Comparing the consequences of induced and constitutive plant resistance for herbivore population dynamics

Although it has been suggested that induced and constitutive plant resistance should have different effects on insect herbivore population dynamics, there is little experimental evidence that plant resistance can influence herbivore populations longer than one season. We used a density-manipulation experiment and model fitting to examine the effects of constitutive and induced resistance on herbivore dynamics over both the short and long term. We used likelihood methods to fit population dynamic models to recruitment data for populations of Mexican bean beetles on soybean varieties with no resistance, constitutive resistance, or induced resistance. We compared model configurations that fit parameters for resistance types separately to models that did not account for resistance type. Models representing the hypothesis that the three resistance types differed in their effects on beetle dynamics received the most support. Induced resistance resulted in lower population growth rates and stronger density dependence than no resistance. Constitutive resistance resulted in lower population growth rates and stronger density dependence than induced resistance. Constitutive resistance had a stronger effect on both short-term beetle recruitment and predicted beetle population dynamics than induced resistance. The results of this study suggest that induced and constitutive resistance can differ in their effects on herbivore populations even in a relatively complex system.     

Simultaneous effects of food limitation and inducible resistance on herbivore population dynamics

Many herbivore populations fluctuate temporally, but the causes of those fluctuations remain unclear. Plant inducible resistance can theoretically cause herbivore population fluctuations, because herbivory may induce plant changes that reduce the survival or reproduction of later-feeding herbivores. Herbivory can also simply reduce the quantity of food available for later feeders and this, too, can cause population fluctuations. Inducible resistance and food limitation often occur simultaneously, yet whether they jointly facilitate or suppress herbivore fluctuations remains largely unexplored. We present models that suggest that food limitation and inducible resistance may have synergistic effects on herbivore population dynamics. The population-level response of the food plant to herbivory and the details of how inducible resistance affects herbivore performance both influence the resulting herbivore dynamics. Our results identify some biological properties of plant-herbivore systems that might determine whether or not cycles occur, and suggest that future empirical and theoretical population dynamics studies should account for the effects of both food limitation and inducible resistance.     

Drought stress affects constitutive but not induced herbivore resistance in apple plants

Plant–herbivore interactions are influenced by chemical plant traits, which can vary depending on the plants’ abiotic and biotic environment. Drought events, which are predicted to become more frequent and prolonged due to climate change, may affect primary and secondary plant metabolites contributing to constitutive resistance. Furthermore, the ability of plants to respond to herbivore attack in terms of induced resistance may be altered under drought conditions. We assessed the effects of drought stress on constitutive and induced apple plant resistance to a generalist insect herbivore by quantifying plant and herbivore responses in concert. Plants were exposed to different drought stress intensities (constitutive resistance) and subsequently to herbivore damage treatments that included different damage durations (induced resistance). As drought stress intensified, plant growth and concentrations of the leaf phenolic phloridzin decreased, whereas leaf glucose concentrations increased. Changes in fructose concentrations and in herbivore feeding preferences indicated a non-monotonic shift in constitutive resistance. Moderately stressed plants showed reduced fructose concentrations and were consumed least, while severely stressed plants were fructose-enriched and consumed most compared to well-watered control plants showing intermediate fructose concentrations and palatability. We found no evidence for effects of drought stress on induced resistance, as herbivore feeding preferences for undamaged over damaged plants were independent of drought intensity. Our results suggest a strong role of primary metabolites for drought-dependent variation in constitutive plant resistance and offer novel experimental insights into the effects of drought stress on induced plant resistance across a gradient of water deprivation.     

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.     

The ecology and evolution of induced responses to herbivory and how plants perceive risk

1. Plants perceive herbivore damage or increased risk and respond. These changes may increase plant fitness, although effects on fitness have often been assumed without supporting evidence. 2. Three models have been proposed to explain induced rather than constitutive defence. The optimal defence model posits that induction allow plants to reduce allocation costs; it predicts demonstrably lower costs when defences are not needed. The moving target model posits that induction increases spatial and temporal variability; it predicts that variability will be difficult for herbivores and will provide defence. The information transfer model posits that induced responses provide cues to other tissues on that individual plant and to other organisms in the community; it predicts that induced cues will provide systemic resistance, deter herbivores, and/or attract enemies of herbivores, thereby benefiting the induced plant. 3. All three models predict that cues must be reliable to be useful. In some cases, cues provide specific information about the damaged plant tissue and the herbivore and this specific information may allow plants to fine-tune responses. Recent theory posits that selection should favour plants that minimise recognition errors and reduce fitness costs associated with errors. 4. Future research should focus on exploring different modalities used by plants to perceive herbivore risk, the benefits and costs of perceiving cues and inducing resistance, and the basic natural history of these phenomena. Induced responses have great unrealised potential in agriculture, and research should focus on host plant resistance rather than attempting to involve other trophic levels.     

