Consequences of variation in plant defense for biodiversity at higher trophic levels

Antagonistic interactions between insect herbivores and plants impose selection on plants to defend themselves against these attackers. Although selection on plant defense traits has typically been studied for pairwise plant-attacker interactions, other community members of plant-based food webs are unavoidably affected by these traits as well. A plant trait might, for example, affect parasitoids and predators feeding on the herbivore. Consequently, defensive plant traits structure the diversity and composition of the complex community associated with the plant, and communities as a whole also feed back to selection on plant traits. Here, we review recent developments in our understanding of how plant defense traits structure insect communities and discuss how molecular mechanisms might drive community-wide effects.     

Global patterns of leaf defenses in oak species

Plant defensive traits drive patterns of herbivory and herbivore diversity among plant species. Over the past 30 years, several prominent hypotheses have predicted the association of plant defenses with particular abiotic environments or geographic regions. We used a strongly supported phylogeny of oaks to test whether defensive traits of 56 oak species are associated with particular components of their climatic niche. Climate predicted both the chemical leaf defenses and the physical leaf defenses of oaks, whether analyzed separately or in combination. Oak leaf defenses were higher at lower latitudes, and this latitudinal gradient could be explained entirely by climate. Using phylogenetic regression methods, we found that plant defenses tended to be greater in oak species that occur in regions with low temperature seasonality, mild winters, and low minimum precipitation, and that plant defenses may track the abiotic environment slowly over macroevolutionary time. The pattern of association we observed between oak leaf traits and abiotic environments was consistent with a combination of a seasonality gradient, which may relate to different herbivore pressures, and the resource availability hypothesis, which posits that herbivores exert greater selection on plants in resource-limited abiotic environments.     

Herbivore‐induced changes in flower scent and morphology affect the structure of flower–visitor networks but not plant reproduction

Herbivory induces various responses in plants, thus altering the plants’ phenotype in chemical and morphological traits. Herbivore‐induced changes in vegetative plant parts, plant‐physiological mechanisms, and effects on plant‐animal interactions have been intensively studied from species to community level. In contrast, we are just beginning to examine herbivore‐induced effects on reproductive plant parts and flower–visitor interactions, especially in a community context. We investigated the effect of herbivory at different plant developmental stages on plant growth, floral and vegetative phenotype and reproduction in Sinapis arvensis (Brassicaceae). Additionally, we tested how herbivore‐induced plant responses affect flower–visitor interactions and plant reproduction in species‐rich communities. Our results indicate that the timing of herbivory affects the magnitude of changes in plant traits. Herbivory in early but not in late development accelerated the plant's flowering phenology, reduced vegetative growth, increased stem trichome density and altered floral morphology and scent. These findings suggest age‐dependent tradeoffs between growth, defense and reproduction. Herbivore‐induced changes in flower traits also affected flower–visitor interactions in a community context with effects on the structure of flower–visitor networks. However, changes in the network structure had neglectable effects on plant reproduction, i.e. plants were able to compensate altered flower visitor behavior. Thus, herbivory is a source of intraspecific variation in reproductive traits, which can be behaviorally relevant for potential pollinators. However, plants were capable to maintain reproductive success suggesting a tolerance against herbivory. We conclude that in our study system induced direct or indirect defenses that have often been shown to decrease negative effects of herbivores on vegetative plant parts come at no costs for plant reproduction.     

