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.     

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.     

Consequences of sequential attack for resistance to herbivores when plants have specific induced responses

Plants in nature are attacked sequentially by herbivores, and theory predicts that herbivore-specific responses allow plants to tailor their defenses. We present a novel field test of this hypothesis, and find that specific responses of Solanum dulcamara lead to season-long consequences for two naturally colonizing herbivores, irrespective of the second herbivore to attack plants. This result indicates that responses induced by the initial herbivore made plants less responsive to subsequent attack. We show that initial herbivory by flea beetles and tortoise beetles induce distinct plant chemical responses. Initial herbivory by flea beetles lowered the occurrence of conspecifics and tortoise beetles relative to controls. Conversely, initial herbivory by tortoise beetles did not influence future herbivory. Remarkably, the experimentally imposed second herbivore to feed on plants did not modify consequences (induced resistance or lack thereof) of the first attacker. Induction of plant chemical responses was consistent with these ecological effects; i.e. the second herbivore did not modify the plant's initial induced response. Thus, canalization of the plant resistance phenotype may constrain defensive responses in a rapidly changing environment.     

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.     

Costs of induced defenses for the invasive plant houndstongue (<Emphasis Type="Italic">Cynoglossum officinale</Emphasis> L.) and the potential importance for weed biocontrol

Inducible plant defenses—those produced in response to herbivore feeding—are thought to have evolved as a cost-saving tactic that allows plants to enact defenses only when needed. The costs of defense can be significant, and loss of plant fitness due to commitment of resources to induced defenses could affect plant populations and play a role in determining the success or failure of weed biocontrol. We used methyl jasmonate (MeJA) to experimentally induce defenses without herbivores in invasive houndstongue plants (Cynoglossum officinale L.) in the field and measured resulting growth and fitness (plant size, seed number, and seed weight). MeJA-treated plants emitted large amounts of plant volatiles and produced leaves with twice as many trichomes as untreated plants. Plants with activated defenses had fewer leaves, were smaller, and produced nutlets that weighed less than plants not investing in defenses. These data indicate that herbivore-induced defenses are costly for houndstongue plants in their invaded range and represent significant indirect costs of herbivory beyond direct feeding damage (e.g., loss of photosynthetic tissue). Notably, the magnitude of defenses elicited upon feeding varies greatly by herbivore species and a better understanding of the costs of defense could help us predict which potential biocontrol herbivores are most likely to be effective.     

Are Defenses of Wild Radish Populations Well Matched with Variability and Predictablity of Herbivory?

Theory predicts that plants should employ constitutive (fixed) defenses when herbivory is consistently strong among years and induced (plastic) defenses when herbivory varies among years but is predictable within a season. We tested this theory by examining the herbivore species and damage censused over three seasons for 20 populations of wild radish in northern California. We conducted assays of constitutive resistance by challenging undamaged plants from these 20 populations with their common herbivores in the greenhouse. We assayed induced resistance by comparing the performance of herbivores on plants that had been experimentally damaged to undamaged plants from the same populations. Following damage, plants generally became more resistant to chewing herbivores (caterpillars) but more susceptible to sucking herbivores (aphids). Constitutive resistance to caterpillars was not stronger for populations that had high levels of herbivory that varied little among years, contrary to theory. Induced resistance may be stronger for plants from populations where herbivory varied more among years, consistent with expectations, although low power makes this conclusion equivocal. Induced resistance was not stronger for populations where early herbivory was a good predictor of late season herbivory. This lack of support for theory could have been caused by inadequacies with the experimental tests or with the theory and its assumptions. The theory assumes a coevolutionary equilibrium; however, high gene flow that has been reported for wild radish could disrupt matches between risk of herbivory and plant defense. The theory also assumes that resistance traits evolved as defenses against herbivory although these traits also serve other functions. Finally, the correlation we measured between early and late season herbivory may be at a temporal scale that is irrelevant since wild radish appears to adjust its defenses very rapidly.     