When can herbivores slow or reverse the spread of an invading plant? A test case from Mount St. Helens

Here we study the spatial dynamics of a coinvading consumer-resource pair. We present a theoretical treatment with extensive empirical data from a long-studied field system in which native herbivorous insects attack a population of lupine plants recolonizing a primary successional landscape created by the 1980 volcanic eruption of Mount St. Helens. Using detailed data on the life history and interaction strengths of the lupine and one of its herbivores, we develop a system of integrodifference equations to study plant-herbivore invasion dynamics. Our analyses yield several new insights into the spatial dynamics of coinvasions. In particular, we demonstrate that aspects of plant population growth and the intensity of herbivory under low-density conditions can determine whether the plant population spreads across a landscape or is prevented from doing so by the herbivore. In addition, we characterize the existence of threshold levels of spatial extent and/or temporal advantage for the plant that together define critical values of "invasion momentum," beyond which herbivores are unable to reverse a plant invasion. We conclude by discussing the implications of our findings for successional dynamics and the use of biological control agents to limit the spread of pest species.     

A flow network model for animal movement on a landscape with application to invasion

Animal movement, whether for foraging, mate-seeking, predator avoidance, dispersal, or migration, is a fundamental aspect of ecology that shapes spatial abundance distributions, genetic compositions, and dynamics of populations. A variety of movement models have been used for predicting the effects of natural or human-caused landscape changes, invading species, or other disturbances on local ecology. Here we introduce the flow network—a general modeling framework for population dynamics and movement in a metapopulation representing a network of habitat sites (nodes). Based on the principles of physical transport phenomena such as fluid flow through pipes (Pouiselle’s Law) and analogously, the flow of electric current across a circuit (Ohm’s Law), the flow network provides a novel way of modeling movement, where flow rates are functions of relative node pressures and the resistance to movement between them. Flow networks offer the flexibility of incorporating abiotic and biotic conditions that affect either pressures, resistance, or both. To illustrate an application of the flow network, we present a theoretical invasion scenario. We consider the effects of spatial structure on the speed of invasion by varying the spatial regularity of node arrangement. In the context of invasion, we model management actions targeting nodes or edges, and consider the effects on speed of invasion, node occupation, and total abundance. The flow network approach offers the flexibility to incorporate spatial heterogeneity in both rates of flow and site pressures and offers an intuitive approach to connecting population dynamics and landscape features to model movement.     

Mammalian Herbivores Alter the Population Growth and Spatial Establishment of an Early-Establishing Grassland Species

Plant-herbivore interactions influence the establishment context of plant species, as herbivores alter the community context in which individual species establish, and the spatial relationship between individuals and their source population as plants invade. This relationship can be described using an establishment kernel, which takes into account movement through seed dispersal, and subsequent establishment of adults. Mammalian herbivores are hypothesized to influence plant population growth and establishment through a combination of consumption of seeds and seedlings, and movement of seeds. While the movement abilities of plants are well known, we have very few empirical mechanistic tests of how biotic factors like mammalian herbivores influence this spread potential. As herbivores of all sizes are abundant on the landscape, we asked the question, how do mammalian herbivores influence the population growth, spatial establishment, and the community establishment context of an early-recruiting native prairie legume, Chamaecrista fasciculata? We planted C. fasciculata in source populations within a four-acre tallgrass prairie restoration in plots with and without herbivores, and monitored its establishment with respect to distance from the source populations. We found that herbivores decreased population growth, and decreased the mean and range establishment distance. Additionally, C. fasciculata established more often without herbivores, and when surrounded by weedy, annual species. Our results provide insight into how the interactions between plants and herbivores can alter the spatial dynamics of developing plant communities, which is vital for colonization and range spread with fragmentation and climate change. Mammalian herbivores have the potential to both slow rates of establishment, but also determine the types of plant communities that surround invading species. Therefore, it is essential to consider the herbivore community when attempting to restore functioning plant communities.     