The ontogeny of plant indirect defenses

Plants frequently attract natural enemies of their herbivores, resulting in a reduction in tissue damage and often in enhanced plant fitness. While such indirect defenses can dramatically change as plants develop, only recently have ecologists begun to explore such changes and evaluate their role in mediating plant–herbivore–natural enemy interactions. Here we review the literature documenting ontogenetic patterns in plant rewards (i.e. extrafloral nectaries (EFNs), food bodies (FBs) and domatia) and volatile organic compounds (VOCs), and identify links between ontogenetic patterns in such traits and the attraction of natural enemies (ants). In the case of reward traits we concentrate in ant–plant studies, which are the most numerous. We report that all indirect defensive traits commonly vary with plant age but ontogenetic trajectories differ among them. Myrmecophytic species, which provide both food and shelter to their defenders, do not produce rewarding traits until a minimum size is reached. Then, a pronounced increase in the abundance of food rewards and domatia often occurs as plants develop, which explains the temporal succession or colony size increase of mutualistic ant species and, in some cases, leads to a reduction in herbivore damage and enhanced fitness as plants age. In contrast, ontogenetic patterns were less consistent in plant species that rely on VOC emissions to attract natural enemies or those that provide only food rewards (EFNs) but not nesting sites to their associated ants, showing an overall decline or lack of trend with plant development, respectively. Future research should focus on uncovering: (i) the costs and mechanisms underlying ontogenetic variation in indirect defenses, (ii) the relative importance of environmental and genetic components shaping these ontogenetic trajectories, and (iii) the consequences of these ontogenetic trajectories on plant fitness. Advances in this area will shed light on the context dependency of bottom-up and top-down controls of herbivore populations and on how natural selection actually shapes the ontogenetic trajectories of these traits.     

Differential induction of plant chemical defenses by parasitized and unparasitized herbivores: consequences for reciprocal,multitrophic interactions

Insect parasitoids can play ecologically important roles in virtually all terrestrial plant–insect herbivore interactions, yet whether parasitoids alter the defensive traits that underlie interactions between plants and their herbivores remains a largely unexplored question. Here, we examined the reciprocal trophic interactions among populations of the wild cabbage Brassica oleracea that vary greatly in their production of defensive secondary compounds – glucosinolates (GSs), a generalist herbivore, Trichoplusia ni, and its polyembryonic parasitoid Copidosoma floridanum. In a greenhouse environment, plants were exposed to either healthy (unparasitized), parasitized, or no herbivores. Feeding damage by herbivores induced higher levels of the indole GSs, glucobrassicin and neoglucobrassicin, but not any of the other measured GSs. Herbivores parasitized by C. floridanum induced cabbage plants to produce 1.5 times more indole GSs than levels induced by healthy T. ni and five times more than uninduced plants. As a gregarious endoparasitoid, C. floridanum causes its host T. ni to feed more than unparasitized herbivores resulting in increased induction of indole GSs. In turn, herbivore fitness parameters (including differential effects on male and female contributions to lifetime fecundity in the herbivore) were negatively correlated with the aliphatic GSs, sinigrin and gluconapin, whereas parasitoid fitness parameters were negatively correlated with the indole GSs, glucobrassicin and neoglucobrassicin. That herbivores and their parasitoids appear to be affected by different sets of GSs was unexpected given the intimate developmental associations between host and parasitoid. This study is the first to demonstrate that parasitoids, through increasing feeding by their herbivorous hosts, can induce higher levels of non‐volatile plant chemical defenses. While parasitoids are widely recognized to be ubiquitous in most terrestrial insect herbivore communities, their role in influencing plant–insect herbivore relationships is still vastly underappreciated.     

Tibor Jermy (1917–2014)

Throughout the course of their evolution, plants have acquired a wide range of chemical and mechanical defenses to protect against herbivores. Ehrlich & Raven's coevolutionary theory suggests that this diversification of defensive traits is driven by the strong impact of novel traits on insect herbivores. However, the impact of plant defenses on insects is difficult to compare between related plant species due to variation in environmental and biotic conditions. We standardized these factors as far as possible by analyzing the effects of chemical and mechanical defensive traits on insects in a local community of 11 Salicaceae species growing in sympatry, and their leaf‐chewing herbivores. Defensive traits (salicylates, flavonoids, tannins, trichomes, and leaf toughness) were generally not inter‐correlated, with the exception of a negative correlation between salicylates and trichomes. The content of salicylates, a novel group of defensive metabolites in the Salicaceae, was correlated with low herbivore diversity and high host specificity. Despite these effects, the phylogeny of the studied species shows loss of salicylates in some Salix species instead of their further diversification. This could be due to salicylates not decreasing the overall abundance of herbivores, despite accounting for up to 22% of the dry leaf mass and therefore being costly. The defense of low‐salicylate willow species is thus probably maintained by other defensive traits, such as trichomes. Our study shows that the balance between costs and benefits of defensive traits is not necessarily in favor of novel compounds and illustrates a process, which may lead to the reduction in a defensive trait.     