Local adaptation: simultaneously considering herbivores and their host plants

? Although a major expectation of coevolutionary theory between plants and herbivores is the occurrence of reciprocal local adaptation, this has remained almost untested. Thus, we evaluated the presence and variation in the patterns of reciprocal local adaptation between an herbivorous insect and its host plant. ? Two four-by-four cross-infestation experiments were performed under similar abiotic conditions. The first one was done under laboratory conditions to estimate herbivore individual performance while the second one was performed in a common garden to simultaneously estimate herbivore population growth rate as well as seed production and plant defenses (resistance and tolerance to herbivory). ? The patterns of population differentiation for the herbivore and the plant were not independent of each other, showing all the possible outcomes from locally adapted to maladapted populations. These results indicate differences in the magnitude of local adaptation. While an association between resistance and herbivore performance was observed, there was no clear pattern between tolerance and herbivore local adaptation. ? Our results demonstrated the occurrence of reciprocal local adaptation following the pattern expected by theory: when the herbivores or the plants were adapted, the other species was non-adapted or even maladapted.     

Can plant–natural enemy communication withstand disruption by biotic and abiotic factors?

相似文献   

Natural and artificial floral damage induces resistance in Nemophila menziesii (Hydrophyllaceae) flowers

Resistance to leaf herbivory is well-documented in plants. In contrast, resistance to herbivory in flowers has received very little attention, even though reproductive tissues are often essential for plant reproduction. Plants may protect reproductive tissues with a range of defenses from constitutive to induced, although ecological costs associated with constitutive defense or resistance are expected to be higher than costs associated with induced responses. Induced responses in flowers may be effective against floral herbivores while minimizing the negative impacts of resistance on pollinators. This study examines induced responses in Nemophila menziesii (Hydrophyllaceae), a plant that frequently receives high levels of floral herbivory. I report that natural caterpillar herbivory increased levels of resistance against caterpillars later in the season. Similarly, artificial clipping to flowers consistently reduced natural damage to flowers vs unclipped controls over two years. Neither whole-plant nor individual seed set was affected by the reduction of floral damage. Induced resistance in reproductive tissues may benefit plants that are exposed to both floral herbivory and pollinator activity and can be an important link between plant antagonists and plant mutualists.     

No evolution of reduced resistance and compensation for psyllid herbivory by the invasive <Emphasis Type="Italic">Genista monspessulana</Emphasis>

The evolution of redirecting resources from plant defense to growth or reproduction may explain why some exotic species are successful invaders in new environments. For example, the evolution of increased competitive ability hypothesis posits that escape from herbivores by invasive plants results in the selection of more vigorous genotypes that reduce their allocation of resources to defense. In addition, understanding the defense strategy of an invasive plant may help forecast the likely impact of herbivory. We tested the prediction of reduced defense (i.e., resistance) in Genista monspessulana, measured indirectly as the performance of a specialist psyllid herbivore, by comparing five native and introduced plant populations. We also examined the ability of G. monspessulana to compensate for herbivory in the presence and the absence of psyllids for a single plant population from the native and introduced regions. Plant origin (native or introduced) did not influence the psyllid’s abundance and population growth rate, suggesting no change in resistance to herbivory for introduced plants. Similarly, we found no overall difference in plant performance between individuals in the presence and the absence of psyllid herbivory, suggesting that G. monspessulana was able to fully compensate for herbivory. Damaged plants compensated by changing the pattern of branching, which also resulted in greater dry leaf biomass. We conclude that evolution of reduced defenses does not explain the success of G. monspessulana as an invader and that compensation for herbivory may limit the efficacy of the psyllid as a biological control agent.     

Transgenerational effects alter plant defence and resistance in nature

Trichomes, or leaf hairs, are epidermal extensions that take a variety of forms and perform many functions in plants, including herbivore defence. In this study, I document genetically determined variation, within‐generation plasticity, and a direct role of trichomes in herbivore defence for Mimulus guttatus. After establishing the relationship between trichomes and herbivory, I test for transgenerational effects of wounding on trichome density and herbivore resistance. Patterns of interannual variation in herbivore density and the high cost of plant defence makes plant–herbivore interactions a system in which transgenerational phenotypic plasticity (TPP) is apt to evolve. Here, I demonstrate that parental damage alters offspring trichome density and herbivore resistance in nature. Moreover, this response varies between populations. This is among the first studies to demonstrate that TPP contributes to variation in nature, and also suggests that selection can modify TPP in response to local conditions.     