Local adaptation,dispersal evolution,and the spatial eco‐evolutionary dynamics of invasion

Local adaptation and dispersal evolution are key evolutionary processes shaping the invasion dynamics of populations colonizing new environments. Yet their interaction is largely unresolved. Using a single‐species population model along a one‐dimensional environmental gradient, we show how local competition and dispersal jointly shape the eco‐evolutionary dynamics and speed of invasion. From a focal introduction site, the generic pattern predicted by our model features a temporal transition from wave‐like to pulsed invasion. Each regime is driven primarily by local adaptation, while the transition is caused by eco‐evolutionary feedbacks mediated by dispersal. The interaction range and cost of dispersal arise as key factors of the duration and speed of each phase. Our results demonstrate that spatial eco‐evolutionary feedbacks along environmental gradients can drive strong temporal variation in the rate and structure of population spread, and must be considered to better understand and forecast invasion rates and range dynamics.     

Trophic Interactions during Primary Succession: Herbivores Slow a Plant Reinvasion at Mount St. Helens

Lupines (Lupinus lepidus var. lobbii), the earliest plant colonists of primary successional habitats at Mount St. Helens, were expected to strongly affect successional trajectories through facilitative effects. However, their effects remain localized because initially high rates of reinvasive spread were short lived, despite widespread habitat availability. We experimentally tested whether insect herbivores, by reducing plant growth and fecundity at the edge of the expanding lupine population, could curtail the rate of reinvasion and whether those herbivores had comparable impacts in the older, more successionally advanced core region. We found that removing insect herbivores increased both the areal growth of individual lupine plants and the production of new plants in the edge region, thereby accelerating the lupine's intrinsic rate of increase at the front of the lupine reinvasion. We found no such impacts of herbivory in the core region, where low plant quality or a complex of recently arrived natural enemies may hold herbivores in check. In the context of invasion theory, herbivore-mediated decreases in lupine population growth rate in the edge region translate into decreased rates of lupine spread, which we quantify here using diffusion models. In the Mount St. Helens system, decreased rate of lupine reinvasion will result in reductions in rates of soil formation, nitrogen input, and entrapment of seeds and detritus that are likely to postpone or alter trajectories of primary succession. If the type of spatial subtleties in herbivore effects we found here are common, with herbivory focused on the edge of an expanding plant population and suppressed or ineffective in the larger, denser central region (where the plants might be more readily noticed and studied), then insect herbivores may have stronger impacts on the dynamics of primary succession and plant invasions than previously recognized.     

Resource-dependent dispersal and the speed of biological invasions

Many mobile organisms exhibit resource-dependent movement in which movement rates adjust to changes in local resource densities through changes in either the probability of moving or the distance moved. Such changes may have important consequences for invasions because reductions in resources behind an invasion front may cause higher dispersal while simultaneously reducing population growth behind the front and thus lowering the number of dispersers. Intuiting how the interplay between population growth and dispersal affects invasions is difficult without mathematical models, yet most models assume dispersal rates are constant. Here we present spatial-spread models that allow for consumer-resource interactions and resource-dependent dispersal. Our results show that when resources affect the probability of dispersal, then the invasion dynamics are no different than if resources did not affect dispersal. When resources instead affect the distance dispersed, however, the invasion dynamics are strongly affected by the strength of the consumer-resource interaction, and population cycles behind the wave front lead to fluctuating rates of spread. Our results suggest that for actively dispersing invaders, invasion dynamics can be determined by species interactions. More practically, our work suggests that reducing invader densities behind the front may be a useful method of slowing an invader's rate of spread.     

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.     

Effects of grazing on above-ground biomass on a mountain snowbed, NW Finland

The density-dependent effect of induced plant resistance on herbivore populations depends on the relationship between the amount of herbivore damage and the level of induced resistance produced by the plant. This relationship should influence the interaction of induced resistance and herbivore population dynamics, and if the relationship varies among plant genotypes, it could be subject to natural selection by herbivores. In this study the relationship between percent leaf area damaged and level of induced resistance was characterized for four genotypes of soybeans grown in a greenhouse. Damage ranging from 8 to 92% of leaf area was imposed using Mexican bean beetle larvae, and induced resistance was measured by bioassay using Mexican bean beetle adults. The level of induced resistance was significantly affected by the amount of damage, and the level of induced resistance varied significantly among the four genotypes. There was also a marginally significant interaction of damage and plant genotype, suggesting that the form of density dependence varies among these four genotypes of soybeans. These results suggest that these genotypes of plants might affect herbivore populations differently. If this variation is heritable, the form of density-dependent effects of induced resistance has the potential to evolve in this system.     