Effects of different secondary metabolite profiles in plant defense syndromes on specialist and generalist herbivores

Plants defend themselves against herbivores not only by a single trait but also by diversified multiple defense strategies. It remains unclear how these multiple defense mechanisms are effectively organized against herbivores. In this study, we focused on Brassicaceae plants, which have one of the most diversified secondary metabolites, glucosinolates (GSLs), as a defense against herbivores. By analyzing various defense traits including GSL profiles among 12 species (11 genera) of Brassicaceae plants, it is revealed that their defense strategies can be divided into three categories as multiple defenses. The GSL profiles differed between these three categories: (i) high nutritional level with long‐chain aliphatic GSLs; (ii) low nutritional level and high physical defenses with short‐chain aliphatic GSLs; and (iii) high nutritional level and low defense. The feeding experiment was conducted using two types of herbivores, Pieris rapae (Lepidoptera: Pieridae) as a specialist herbivore and the Eri silkmoth Samia cynthia ricini (Lepidoptera: Saturniidae) as a generalist, to assess the ability of each plant in multiple defense strategy. It was observed that the Eri silkmoth's performance differed according to which defense strategy it was exposed to. However, the growth rate of P. rapae did not vary among the three categories of defense strategy. These results suggest that the diversified defense strategies of Brassicaceae species have evolved to cope with diversified herbivores.     

Geographic variation and temporal changes in plant–herbivore interaction: Case studies with Solidago altissima in native and introduced ranges

Plants are subjected to environmental gradients and may encounter various herbivores, leading to geographic variation in defensive traits. The present review highlights that biological invasions are remarkable natural experiments for studying geographic variation in plant–herbivore interaction and tracking temporal dynamics in plant defense in response to environmental changes. Studies from this viewpoint can challenge various general topics in plant ecology, including the evolution of plant defense and indirect interactions among plants. First, I provide a brief overview on how the introduction of exotic herbivores drives rapid evolution after the establishment of exotic plants and its impacts on native plants. Second, I present a series of case studies investigating the patterns and mechanisms of geographic variation in the interaction between Solidago altissima and Corythucha marmorata (lace bug) in the native range in the United States and the introduced range in Japan. By combining biogeographical and experimental approaches, my collaborators and I unraveled the temporal dynamics of S. altissima's resistance to lace bugs and explored the drivers of differentiation in resistance between native and introduced ranges. These studies provide new insight into the geographic variation in exotic plant–herbivore interaction by unraveling the mechanisms and the temporal scale that cause the variation. These findings are vital not only for predicting invasiveness of exotic plants but also for understanding the evolution of plant–herbivore interaction in community contexts and under climate change.     

Fungal grass endophytes and arthropod communities: lessons from plant defence theory and multitrophic interactions

Alkaloids produced by systemic fungal endophytes of grasses are thought to act as defensive agents against herbivores. Endophytic alkaloids may reduce arthropod herbivore abundances and diversity in agronomic grasses. Yet, accumulating evidence, particularly from native grasses, shows that herbivore preference, abundances and species richness are sometimes greater on endophyte-infected plants, even those with high alkaloids, contrary to the notion of defensive mutualism. We argue that these conflicting results are entirely consistent with well-developed concepts of plant defence theory and tri-trophic interactions. Plant secondary chemicals and endophytic alkaloids often fail to protect plants because: (1) specialist herbivores evolve to detoxify and use defensive chemicals for growth and survival; and (2) natural enemies of herbivores may be more negatively affected by alkaloids than are herbivores. Endophytes and their alkaloids may have profound, but often highly variable, effects on communities, which are also consistent with existing theories of plant defence and community genetics.     

