noctuidae) is exceptional among generalist herbivores for its ability to tolerate and thrive when feeding upon IG‐producing plant species; however, it is not known whether the compounds themselves have a harmful effect on T. ni and whether the effects in turn affect its oligophagous endoparasitoid Copidosoma floridanum Ashmead (Hymenoptera: Encyrtidae). To examine these effects, a semi‐purified extract of the IG‐containing plant Plantago lanceolata L. (Plantaginaceae), containing the IGs aucubin and catalpol, was added to artificial diets at 0, 1, 5, or 10% diet dry weight. These diets were fed to both C. floridanum‐parasitized and unparasitized T. ni. Diets higher in IGs tended to be more toxic to both parasitized and unparasitized larvae: host larvae that did survive were slightly smaller and took longer to develop on higher IG diets and total clutch size and survival of the parasitoid C. floridanum were greatly reduced as the host's dietary intake of IGs increased. Only small amounts of aucubin were detected inside the T. ni hemocoel, suggesting that the negative effect of these compounds on C. floridanum is due to nutritional quality of the host being reduced rather than direct toxic effects of the compounds.     

Foraging behavior of specialist and generalist caterpillars on plantain (Plantago lanceolata) altered by predatory stinkbugs

Summary To examine the effects of predators and plant genotype on the behavior, patterns of herbivory, growth and survivorship of caterpillars, we used an experimental garden in which we contrasted two hostplant genotypes of plantain (Plantago lanceolata), two kinds of herbivores (specialist Junonia coenia vs. generalist Pyrrharctia isabella) and two levels of caterpillar predation (with and without Podisus maculiventris stinkbugs). Each of the replicate plots per treatment contained two plants of the same genotype. The stinkbugs reduced the survivorship of the specialist caterpillars but not that of the generalists, which reflects the differences in predatoravoidance behaviors of these species. Nonetheless, the stinkbugs influenced the behavior of both caterpillar species. When stinkbugs were present, both specialist and generalist caterpillars were less likely to be found on the plant upon which they were initially placed (=initial plant), and they were more likely to be off both plants within the plot than larvae in the absence of predators. Consequently in the presence of the stinkbug predators, the proportion of the initial plants consumed was less than in the absence of the predators. Plant genotype influenced plant size and the proportion of individual plants eaten, but it did not affect larval location on the plots. Neither presence of predators nor plant genotype had an effect on relative growth rate of the caterpillars.     

Comparison of tree genotypic diversity and species diversity effects on different guilds of insect herbivores

Although the effects of plant diversity on herbivores are contingent upon herbivore traits and the source of plant diversity (e.g. intra‐ and interspecific), most studies have analyzed these effects separately. We compared the effects of genotypic diversity of big‐leaf mahogany Swietenia macrophylla with that of tree species diversity on two specialist caterpillars (Hypsipyla grandella stem borers and Phyllocnistis meliacella leaf miners) and three generalist leafhoppers (Cicadellidae) feeding on mahogany in a large‐scale (7.2 ha) forest diversity experiment in southern Mexico. The experiment consisted of fifty‐nine 21 × 21‐m plots, with 64 tree saplings each (3‐m spacing between plants). Plots were either mahogany monocultures or species polycultures of four species (including mahogany) and – within each of these two plot types – mahogany was represented by either one or four genotypes. Throughout a five‐month period, beginning six months after planting, we measured mahogany growth and monitored herbivore and predator (spider) abundance. We found no effect of mahogany genotypic diversity on either specialist caterpillars or generalist leafhoppers, and this result was consistent across levels of tree species diversity. In contrast, species diversity had significant effects on both specialists but neither of the generalist herbivores. Specifically, species diversity lowered H. grandella attack at the middle of the sampling season, but increased attack at the end of the season, whereas P. meliacella abundance was consistently reduced. Such effects were not mediated by effects of species diversity on plant growth (of which there were none), but rather through resource heterogeneity. Diversity did not influence spider abundance. This study is one of few to directly compare sources of plant diversity, and uniquely compares such effects among herbivores with contrasting life histories (e.g. diet breadths). Overall, we demonstrate that plant species diversity effects outweigh those of genotypes, and our results suggest that such effects are stronger on specialist than generalist herbivores.     

