Induced resistance in a brown alga: phlorotannins, genotypic variation and fitness costs for the crustacean herbivore

In the marine littoral, strong grazing pressure selects for macroalgal defenses such as the constitutive and inductive production of defense metabolites. Induced defenses are expected under spatiotemporally varying grazing pressure and should be triggered by a reliable cue from herbivory, thereby reducing grazing pressure via decreased herbivore preference and/or performance. Although induced resistance has frequently been demonstrated in brown macroalgae, it is yet to be investigated whether induced macroalgal resistance shows genetic variation, a prerequisite for evolutionary responses to selection. In addition, consequences of induced resistance on herbivore performance have rarely been tested while the role of brown algal phlorotannins as inducible defense metabolites remains ambiguous. Using preference bioassays, we tested various cues, e.g., natural grazing, waterborne cues or simulated grazing to induce resistance in the brown alga Fucus vesiculosus. Further, we investigated whether there are induced responses in phlorotannin content, genetic variation in induced resistance or incurred performance costs to the mesoherbivore isopod, Idotea baltica. We found that both direct grazing and waterborne grazing cues decreased the palatability of F. vesiculosus, while increasing the total phlorotannin content. Since the sole presence of the herbivore also increased the total soluble phlorotannins, yet failed to stimulate deterrence, we concluded that phlorotannins alone do not explain increased resistance. Induced resistance varied between algal genotypes and thus showed potential for evolutionary responses to variation in grazing pressure. Induced resistance also incurred performance costs for female I. baltica via reduced egg production. Our results show that the induced resistance of F. vesiculosus decreases grazing pressure by deterring herbivores as well as impairing their performance. Resistance may be induced in advance by waterborne cues and spread effectively throughout the F. vesiculosus belt. Through lowering herbivore performance, induced resistance may also reduce future grazing pressure by decreasing the population growth rate of I. baltica.     

Higher resistance to herbivory in introduced compared to native populations of a seaweed

Non-indigenous species (NIS) are important components of global change, and in order to manage such species it is important to understand which factors affect their success. Interactions with enemies in the new range have been shown to be important for the outcome of introductions, but thus far most studies on NIS–enemy interactions have considered only specialist herbivores in terrestrial systems. Here we present the results from the first biogeographic study that compares herbivore resistance between populations in the native and new region of a non-indigenous seaweed. We show that low consumption of the non-indigenous seaweed by a generalist herbivore is caused by higher chemical defence levels and herbivore resistance in the new range—and not by the failure of the herbivore to recognise the non-indigenous seaweed as a suitable host. Since most seaweed–herbivore interactions are dominated by generalist herbivores, this pattern could be common in marine communities. Our results also reveal that traits used to predict the invasive potential of species, such as their resistance to enemies, can change during the invasion process, but not always in the way predicted by dominant theories.     

Comparing the Relative Importance of Water-Borne Cues and Direct Grazing for the Induction of Defenses in the Brown Seaweed Fucus vesiculosus

Some seaweed species have been shown to release water-borne cues after herbivore attack, for example, to attract natural enemies of the herbivore. These cues may also be sensed by neighboring seaweeds and used to adjust their defenses in anticipation of a possible herbivore attack. Several studies indicated information transfer between seaweed individuals in the past, including the brown seaweed Fucus vesiculosus. Previous work showed induction of defenses in F. vesiculosus in response to water-borne cues released by isopod-grazed conspecifics. In contrast, another study on induced responses after exposure to cues from isopod-grazed neighbors using the same seaweed species yielded contradictory results. This study reassessed the ability of F. vesiculosus individuals to sense water-borne cues released by isopod-grazed neighbors in a series of experiments that monitored F. vesiculosus palatability in response to direct grazing by Idotea baltica and water-borne cues from isopod-grazed neighbors relative to unmanipulated seaweed pieces. Two-choice feeding assays were conducted with both fresh and reconstituted seaweed pieces. Direct grazing by I. baltica induced a chemical defense in F. vesiculosus, confirming results of previous studies. In contrast, evidence for increased herbivore resistance in seaweed pieces that were located downstream of isopod-grazed F. vesiculosus could not be provided. The lack of defense induction in response to grazing of conspecific neighbors may be explained by the environmental conditions and the scattered distribution of F. vesiculosus individuals in the intertidal zone of Helgoland, which may render resource investment in the emission and/or response to water-borne cues at this site unprofitable.     