Insect herbivory and herbivores of Ficus species along a rain forest elevational gradient in Papua New Guinea

Classic research on elevational gradients in plant–herbivore interactions holds that insect herbivore pressure is stronger under warmer climates of low elevations. However, recent work has questioned this paradigm, arguing that it oversimplifies the ecological complexity in which plant–insect herbivore interactions are embedded. Knowledge of antagonistic networks of plants and herbivores is however crucial for understanding the mechanisms that govern ecosystem functioning. We examined herbivore damage and insect herbivores of eight species of genus Ficus (105 saplings) and plant constitutive defensive traits of two of these species, along a rain forest elevational gradient of Mt. Wilhelm (200–2,700 m a.s.l.), in tropical Papua New Guinea. We report overall herbivore damage 2.4% of leaf area, ranging from 0.03% in Ficus endochaete at 1,700 m a.s.l. to 6.1% in F. hombroniana at 700 m a.s.l. Herbivore damage and herbivore abundances varied significantly with elevation, as well as among the tree species, and between the wet and dry season. Community-wide herbivore damage followed a hump-shaped pattern with the peak between 700 and 1,200 m a.s.l. and this pattern corresponded with abundance of herbivores. For two tree species surveyed in detail, we observed decreasing and hump-shaped patterns in herbivory, in general matching the trends found in the set of plant defenses measured here. Our results imply that vegetation growing at mid-elevations of the elevational gradient, that is at the climatically most favorable elevations where water is abundant, and temperatures still relatively warm, suffers the maximum amount of herbivorous damage which changes seasonally, reflecting the water availability.     

Natural selection and the joint evolution of toleranceand resistance as plant defenses

Plants can defend themselves against the damaging effects of herbivory in at least two ways. Resistant plants avoid or deter herbivores and are therefore fed upon less than susceptible plants. Tolerant plants are not eaten less than plants with little tolerance, but the effects of herbivore damage are not so detrimental to a tolerant plant as they are to a less tolerant plant. Biologists have suggested that these two strategies might represent two alternative and redundant defenses against herbivory since they appear to serve the same function for plants. I explore the relationship between resistance and tolerance, particularly with regards to how the joint evolution of these two traits will influence the evolution of plant defense. Although I briefly review some of the contributions of theory to the study of tolerance, I concentrate on an empirical, ecological genetic approach to the study of the evolution of these characters and the coevolution of tolerance and herbivores. In order to understand the evolution of any trait, we must understand the evolutionary forces acting on the trait. Specifically, we must understand how natural selection acts on tolerance. I review several studies that have specifically measured the form of selection acting on tolerance and tested the hypothesis that resistance and tolerance are alternative strategies. I also present a statistical analysis that does not support the hypothesis that herbivores are selective agents on tolerance. Finally, I consider a variety of constraints that possibly restrict the evolution of tolerance. This revised version was published online in July 2006 with corrections to the Cover Date.     

Mechanisms of plant defense against insect herbivores

Plants respond to herbivory through various morphological, biochemicals, and molecular mechanisms to counter/offset the effects of herbivore attack. The biochemical mechanisms of defense against the herbivores are wide-ranging, highly dynamic, and are mediated both by direct and indirect defenses. The defensive compounds are either produced constitutively or in response to plant damage, and affect feeding, growth, and survival of herbivores. In addition, plants also release volatile organic compounds that attract the natural enemies of the herbivores. These strategies either act independently or in conjunction with each other. However, our understanding of these defensive mechanisms is still limited. Induced resistance could be exploited as an important tool for the pest management to minimize the amounts of insecticides used for pest control. Host plant resistance to insects, particularly, induced resistance, can also be manipulated with the use of chemical elicitors of secondary metabolites, which confer resistance to insects. By understanding the mechanisms of induced resistance, we can predict the herbivores that are likely to be affected by induced responses. The elicitors of induced responses can be sprayed on crop plants to build up the natural defense system against damage caused by herbivores. The induced responses can also be engineered genetically, so that the defensive compounds are constitutively produced in plants against are challenged by the herbivory. Induced resistance can be exploited for developing crop cultivars, which readily produce the inducible response upon mild infestation, and can act as one of components of integrated pest management for sustainable crop production.     

