Density dependence in insect performance within individual plants: induced resistance to Spodoptera exigua in tomato

Net intraspecific density dependence experienced by insect herbivores at the scale of single plants can be a function both of induced resistance in the plant and other interactions among individual herbivores. Theory suggests that non‐linearity in the form of this density dependence can influence the effects of plants on herbivore population dynamics. This study examined both net density dependence at the scale of single plants, and changes in plant quality with herbivore density for Spodoptera exigua caterpillars on tomato plants. One experiment measured the growth of caterpillars moving freely about the plant at different densities, the distribution of damage by these caterpillars, and the quality of the plant as food for caterpillars (growth of caterpillars on undamaged leaf tissue excised from the plant). A second experiment measured plant quality for plants with different amounts of damage by caterpillars confined to particular leaves in mesh bags. Growth of S. exigua caterpillars was found to be negatively density dependent, and this was in part due to decreases in plant quality both as herbivore density increased and as the amount of damage increased. The response of plant quality to herbivores was found to have non‐linear features; there was both a threshold below which no significant decreases in quality (as measured by herbivore growth) occurred, and the decrease in herbivore performance saturated at the highest damage levels. In addition, it was found that caterpillar damage was significantly more aggregated than expected when multiple caterpillars occupy a single plant. This study confirms that host plants have the potential to be a source of density dependence that affects herbivore performance.     

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.     

Host‐plant genotypic diversity and community genetic interactions mediate aphid spatial distribution

Genetic variation in plants can influence the community structure of associated species, through both direct and indirect interactions. Herbivorous insects are known to feed on a restricted range of plants, and herbivore preference and performance can vary among host plants within a species due to genetically based traits of the plant (e.g., defensive compounds). In a natural system, we expect to find genetic variation within both plant and herbivore communities and we expect this variation to influence species interactions. Using a three‐species plant‐aphid model system, we investigated the effect of genetic diversity on genetic interactions among the community members. Our system involved a host plant (Hordeum vulgare) that was shared by an aphid (Sitobion avenae) and a hemi‐parasitic plant (Rhinanthus minor). We showed that aphids cluster more tightly in a genetically diverse host‐plant community than in a genetic monoculture, with host‐plant genetic diversity explaining up to 24% of the variation in aphid distribution. This is driven by differing preferences of the aphids to the different plant genotypes and their resulting performance on these plants. Within the two host‐plant diversity levels, aphid spatial distribution was influenced by an interaction among the aphid's own genotype, the genotype of a competing aphid, the origin of the parasitic plant population, and the host‐plant genotype. Thus, the overall outcome involves both direct (i.e., host plant to aphid) and indirect (i.e., parasitic plant to aphid) interactions across all these species. These results show that a complex genetic environment influences the distribution of herbivores among host plants. Thus, in genetically diverse systems, interspecific genetic interactions between the host plant and herbivore can influence the population dynamics of the system and could also structure local communities. We suggest that direct and indirect genotypic interactions among species can influence community structure and processes.     

Density dependence in northern ungulates: interactions with predation and resources

Variation in the abundance of animals has traditionally been explained as the outcome of endogenous forcing from density dependence and exogenous forcing arising from variation in weather and predation. Emerging evidence suggests that the effects of density dependence interact with external influences on population dynamics. In particular, spatial heterogeneity in resources and the presence of capable predators may weaken feedbacks from density dependence to growth of populations. We used the Kalman filter to analyze 23 time series of estimates of abundance of northern ungulate populations arrayed along a latitudinal gradient (latitude range of 40°–70°N) to evaluate the influence of spatial heterogeneity in resources and predation on density dependence. We also used contingency tables to test whether density dependence was independent of the presence of carnivores (our estimate of predation) and multiple regressions to determine the effects of spatial heterogeneity in resources, predation, and latitude on the strength of density dependence. Our results showed that the strength of density dependence of ungulate populations was low in the presence of large carnivores, particularly at northern latitudes with low primary productivity. We found that heterogeneity in elevation, which we assume acted as a surrogate for spatial heterogeneity in plant phenology, also reduced effects of density dependence. Thus, we show that external forces created by heterogeneity in resources and predation interact with internal feedbacks from population density to shape dynamics of populations of northern ungulates.     