Grazers: biocatalysts of terrestrial silica cycling

Silica is well known for its role as inducible defence mechanism countering herbivore attack, mainly through precipitation of opaline, biogenic silica (BSi) bodies (phytoliths) in plant epidermal tissues. Even though grazing strongly interacts with other element cycles, its impact on terrestrial silica cycling has never been thoroughly considered. Here, BSi content of ingested grass, hay and faeces of large herbivores was quantified by performing multiple chemical extraction procedures for BSi, allowing the assessment of chemical reactivity. Dissolution experiments with grass and faeces were carried out to measure direct availability of BSi for dissolution. Average BSi and readily soluble silica numbers were higher in faeces as compared with grass or hay, and differences between herbivores could be related to distinct digestive strategies. Reactivity and dissolvability of BSi increases after digestion, mainly due to degradation of organic matrices, resulting in higher silica turnover rates and mobilization potential from terrestrial to aquatic ecosystems in non-grazed versus grazed pasture systems (2 versus 20 kg Si ha⁻¹ y⁻¹). Our results suggest a crucial yet currently unexplored role of herbivores in determining silica export from land to ocean, where its availability is linked to eutrophication events and carbon sequestration through C–Si diatom interactions.     

Inducible defenses,competition and shared predation in planktonic food chains

Ecologists have long debated the role of predation in mediating the coexistence of prey species. Theory has mainly taken a bitrophic perspective that excludes the effects of inducible defenses at different trophic levels. However, inducible defenses could either limit or enhance the effects of predation on coexistence, by means of effects on bottom-up control and population stability. Our aim was to investigate how inducible defenses at different trophic levels affect the possibilities for predator-mediated coexistence, as opposed to competitive exclusion, in replicated experimental plankton communities. In particular, we analyzed how the presence or absence of inducible defenses in algal basal prey affected the outcome of competition between an inducible defended and an undefended herbivore, in the presence or absence of a carnivore. We found the undefended herbivore to be a superior competitor in the absence of predation. This outcome was reversed in the presence of a shared carnivore: populations of the undefended herbivore then strongly declined. The extent of this population decline differed between food webs based on undefended as opposed to inducible defended algal prey. In the former the undefended herbivore became undetectable for most of the duration of the experiment. In the latter the undefended herbivore also crashed to low densities, but it could still be detected during most of the experiment. In food webs based on inducible defended algae, the carnivore failed to reach high densities and exerted weaker top-down control on the two competing herbivores. We conclude that the inducible defense in one of our two competing herbivores allowed the outcome of competition to be reversed when a shared carnivore was added. Inducible defenses in algae did not change this outcome, but they significantly delayed extinction of the undefended herbivore. Predation itself did not promote coexistence in these experimental plankton communities.     

Modeling herbivore competition mediated by inducible changes in plant quality

Competition between herbivorous insects often occurs as a trait mediated indirect effect mediated by inducible changes in plant quality rather than a direct effect mediated by plant biomass. While plant-mediated competition likely influences many herbivores, progress linking studies of plant-mediated competition in terrestrial phytophagous insects to longer-term consequences for herbivore communities has been elusive, and there is little relevant theory to guide this effort. We present simple models describing plant-mediated interactions between two herbivorous insects or other functionally equivalent organisms. These models consider general features of plant-mediated competition including specificity of elicitation by and effects on herbivores, positive and negative interactions among herbivores, competition independent of changes in plant biomass, and the existence of multiple relevant plant traits. Our analyses generate four important conclusions. First, herbivores competing strongly via only one plant quality phenotype exhibit a limited range of outcomes. These include coexistence and competitive exclusion of either herbivore, but do not include initial condition dependence. Second, when the outcome of competition is competitive exclusion, the herbivore that persists is the one that can do so under the highest inducible reductions in plant quality. Third, competition via more than one inducible phenotype can exhibit a wider range of outcomes including multiple equilibria and initial condition dependence. Finally, transient dynamics may not predict the eventual outcome of competition when changes in plant quality are slow relative to herbivore population growth, especially when herbivores compete through multiple phenotypes. We interpret our results in terms of competition outcomes reported in the literature, and suggest directions for the future empirical study of herbivore competition mediated by inducible changes in plant quality.     

