Intraspecific chemical diversity among neighbouring plants correlates positively with plant size and herbivore load but negatively with herbivore damage

Intraspecific plant diversity can modify the properties of associated arthropod communities and plant fitness. However, it is not well understood which plant traits determine these ecological effects. We explored the effect of intraspecific chemical diversity among neighbouring plants on the associated invertebrate community and plant traits. In a common garden experiment, intraspecific diversity among neighbouring plants was manipulated using three plant populations of wild cabbage that differ in foliar glucosinolates. Plants were larger, harboured more herbivores, but were less damaged when plant diversity was increased. Glucosinolate concentration differentially correlated with generalist and specialist herbivore abundance. Glucosinolate composition correlated with plant damage, while in polycultures, variation in glucosinolate concentrations among neighbouring plants correlated positively with herbivore diversity and negatively with plant damage levels. The results suggest that intraspecific variation in secondary chemistry among neighbouring plants is important in determining the structure of the associated insect community and positively affects plant performance.     

Relationship of different feeding groups of true bugs (Hemiptera: Heteroptera) with habitat and landscape features in Pannonic salt grasslands

Eastern European grasslands are still inhabited by a rich arthropod fauna, but the drivers and mechanisms influencing their communities have to be understood to ensure their future survival. Heteroptera communities were studied in 20 plot-pairs in Pannonic salt steppe–salt marsh mosaics in Hungary. The effects of vegetation characteristics, landscape diversity and the proportion of surrounding grasslands on the composition, species richness and abundance of different feeding groups of true bugs (carnivores, specialist and generalist herbivores) were examined using ordinations and mixed-effect models. We found distinct herbivorous assemblages corresponding to microtopography-driven differences in water regime and vegetation between steppe and marsh plots, but this pattern was less pronounced in carnivorous assemblages. A higher species richness of true bugs was found in the more diverse steppe vegetation than in the salt marsh vegetation, while the abundance pattern of true bugs was opposite. Landscape diversity had a positive effect on the species richness and abundance of generalist herbivores and carnivores. Our results suggested that generalist herbivores and carnivores appear to drive diversity patterns in the local landscape due to their high dispersal abilities and the broader range of resources they can utilize. Specialist herbivores strongly influence the local insect biomass in relation to the distribution and density of their host plants. The present study highlights the importance of both habitat and landscape diversity for local insect diversity in Pannonic salt grasslands and suggests that the main threats for arthropod diversity are those processes and activities that homogenize these areas.     

Herbivore preference for native vs. exotic plants: generalist herbivores from multiple continents prefer exotic plants that are evolutionarily naïve

Enemy release and biotic resistance are competing, but not mutually exclusive, hypotheses addressing the success or failure of non-native plants entering a new region. Enemy release predicts that exotic plants become invasive by escaping their co-adapted herbivores and by being unrecognized or unpalatable to native herbivores that have not been selected to consume them. In contrast, biotic resistance predicts that native generalist herbivores will suppress exotic plants that will not have been selected to deter these herbivores. We tested these hypotheses using five generalist herbivores from North or South America and nine confamilial pairs of native and exotic aquatic plants. Four of five herbivores showed 2.4-17.3 fold preferences for exotic over native plants. Three species of South American apple snails (Pomacea sp.) preferred North American over South American macrophytes, while a North American crayfish Procambarus spiculifer preferred South American, Asian, and Australian macrophytes over North American relatives. Apple snails have their center of diversity in South America, but a single species (Pomacea paludosa) occurs in North America. This species, with a South American lineage but a North American distribution, did not differentiate between South American and North American plants. Its preferences correlated with preferences of its South American relatives rather than with preferences of the North American crayfish, consistent with evolutionary inertia due to its South American lineage. Tests of plant traits indicated that the crayfish responded primarily to plant structure, the apple snails primarily to plant chemistry, and that plant protein concentration played no detectable role. Generalist herbivores preferred non-native plants, suggesting that intact guilds of native, generalist herbivores may provide biotic resistance to plant invasions. Past invasions may have been facilitated by removal of native herbivores, introduction of non-native herbivores (which commonly prefer native plants), or both.     

