Linking herbivore-induced defences to population dynamics

1. Theoretical studies have shown that inducible defences have the potential to affect population stability and persistence in bi‐ and tritrophic food chains. Experimental studies on such effects of prey defence strategies on the dynamics of predator–prey systems are still rare. We performed replicated population dynamics experiments using the herbivorous rotifer Brachionus calyciflorus and four strains of closely related algae that show different defence responses to this herbivore. 2. We observed herbivore populations to fluctuate at a higher frequency when feeding on small undefended algae. During these fluctuations minimum rotifer densities remained sufficiently high to ensure population persistence in all the replicates. The initial growth of rotifer populations in this treatment coincided with a sharp drop in algal density. Such a suppression of algae by herbivores was not observed in the other treatments, where algae were larger due to induced or permanent defences. In these treatments we observed rotifer population densities to first rise and then decline. The herbivore went extinct in all replicates with large permanently defended algae. The frequency of herbivore extinctions was intermediate when algae had inducible defences. 3. A variety of alternative mechanisms could explain differential herbivore persistence in the different defence treatments. Our analysis showed the density and fraction of highly edible algal particles to better explain herbivore persistence and extinctions than total algal density, the fraction of highly inedible food particles or the accumulation of herbivore waste products or autotoxins. 4. We argue that the rotifers require a minimum fraction and density of edible food particles for maintenance and reproduction. We conjecture that induced defences in algae may thus favour larger zooplankton species such as Daphnia spp. that are less sensitive to shifts in their food size spectrum, relative to smaller zooplankton species, such as rotifers and in this way contributes to the structuring of planktonic communities.     

Catastrophic vegetation shifts and soil degradation in terrestrial grazing systems

It has long been recognized that alternative vegetation states may occur in terrestrial grazing systems. This phenomenon may be of great importance as small environmental fluctuations may lead to relatively sudden and irreversible jumps between vegetation states. Early theoretical studies emphasized saturation of herbivore feeding to explain multiple stable states and catastrophic behaviour. Recent studies on semi-arid grasslands and arctic salt marshes, however, relate catastrophic events in these systems to plant-soil interactions.     

Spatial dynamics of lions and their prey along an environmental gradient

Establishing the ecological determinants of the spatial dynamics of large African savanna mammals is necessary for understanding the cumulative impacts on the suitability and resilience of their natural habitats, of progressive habitat fragmentation and temporal shifts in climate, fire regimes and elephant browsing. Systematic directional gradients and small‐scale spatial dependence were evident in rainfall, herbivore biomass and lion density in the Masai Mara National Reserve during September 1990 to July 1992. Lion density, the biomass of resident and all herbivore species were autocorrelated within 4.3, 4.1 and 3.3 km, respectively, and peaked in areas of relatively low rainfall but higher microtopographic and vegetation heterogeneity and complexity and more diverse drainage systems. Rainfall influenced herbivore biomass and hence lion density non‐linearly and that influence was apparently modified by forage mineral nutrients, structural habitat complexity, degree of drainage and distance to waterpoints. Lion density was related to the biomass of resident herbivores, even after controlling for rainfall and spatial trends. Persistence of the recent decline in Mara woodlands and increasing human population along the reserve–ranch boundary would likely reduce the reserve's lion population because most lions spent the daytime within the vegetation mosaic fringing drainage lines, away from humans and domestic livestock.     

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.     

Spatial heterogeneity and irreversible vegetation change in semiarid grazing systems

Recent theoretical studies have shown that spatial redistribution of surface water may explain the occurrence of patterns of alternating vegetated and degraded patches in semiarid grasslands. These results implied, however, that spatial redistribution processes cannot explain the collapse of production on coarser scales observed in these systems. We present a spatially explicit vegetation model to investigate possible mechanisms explaining irreversible vegetation collapse on coarse spatial scales. The model results indicate that the dynamics of vegetation on coarse scales are determined by the interaction of two spatial feedback processes. Loss of plant cover in a certain area results in increased availability of water in remaining vegetated patches through run-on of surface water, promoting within-patch plant production. Hence, spatial redistribution of surface water creates negative feedback between reduced plant cover and increased plant growth in remaining vegetation. Reduced plant cover, however, results in focusing of herbivore grazing in the remaining vegetation. Hence, redistribution of herbivores creates positive feedback between reduced plant cover and increased losses due to grazing in remaining vegetated patches, leading to collapse of the entire vegetation. This may explain irreversible vegetation shifts in semiarid grasslands on coarse spatial scales.     