Ecological costs of biotrophic versus necrotrophic pathogen resistance, the hypersensitive response and signal transduction

Recent advances along numerous research avenues show that plant interactions with biotrophic and necrotrophic pathogens use similar pathways with opposing effects. The hypersensitive response is associated with increased biotroph resistance but decreased necrotroph resistance. In plant/herbivore interactions, opposing effects of defenses against specialist versus generalist herbivores are controlled by plant secondary metabolites, where a metabolite that provides resistance to generalist herbivores may stimulate specialist herbivores. This multi-trophic interaction is presented as an ecological cost of plant resistance, but similar concepts are rarely applied to plant interactions with different classes of pathogens. In this review, we begin to describe how necrotrophic pathogens may place an ecological cost upon plant resistance to biotrophic pathogens. We separate these potential ecological costs into three concepts: (1) the local cost of the hypersensitive response, (2) organismal cost of having machinery for a hypersensitive response and (3) antagonism between salicylate and jasmonate signaling. We describe the literature supporting these concepts and some predictions that they generate.     

Mesoherbivores reduce net growth and induce chemical resistance in natural seaweed populations

Herbivory on marine macroalgae (seaweeds) in temperate areas is often dominated by relatively small gastropods and crustaceans (mesoherbivores). The effects of these herbivores on the performance of adult seaweeds have so far been almost exclusively investigated under artificial laboratory conditions. Furthermore, several recent laboratory studies with mesoherbivores indicate that inducible chemical resistance may be as common in seaweeds as in vascular plants. However, in order to further explore and test the possible ecological significance of induced chemical resistance in temperate seaweeds, data are needed that address this issue in natural populations. We investigated the effect of grazing by littorinid herbivorous snails (Littorina spp.) on the individual net growth of the brown seaweed Ascophyllum nodosum in natural field populations. Furthermore, the capacity for induced resistance in the seaweeds was assessed by removing herbivores and assaying for relaxation of defences. We found that ambient densities of gastropod herbivores significantly reduced net growth by 45% in natural field populations of A. nodosum. Seaweeds previously exposed to grazing in the field were less consumed by gastropod herbivores in feeding bioassays. Furthermore, the concentration of phlorotannins (polyphenolics), which have been shown to deter gastropod herbivores, was higher in the seaweeds that were exposed to gastropod herbivores in the field. This field study corroborates earlier laboratory experiments and demonstrates that it is important to make sure that the lack of experimental field data on marine mesoherbivory does not lead to rash conclusions about the lack of significant effects of these herbivores on seaweed performance. The results strongly suggest that gastropods exert a significant selection pressure on the evolution of defensive traits in the seaweeds, and that brown seaweeds can respond to attacks by natural densities of these herbivores through increased chemical resistance to further grazing.     

Symbiont-mediated changes in Lolium arundinaceum inducible defenses: evidence from changes in gene expression and leaf composition

Plants have multiple strategies to deal with herbivory, ranging from chemical or physical defenses to tolerating damage and allocating resources for regrowth. Grasses usually tolerate herbivory, but for some cool-season grasses, their strategy may depend upon their interactions with intracellular symbionts. Neotyphodium endophytes are common symbionts in pooid grasses, and, for some host species, they provide chemical defenses against both vertebrate and invertebrate herbivores. Here, it was tested whether defenses provided by Neotyphodium coenophialum in Lolium arundinaceum (tall fescue) are inducible by both mechanical damage and herbivory from an invertebrate herbivore, Spodoptera frugiperda (fall armyworm), via a bioassay and by quantifying mRNA expression for lolC, a gene required for loline biosysnthesis. Both mechanical and herbivore damage had a negative effect on the reproduction of a subsequent herbivore, Rhopalosiphum padi (bird cherry-oat aphid), and herbivore damage caused an up-regulation of lolC. Uninfected grass hosts also had significantly higher foliar N% and lower C:N ratio compared with infected hosts, suggesting greater allocation to growth rather than defense. For L. arundinaceum, N. coenophialum appears to switch its host's defensive strategy from tolerance via compensation to resistance.     