Genetically based latitudinal variation in Artemisia californica secondary chemistry

Steep climatic gradients may select for clinal adaptation in plant functional traits with implications for interspecific interactions and response to future climate change. Terpenes are common in Mediterranean environments and mediate plant interactions with both the abiotic and biotic environment, including herbivores. Clines in traits such as terpenes have received much attention because they are linked to plant fitness and experience strong selection from the abiotic and biotic environment. In this study, we tested for intraspecific variation in Artemisia californica terpene chemistry in a common garden of plants sourced from populations spanning a large precipitation gradient (6° latitude) and grown in treatments of high and low precipitation. We found genetic variation in terpene richness, diversity, concentration and composition among A. californica populations spanning this species’ range. Of these traits, terpene composition and monoterpene concentration varied clinally with respect to source site latitude. Regarding terpene composition, pairwise dissimilarity among populations increased in parallel with geographic distance between source sites. At the same time, monoterpene concentration decreased monotonically from plants of southern origin (source sites with high temperature, aridity, and precipitation variability) to plants of northern origin. Our precipitation manipulation suggests that phenotypic selection by precipitation may underlie this clinal variation in monoterpene concentration, and that monoterpene concentration and other aspects of terpene chemistry are not phenotypically plastic. In summary, this study provides novel evidence for a genetically based latitudinal cline in plant secondary chemistry and suggests that adaptation to a key aspect of the abiotic environment may contribute to this intraspecific variation. Accordingly, changes in terpene chemistry under projected future climates will likely occur solely through the relatively slow process of adaptation, with important consequences for plant interactions with the abiotic environment and a diverse community of associates.     

Attracting friends to feast on foes: engineering terpene emission to make crop plants more attractive to herbivore enemies

When attacked by herbivorous insects or mites, some plant species call on other arthropods for help. They emit mixtures of volatile compounds, dominated by terpenes, to attract carnivorous arthropods that prey on or parasitise herbivores and so reduce further damage. This fascinating defence strategy offers a new, environmentally friendly approach to crop protection. Using recent advances in the biochemistry and molecular genetics of terpene biosynthesis, it should now be possible to engineer crop plants that release terpenes for attracting herbivore enemies. By introducing or selectively altering the existing rate of terpene emission and composition, plant breeders could enable attacked plants to attract enemies and reduce additional herbivory, without compromising the effectiveness of other modes of defence.     

Plant functional traits reveal the relative contribution of habitat and food preferences to the diet of grasshoppers

Food preferences and food availability are two major determinants of the diet of generalist herbivores and of their spatial distribution. How do these factors interact and eventually lead to diet differentiation in co-occurring herbivores? We quantified the diet of four grasshopper species co-occurring in subalpine grasslands using DNA barcoding of the plants contained in the faeces of individuals sampled in the field. The food preferences of each grasshopper species were assessed by a choice (cafeteria) experiment from among 24 plant species common in five grassland plots, in which the four grasshoppers were collected, while the habitat was described by the relative abundance of plant species in the grassland plots. Plant species were characterised by their leaf economics spectrum (LES), quantifying their nutrient vs. structural tissue content. The grasshoppers’ diet, described by the mean LES of the plants eaten, could be explained by their plant preferences but not by the available plants in their habitat. The diet differed significantly across four grasshopper species pairs out of six, which validates food preferences assessed in standardised conditions as indicators for diet partitioning in nature. In contrast, variation of the functional diversity (FD) for LES in the diet was mostly correlated to the FD of the available plants in the habitat, suggesting that diet mixing depends on the environment and is not an intrinsic property of the grasshopper species. This study sheds light on the mechanisms determining the feeding niche of herbivores, showing that food preferences influence niche position whereas habitat diversity affects niche breadth.     