Community heterogeneity and the evolution of interactions between plants and insect herbivores

Plant communities vary tremendously in terms of productivity, species diversity, and genetic diversity within species. This vegetation heterogeneity can impact both the likelihood and strength of interactions between plants and insect herbivores. Because altering plant-herbivore interactions will likely impact the fitness of both partners, these ecological effects also have evolutionary consequences. We review several hypothesized and well-documented mechanisms whereby variation in the plant community alters the plant-herbivore interaction, discuss potential evolutionary outcomes of each of these ecological effects, and conclude by highlighting several avenues for future research. The underlying theme of this review is that the neighborhood of plants is an important determinant of insect attack, and this results in feedback effects on the plant community. Because plants exert selection on herbivore traits and, reciprocally, herbivores exert selection on plant-defense traits, variation in the plant community likely contributes to spatial and temporal variation in both plant and insect traits, which could influence macroevolutionary patterns.     

Specificity of induced plant responses to specialist herbivores of the common milkweed Asclepias syriaca

Induced plant responses to herbivory appear to be universal, yet the degree to which they are specific to sets of herbivores is poorly understood. The generalist/specialist hypothesis predicts that generalist herbivores are more often negatively affected by host plant defenses, wheras specialists may be either unaffected by or attracted to these same "plant defenses". Therefore, specialists should be less predictable than generalists in their responses to induced plant resistance traits. To better understand the variation in plant responses to herbivore attack, and the impacts these responses have on specialist herbivores, we conducted a series of experiments examining pairwise interactinos between two specialaist herbivores of the common milkweed ( Asclepias syriaca ). We damaged plants mechnically, with swamp milkweed beetles ( Labidomera clivicollis ), or with monarchs ( Danaus plexippus ), and then asessed specificity of elicitation, both by measuring a putative defensive trait (latex volume) and by challenging plants with insects of both species in bioasays. Latex production increased by 34% and 13% following beetle and monarch herbivory, respectively, but only beetles significantly elevated latex production compared to undamaged controls. While beetle growth was negatively affected by latex across all experiments, beetles were not affected by previous damage caused by conspecifies or by monarchs. In contrast, monarchs feeding on previously damaged plants were 20% smaller, and their response was the same on plants damaged mechnically or by either herbivore. Therefore, these specialist herbivores exhibit both specificity of elicitation in plant responses and specificity of effects in response to prior damage.     

Rapid evolution of Medicago polymorpha during invasion shifts interactions with the soybean looper

The Enemy Release Hypothesis posits that invasion of novel habitats can be facilitated by the absence of coevolved herbivores. However, a new environment and interactions with unfamiliar herbivores may impose selection on invading plants for traits that reduce their attractiveness to herbivores or for enhanced defenses compared to native host plants, leading to a pattern similar to enemy release but driven by evolutionary change rather than ecological differences. The Shifting Defense Hypothesis posits that plants in novel habitats will shift from specialized defense mechanisms to defense mechanisms effective against generalist herbivores in the new range. We tested these ideas by comparing herbivore preference and performance of native (Eurasia)‐ and invasive (New World)‐range Medicago polymorpha, using a generalist herbivore, the soybean looper, that co‐occurs with M. polymorpha in its New World invaded range. We found that soybean loopers varied in preference and performance depending on host genotype and that overall the herbivore preferred to consume plant genotypes from naïve populations from Eurasia. This potentially suggests that range expansion of M. polymorpha into the New World has led to rapid evolution of a variety of traits that have helped multiple populations become established, including those that may allow invasive populations to resist herbivory. Thus, enemy release in a novel range can occur through rapid evolution by the plant during invasion, as predicted by the Shifting Defense Hypothesis, rather than via historical divergence.     