Population spread in patchy landscapes under a strong Allee effect

Many species of invasive insects establish and spread in regions around the world, causing enormous economical and environmental damage, in particular in forests. Some of these insects are subject to an Allee effect whereby the population must surpass a certain threshold in order to establish. Recent studies have examined the possibility of exploiting an Allee effect to improve existing control strategies. Forests and most other ecosystems show natural spatial variation, and human activities frequently increase the degree of spatial heterogeneity. It is therefore imperative to understand how the interplay between this spatial variation and individual movement behavior affects the overall speed of spread of an invasion. To this end, we study an integrodifference equation model in a patchy landscape and with Allee growth dynamics. Movement behavior of individuals varies according to landscape quality. Our study focuses on how the speed of the resulting traveling periodic wave depends on the interaction between landscape fragmentation, patch-dependent dispersal, and Allee population dynamics.     

Herbivore-induced resistance in Betula pendula: the role of plant vascular architecture

We studied the role of plant vascular architecture in the determination of the spatial extent of herbivore induced responses within Betula pendula Roth saplings. The induced responses were measured in bioassays in terms of the relative growth rate of larvae of a geometrid moth, Epirrita autumnata. We hypothesised that the level of induced resistance of a certain leaf would be determined by the degree of vascular connectivity between the leaf in question and a damaged leaf, as suggested by recent theoretical and empirical studies. A comparison of the control plants with the damaged plants indicated that damaging one leaf of a sapling was sufficient to induce an increase in the resistance level. There were also differences among the leaves within a plant in the resistance level, but these differences could not be explained by the degree of vascular connectivity with the damaged leaf. These results suggest that the vascular connections have low power as explanations of the spread and spatial extent of the induced resistance in Betula pendula saplings Instead, the resistance level of all leaves within a sapling increased following the damage. We suggest that the pattern of increased resistance observed in this experiment may be beneficial for the young saplings studied. For young saplings at their early stages of development, it may be beneficial to be able to distribute the induction signal to all leaves as fast as possible and thus repel the herbivore totally. For a young sapling, the capability of repelling the herbivore totally might thus be a feasible strategy whereas an older sapling may tolerate localised damage better and compensate for the damage within the undamaged plant parts.     

Variation in plant quality and the population dynamics of herbivores: there is nothing average about aphids

In the attempt to use results from small-scale studies to make large-scale predictions, it is critical that we take into account the greater spatial heterogeneity encountered at larger spatial scales. An important component of this heterogeneity is variation in plant quality, which can have a profound influence on herbivore population dynamics. This influence is particularly relevant when we consider that the strength of density dependence can vary among host plants and that the strength of density dependence determines the difference between exponential and density- dependent growth. Here, we present some simple models and analyses designed to examine the impact of variable plant quality on the dynamics of insect herbivore populations, and specifically the consequences of variation in the strength of density dependence among host plants. We show that average values of herbivore population growth parameters, calculated from plants that vary in quality, do not predict overall population growth. Furthermore, we illustrate that the quality of a few individual plants within a larger plant population can dominate herbivore population growth. Our results demonstrate that ignoring spatial heterogeneity that exists in herbivore population growth on plants that differ in quality can lead to a misunderstanding of the mechanisms that underlie population dynamics.     

Damage-induced changes in woody plants and their effects on insect herbivore performance: a meta-analysis

We conducted a meta‐analysis of 68 studies published between 1982 and 2000 in which the responses of woody plants to natural or simulated herbivore damage and/or insect herbivore performance on control and damaged plants were measured. Cumulative meta‐analyses revealed dramatic temporal changes in the magnitude and direction of the plant and herbivore responses reported during the last two decades. Studies conducted in the 1980s reported increase in phenolic concentrations, reduction in nutrient concentrations and negative effect on herbivore performance, consistently with the idea of induced resistance. In contrast, in the early 1990s when the idea that some types of plant damage may result in induced susceptibility was generally accepted, studies reported non‐significant results or induced susceptibility, and smaller effects on herbivores. The above changes may reflect paradigm shifts in the theory of induced defenses and/or the differences between study systems used in the early and the more recent studies. Overall, plant growth and carbohydrate concentrations were reduced in damaged plants despite enhanced photosynthetic rates. Damage increased the concentrations of carbon and phenolics, while terpene concentrations tended to decrease after damage; changes in nutrient concentrations after damage varied according to nutrient mobility, inherent plant growth rate, ontogenetic stage and plant type (deciduous/evergreen). Early season damage caused more pronounced changes in plants than late season damage, which is in accordance with the assumption that vigorously growing foliage has a greater capacity to respond to damage. Insect growth rate and female pupal weight decreased on previously damaged plants, while herbivore survival, consumption and male pupal weight were not significantly affected. The magnitude and direction of herbivore responses depended on the type of plant, the type of damage, the time interval between the damage and insect feeding (rapid/delayed induced resistance), and the timing of the damage.     