Plant damage and herbivore performance change with latitude for two old‐field plant species,but rarely as predicted

A long standing hypothesis in biogeography is that latitudinal gradients in plant defenses (LGPD) should arise because selection for plant defenses is greater in the tropics compared to temperate areas. Previous studies have focused on plant traits thought to confer resistance, yet many traits may not actually confer resistance (putative resistance) or interact to influence herbivore performance. In this study, I used a multi‐trophic approach to examine relationships between latitude, herbivore pressure, and plant resistance (measured as the growth rates of herbivores) of two old‐field plant species (Solanum carolinense and Solidago altissima) using a field survey across a 12 degree gradient in the eastern US combined with laboratory bioassays measuring the performance of generalist and specialist herbivores. I used structural equation modeling to examine the direct and indirect pathways by which latitude influences herbivore pressure and plant resistance. A latitudinal gradient in plant damage was observed in the expected direction for S. caroliense (damage decreased with latitude), but the opposite relationship was observed for S. altissima. Damage to both plant species was mediated by herbivore abundances, which was in turn influenced by predator abundances. Resistance to herbivores also varied with latitude but the form of the relationship was dependent on herbivore and plant species. There were direct, non‐linear relationships between latitude and resistance (for Spodoptera exigua and Schistocerca americana feeding on S. altissima; S. exigua and Manduca sexta feeding on S. carolinense). Herbivore growth rates were also mediated by the density of S. carolinense for Leptinotarsa juncta and S. americana feeding on S. carolinense. There was no relationship between plant resistance and herbivore pressure and no indication of feedbacks. Results from this study indicate that latitudinal variation in plant resistance is complex, possibly constrained by resource availability and tradeoffs in plant defenses.     

Interactions between plants and herbivores: A review of plant defense

Ecologists have long ignored or underestimated the importance of plant–herbivore interactions owing to the diversities of herbivores, plant defensive strategies and ecological systems. In this review, we briefly discussed the categories of herbivores. Then we reviewed the major types of plant defenses against herbivores. Selective forces of herbivore pressures have led to the evolution of various defensive mechanisms in plants, which can be classified into (i) resistance traits that reduce the amount of damage received, including physical, chemical, and biotic traits; (ii) tolerance mechanisms that decrease the impact of herbivore damage, and (iii) escape strategies that reduce the probability of plants to be found by herbivores. These strategies have been studied at different levels from molecular genetics and genomics, to chemistry and physiology, to community and ecosystem ecology. We summarized the development of the methodology for studying plant defenses against herbivores. Particularly, 24 of those hypotheses and models, which are influential in the international community concerning the relationship between plants and herbivores, including the defensive mimicry hypothesis, the compensatory continuum hypothesis, the slow-growth-high-mortality hypothesis, etc, were introduced and grouped into four categories according to plant defense strategies in the present review. Finally, we also reviewed the research progress of plant–herbivore interactions in China, and discussed the perspectives of studies on plant–herbivore interactions.     

Effects of invasive seaweeds on feeding preference and performance of a keystone Mediterranean herbivore

The consequences of invasive species on ecosystem processes and ecological interactions remain poorly understood. Predator–prey interactions are fundamental in shaping species evolution and community structure and can be strongly modified by species introductions. To fully understand the ecological effects of invasive species on trophic linkages it is important to characterize novel interactions between native predators and exotic prey and to identify the impacts of invasive species on the performance of native predators. Although seaweed invasions are a growing global concern, our understanding of invasive algae—herbivore interactions is still very limited. We used a series of feeding experiments between a native herbivore and four invasive algae in the Mediterranean Sea to examine the potential of native sea urchins to consume invasive seaweeds and the impacts of invasive seaweed on herbivore performance. We found that three of the four invasive species examined are avoided by native herbivores, and that feeding behaviour in sea urchins is not driven by plant nutritional quality. On the other hand, Caulerpa racemosa is readily consumed by sea urchins, but may escape enemy control by reducing their performance. Recognizing the negative impacts of C. racemosa on herbivore performance has highlighted an enemy escape mechanism that contributes to explaining how this widespread invasive alga, which is preferred and consumed by herbivores, is not eradicated by grazing in the field. Furthermore, given the ecological and economic importance of sea urchins, negative impacts of invasive seaweeds on their performance could have dramatic effects on ecosystem function and services, and should be accounted for in sea urchin population management strategies.     