Modeling herbivore functional responses causing boom‐bust dynamics following predator removal

Native biodiversity is threatened by invasive species in many terrestrial and marine systems, and conservation managers have demonstrated successes by responding with eradication or control programs. Although invasive species are often the direct cause of threat to native species, ecosystems can react in unexpected ways to their removal or reduction. Here, we use theoretical models to predict boom‐bust dynamics, where the removal of predatory or competitive pressure from a native herbivore results in oscillatory population dynamics (boom‐bust), which can endanger the native species’ population in the short term. We simulate control activities, applied to multiple theoretical three‐species Lotka‐Volterra ecosystem models consisting of vegetation, a native herbivore, and an invasive predator. Based on these communities, we then develop a predictive tool that—based on relative parameter values—predicts whether control efforts directed at the invasive predator will lead to herbivore release followed by a crash. Further, by investigating the different functional responses, we show that model structure, as well as model parameters, are important determinants of conservation outcomes. Finally, control strategies that can mitigate these negative consequences are identified. Managers working in similar data‐poor ecosystems can use the predictive tool to assess the probability that their system will exhibit boom‐bust dynamics, without knowing exact community parameter values.     

Top–down limits on prey populations may be more severe in larger prey species,despite having fewer predators

Variation in the vulnerability of herbivore prey to predation is linked to body size, yet whether this relationship is size‐nested or size‐partitioned remains debated. If size‐partitioned, predators would be focused on prey within their preferred prey size range. If size‐nested, smaller prey species should become increasingly more vulnerable because increasingly more predators are capable of catching them. Yet, whether either of these strategies manifests in top–down prey population limitation would depend both on the number of potential predator species as well as the total mortality imposed. Here we use a rare ecosystem scale ‘natural experiment’ comparing prey population dynamics between a period of intense predator persecution and hence low predator densities and a period of active predator protection and population recovery. We use three decades of data on herbivore abundance and distribution to test the role of predation as a mechanism of population limitation among prey species that vary widely in body size. Notably, we test this within one of the few remaining systems where a near‐full suite of megaherbivores occur in high density and are thus able to include a thirtyfold range in herbivore body size gradient. We test whether top–down limitation on prey species of particular body size leads to compositional shifts in the mammalian herbivore community. Our results support both size‐nested and size‐partitioning predation but suggest that the relative top–down limiting impact on prey populations may be more severe for intermediate sized species, despite having fewer predators than small species. In addition we show that the gradual recovery of predator populations shifted the herbivore community assemblage towards large‐bodied species and has led to a community that is strongly dominated by large herbivore biomass.     

Host-parasite population dynamics under combined frequency- and density-dependent transmission

Many host‐parasite models assume that transmission increases linearly with host population density (‘density‐dependent transmission’), but various alternative transmission functions have been proposed in an effort to capture the complexity of real biological systems. The most common alternative (usually applied to sexually transmitted parasites) assumes instead that the rate at which hosts contact one another is independent of population density, leading to ‘frequency‐dependent’ transmission. This straight‐forward distinction generates fundamentally different dynamics (e.g. deterministic, parasite‐driven extinction with frequency‐ but not density‐dependence). Here, we consider the situation where transmission occurs through two different types of contact, one of which is density‐dependent (e.g. social contacts), the other density‐independent (e.g. sexual contacts). Drawing on a range of biological examples, we propose that this type of contact structure may be widespread in natural populations. When our model is characterized mainly by density‐dependent transmission, we find that allowing even small amounts of transmission to occur through density‐independent contacts leads to the possibility of deterministic, parasite‐driven extinction (and lowers the threshold for parasite persistence). Contrastingly, allowing some density‐dependent transmission to occur in a model characterized mainly by density‐independent contacts (i.e. by frequency‐dependent transmission) does not affect the extinction threshold, but does increase the likelihood of parasite persistence. The idea that directly transmitted parasites exploit different types of host contact is not new, but here we show that the impact on dynamics can be fundamental even in the simplest cases. For example, in systems where density‐dependent transmission is normally assumed de facto, we show that parasite‐driven extinction can occur if a small amount of transmission occurs through density‐independent contacts. Many empirical studies are still guided by the traditional density/frequency dichotomy, but our combined transmission function may provide a better model for systems in which both types of transmission occur.     

