A comparison of the dynamical impact of seasonal mechanisms in a herbivore–plant defence system

Plant defences can reduce herbivore fitness and may promote cycles in some herbivore populations. In this study, we model the interaction between plant defences and herbivores and include seasonal forcing, a ubiquitous environmental influence in natural systems. We compare the impacts of two different seasonal mechanisms on the dynamics of the herbivore–plant defence system. The first mechanism involves a fixed breeding season length and a variable birth rate within the breeding season; the second involves a variable breeding season length and a fixed birth rate within the breeding season. When parameterised for a specific cyclic system, namely field voles and silica, our model predicts that a variable season length gives multi-year cycles for a larger region in parameter space than a variable birth rate. Our results highlight the complexity of the dynamical effects of seasonal forcing and that these effects are strongly dependent on the type of seasonal mechanism.     

Thresholds in plant–herbivore interactions: predicting plant mortality due to herbivore browse damage

Patterns of herbivore browse at small scales, such as the rate of leaf consumption or plant preferences, drive the impact of herbivores on whole-plant processes, such as growth or survival, and subsequent changes in plant population structure. However, herbivore impacts are often non-linear, highly variable and context-dependent. Understanding the effect of herbivores on plant populations therefore requires a detailed understanding of the relationships that drive small-scale processes, and how these interact to generate dynamics at larger scales. We derive a mathematical model to predict annual rates of browse-induced tree mortality. We model individual plant mortality as a result of rates of foliage production, turnover and herbivore intake, and extend the model to the population scale by allowing for between-tree variation in levels of herbivore browse. The model is configurable for any broadleaved tree species subject to vertebrate or invertebrate browse, and is designed to be parameterized from field data typically collected as part of browse damage assessments. We parameterized and tested the model using data on foliage cover and browse damage recorded on kamahi trees (Weinmannia racemosa) browsed by possums (Trichosurus vulpecula) in New Zealand forests. The model replicated observed patterns of tree mortality at 12 independent validation sites with a wide range of herbivore densities and browse damage. The model reveals two key thresholds; in plant foliar cover, indicating when individual trees may be at high risk from browse-induced mortality, and in herbivore intake, leading to high rates of mortality across the whole population.     

Omnivores as plant bodyguards—A model of the importance of plant quality

The importance of omnivores in ecological systems is increasingly being recognized, not least due to their intensified use as biocontrol agents in crop production. We model a simple plant–herbivore–omnivore (predator) system to explore the effects of plant suitability as food for omnivores on the outcome of omnivore–herbivore interactions. The model predicts that increasing plant suitability relative to herbivore suitability for the omnivore will catalyze the extinction of herbivores or omnivores, depending on the relative growth rate of omnivores feeding solely on plants or herbivores. When omnivore growth is higher on plants, either the omnivore or the herbivore goes extinct. When omnivore growth is higher on herbivores, the possible consequences are extinction, stable coexistence, and limit cycles, depending on the combination of species properties. Our results suggest that plants in some situations may evolve towards becoming more suitable to omnivores to escape detrimental herbivores and that breeders could manipulate crop suitability to omnivore species to reach a desired outcome of omnivore–herbivore interactions.     

Evolution and spatial structure interact to influence plant–herbivore population and community dynamics

An individual-based model of plant–herbivore interactions was developed to test the potentially interactive effects of explicit space and coevolution on population and community dynamics. Individual plants and herbivores resided in cells on a lattice and carried linked interaction genes. Interaction strength between individual plants and herbivores depended on concordance between these genes (gene-for-gene coevolution). Mating and dispersal among individuals were controlled spatially within variably sized neighbourhoods. Without evolution we observed high-frequency plant–herbivore oscillations (blue spectra) with small individual neighbourhoods, and stochastic fluctuations (white spectra) with large neighbourhoods. Evolution resulted in decreased interaction strength, decreased herbivore-induced plant mortality, increased population sizes, and longer-term fluctuations (reddened spectra). Small herbivore neighbourhoods led to herbivore extinction only with evolution. To explore the increased population size response to evolution we ran simulations without evolution while tuning plant–herbivore interaction strength from high to none. We found that herbivore populations were maximized at intermediate levels of interaction strength that coincided with the interaction strength achieved when the system tuned itself through evolution. Overall, our model shows that the small-scale details of phenotypically variable individual-level interactions, leading to evolutionary dynamics, affect large-scale population and community dynamics.     