Galactolipids rather than phlorotannins as herbivore deterrents in the brown seaweed<Emphasis Type="Italic"> Fucus vesiculosus</Emphasis>

The first investigation of seaweed chemical defense against herbivores involved the brown seaweed Fucus vesiculosus and suggested defense via phlorotannins. The first demonstration of seaweed induction of secondary metabolites in response to herbivory also involved the genus Fucus and assumed a defensive function for phlorotannins. Many other investigations correlate herbivore feeding preference with changing levels of phlorotannins in this genus and others, but few directly test the effects of phlorotannins. No studies have assessed Fucus chemical defenses using bioassay-guided separation to investigate the complete complement of compounds deterring herbivores. We investigated the deterrence of F. vesiculosus chemical extracts using herbivore bioassays to guide our chemical investigations. Although crude extracts from F. vesiculosus strongly deterred feeding by the sea urchin Arbacia punctulata, phlorotannins from this extract did not deter feeding at 2x or 4x natural concentration by dry mass. Feeding deterrence was due to: (1) a polar galactolipid in the ethyl acetate-soluble extract, and (2) a non-phenolic compound, or compounds, in the water-soluble extract. Although this is the first evidence of galactolipids deterring herbivores, such defenses could be geographically and taxonomically widespread. The galactolipid we discovered in Fucus occurs in marine dinoflagellates, and a related metabolite that deters herbivory has recently been discovered in a tropical green seaweed. We were unable to identify the second deterrent compound, but deterrence occurred in a fraction containing carbohydrates, including sulfated sugars, but no phlorotannins. Given the polarity of these chemical deterrents, they could co-occur with and confound bioassays of phlorotannins if investigators test phlorotannin-containing algal extracts without further purification.     

Comparative analysis of quantitative trait loci controlling glucosinolates,myrosinase and insect resistance in Arabidopsis thaliana

Evolutionary interactions among insect herbivores and plant chemical defenses have generated systems where plant compounds have opposing fitness consequences for host plants, depending on attack by various insect herbivores. This interplay complicates understanding of fitness costs and benefits of plant chemical defenses. We are studying the role of the glucosinolate-myrosinase chemical defense system in protecting Arabidopsis thaliana from specialist and generalist insect herbivory. We used two Arabidopsis recombinant inbred populations in which we had previously mapped QTL controlling variation in the glucosinolate-myrosinase system. In this study we mapped QTL controlling resistance to specialist (Plutella xylostella) and generalist (Trichoplusia ni) herbivores. We identified a number of QTL that are specific to one herbivore or the other, as well as a single QTL that controls resistance to both insects. Comparison of QTL for herbivory, glucosinolates, and myrosinase showed that T. ni herbivory is strongly deterred by higher glucosinolate levels, faster breakdown rates, and specific chemical structures. In contrast, P. xylostella herbivory is uncorrelated with variation in the glucosinolate-myrosinase system. This agrees with evolutionary theory stating that specialist insects may overcome host plant chemical defenses, whereas generalists will be sensitive to these same defenses.     

Interactions of plant stress and herbivory: intraspecific variation in the susceptibility of a palatable versus an unpalatable seaweed to sea urchin grazing

Summary Interactions among environmental stresses, plant defensive characteristics, and plant nutrient status may significantly affect an alga's susceptibility to herbivores. Following desiccation, the palatable seaweed Gracilaria tikvahiae was less susceptible to grazing by the sea urchin Arbacia punctulata while the unpalatable alga Padina gymnospora became more susceptible. Increased grazing on desiccated Padina appeared to result from a loss of chemical defenses following desiccation. Palatable plants treated with organic extracts from desiccated Padina plants were consumed at more than twice the rate of plants treated with extracts from undesiccated plants. Increased susceptibility of Padina did not correlate with changes in protein content of the alga; reduced grazing on desiccated Gracilaria was associated with a decrease in protein content. When Padina was grazed by Arbacia or mechanically damaged to mimic urchin grazing, its susceptibility to Arbacia decreased within 1 to 5 days. These results demonstrate that history of physical or biological stress may affect a plant's susceptibility to herbivory. We hypothesize that urchins cue primarily on attractiveness features (e.g. nutrient content) of highpreference algae and deterrent features (e.g. chemical defenses) of low-preference algae. Stresses may therefore increase, decrease, or not affect a plant's susceptibility to herbivory depending upon the primary feeding cues used by the herbivore, the defensive mechanisms used by the plant, and the way these are altered by various environmental stresses.     

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.     