Predator-prey coevolution driven by size selective predation can cause anti-synchronized and cryptic population dynamics

Population dynamics and evolutionary dynamics can occur on similar time scales, and a coupling of these two processes can lead to novel population dynamics. Recent theoretical studies of coevolving predator-prey systems have concentrated more on the stability of such systems than on the characteristics of cycles when they are unstable. Here I explore the characteristics of the cycles that arise due to coevolution in a system in which prey can increase their ability to escape from predators by becoming either significantly larger or significantly smaller in trait value (i.e., a bidirectional trait axis). This is a reasonable model of body size evolution in some systems. The results show that antiphase population cycles and cryptic cycles (large population fluctuation in one species but almost no change in another species) can occur in the coevolutionary system but not systems where only a single species evolves. Previously, those dynamical patterns have only been theoretically shown to occur in single species evolutionary models and the coevolutionary model which do not involve a bi-directional axis of adaptation. These unusual dynamics may be observed in predator-prey interactions when the density dependence in the prey species is strong.     

Can hyperparasitoids cause large‐scale outbreaks of insect herbivores?

Synchronous population fluctuations occur in many species and have large economic impacts, but remain poorly understood. Dispersal, climate and natural enemies have been hypothesized to cause synchronous population fluctuations across large areas. For example, insect herbivores cause extensive forest defoliation and have many natural enemies, such as parasitoids, that may cause landscape‐scale changes in density. Between outbreaks, parasitoid‐caused mortality of hosts/herbivores is high, but it drops substantially during outbreak episodes. Because of their essential role in regulating herbivore populations, we need to include parasitoids in spatial modelling approaches to more effectively manage insect defoliation. However, classic host‐parasitoid population models predict parasitoid density, and parasitoid density is difficult to relate to host‐level observations of parasitoid‐caused mortality. We constructed a novel model to study how parasitoids affect insect outbreaks at the landscape scale. The model represents metacommunity dynamics, in which herbivore regulation, colonisation and extinction are driven by interactions with the forest, primary parasitoids and hyperparasitoids. The model suggests that parasitoid spatial dynamics can produce landscape‐scale outbreaks. Our results propose the testable prediction that hyperparasitoid prevalence should increase just before the onset of an outbreak because of hyperparasitoid overexploitation. If verified empirically, hyperparasitoid distribution could provide a biotic indicator that an outbreak will occur.     

Simulation of the effects of deer browsing on forest dynamics

I introduced forest dynamics to a deterministic herbivore-vegetation model to examine the effects of vertically stratified forest structure on the dynamics of the herbivore–vegetation system, the resilience and stable states of vegetation, and the interactions between deer populations and vegetation. I constructed a model based on data from field studies performed in Hokkaido, northern Japan. Three phases of state were identified for a given deer density: (1) understory vegetation is maintained with a equilibrium proportion of canopy gaps in the absence of deer; (2) if the equilibrium proportion of canopy gaps is greater than that in the equilibrium state in the absence of deer, the understory vegetation can be maintained; and (3) the understory vegetation cannot be maintained. At the boundary between phases 2 and 3, the herbivore population level had discontinuous effects on vegetation. When the deer density was held below the threshold, forest vegetation had resilience to recover to the equilibrium stable state at the given deer density, although the equilibrium canopy gap ratio and vegetation biomass differed with deer density. However, the forest vegetation–herbivore system could not be maintained in a stable state without artificial deer population management if food limitation was the only mechanism to keep the deer population at low levels. The deer population must be kept below the boundary between phases 1 and 2 to maintain the forest regeneration processes. The level cannot be determined by observing the deer population; careful observation of forest regeneration processes is required.     