Plant compensatory growth: a conquering strategy in plant–herbivore interactions?

We present a theoretical analysis that considers the phenotypic trait of compensatory growth ability in a context of population dynamics. Our model depicts a system of three interactors: herbivores and two different plant types referred to as ordinary and compensating. The compensating plant type has the ability to increase its intrinsic rate of biomass increase as a response to damage. This compensatory growth ability is maintained at the expense of a reduced growth rate in the absence of damage, where the ordinary plant type has the higher growth rate. Analysis of this system suggests that, even though a compensatory capacity of this kind will not imply an increase in equilibrium plant density, it will give a competitive advantage in relation to other plants, in the presence of a sufficiently efficient herbivore. Invasion of compensating plants into a population of non-compensating plants is facilitated by a high compensatory growth ability and a high intrinsic rate of plant biomass increase. Conversely, an ordinary plant can invade and outcompete a compensating plant when the herbivore is characterised by a relatively low attack rate, and/or when plant intrinsic growth rate is decreased.     

Spatial ecology of large herbivore populations

Models of the dynamics of large herbivore populations represent density feedbacks on the population growth rate either directly or indirectly through interactions with vegetation resources. Neither approach incorporates the spatial heterogeneity that is an essential feature of most natural environments, and modifies the population dynamics generated. This is especially true for large herbivores exploiting food resources that are rooted in space but temporally variable in quantity and quality both seasonally and annually. In this review I explore how environmental variation at different spatiotemporal scales influences the abundance of herbivore populations controlled via resources, predators or social mechanisms. Changes in abundance can be spatially disparate and dependent on different resource components at different stages of the seasonal cycle, including buffer resources restricting population crashes in extremely adverse years. GPS telemetry enables movement responses generating spatial patterns to be documented in fine spatiotemporal detail, including migration and dispersal. Models incorporating spatial heterogeneity either implicitly or explicitly are outlined, exemplifying how herbivores cope with temporal variability by exploiting spatial variability in resources and conditions. Global human dominance is generating widened climatic variation while opportunities for herbivore movements are becoming constricted. Theoretical population ecologists need to shift their focus from the workings of demographic structure towards effects of changing environmental contexts, in order to project the likely trajectories of large herbivore populations through the Anthropocene.     

Genetic and soil-nutrient effects on the abundance of herbivores on willow

The effects of soil-nutrient environment, plant genotype, and the interaction between the two on the resistance of the willow, Salix sericea, to insect species in a diverse herbivore community was measured. We found that soil-nutrient environment influenced plant growth and the abundance of most herbivores of S. sericea. However, environmental effects on herbivore abundance were often modified by plant genetics; the abundance of four of seven herbivores exhibited significant genotypeby-environment interaction effects. Pure genotype effects were mostly small and non-significant. The effects of fertilization differed among herbivores. Several herbivores were more abundant on fertilized plants, one was less abundant, and the abundance of others did not change. We found that feeding guild was a poor predictor of herbivore response. Finally we found significant phenotypic and genetic correlations among growth rate, internode length, and the abundances of several herbivores.     

On the correlation between allocation to defence and regrowth in plants

Because storage of resources to regrow after damage and investment in defence draw upon the same resource pool, it has been argued that they should show a negative correlation. We sketch a model for optimal allocation to defence and to storage for regrowth. In the model generalist herbivores exert a constant herbivore pressure against which the plant can defend itself. With discrete intervals, disturbance occurs by an external cause against which the plant cannot defend. This could be an abiotic disturbance or the outbreak of a specialist herbivore that is unaffected by the defence. If we compare genotypes or species, each adapted to its own habitat, then a positive correlation or no correlation between allocation to defence and to regrowth is to be expected. The parameter space in which plants should both defend and store resources for regrowth is limited. Especially under favourable growing conditions, plants should only allocate to growth. We discuss some experimental measures of the regrowth capacity of plants in the context of our model and argue that these should be used with caution.     