A fully coupled, mechanistic model for infectious disease dynamics in a metapopulation: movement and epidemic duration

The drive to understand the invasion, spread and fade out of infectious disease in structured populations has produced a variety of mathematical models for pathogen dynamics in metapopulations. Very rarely are these models fully coupled, by which we mean that the spread of an infection within a subpopulation affects the transmission between subpopulations and vice versa. It is also rare that these models are accessible to biologists, in the sense that all parameters have a clear biological meaning and the biological assumptions are explained. Here we present an accessible model that is fully coupled without being an individual-based model. We use the model to show that the duration of an epidemic has a highly non-linear relationship with the movement rate between subpopulations, with a peak in epidemic duration appearing at small movement rates and a global maximum at large movement rates. Intuitively, the first peak is due to asynchrony in the dynamics of infection between subpopulations; we confirm this intuition and also show the peak coincides with successful invasion of the infection into most subpopulations. The global maximum at relatively large movement rates occurs because then the infectious agent perceives the metapopulation as if it is a single well-mixed population wherein the effective population size is greater than the critical community size.     

Effects of nitrogen deposition on the interaction between an aphid and its host plant

Abstract 1. Anthropogenic increases in nitrogen deposition are impacting terrestrial ecosystems worldwide. While some of the direct ecosystem‐level effects of nitrogen deposition are understood, the effects of nitrogen deposition on plant–insect interactions and on herbivore population dynamics have received less attention. 2. Nitrogen deposition will potentially influence both plant resource availability and herbivore population growth. If increases in herbivore population growth outstrip increases in resource availability, then increases in the strength of density dependence expressed within the herbivore population would be predicted. Alternatively, if plant resources respond more vigorously to nitrogen deposition than do herbivore populations, a decline in the strength of density dependence would be expected. No change in the strength of density dependence acting upon the herbivore population would suggest equivalent responses by herbivores and plants. 3. A density manipulation experiment was performed to examine the effect of nitrogen deposition on the interaction between a host plant, Asclepias tuberosa, and its herbivore, Aphis nerii. Aphid maximum per capita growth rate (R_max), carrying capacity (K), and the strength of density dependence were measured under three nitrogen deposition treatments. The effect of nitrogen deposition on the relationship among these three measures of insect population dynamics was explored. 4. Simulated nitrogen deposition increased aphid per capita population growth, plant foliar nitrogen concentrations, and plant biomass. Nitrogen deposition caused R_max and K to increase proportionally, leading to no overall change in the strength of density dependence. In this system, potential changes in the negative feedback processes operating on herbivore populations following nitrogen deposition appear to be buffered by concomitant changes in resource availability.     

Herbivore‐induced plant responses in Brassica oleracea prevail over effects of constitutive resistance and result in enhanced herbivore attack

1. Plant responses to herbivore attack may have community‐wide effects on the composition of the plant‐associated insect community. Thereby, plant responses to an early‐season herbivore may have profound consequences for the amount and type of future attack. 2. Here we studied the effect of early‐season herbivory by caterpillars of Pieris rapae on the composition of the insect herbivore community on domesticated Brassica oleracea plants. We compared the effect of herbivory on two cultivars that differ in the degree of susceptibility to herbivores to analyse whether induced plant responses supersede differences caused by constitutive resistance. 3. Early‐season herbivory affected the herbivore community, having contrasting effects on different herbivore species, while these effects were similar on the two cultivars. Generalist insect herbivores avoided plants that had been induced, whereas these plants were colonised preferentially by specialist herbivores belonging to both leaf‐chewing and sap‐sucking guilds. 4. Our results show that community‐wide effects of early‐season herbivory may prevail over effects of constitutive plant resistance. Induced responses triggered by prior herbivory may lead to an increase in susceptibility to the dominant specialists in the herbivorous insect community. The outcome of the balance between contrasting responses of herbivorous community members to induced plants therefore determines whether induced plant responses result in enhanced plant resistance.