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.     

Ecological and Evolutionary Interactions between Wild Crucifers and Their Herbivorous Insects

Abstract Insects feeding on ten species of wild crucifer were investigated. Differences in host plant range and insect community structure were examined with regard to anti-herbivore defense mechanisms. Most of the crucifer species deterred insect herbivory by disappearing in the summer or by lowering their intrinsic quality as food for insects. Species with these defense mechanisms were exploited by only a few specialized herbivorous insects that seemed to have counter defenses. The plants without these defense mechanisms were used by many herbivorous insect species. Rorippa indica lacked direct defenses, but supported a low total density of herbivore individuals. This crucifer has an indirect defense mechanism: ants attracted to floral nectar defended the plant from deleterious herbivores. Crucifers that disappeared seasonally lacked other anti-herbivore defense mechanisms. This suggests that the phonological response is an alternative other responses to herbivore attack.     

Variation in insect herbivory across a salt marsh tidal gradient influences plant survival and distribution

Herbivore damage and impact on plants often varies spatially across environmental gradients. Although such variation has been hypothesized to influence plant distribution, few quantitative evaluations exist. In this study I evaluated patterns of insect herbivory on an annual forb, Atriplex patula var. hastata, across a salt marsh tidal gradient, and performed experiments to examine potential causes and consequences of variation in herbivory. Damage to plants was generally twice as great at mid-tidal elevations, which are more frequently inundated, than at higher, less stressful, elevations at five of six surveyed sites. Field herbivore assays and herbivore preference experiments eliminated the hypothesis that plant damage was mediated by herbivore response to differences in host plants across the gradient. Alternately, greater herbivore densities in the mid-marsh, where densities of an alternate host plant (Salicornia europaea) were high, were associated with greater levels of herbivory on Atriplex, suggesting spillover effects. The effect of insect herbivores on host plant performance varied between the two sites studied more intensively. Where overall herbivore damage to plants was low, herbivory had no detectable effect on plant survival or seed production, and plant performance did not significantly differ between zones. However, where herbivore damage was high, herbivores dramatically reduced both plant survival (>50%) and fruit production (40-70%), and their effects were stronger in the harsher mid-marsh than the high marsh. Thus herbivores likely play a role in maintaining lower Atriplex densities in mid-marsh. Overall, these results suggest that variation in herbivore pressure can be an important determinant of patterns of plant abundance across environmental gradients.     

Urbanization alters plastic responses in the common dandelion Taraxacum officinale

Urban environments expose species to contrasting selection pressures relative to rural areas due to altered microclimatic conditions, habitat fragmentation, and changes in species interactions. To improve our understanding on how urbanization impacts selection through biotic interactions, we assessed differences in plant defense and tolerance, dispersal, and flowering phenology of a common plant species (Taraxacum officinale) along an urbanization gradient and their reaction norms in response to a biotic stressor (i.e., herbivory). We raised plants from 45 lines collected along an urbanization gradient under common garden conditions and assessed the impact of herbivory on plant growth (i.e., aboveground biomass), dispersal capacity (i.e., seed morphology), and plant phenology (i.e., early seed production) by exposing half of our plants to two events of herbivory (i.e., grazing by locusts). Independent from their genetic background, all plants consistently increased their resistance to herbivores by which the second exposure to locusts resulted in lower levels of damage suffered. Herbivory had consistent effects on seed pappus length, with seeds showing a longer pappus (and, hence, increased dispersal capacities) regardless of urbanization level. Aboveground plant biomass was neither affected by urbanization nor herbivore presence. In contrast to consistent responses in plant defenses and pappus length, plant fitness did vary between lines. Urban lines had a reduced early seed production following herbivory while rural and suburban lines did not show any plastic response. Our results show that herbivory affects plant phenotypes but more importantly that differences in herbivory reaction norms exist between urban and rural populations.     