Functional responses of adaptive consumers and community stability with emphasis on the dynamics of plant-herbivore systems

A comparatively recent focus in consumer–resource theory has been the examination of whether adaptive foraging by consumers, manifested through the functional response, can stabilize consumer–resource dynamics. We offer a brief synthesis of progress on this body of theory and identify the conditions likely to lead to stability. We also fill a gap in our understanding by analysing the potential for adaptively foraging herbivores, which are constrained by time available to feed and digestive capacity, to stabilize dynamics in a single-herbivore/two-plant resource system. Because foraging parameters of the adaptive functional response scale allometrically with herbivore body size, we parameterized our model system using published foraging data for an insect, a small mammal and a large mammal spanning four orders of magnitude in body size, and examined numerically the potential for herbivores to stabilize the consumer–resource interactions. We found in general that the herbivore–plant equilibrium will be unstable for all biologically realistic herbivore population densities. The instability arose for two reasons. First, each herbivore exhibited destabilizing adaptive consumer functional responses (i.e. density-independent or inversely density-dependent) whenever they selected a mixed diet. Secondly, the numerical response of herbivores, based on our assumption of density-independent herbivore population growth, results in herbivores reaching densities that enable them to exploit their resource populations to extinction. Our results and those of studies we reviewed indicate that, in general, adaptive consumers are unlikely to stabilize the dynamics of consumer–resource systems solely through the functional response. The implications of this for future work on consumer–resource theory are discussed.     

Optimal feeding under stoichiometric constraints: a model of compensatory feeding with functional response

When the nutrient content of food is limited, herbivores often increase their feeding rates. Such an increase in the feeding rate is called ‘compensatory feeding’. Although it has a number of implications for herbivore population and plant–forager dynamics, the compensatory feeding is not yet functionally formulated especially in relation with ecological stoichiometry. Therefore, we constructed a simple mathematical model by incorporating the optimal feeding rate into the type II functional response to maximize a forager's growth rate under constraints of carbon or nutritionally important element like phosphorus (P). We used the planktonic herbivore Daphnia as a model herbivore. The model revealed that the optimal feeding rate increased by using excess carbon when relative P content of food was less than a certain level, which is known as the threshold elemental ratio. This level changed with the change of food abundance. It also showed that whether or not foragers should exhibit compensatory feeding depends on their stoichiometric characteristics and digestive traits, and also on the assimilability of a given food. These findings are helpful to test the feeding conditions under which compensatory feeding is advantageous for a given animal. Our model can be easily incorporated into forager population dynamics and prey‐consumer interaction models because the optimal feeding rate can be analytically given.     

Competition and facilitation in multispecies plant-herbivore systems of productive environments

We develop a multispecies plant-herbivore model to explore how plant competition for light and the selectivity of herbivores affect abundance patterns of plants and herbivores along productivity gradients. The model considers a small and a tall plant species, a generalist herbivore, and a selective herbivore. The selective herbivore feeds only on the small plant species. In the absence of the generalist herbivore, the tall plant species becomes increasingly dominant with increasing productivity, and the small plant and its selective herbivore disappear. The model shows that generalist herbivores can facilitate selective herbivores by suppressing competition for light. This favours the small plant species, and thereby the selective herbivores. The model predictions are qualitatively consistent with field studies of multispecies plant-herbivore systems.     

Experimental Infection of Plants with an Herbivore-Associated Bacterial Endosymbiont Influences Herbivore Host Selection Behavior

Although bacterial endosymbioses are common among phloeophagous herbivores, little is known regarding the effects of symbionts on herbivore host selection and population dynamics. We tested the hypothesis that plant selection and reproductive performance by a phloem-feeding herbivore (potato psyllid, Bactericera cockerelli) is mediated by infection of plants with a bacterial endosymbiont. We controlled for the effects of herbivory and endosymbiont infection by exposing potato plants (Solanum tuberosum) to psyllids infected with “Candidatus Liberibacter solanacearum” or to uninfected psyllids. We used these treatments as a basis to experimentally test plant volatile emissions, herbivore settling and oviposition preferences, and herbivore population growth. Three important findings emerged: (1) plant volatile profiles differed with respect to both herbivory and herbivory plus endosymbiont infection when compared to undamaged control plants; (2) herbivores initially settled on plants exposed to endosymbiont-infected psyllids but later defected and oviposited primarily on plants exposed only to uninfected psyllids; and (3) plant infection status had little effect on herbivore reproduction, though plant flowering was associated with a 39% reduction in herbivore density on average. Our experiments support the hypothesis that plant infection with endosymbionts alters plant volatile profiles, and infected plants initially recruited herbivores but later repelled them. Also, our findings suggest that the endosymbiont may not place negative selection pressure on its host herbivore in this system, but plant flowering phenology appears correlated with psyllid population performance.     