Phytochemical defences and performance of specialist and generalist herbivores: a meta-analysis

1. Phytochemical coevolution theory, a long-standing paradigm in plant–insect interactions, predicts that specialist herbivores are less negatively affected by the allelochemicals of their host plants than are generalist herbivores. Although this theory is prevalent in plant–insect science, it is not always supported by empirical studies measuring the performance of specialist and generalist insects in response to allelochemicals. 2. The present study aimed to investigate: (i) whether there a difference between specialist and generalist performance in response to allelochemicals and (ii) whether the effect of allelochemicals on specialists and generalists depend upon allelochemical class or insect order. 3. A meta-analysis was conducted incorporating 76 effect sizes drawn from studies that directly compared the performance of specialist and generalist insects in response to treatment and control diets. Most of the effect sizes were related to the performance metric growth, the insect order Lepidoptera, and the allelochemical class nitrogen-containing compounds. 4. As predicted by phytochemical coevolution theory, specialist insects responded less negatively to allelochemicals of their hosts than generalist insects in terms of growth. There were no significant differences in terms of fecundity or survival, or among allelochemical classes or insect orders. 5. These results support the prediction of phytochemical coevolution theory that specialist insects respond less negatively to allelochemicals of their hosts than generalists, although only in terms of growth.     

Plant chemical defense against herbivores and pathogens: generalized defense or trade-offs?

Plants are often attacked by multiple enemies, including pathogens and herbivores. While many plant secondary metabolites show specific effects toward either pathogens or herbivores, some can affect the performance of both these groups of natural enemies and are considered to be generalized defense compounds. We tested whether aucubin and catalpol, two iridoid glycosides present in ribwort plantain (Plantago lanceolata), confer in vivo resistance to both the generalist insect herbivore Spodoptera exigua and the biotrophic fungal pathogen Diaporthe adunca using plants from P. lanceolata lines that had been selected for high- and low-leaf iridoid glycoside concentrations for four generations. The lines differed approximately three-fold in the levels of these compounds. Plants from the high-selection line showed enhanced resistance to both S. exigua and D. adunca, as evidenced by a smaller lesion size and a lower fungal growth rate and spore production, and a lower larval growth rate and herbivory under both choice and no-choice conditions. Gravimetric analysis revealed that the iridoid glycosides acted as feeding deterrents to S. exigua, thereby reducing its food intake rate, rather than having post-ingestive toxic effects as predicted from in vitro effects of hydrolysis products. We suggest that the bitter taste of iridoid glycosides deters feeding by S. exigua, whereas the hydrolysis products formed after tissue damage following fungal infection mediate pathogen resistance. We conclude that iridoid glycosides in P. lanceolata can serve as broad-spectrum defenses and that selection for pathogen resistance could potentially result in increased resistance to generalist insect herbivores and vice versa, resulting in diffuse rather than pairwise coevolution.     

The effect of β-aminobutyric acid on the growth of herbivorous insects feeding on Brassicaceae

dl ‐β‐Aminobutyric acid (BABA) is a nonprotein amino acid that can enhance defences in a variety of plants against a wide range of pathogens. BABA can also reduce infestation by phytopathogenic nematodes and has recently been shown to suppress the growth of aphids feeding on legumes. This investigation examined the effect of applying BABA as a root drench to a range of Brassicaceae, including Arabidopsis thaliana, on the performance of two species of aphid (Myzus persicae and Brevicoryne brassicae) and the larvae of two species of Lepidoptera (Trichoplusia ni and Plutella xylostella). Application of BABA reduced the performance of all four insect species, and inhibition of insects occurred on all the plants tested. The results illustrate that BABA‐induced resistance (BABA‐IR) can affect generalist and specialist insect herbivores and inhibit insects feeding with mandibulate as well as sap‐feeding mouthparts. The BABA‐induced suppression of B. brassicae and P. xylostella feeding on A. thaliana provides a means to further examine the mechanisms of BABA‐IR to insects using this model plant.