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.     

Diversity protects plant communities against generalist molluscan herbivores

Wildflower strips are used to increase natural enemies of crop pests and to conserve insect diversity on farmland. Mollusks, especially slugs, can affect the vegetation development in these strips considerably. Although recent theoretical work suggests that more diverse plant communities will exhibit greater resistance against herbivore pressure, empirical studies are scarce. We conducted a semi‐natural experiment in wildflower strips, manipulating trophic structure (reduction in herbivorous mollusks and reduction in major predators) and plant diversity (2, 6, 12, 20 and 24 sown species). This design allowed us to assess the effect of plant diversity, biomass and composition on mollusks, and vice versa, the effect of mollusc abundance on vegetation. Seven species of mollusks were found in the strips, with the slugs Arion lusitanicus, Deroceras reticulatum and Deroceras panormitanum being most frequent. We found a negative relationship between plant diversity and mollusk abundance, which was due predominantly to a decrease in the agricultural pest species A. lusitanicus. These results are consistent with the hypothesis that plant diversity can reduce the impact of herbivores. However, plant identity also had an effect on mollusks, and accounted for a much larger fraction of the variation in mollusk communities than biodiversity effects. While overall plant diversity decreased during the 3 years of the study, in the final year the highest plant diversity was found in the plots where mollusk populations were experimentally reduced. We conclude that selective feeding by generalist herbivores leads to changes in plant community composition and hence reduced plant diversity. Our results highlight the importance of plant biodiversity as protection against generalist herbivores, which if abundant can in the long term negatively impact plant diversity, driving the system along a “low plant diversity – high mollusk abundance” trajectory.     

Temporal dynamics in non-additive responses of arthropods to host-plant genotypic diversity

Genotypic diversity within host‐plant populations has been linked to the diversity of associated arthropod communities, but the temporal dynamics of this relationship, along with the underlying mechanisms, are not well understood. In this study, we employed a common garden experiment that manipulated the number of genotypes within patches of Solidago altissima, tall goldenrod, to contain 1, 3, 6 or 12 genotypes m^?2 and measured both host‐plant and arthropod responses to genotypic diversity throughout an entire growing season. Despite substantial phenological changes in host plants and in the composition of the arthropod community, we detected consistent positive responses of arthropod diversity to host‐plant genotypic diversity throughout all but the end of the growing season. Arthropod richness and abundance increased with genotypic diversity by up to～65%. Furthermore, arthropod responses were non‐additive for most of the growing season, with up to 52% more species occurring in mixtures than the number predicted by summing the number of arthropods associated with component genotypes in monoculture. Non‐additive arthropod responses were likely driven by concurrent non‐additive increases in host‐plant aboveground biomass. Qualitative differences among host‐plant genotypes were also important early in the season, when specialist herbivores dominated the arthropod community. Neither arthropod diversity nor flower number was associated with genotypic diversity at the end of the growing season, when generalist floral‐associated herbivores dominated. Taken together, these results show that focusing on the temporal dynamics in the quantity and quality of co‐occurring host‐plant genotypes and associated community composition can help uncover the mechanisms that link intraspecific host‐plant diversity to the structure of arthropod communities. Furthermore, consistent non‐additive effects in genotypically diverse plots may limit the predictability of the arthropod community based solely on the genetic make‐up of a host‐plant patch.     