Population dynamics and sex ratio of a parasitoid altered by fungal-infected diet of host butterfly

Variation of host quality affects population dynamics of parasitoids, even at the landscape scale. What causes host quality to vary and the subsequent mechanisms by which parasitoid population dynamics are affected can be complex. Here, we examine the indirect interaction of a plant pathogen with a parasitoid wasp. Under laboratory conditions, parasitoids from hosts fed fungus-infected plants weighed less than those from hosts fed uninfected plants, indicating that the fungus causes the hosts to be of poor quality. However, parasitoids reared from hosts fed fungal-infected diet also tended to be female, a characteristic associated with high host quality. The pathogen, herbivore and parasitoid persist regionally as metapopulations in a shared landscape in Aland, Finland. In an analysis of the metapopulation dynamics of the parasitoid over 6 years, the probability of colonization of a host population increased by more than twofold in patches occupied by the plant pathogen. While we cannot determine that the relationship is causal, a compelling explanation is that the plant pathogen facilitates the establishment by the parasitoid by increasing the fraction of female offspring. This is a novel mechanism of spatial multi-trophic level interactions.     

Intraspecific difference among herbivore lineages and their host‐plant specialization drive the strength of trophic cascades

Trophic cascades – the indirect effect of predators on non‐adjacent lower trophic levels – are important drivers of the structure and dynamics of ecological communities. However, the influence of intraspecific trait variation on the strength of trophic cascade remains largely unexplored, which limits our understanding of the mechanisms underlying ecological networks. Here we experimentally investigated how intraspecific difference among herbivore lineages specialized on different host plants influences trophic cascade strength in a terrestrial tri‐trophic system. We found that the occurrence and strength of the trophic cascade are strongly influenced by herbivores’ lineage and host‐plant specialization but are not associated with density‐dependent effects mediated by the growth rate of herbivore populations. Our findings stress the importance of intraspecific heterogeneities and evolutionary specialization as drivers of trophic cascade strength and underline that intraspecific variation should not be overlooked to decipher the joint influence of evolutionary and ecological factors on the functioning of multi‐trophic interactions.     

Variation in and correlation between intrinsic rate of increase and carrying capacity

Intrinsic population growth rate and density dependence are fundamental components of population dynamics. Theory suggests that variation in and correlations between these parameters among patches within a population can influence overall population size, but data on the degree of variation and correlation are rare. Replicate populations of a specialist aphid (Chaetosiphon fragaefolii) were followed on 11 genotypes of host plant (Fragaria chiloensis) in the greenhouse. Population models fit to these census data provide estimates of intrinsic growth rate and carrying capacity for aphid populations on each plant genotype. Growth rate and carrying capacity varied substantially among plant genotypes, and these two parameters were not significantly correlated. These results support the existence of spatial variation in population dynamic parameters; data on frequency distributions and correlations of these parameters in natural populations are needed for evaluation of the importance of variation in growth rate and density dependence for population dynamics in the field.     

Insect herbivore stoichiometry: the relative importance of host plants and ant mutualists

Abstract.  1. Mutualistic associations can vary over spatial and ecological gradients. For herbivorous insects that engage in mutualisms with ants, plant quality can be a particularly important source of variation, because of the upward transfer of nutrients from plants to herbivores to ants.
2. A previous study demonstrated that mutualistic ants, Formica obscuripes , exert a top-down effect on the carbon and nitrogen concentrations (stoichiometry) in an herbivorous membracid, Publilia modesta . We characterised the consequences of mutualism for carbon and nitrogen stoichiometry between the same species pair, yet on an alternative, geographically-distinct host plant.
3. We found no top-down effect of ants on the carbon or nitrogen in the herbivore, but a strong, bottom-up effect of individual plants on membracid nitrogen concentration.
4. These results suggests that spatial heterogeneity in host plant traits, and ultimately the diet breadth of herbivore mutualists, may be important factors mediating stoichiometric patterns in mutualistic associations.     

Asynchrony, fragmentation, and scale determine benefits of landscape heterogeneity to mobile herbivores