Dynamics of herbivores and resources on a landscape with interspersed resources and refuges

A tradeoff between energy gain from foraging and safety from predation in refuges is a common situation for many herbivores that are vulnerable to predation while foraging. This tradeoff affects the population dynamics of the plant–herbivore–predator interaction. A new functional response is derived based on the Holling type 2 functional response and the assumption that the herbivore can forage at a rate that maximizes its fitness. The predation rate on the herbivore is assumed to be proportional to the product of the time that the herbivore spends foraging and a risk factor that reflects the habitat complexity; where greater complexity means greater interspersion of high food quality habitat and refuge habitat, which increases the amount of the edge zone between refuge and foraging areas, making foraging safer. The snowshoe hare is chosen as an example to demonstrate the resulting dynamics of an herbivore that has been intensely studied and that undergoes well-known cycling. Two models are studied in which the optimal foraging by hares is assumed, a vegetation–hare–generalist predator model and a vegetation–hare–specialist predator model. In both cases, the results suggest that the cycling of the snowshoe hare population will be greatly moderated by optimal foraging in a habitat consisting of interspersed high quality foraging habitat and refuge habitat. However, there are also large differences in the dynamics produced by the two models as a function of predation pressure.     

Multiple sources of evidence for density dependence in the endangered Hawaiian stilt (Himantopus mexicanus knudseni)

Hawaiian stilts (Himantopus mexicanus knudseni) are an endangered subspecies of the Black-necked stilt endemic to the Hawaiian Islands. Despite long-term study, the main drivers of Hawaiian stilt population dynamics are poorly understood. We tested for density dependence using two sources of evidence: a 30-year time series of annual estimated range-wide abundance, and two 15+ year time series of reproductive success. Using separate methods with independent data, sources allowed us to make up for the potentially positive bias of one approach with the more conservative nature of the second. We compared nonlinear density-dependent and density-independent population model fits to our time-series data, using both frequentist and Bayesian state-space approaches. Across both approaches, density-dependent models best fit observed population dynamics, with lower AICc and cross-validation statistics compared to density-independent models. Among density-dependent models, a conditional model in which density-independent dynamics occur below a population size threshold (~850–1,000 birds), and then density-dependent dynamics occur above that threshold, performed best across Bayesian and frequentist model comparisons, with the Ricker model ranked next or equivalently. Our analysis of reproduction data revealed a strong negative effect of local adult density on nest success (proportion of nests hatching at least one chick) at Kealia National Wildlife Refuge on Maui, where few alternative breeding habitats are available, but no such effect at another site where many nearby alternative wetlands are available. These congruent results across independent datasets and analytical approaches support the hypothesis that Hawaiian stilts exhibit density dependence across their range.     

Asymmetric interactions between plants and seed-harvesting ants in a Mediterranean pasture

A four-year study on the interactions between plants and seed-harvesting ants in a Mediterranean pasture is reviewed in this paper. As previously reported in many studies on plant–herbivore interactions, ant–plant relationships are also asymmetric; plants had a larger impact on herbivore dynamics than vice versa. However, the asymmetry did not refer to population dynamics but rather to animal foraging strategies. Ants did not exert a significant influence on vegetation dynamics in terms of plant abundance. The main constraints underlying vegetation change were self-regulation and rainfall. In contrast, the structural characteristics and abundance of vegetation had a significant impact on several important features of food harvesting by ants. This influence was not only associated with their feeding requirements but also with their foraging activities.     

Carbon storage in terrestrial ecosystems: do browsing and grazing herbivores matter?