Seasonality of herbivory and communication between individuals of sagebrush

Seasonal changes in herbivore numbers and in plant defenses are well known to influence plant–herbivore interactions. Some plant defenses are induced in response to herbivore attack or cues correlated with risk of attack although seasonal variation in these defenses is relatively poorly known. We previously reported that sagebrush becomes more resistant to its herbivores when neighboring plants have been experimentally clipped with scissors. In this study we asked whether herbivory to leaves of sagebrush varied seasonally and whether there was seasonal variation in natural levels of damage when neighbors were clipped. We found that sagebrush accumulated most chewing damage early in the season, soon after the spring flush of new leaves. This damage was caused by generalist grasshoppers, deer, specialist caterpillars, beetles, gall makers, and other less common herbivores. Sagebrush showed no evidence of preferentially abscising leaves that had been experimentally clipped. Experimental clipping by Trirhabda pilosa beetle larvae caused neighbors to accumulate less herbivore damage later that season, similar to results in which clipping was done with scissors. Induced resistance caused by experimentally clipping a neighbor was affected by season; plants with neighbors clipped in May accumulated less damage throughout the season relative to plants with unclipped neighbors or neighbors clipped later in the summer. We found a correlation between seasonal herbivore pressure, damage accumulated by plants, and induced responses to experimentally clipping neighbors. The causal mechanisms responsible for this correlation are unknown although a strong seasonal effect was clear.     

POSITIVE FEEDBACK AND THE DEVELOPMENT AND PERSISTENCE OF ECOSYSTEM DISRUPTIVE ALGAL BLOOMS1

Harmful algal blooms (HABs) have occurred with increasing frequency in recent years with eutrophication and other anthropogenic alterations of coastal ecosystems. Many of these blooms severely alter or degrade ecosystem function, and are referred to here as ecosystem disruptive algal blooms (EDABs). These blooms are often caused by toxic or unpalatable species that decrease grazing rates by planktonic and benthic herbivores, and thereby disrupt the transfer of nutrients and energy to higher trophic levels, and decrease nutrient recycling. Many factors, such as nutrient availability and herbivore grazing have been proposed to separately influence EDAB dynamics, but interactions among these factors have rarely been considered. Here we discuss positive feedback interactions among nutrient availability, herbivore grazing, and nutrient regeneration, which have the potential to substantially influence the dynamics of EDAB events. The positive feedbacks result from a reduction of grazing rates on EDAB species caused by toxicity or unpalatability of these algae, which promotes the proliferation of the EDAB species. The decreased rates also lower grazer‐mediated recycling of nutrients and thereby decrease nutrient availability. Since many EDAB species are well‐adapted to nutrient‐stressed environments and many exhibit increased toxin production and toxicity under nutrient limitation, positive feedbacks are established which can greatly increase the rate of bloom development and the adverse effects on the ecosystem. An understanding of how these feedbacks interact with other regulating factors, such as benthic/pelagic nutrient coupling, physical forcing, and life cycles of EDAB species provides a substantial future challenge.     

Latitudinal variation in resistance and tolerance to herbivory of a salt marsh shrub

Interactions between plants and herbivores often vary on a geographic scale. Although theory about plant defenses and tolerance is predicated on temporal or spatial variation in herbivore damage, no single study has compared the pattern of herbivory, plant defenses and tolerance to herbivory of a single species across a latitudinal gradient. In 2002–2005 we surveyed replicate salt marshes along the Atlantic coast of the United States from Florida to Maine. At each field site we scored leaves of Iva frutescens for herbivore damage. In laboratory experiments we measured constitutive resistance and induced resistance in I. frutescens from high and low latitude sites along the Atlantic Coast. In another common garden experiment we studied tolerance to herbivory of I. frutescens from various sites. Theory predicts that constitutive resistance should matter more when damage is high, and induced resistance when herbivory is high but variable. In the field, average levels of herbivore damage, and spatial and temporal variation in herbivore damage were all greater at low versus high latitudes, indicating that constitutive as well as induced resistance should be stronger at low latitudes. Consistent with this prediction, constitutive resistance to herbivory was stronger at low latitudes. Induced resistance to herbivores was also stronger at low latitudes: it was deployed faster and lasted longer. Theory also predicts that tolerance to herbivory should be greater where average herbivory damage is greater; however, tolerance to herbivory in Iva did not depend on geographic origin. Our results emphasize the value of considering multiple ways in which plants respond to herbivores when examining geographic variation in plant–herbivore interactions.