Understanding the ways that resource heterogeneity shapes the performance of individuals and the dynamics of populations offers a central challenge in contemporary ecology. Emerging evidence shows that herbivores track heterogeneity in nutritional quality of vegetation by responding to phenological differences in plants, differences that result from spatial and temporal variation in conditions favoring plant growth. Theory predicts that when spatial variation in temperature, nutrients, or moisture results in spatially asynchronous pulses of plant growth, herbivores are able to prolong the period during which they have access to forage of peak nutritional value. Although this idea has substantial support from observational and modeling studies, it has not been examined experimentally. We hypothesized that access to asynchronous resources enhances nutritional status and growth of herbivores and that the magnitude of this effect depends on the scale of access relative to the grain of resources. We tested these hypotheses in mesocosm experiment using the migratory grasshopper, Melanoplus sanguinipes, feeding on young wheat and protein-rich bran as a model system. We demonstrated access to asynchronous pulses in resources enhanced the efficiency of use of high quality resource use and increased growth of individuals by 13%. Disruption of this mechanism when landscapes were fragmented lowered efficiency of resource use and caused growth of individuals to decline by 15%. However, the strength of the effects of fragmentation on herbivore performance depended on the spatial extent of fragmentation relative to the spatial and temporal grain of resource emergence. Our findings add experimental support to modeling and observational studies that have linked herbivore performance to spatial and temporal variation in plant phenology. We also offer evidence that fragmentation can impair herbivore performance, even when the total amount and quality of resources on landscapes remains unchanged.     

Effects of variation among plant species on the interaction between a herbivore and its parasitoid

Abstract.  1. Previous studies have demonstrated that phenotypic traits of plants have the potential to affect interactions between herbivores and their natural enemies. Consequently, the impact of natural enemies on herbivore vital rates and population dynamics may vary among plant species. This study was designed to investigate the potential for density-dependent parasitism of an aphid herbivore feeding on six different host plant species.
2. Population densities of the aphid Aphis nerii B de F (Homoptera: Aphididae) and its parasitoid Lysiphlebus testaceipes Cresson (Hymenoptera: Braconidae) were recorded within a single growing season on six different species of milkweed in the genus Asclepias L. (Asclepiadaceae). Asclepias species are known to vary in their quality as food for herbivores. Although data on plant quality were not available in this study, population data were analysed to determine the effects of different Asclepias species on rates of parasitism and aphid population growth.
3. Parasitism rates of A. nerii varied among Asclepias species but were temporally density dependent over at least some range of aphid density on all plant species. Aphid population growth rates also varied among Asclepias species, and declined with an increase in the maximum parasitism rates among plant species; however, in no case was density-dependent parasitism sufficient to prevent exponential population growth of aphids within the growing season. The results serve to emphasise that, if natural enemies are to regulate herbivore populations, density-dependent mortality is a necessary, but not sufficient, condition for regulation.     

Selection on offspring size varies within and among families in relation to host nutritional quality

Life history theory often assumes a positive relationship between offspring size and fitness, although the strength and form of this relationship is expected to vary with environmental conditions. In arthropods, surprisingly few studies have examined the influence of larval environment on the offspring size–fitness relation. In phytophagous insects, the few studies that have examined variation in larval host plants have found a negative correlation between host plant nutritional quality and the strength of selection favoring larger offspring size, suggesting that this pattern might be general. I present experimental evidence for such a relationship in a population of the moth Rothschildia lebeau feeding on its three primary host plant species. Unlike previous studies, I consider the effect of offspring size on growth and survival at two levels, both among families and among siblings within families. Neonate caterpillar mass had a significant effect on growth and survival. The effect on growth, however, was weak, resulted primarily from variation among families, and did not differ among host plant diets. The effect on survival was stronger and varied among host plant diets, among families, and within families on different host plants in a manner that was generally consistent with the hypothesized negative correlation between host plant nutritional quality and the strength of selection favoring larger offspring size. Overall, results suggest that the consequences of variation in offspring size for survival within and among families are host plant-dependent in this system.     

Population consequences of constitutive and inducible plant resistance: herbivore spatial spread

Abstract Little attention has been paid to the impact that constitutive and inducible plant resistance traits will have on herbivore spatial dynamics. We investigate mathematical models in which herbivore demographic rates and movement rates respond to host plant quality, which in turn is determined by constitutive and inducible resistance. Models with and without induced resistance yield the same analytic expression for the asymptotic speed at which a herbivore population will spread through an initially uninduced plant population, suggesting that induced resistance will have no effect on the rate of invasion of herbivores that respond to plant resistance on small spatial scales. In contrast, constitutive resistance will influence the speed of an invasion. If herbivore movement is quite sensitive to plant quality, an increase in constitutive resistance can actually accelerate the rate of herbivore spread even while it reduces the herbivore's intrinsic rate of increase. In other scenarios, the rate of invasion attains a maximum at intermediate levels of constitutive resistance. These results argue that our view of plant resistance should be broadened to include herbivore movement if we are to understand fully the implications of differences in resistance for the dynamics of herbivore populations in natural and managed settings.     