How do two specialist butterflies determine growth and biomass of a shared host plant?

Although insect herbivory can modify subsequent quantity and quality of their host plants, change in plant quantity following herbivory has received less attention than plant quality. In particular, little is known about how previous herbivore damage determines plant growth and biomass in an insect species-specific manner. We explored whether herbivore species-specific food demand influences plant growth and biomass. To do this, we conducted a series of experiments and field survey using two specialist butterflies, Sericinus montela and Atrophaneura alcinous, and their host plant, Aristolochia debilis. It is known that A. alcinous larva requires four times more food resources to fulfill its development than S. montela larva. Despite that A. alcinous larvae imposed greater damage on plants than S. montela larvae, plant growth did not differ due to herbivory by these species both in single and multiple herbivory events. On the other hand, total aboveground biomass of the plants was reduced more by A. alcinous than S. montela feeding regardless of the number of herbivory events. Feeding on plants with a history of previous herbivory neither decreased nor increased larval growth. Our results suggest that food demand of the two butterfly species determined subsequent plant biomass, although the plant response may depend on tolerance of the host plant (i.e., ability to compensate for herbivore damage). Such difference in the effects of different herbivore species on host plant biomass is more likely to occur than previously thought, because food demand differs in most herbivore species sharing a host plant.     

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.     

High elevation Plantago lanceolata plants are less resistant to herbivory than their low elevation conspecifics: is it just temperature?

Traits that mediate species interactions are evolutionarily shaped by biotic and abiotic drivers, yet we know relatively little about the relative importance of these factors. Herbivore pressure, along with resource availability and ‘third‐party’ mutualists, are hypothesized to play a major role in the evolution of plant defence traits. Here, we used the model system Plantago lanceolata, which grows along steep elevation gradients in the Swiss Alps, to investigate the effect of elevation, herbivore pressure, mycorrhizal inoculation and temperature on plant resistance. Over a 1200 m elevation gradient, the levels of herbivory and iridoid glycosides (IGs) declined with increasing elevation. By planting seedlings at three different elevations, we further showed that both low‐elevation growing conditions and mycorrhizal inoculation resulted in increased plant resistance to herbivores. Finally, using a temperature‐controlled experiment comparing high‐ and low‐elevation ecotypes, we showed that high‐elevation ecotypes are less resistant to herbivory, and that lower temperatures impair IGs deployment after herbivore attack. We thus propose that both lower herbivore pressure, and colder temperatures relax the defense syndrome of high elevation plants.     

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.     

Herbivore-specific plant volatiles prime neighboring plants for nonspecific defense responses

Plants produce species-specific herbivore-induced plant volatiles (HIPVs) after damage. We tested the hypothesis that herbivore-specific HIPVs prime neighboring plants to induce defenses specific to the priming herbivore. Since Manduca sexta (specialist) and Heliothis virescens (generalist) herbivory induced unique HIPV profiles in Nicotiana benthamiana, we used these HIPVs to prime receiver plants for defense responses to simulated herbivory (mechanical wounding and herbivore regurgitant application). Jasmonic acid (JA) accumulations and emitted volatile profiles were monitored as representative defense responses since JA is the major plant hormone involved in wound and defense signaling and HIPVs have been implicated as signals in tritrophic interactions. Herbivore species-specific HIPVs primed neighboring plants, which produced 2 to 4 times more volatiles and JA after simulated herbivory when compared to similarly treated constitutive volatile-exposed plants. However, HIPV-exposed plants accumulated similar amounts of volatiles and JA independent of the combination of priming or challenging herbivore. Furthermore, volatile profiles emitted by primed plants depended only on the challenging herbivore species but not on the species-specific HIPV profile of damaged emitter plants. This suggests that feeding by either herbivore species primed neighboring plants for increased HIPV emissions specific to the subsequently attacking herbivore and is probably controlled by JA.