Experimental climate change weakens the insurance effect of biodiversity

Ecosystems are simultaneously affected by biodiversity loss and climate change, but we know little about how these factors interact. We predicted that climate warming and CO (2) -enrichment should strengthen trophic cascades by reducing the relative efficiency of predation-resistant herbivores, if herbivore consumption rate trades off with predation resistance. This weakens the insurance effect of herbivore diversity. We tested this prediction using experimental ocean warming and acidification in seagrass mesocosms. Meta-analyses of published experiments first indicated that consumption rate trades off with predation resistance. The experiment then showed that three common herbivores together controlled macroalgae and facilitated seagrass dominance, regardless of climate change. When the predation-vulnerable herbivore was excluded in normal conditions, the two resistant herbivores maintained top-down control. Under warming, however, increased algal growth outstripped control by herbivores and the system became algal-dominated. Consequently, climate change can reduce the relative efficiency of resistant herbivores and weaken the insurance effect of biodiversity.     

More is not necessarily better: the impact of limiting and excessive nutrients on herbivore population growth rates

Abstract 1. The body tissues of insect herbivores contain higher concentrations of nitrogen and phosphorus than do their host plants, leading to an elemental mismatch that can limit herbivore growth, fecundity and ultimately influence population dynamics. While low nutrient availability can limit herbivore growth and reproduction, nutrient levels that exceed an organism’s nutritional requirements, i.e. an organisms’ threshold elemental ratio, can also decrease performance. 2. We conducted a laboratory experiment to examine the impacts of nitrogen and phosphorus additions on population growth rates of a phloem‐feeding insect herbivore. 3. Herbivore per capita population growth rates were highest at intermediate foliar nitrogen concentrations, indicating a performance cost on the highest nitrogen foliage. While there was no direct effect of foliar phosphorus concentration on insect performance, there was a strong and unexpected indirect effect. High soil phosphorus availability increased both foliar nitrogen concentrations and aphid tissue nitrogen, resulting in low population growth rates when both soil nitrogen and phosphorus availabilities were high. 4. In this study, experimental increases in foliar nitrogen levels led to a decrease in herbivore performance suggesting that excessive nutrient levels can limit herbivore population growth rates.     

Reciprocal interactions between native and introduced populations of common milkweed,Asclepias syriaca,and the specialist aphid,Aphis nerii

Following its introduction into Europe (EU), the common milkweed (Asclepias syriaca) has been free of most specialist herbivores that are present in its native North American (NA) range, except for the oleander aphid Aphis nerii. We compared EU and NA populations of A. nerii on EU and NA milkweed populations to test the hypothesis that plant–insect interactions differ on the two continents. First, we tested if herbivore performance is higher on EU plants than on NA plants, because the former have escaped most of their herbivores and have perhaps been selected for lower defence levels following introduction. Second, we compared two A. nerii lines (one from each continent) to test whether genotypic differences in the herbivore may influence species interactions in plant–herbivore communities in the context of species introductions. The NA population of A. nerii developed faster, had higher fecundity and attained higher population growth rates than the EU population. There was no overall significant continental difference in aphid resistance between the plants. However, milkweed plants from EU supported higher population growth rates and faster development of the NA line of A. nerii than plants from NA. In contrast, EU aphids showed similar (low) performance across plant populations from both continents. In a second experiment, we examined how chewing herbivores indirectly mediate interactions between milkweeds and aphids, and induced A. syriaca plants from each continent by monarch caterpillars (Danaus plexippus) to compare the resulting changes in plant quality on EU aphid performance. As specialist chewing herbivores of A. syriaca are only present in NA, we expected that plants from the two continents may affect aphid growth in different ways when they are challenged by a specialist chewing herbivore. Caterpillar induction decreased aphid developmental times on NA plants, but not on EU plants, whereas fecundity and population growth rates were unaffected by induction on both plant populations. The results show that genetic variation in the plants as well as in the herbivores can determine the outcome of plant–herbivore interactions.     