Consequences for a host–parasitoid interaction of host-plant aggregation, isolation, and phenology

Abstract.  1. Spatial habitat structure can influence the likelihood of patch colonisation by dispersing individuals, and this likelihood may differ according to trophic position, potentially leading to a refuge from parasitism for hosts.
2. Whether habitat patch size, isolation, and host-plant heterogeneity differentially affected host and parasitoid abundance, and parasitism rates was tested using a tri-trophic thistle–herbivore–parasitoid system.
3.  Cirsium palustre thistles ( n = 240) were transplanted in 24 blocks replicated in two sites, creating a range of habitat patch sizes at increasing distance from a pre-existing source population. Plant architecture and phenological stage were measured for each plant and the numbers of the herbivore Tephritis conura and parasitoid Pteromalus elevatus recorded.
4. Mean herbivore numbers per plant increased with host-plant density per patch, but parasitoid numbers and parasitism rates were unaffected. Patch distance from the source population did not influence insect abundance or parasitism rates. Parasitoid abundance was positively correlated with host insect number, and parasitism rates were negatively density dependent. Host-plant phenological stage was positively correlated with herbivore and parasitoid abundance, and parasitism rates at both patch and host-plant scales.
5. The differential response between herbivore and parasitoid to host-plant density did not lead to a spatial refuge but may have contributed to the observed parasitism rates being negatively density dependent. Heterogeneity in patch quality, mediated by variation in host-plant phenology, was more important than spatial habitat structure for both the herbivore and parasitoid populations, and for parasitism rates.     

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.     

Density dependent population growth of the two-spotted spider mite, Tetranychus urticae, on the host plant Leonurus cardiaca

We observed Tetranychus urticae (Koch), a polyphagous spider mite herbivore, on Leonurus cardiaca (L.) at several sites in eastern North America at variable density, ranging from extremely dense to sparse. To understand the nature of T. urticae 's population dynamics we experimentally manipulated population densities on L. cardiaca and assessed per capita growth after 1 to 2 generations in laboratory and field experiments. In particular, we took a 'bottom-up' approach, manipulating both plant size and quality to examine effects on mite dynamics. Per capita growth was strongly dependent on the initial density of the mite population. Spider mite populations grew (1) in a negatively density dependent manner on small plants and (2) unhindered by density dependence on large plants. Mean per capita growth was 59% higher on small plants compared to large plants, irrespective of mite density. We also found evidence for density dependent induced susceptibility to spider mites in small plants and density dependent induced resistance in large plants. Hence, spider mite populations grew at a relatively fast rate on small plants, and this was associated with negative density dependence due to factors that depress population growth, such as food deterioration or limitation. On large plants, spider mite populations grew at a relatively slow rate, apparently resulting in herbivore densities that may not have been high enough to cause intraspecific competition or other forms of negative density dependence.     

Invasion and persistence of plant parasites in a spatially structured host population

Spatial structure is of central importance in the dynamics of plant-parasite interactions and is imposed by the growth habit and distribution of host plants and by parasite dispersal which is frequently restricted. To investigate the effects of spatial heterogeneity on the dynamics of plant parasites we introduce a simple model for epidemic development within a spatially structured host population. Here the host population is subdivided into a number of patches which are linked to allow for transmission from one patch to another with the connections defining the spatial structure of the host population. Three key parameters are identified that play a critical role in the ability of the parasite to invade and persist within the host population: the within-patch parasite basic reproductive number which characterises the infection dynamics at the local spatial scale; and the neighbourhood of interaction which describes which patches interact with which and the strength of coupling between patches within the neighbourhood which together characterise the spread of the parasite over larger spatial scales. Using both deterministic and stochastic formulations of the model, we investigate how the thresholds and probabilities of invasion and persistence are affected by these parameters, by demographic stochasticity and by differences in the initial level of infection.     

Multiple life stages with multiple replicated density levels are required to estimate density dependence for plants