Community- Weighted Mean Plant Traits Predict Small Scale Distribution of Insect Root Herbivore Abundance

Small scale distribution of insect root herbivores may promote plant species diversity by creating patches of different herbivore pressure. However, determinants of small scale distribution of insect root herbivores, and impact of land use intensity on their small scale distribution are largely unknown. We sampled insect root herbivores and measured vegetation parameters and soil water content along transects in grasslands of different management intensity in three regions in Germany. We calculated community-weighted mean plant traits to test whether the functional plant community composition determines the small scale distribution of insect root herbivores. To analyze spatial patterns in plant species and trait composition and insect root herbivore abundance we computed Mantel correlograms. Insect root herbivores mainly comprised click beetle (Coleoptera, Elateridae) larvae (43%) in the investigated grasslands. Total insect root herbivore numbers were positively related to community-weighted mean traits indicating high plant growth rates and biomass (specific leaf area, reproductive- and vegetative plant height), and negatively related to plant traits indicating poor tissue quality (leaf C/N ratio). Generalist Elaterid larvae, when analyzed independently, were also positively related to high plant growth rates and furthermore to root dry mass, but were not related to tissue quality. Insect root herbivore numbers were not related to plant cover, plant species richness and soil water content. Plant species composition and to a lesser extent plant trait composition displayed spatial autocorrelation, which was not influenced by land use intensity. Insect root herbivore abundance was not spatially autocorrelated. We conclude that in semi-natural grasslands with a high share of generalist insect root herbivores, insect root herbivores affiliate with large, fast growing plants, presumably because of availability of high quantities of food. Affiliation of insect root herbivores with large, fast growing plants may counteract dominance of those species, thus promoting plant diversity.     

PRODUCTION OF SECONDARY METABOLITES BY FILAMENTOUS TROPICAL MARINE CYANOBACTERIA: ECOLOGICAL FUNCTIONS OF THE COMPOUNDS

Cyanobacterial blooms are becoming more common in many reef habitats. The broadly acting feeding deterrent compound ypaoamide, produced by a mixed cyanobacterial assemblage, has been linked to bloom formation and mass fish die-offs ( Siganus argenteus and Siganus spinus ) in Guam. Specific metabolites produced by Lyngbya majuscula Gomont act as both feeding attractants to the specialist herbivore Stylocheilus longicauda , and as effective feeding deterrents to generalist fishes. Two-dimensional TLC (2D-TLC) analysis of cyanobacterial crude extracts was used to select chemically distinct populations (chemotypes) of bloom-forming filamentous cyanobacteria for chemical and ecological evaluation. Crude extracts produced by different species, chemotypes, and chemically distinct Micronesian marine cyanobacterial assemblages deter feeding activity of generalist reef herbivores. The ecological function of cyanobacterial secondary metabolites, especially as related to diversity of compound production and the relationship of metabolite production to bloom formation is discussed.     

Grasshopper Herbivory Affects Native Plant Diversity and Abundance in a Grassland Dominated by the Exotic Grass Agropyron cristatum

The indirect effects of native generalist insect herbivores on interactions between exotic and native grassland plants have received limited attention. Crested wheatgrass ( Agropyron cristatum ) is the most common exotic rangeland grass in western North America. Crested wheatgrass communities are resistant to colonization by native plant species and have strong competitive effects on native species, imposing problems for the restoration of native grasslands. Grasshoppers are generalist herbivores that are often abundant in Crested wheatgrass–dominated sites in the northern Great Plains. We conducted two experiments in a Crested wheatgrass–dominated grassland in western North Dakota to test the hypothesis that grasshopper herbivory influences local Crested wheatgrass community composition by impeding native seedlings. Grasshopper herbivory negatively affected the species richness, abundance, and Shannon diversity of native plants in 3 of 4 years. Although additional research is needed to determine if grasshoppers actively select native plants, the effects of grasshopper herbivory may be an important consideration in the restoration of Crested wheatgrass areas. Our findings illustrate the importance of understanding the impact of native generalist invertebrate herbivores on the relationships between exotic and native plants.     