Landscape structure,dispersal and the evolution of antagonistic plant–herbivore interactions

Different species have different dispersal capabilities and in the field, species interact with each other within dynamic, heterogeneous and complex landscapes. While plants and certain herbivore species may disperse considerable distances by means of seed dispersal or flight, other herbivores (e.g. root‐feeding nematodes or non‐winged insect herbivores) are more limited in their dispersal capacities. This difference in dispersal capabilities results in mosaics of plant–herbivore interactions that shift over time and space leading to spatio‐temporal variation in both the presence and absence of the species and their interactions. We developed an individual based simulation model in which we examined how multi‐species interactions are affected by their mobility within structurally complex landscapes. The main objective was to address the consequences for the arms race between plant defence and herbivore resistance to changes in fundamental landscape and community attributes. We demonstrate that feedbacks between landscape structure, community structure and the specific dispersal rate of the species involved affect the evolutionary dynamics between plants and herbivore antagonists. While three‐species interactions result in increased plant defence and herbivore resistance, effects of dispersal have diverse effects depending on the prevailing landscape structure.     

Dynamics of a plant-herbivore-predator system with plant-toxicity

A system of ordinary differential equations is considered that models the interactions of two plant species populations, an herbivore population, and a predator population. We use a toxin-determined functional response to describe the interactions between plant species and herbivores and use a Holling Type II functional response to model the interactions between herbivores and predators. In order to study how the predators impact the succession of vegetation, we derive invasion conditions under which a plant species can invade into an environment in which another plant species is co-existing with a herbivore population with or without a predator population. These conditions provide threshold quantities for several parameters that may play a key role in the dynamics of the system. Numerical simulations are conducted to reinforce the analytical results. This model can be applied to a boreal ecosystem trophic chain to examine the possible cascading effects of predator-control actions when plant species differ in their levels of toxic defense.     

Demographic effects of large, introduced herbivores on a long-lived endemic plant

The introduction of alien ungulates is a major threat for the survival of endangered plants, especially in island ecosystems. However, very few studies have investigated the potential damage of large herbivores on plant diversity in Mediterranean protected areas. In this study, we describe the population structure and the long-term dynamics of the main populations of the Sardinian narrow endemic Centaurea horrida Bad. (Asteraceae), by means of permanent plots where individual plants were tagged and monitored through 6?years (2004?C2009). We monitored this endangered plant at three sites: two were protected areas where introduced and feral ungulates are present, and the other one was a non-protected site without introduced ungulates. We found that adults and saplings were more abundant at the non-protected site. Through matrix models, we also highlighted that the non-protected population showed the highest population growth rate. Finally, by means of an exclusion experiment for ungulates at one protected site, we demonstrated that herbivores had a negative effect on the survival of seedlings and adult plants, and reduced the stochastic population growth rate. An LTRE analysis showed that differences in the survival, especially of adult individuals, had the highest responsibility in explaining the higher population growth rate when herbivores are excluded. Our study constitutes a clear example on how the protection of alien large herbivores can have opposite effects on the conservation of an endangered plant. Some management options are proposed, and the urgent need of manipulative experiments on species-specific interactions between protected plants and alien herbivore species is invoked.     

Spatial Coupling of Plant and Herbivore Dynamics: The Contribution of Herbivore Dispersal to Transient and Persistent "Waves" of Damage

Spatial variations in the abundance of insect herbivores and in herbivore damage are both striking an commonplace. The standard explanations for heterogeneity in herbivore attack emphasize spatial variations in plant genetype, soils, or physical environment. Here I examine an alternative hypothesis-that heterogeneity arises in plant-herbivore systems, even in homogeneous environments, as a result of the direct coupling of herbivore movement to herbivore density and plant quality. Using a mathematical model for plant quality and herbivore growth and dispersal, I demonstrate how spatial instabilities about homogeneous steady state values result in both transient and stationary waves of damage to the plant. Key herbivore movement behaviors include the tendendy for herbivores to aggregate over a range of spatial scales for increased feeding efficiency and the tendency for herbivores to move up gradients in plant quality (herbivory-taxis). My approach translates the biased "random walk" behavior of individual herbivores into a continuum partial differential equation model. Analytical and numerical methods are used to demonstrate the nature of the spatio-temporal variations in plant quality and herbivore density.     

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.