Herbivore induced plant volatiles: Their role in plant defense for pest management

Plants respond to herbivory through different defensive mechanisms. The induction of volatile emission is one of the important and immediate response of plants to herbivory. Herbivore-induced plant volatiles (HIPVs) are involved in plant communication with natural enemies of the insect herbivores, neighboring plants, and different parts of the damaged plant. Release of a wide variety of HIPVs in response to herbivore damage and their role in plant-plant, plant-carnivore and intraplant communications represents a new facet of the complex interactions among different trophic levels. HIPVs are released from leaves, flowers, and fruits into the atmosphere or into the soil from roots in response to herbivore attack. Moreover, HIPVs act as feeding and/or oviposition deterrents to insect pests. HIPVs also mediate the interactions between the plants and the microorganisms. This review presents an overview of HIPVs emitted by plants, their role in plant defense against herbivores and their implications for pest management.     

Mechanisms and ecological consequences of plant defence induction and suppression in herbivore communities

Background Plants are hotbeds for parasites such as arthropod herbivores, which acquire nutrients and energy from their hosts in order to grow and reproduce. Hence plants are selected to evolve resistance, which in turn selects for herbivores that can cope with this resistance. To preserve their fitness when attacked by herbivores, plants can employ complex strategies that include reallocation of resources and the production of defensive metabolites and structures. Plant defences can be either prefabricated or be produced only upon attack. Those that are ready-made are referred to as constitutive defences. Some constitutive defences are operational at any time while others require activation. Defences produced only when herbivores are present are referred to as induced defences. These can be established via de novo biosynthesis of defensive substances or via modifications of prefabricated substances and consequently these are active only when needed. Inducibility of defence may serve to save energy and to prevent self-intoxication but also implies that there is a delay in these defences becoming operational. Induced defences can be characterized by alterations in plant morphology and molecular chemistry and are associated with a decrease in herbivore performance. These alterations are set in motion by signals generated by herbivores. Finally, a subset of induced metabolites are released into the air as volatiles and function as a beacon for foraging natural enemies searching for prey, and this is referred to as induced indirect defence.Scope The objective of this review is to evaluate (1) which strategies plants have evolved to cope with herbivores and (2) which traits herbivores have evolved that enable them to counter these defences. The primary focus is on the induction and suppression of plant defences and the review outlines how the palette of traits that determine induction/suppression of, and resistance/susceptibility of herbivores to, plant defences can give rise to exploitative competition and facilitation within ecological communities “inhabiting” a plant.Conclusions Herbivores have evolved diverse strategies, which are not mutually exclusive, to decrease the negative effects of plant defences in order to maximize the conversion of plant material into offspring. Numerous adaptations have been found in herbivores, enabling them to dismantle or bypass defensive barriers, to avoid tissues with relatively high levels of defensive chemicals or to metabolize these chemicals once ingested. In addition, some herbivores interfere with the onset or completion of induced plant defences, resulting in the plant’s resistance being partly or fully suppressed. The ability to suppress induced plant defences appears to occur across plant parasites from different kingdoms, including herbivorous arthropods, and there is remarkable diversity in suppression mechanisms. Suppression may strongly affect the structure of the food web, because the ability to suppress the activation of defences of a communal host may facilitate competitors, whereas the ability of a herbivore to cope with activated plant defences will not. Further characterization of the mechanisms and traits that give rise to suppression of plant defences will enable us to determine their role in shaping direct and indirect interactions in food webs and the extent to which these determine the coexistence and persistence of species.     