Evidence for local specialization in a generalist mammalian herbivore, Neotoma fuscipes

Herbivores with very plastic dietary requirements, or so-called generalist species, can include individuals that develop specialized feeding habits through their experience with local chemically-defended plants. Local specialization has important implications for understanding a variety of ecological and evolutionary dynamics. However, the extent to which individuals within a generalist species specialize on local plants and the consequences of such specialization remain poorly understood, especially in non-insect herbivores. To better understand this phenomenon, we determined the diet and food preferences of a generalist mammalian herbivore, the dusky-footed woodrat ( Neotoma fuscipes ), in two adjacent but distinct plant communities. Based on a combination of cafeteria trials and stable isotope analyses (δ¹³C and δ¹⁵N), our results indicate that woodrats display preferences for local plants and tend to avoid novel chemically-defended plants. Moreover, both methodologies support the conclusion that individual woodrats are dietary specialists restricting their diets to only a few (2-3) of the available plant species. In juniper woodland, woodrats prefer western juniper ( Juniperus occidentalis ), while less than one km away in mixed-coniferous forest, woodrats prefer incense cedar ( Calocedrus decurrens ). Both plants contain high levels of plant secondary compounds that require detoxification mechanisms within consumers. Therefore, preferences are likely indicative of underlying physiological adaptations that could promote further behavioral, physiological and ultimately genetic differences between woodrats in different habitats. This study provides additional evidence for local specialization and urges caution when using the term generalist to characterize feeding behaviors at the individual level.     

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.     

Arbuscular mycorrhizal fungi species-specifically affect induced plant responses to a spider mite

It is widely recognized that arbuscular mycorrhizal fungi (AMF) improve plant growth and nutrient conditions, but their effects can vary from negative to positive depending on AMF species. Since the performance of herbivorous arthropods varies with plant quality, different AMF species should differently affect the density of herbivorous arthropods on plants and the herbivore-induced plant responses. We examined the indirect effects of AMF on the number of spider mites (Tetranychus urticae) and the number of damaged leaves in an outdoor glass-chamber experiment, using Lotus japonicus plants inoculated with one of four different AMF species (Gigaspora margarita, Glomus etunicatum, Gl. intraradices, and Acaulospora longula). Plants with Gi. margarita and A. longula had significantly fewer female mites than plants with Gl. etunicatum and Gl. intraradices, and plants with Gi. margarita had the fewest damaged leaves, followed by plants with A. longula, Gl. intraradices, and Gl. etunicatum. To examine species-specific effects of AMF on herbivore-induced plant responses, we carried out a bioassay with eggs laid by spider mites, and analyses of leaf chemicals (carbon, nitrogen, phosphorus, and total phenolics) using plants subjected or not subjected to herbivory. The bioassay showed that mite egg production and its changes following mite herbivory changed depending on the AMF species. In addition, Principal component analysis for leaf chemicals revealed not only mite-induced changes in leaf chemical composition, but also AMF effects on the herbivore-induced response in a species-specific way. Thus, we need to pay more attention to the species identity of AMF as an important factor in determining the strength of effects of belowground AMF on the performance and/or preferences of aboveground herbivores.     

Leaf traits and herbivore selection in the field and in cafeteria experiments

Abstract Despite the vast diversity and complexity of herbivores, plants and their interactions, most authors agree that a small number of components of leaf quality affect preference by generalist herbivores in a predictable way. However, herbivore preference is determined not only by intrinsic plant attributes and herbivore biology but also by the environmental context. Within this framework, we aimed to analyse general interspecific trends in the association between herbivory and leaf traits over a wide range of angiosperms from central Argentina. We (i) tested for consistent associations between leaf traits, consumption in the field, and preference of generalist invertebrate herbivores in cafeteria experiments; (ii) assessed how well herbivore preferences in cafeterias matched leaf consumption in the field; and (iii) developed a simple conceptual model linking leaf traits, herbivore preference in cafeterias and consumption in the field. In general, we found that tender leaves with higher nutritional quality were preferred by herbivores, both in the field and in cafeteria experiments. According to our model, this relationship between field and cafeteria consumption and leaf quality is observed when generalist herbivores and plants of high accessibility are considered. However, differences between leaf consumption in the field and in cafeteria experiments can also be found. At least two reasons can account for this: (i) specialized plant–herbivore relationships often occur in the field, whereas cafeteria experiments tend to consider only one or a few generalist herbivores; (ii) different plant species growing in the field often differ in their degree of accessibility to herbivores, whereas in cafeteria experiments all species are equally accessible. Our results add new evidence to a growing consensus that, although herbivory in the field is determined by many factors, consistent patterns of differential susceptibility to foliar feeders can be found in leaves differing in nutritional quality and thus in resource‐use strategy.     