Negative density dependence resulting from intraspecific competition can regulate plant populations by limiting demographic rates (survival, growth, fecundity). However, the strength of intraspecific competition can vary within and among populations due to spatial or temporal environmental heterogeneity, or genetic differences. Quantification of variation under a relatively constant environment is needed to assess the inherent potential for density dependence to vary. This knowledge will help adjust data collection effort required for parameterisation of density dependence. Our review of published plant demographic studies revealed that only half of the studies included the whole life‐cycle in the analysis of density dependence. Approximately half of the studies manipulated density, while the rest examined density dependence from observed densities in the field. Regardless of the design used, density dependence was estimated from a small number of replicates. To investigate inherent variation in density dependence during the life‐cycle, and the effect of low replication on density dependence estimates, we combined an experimental approach with simulations for an invasive herb Senecio madagascariensis. We found significant negative density dependence for five out of six examined demographic rates in a constant environment, with the strength of density dependence increasing during the life‐cycle. An exception was plant growth, in which the direction of density dependence varied from positive to negative depending on the life stage. Simulations showed substantial deviation for density dependence parameterised from a small number of replicates even when environmental variation was minimal. This suggests that data collection procedures currently used to assess the effect of density on plant demographic rates may produce inaccurate estimates, increasing uncertainty in demographic models. Due to variation in the direction and strength of density dependence during the life‐cycle, multiple life stages with multiple replicated density levels are required to parameterise density dependence for demographic rates.     

Inbreeding alters resistance to insect herbivory and host plant quality in Mimulus guttatus (Scrophulariaceae)

Previous studies have demonstrated genetic variation for resistance to insect herbivores and host plant quality. The effect of plant mating system, an important determinant of the distribution of genetic variation, on host plant characteristics has received almost no attention. This study used a controlled greenhouse experiment to examine the effect of self- and cross-pollination in Mimulus guttatus (Scrophulariaceae) on resistance to and host plant quality for the xylem-feeding spittlebug Philaenus spumarius (Homoptera: Cercopidae). Spittlebugs were found to have a negative effect on two important fitness components in M. guttatus, flower production and above ground biomass. One of two M. guttatus populations examined showed a significant interaction between the pollination and herbivore treatments. In this case, the detrimental effects of herbivores on biomass and flower production were much more pronounced in inbred (self) plants. The presence of spittlebug nymphs increased inbreeding depression by as much as three times. Pollination treatments also had significant effects on important components of herbivore fitness, but these effects were in opposite directions in our two host plant populations. Spittlebug nymphs maturing on self plants emerged as significantly larger adults in one of our host plant populations, indicating that inbreeding increased host plant quality. In our second host plant population, spittlebug nymphs took significantly longer to develop to adulthood on self plants, indicating that inbreeding decreased host plant quality. Taken together these results suggest that the degree of inbreeding in host plant populations can have important and perhaps complex effects on the dynamics of plant-herbivore interactions and on mating-system evolution in the host.     

Community heterogeneity and the evolution of interactions between plants and insect herbivores

Plant communities vary tremendously in terms of productivity, species diversity, and genetic diversity within species. This vegetation heterogeneity can impact both the likelihood and strength of interactions between plants and insect herbivores. Because altering plant-herbivore interactions will likely impact the fitness of both partners, these ecological effects also have evolutionary consequences. We review several hypothesized and well-documented mechanisms whereby variation in the plant community alters the plant-herbivore interaction, discuss potential evolutionary outcomes of each of these ecological effects, and conclude by highlighting several avenues for future research. The underlying theme of this review is that the neighborhood of plants is an important determinant of insect attack, and this results in feedback effects on the plant community. Because plants exert selection on herbivore traits and, reciprocally, herbivores exert selection on plant-defense traits, variation in the plant community likely contributes to spatial and temporal variation in both plant and insect traits, which could influence macroevolutionary patterns.     

Travel costs, oviposition behaviour and the dynamics of insect–plant systems

Insect attack can have major consequences for plant population dynamics. We used individually based simulation models to ask how insect oviposition behaviour influences persistence and potential stability of an herbivore–plant system. We emphasised effects on system dynamics of herbivore travel costs and of two kinds of behaviour that might evolve to mitigate travel costs: insect clutch size behaviour (whether eggs are laid singly or in groups) and female aggregation behaviour (whether females prefer or avoid plants already bearing eggs). Travel costs that increase as plant populations drop lead to inverse density dependence of plant reproduction under herbivore attack. Female clutch size and aggregation behaviours also strongly affect system dynamics. When females lay eggs in large clutches or aggregate their clutches, herbivore damage varies strongly among plants, providing probabilistic refuges that permit plant reproduction and persistence. However, the population dynamics depend strongly on whether insect behaviour is fixed or responds adaptively to plant population size: when (and only when) females increase clutch size or aggregation as plants become rare, refuges from herbivory weaken at high plant density, creating inverse density dependence in plant reproduction. Both herbivore travel costs themselves, and also insect behaviour that might evolve in response to travel costs, can thus create plant density dependence—a basic requirement for regulation of plant populations by their insect herbivores.