Indirect plant defense against insect herbivores: a review

Plants respond to herbivore attack by launching 2 types of defenses: direct defense and indirect defense. Direct defense includes all plant traits that increase the resistance of host plants to insect herbivores by affecting the physiology and/or behavior of the attackers. Indirect defense includes all traits that by themselves do not have significant direct impact on the attacking herbivores, but can attract natural enemies of the herbivores and thus reduce plant loss. When plants recognize herbivore‐associated elicitors, they produce and release a blend of volatiles that can attract predators, parasites, and other natural enemies. Known herbivore‐associated elicitors include fatty acid–amino acid conjugates, sulfur‐containing fatty acids, fragments of cell walls, peptides, esters, and enzymes. Identified plant volatiles include terpenes, nitrogenous compounds, and indoles. In addition, constitive traits including extrafloral nectars, food bodies, and domatia can be further induced to higher levels and attract natural enemies as well as provide food and shelter to carnivores. A better understanding of indirect plant defense at global and componential levels via advanced high throughput technologies may lead to utilization of indirect defense in suppression of herbivore damage to plants.     

Family matters: effect of host plant variation in chemical and mechanical defenses on a sequestering specialist herbivore

Insect herbivores contend with various plant traits that are presumed to function as feeding deterrents. Paradoxically, some specialist insect herbivores might benefit from some of these plant traits, for example by sequestering plant chemical defenses that herbivores then use as their own defense against natural enemies. Larvae of the butterfly species Battus philenor (L.) (Papilionidae) sequester toxic alkaloids (aristolochic acids) from their Aristolochia host plants, rendering larvae and adults unpalatable to a broad range of predators. We studied the importance of two putative defensive traits in Aristolochia erecta: leaf toughness and aristolochic acid content, and we examined the effect of intra- and interplant chemical variation on the chemical phenotype of B. philenor larvae. It has been proposed that genetic variation for sequestration ability is ??invisible to natural selection?? because intra- and interindividual variation in host-plant chemistry will largely eliminate a role for herbivore genetic variation in determining an herbivore??s chemical phenotype. We found substantial intra- and interplant variation in leaf toughness and in the aristolochic acid chemistry in A. erecta. Based on field observations and laboratory experiments, we showed that first-instar larvae preferentially fed on less tough, younger leaves and avoided tougher, older leaves, and we found no evidence that aristolochic acid content influenced first-instar larval foraging. We found that the majority of variation in the amount of aristolochic acid sequestered by larvae was explained by larval family, not by host-plant aristolochic acid content. Heritable variation for sequestration is the predominant determinant of larval, and likely adult, chemical phenotype. This study shows that for these highly specialized herbivores that sequester chemical defenses, traits that offer mechanical resistance, such as leaf toughness, might be more important determinants of early-instar larval foraging behavior and development compared to plant chemical defenses.     

The effects of qualitative and quantitative variation of aristolochic acids on preference and performance of a generalist herbivore

Nearly all plants possess chemicals that are inferred to play a role in anti‐herbivore defense or resistance. The effects of various chemical defenses can vary among herbivores. Often, plant defensive compounds are examined in broad, inclusive categories, with an emphasis on total quantity, which might ignore qualitative variation in activity. Aristolochic acids are alkaloids characteristic of plants of the genus Aristolochia (Aristolochiaceae). Although aristolochic acids have been documented as effective herbivore deterrents, it remains unknown whether different kinds of aristolochic acid vary in their efficacy as defense against herbivores. We manipulated the aristolochic acid content of artificial diet to examine the effects of four aristolochic acids on larval preference and performance of the generalist herbivore Spodoptera exigua Hübner (Lepidoptera: Noctuidae). Using choice tests, we observed that the four aristolochic acids tested varied in their deterrent effectiveness, with AA‐I having the strongest effect and AA‐II having the weakest effect. No‐choice tests were used to examine larval performance. The effect on performance varied among the aristolochic acids tested. Higher concentrations of aristolochic acid were generally associated with reduced larval developmental rate and larger size at pupation. These results indicate that various forms of aristolochic acid can vary in their effect on herbivores and that simple aggregate measures of total concentration might not reflect the chemical defensive phenotype of the plant.