Large mammalian herbivores manifest a strong top‐down control on ecosystems that can transform entire landscapes, but their impacts have not been reviewed in the context of terrestrial carbon storage. Here, we evaluate the effects of plant biomass consumption by large mammalian herbivores (>10 kg adult biomass), and the responses of ecosystems to these herbivores, on carbon stocks in temperate and tropical regions, and the Arctic. We calculate the difference in carbon stocks resulting from herbivore exclusion using the results of 108 studies from 52 vegetation types. Our estimates suggest that herbivores can reduce terrestrial above‐ and below‐ground carbon stocks across vegetation types but reductions in carbon stocks may approach zero given sufficient periods of time for systems to respond to herbivory (i.e. decades). We estimate that if all large herbivores were removed from the vegetation types sampled in our review, increases in terrestrial carbon stocks would be up to three orders of magnitude less than many of the natural and human‐influenced sources of carbon emissions. However, we lack estimates for the effects of herbivores on below‐ground biomass and soil carbon levels in many regions, including those with high herbivore densities, and upwards revisions of our estimates may be necessary. Our results provide a starting point for a discussion on the magnitude of the effects of herbivory on the global carbon cycle, particularly given that large herbivores are common in many ecosystems. We suggest that herbivore removal might represent an important strategy towards increasing terrestrial carbon stocks at local and regional scales within specific vegetation types, since humans influence populations of most large mammals.     

Population dynamics and mutualism: functional responses of benefits and costs

We develop an approach for studying population dynamics resulting from mutualism by employing functional responses based on density-dependent benefits and costs. These functional responses express how the population growth rate of a mutualist is modified by the density of its partner. We present several possible dependencies of gross benefits and costs, and hence net effects, to a mutualist as functions of the density of its partner. Net effects to mutualists are likely a monotonically saturating or unimodal function of the density of their partner. We show that fundamental differences in the growth, limitation, and dynamics of a population can occur when net effects to that population change linearly, unimodally, or in a saturating fashion. We use the mutualism between senita cactus and its pollinating seed-eating moth as an example to show the influence of different benefit and cost functional responses on population dynamics and stability of mutualisms. We investigated two mechanisms that may alter this mutualism's functional responses: distribution of eggs among flowers and fruit abortion. Differences in how benefits and costs vary with density can alter the stability of this mutualism. In particular, fruit abortion may allow for a stable equilibrium where none could otherwise exist.     

Are silica defences in grasses driving vole population cycles?

Understanding the factors that drive species population dynamics is fundamental to biology. Cyclic populations of microtine rodents have been the most intensively studied to date, yet there remains great uncertainty over the mechanisms determining the dynamics of most of these populations. For one such population, we present preliminary evidence for a novel mechanism by which herbivore-induced reductions in plant quality alter herbivore life-history parameters and subsequent population growth. We tested the effect of high silica levels on the population growth and individual performance of voles (Microtus agrestis) reared on their winter food plant (Deschampsia caespitosa). In sites where the vole population density was high, silica levels in D. caespitosa leaves collected several months later were also high and vole populations subsequently declined; in sites where the vole densities were low, levels of silica were low and population density increased. High silica levels in their food reduced vole body mass by 0.5% a day. We argue that silica-based defences in grasses may play a key role in driving vole population cycles.     

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.     

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.     

Density dependent and temporal variability in habitat selection by a large herbivore; an experimental approach

Both density dependent and density independent processes such as climate affect population dynamics in large herbivores. Understanding herbivore foraging patterns is essential to identify the underlying mechanisms behind variation in vital rates. However, very little is known about how animals vary their selection of habitat temporally, alone or in interaction with density during summer. At the foraging scale, we tested using a fully replicated experiment whether domestic sheep Ovis aries stocked at high (80  per  km²) and low (25  per  km²) densities (spatial contrasts) varied their habitat selection temporally over a four year period. We predicted reduced selection of high productivity vegetation types with increasing density, and that seasonal and annual variation in climate would affect this density dependent selection pattern by increasing competition for high quality habitats in late grazing season and in years with poor vegetation development and over time related to vegetation responses to grazing. As predicted from the Ideal free distribution model, selection of high productivity habitat decreased at high density. There was also a marked temporal variation in habitat selection. Selection of the most productive vegetation types declined towards the end of each grazing season, but increased over years both at low and high sheep density. There was only weak evidence for interactions, as selection ratio of highly productive habitats tended to increase more over years at low density as compared to high density. Limited interactive effects of density and annual variation on habitat selection during summer may explain why similar interactions in vital rates have rarely been reported for summer seasons. Our results are consistent with the view that variation in habitat selection is a central mechanism for climate and density related variation in vital rates.