Plant coexistence alters terpene emission and content of Mediterranean species

There is evidence that secondary metabolism may modulate plant interactions and is modified by different biotic stress agents, such as herbivores or pathogens. However, it is poorly understood whether secondary metabolism is altered during competition among plants. The intraspecific and interspecific coexistence of some Mediterranean potted seedlings, namely Rosmarinus officinalis, Pinus halepensis, Cistus albidus and Quercus coccifera was investigated through their terpene accumulation within leaves (except for Q. coccifera, a non-storing species) and terpene emissions (for all species). Competition had both positive and negative effects for both terpene emissions and content, depending on the species a seedling coexisted with. For R. officinalis, terpene concentrations (1.8-cineole and camphor) and terpene emissions (camphene, camphor and overall monoterpenes) were lower when the neighbour species was P. halepensis. For C. albidus, no changes were observed in its content, while the overall sesquiterpene emissions (70% of total emissions) were reduced in all competition conditions, except in intraspecific competition. In the case of P. halepensis, the highest terpene content occurred when it grew with C. albidus, and in intraspecific competition, while its emissions were reduced under these conditions. Only emissions of Q. coccifera showed no significant changes in the different competition treatments.     

Dietary shift and lowered biomass gain of a generalist herbivore in species-poor experimental plant communities

Species loss of primary producers is likely to affect processes on other trophic levels. We studied consumption and individual performance of the generalist herbivore Parapleurus alliaceus (Orthoptera) in relation to the species richness of primary producers. Adult grasshoppers were caged and left to feed for 2 weeks on experimental grassland communities ranging in plant species richness from one, two, four, eight to 32 species. Low plant diversity had a negative effect on both plant community biomass and on biomass gain of female grasshoppers, feeding to produce eggs (male grasshoppers did not gain biomass during the feeding period). This was surprising because plots with high plant diversity had a low proportion of grass biomass and grasshoppers preferentially selected grasses, leading to a greater exploitation of grasses in experimental communities of higher diversity. Thus, the concurrent increase in non-grass species in the diet from these high-diversity communities must have been beneficial to the generalist herbivore. In addition to the positive effects of plant diversity, the presence of legumes in a mixture with grasses further enhanced the biomass gain of grasshoppers at a given level of diversity. These findings suggest that plant species loss may lead to shifts in herbivore population sizes, reducing those of generalists and benefiting specialists of the remaining plant species. Our results further suggest that generalist herbivores, by having feeding preferences, can also change the relative abundances of plant species with different functional characteristics. This may feedback on both composition and diversity of plant communities.     

Attract and deter: a dual role for pyrrolizidine alkaloids in plant–insect interactions

Pyrrolizidine alkaloids (PAs) are the major defense compounds of plants in the Senecio genus. Here I will review the effects of PAs in Senecio on the preference and performance of specialist and generalist insect herbivores. Specialist herbivores have evolved adaptation to PAs in their host plant. They can use the alkaloids as cue to find their host plant and often they sequester PAs for their own defense against predators. Generalists, on the other hand, can be deterred by PAs. PAs can also affect survival of generalist herbivores. Usually generalist insects avoid feeding on young Senecio leaves, which contain a high concentration of alkaloids. Structurally related PAs can differ in their effects on insect herbivores, some are more toxic than others. The differences in effects of PAs on specialist and generalists could lead to opposing selection on PAs, which may maintain the genetic diversity in PA concentration and composition in Senecio species.