Peter A. Hambäck

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.

ASSOCIATIONAL RESISTANCE: INSECT DAMAGE TO PURPLE LOOSESTRIFE REDUCED IN THICKETS OF SWEET GALE

Associational resistance occurs when herbivore damage to a focal plant is reduced by the presence of other plant species. Neighboring plants can reduce herbivore damage (1) by their effects on the predator community, (2) by reducing the ability of herbivores to find their host plants, and (3) by reducing the time herbivores remain on their host plants. We examined how the presence of the aromatic low shrub Myrica gale and of predatory lady beetles affected herbivore damage and reproductive output in a population of the perennial herb Lythrum salicaria in northern Sweden. An observational study showed that L. salicaria growing in Myrica thickets were less damaged by herbivores, had a lower abundance of the monophagous, leaf-feeding, chrysomelid beetle Galerucella calmariensis, and had higher flower and seed production than L. salicaria outside Myrica thickets. To test whether these differences could be explained by (a) differences in some aspect of plant quality, or (b) differences in predator abundance, we placed potted L. salicaria within and outside Myrica thickets. To determine whether differences in the abundance of G. calmariensis were primarily the result of different rates of colonization or emigration, we marked adult beetles and placed them on a second set of potted plants in the two microhabitats. The results show that differences in herbivore abundance, plant damage, and reproductive output between potted L. salicaria placed within and outside Myrica thickets were in the same direction and of the same magnitude as those observed for naturally occurring plants, indicating that the observed patterns were not an effect of differences in the chemical composition of the host plant. Moreover, we found no support for the hypothesis that a higher abundance of insect predators could explain the lower abundance of G. calmariensis on L. salicaria in Myrica thickets. On the contrary, lady beetles (Coccinella quinqempunctata and Coccinella septempunctata) were observed on a greater proportion of the plants placed outside the Myrica thickets. The monitoring of marked beetles indicated that differences in the abundance of G. calmariensis were the result of a markedly higher colonization rate and a somewhat lower emigration rate from L. salicaria outside Myrica thickets. Outside the Myrica thickets, the survival of G. calmariensis and the magnitude of herbivore damage were lower, and fruit and seed output were higher on plants with observations of lady beetles than on plants without lady beetles. The results indicate that the abundance of the specialist herbivore G. calmariensis, and the herbivore damage and reproductive output of its host plant, L. salicaria, are affected both by the presence of the nonhost Myrica and by predation from lady beetles. We suggest that the most likely mechanism causing decreased feeding on L. salicaria growing in Myrica thickets is that Myrica affects the ability of G. calmariensis to find its host, either through visual or olfactory interference.

A CONCEPTUAL FRAMEWORK FOR ASSOCIATIONAL EFFECTS: WHEN DO NEIGHBORS MATTER AND HOW WOULD WE KNOW?

Interactions between individual consumer and resource organisms can be modified by neighbors, e.g., when herbivory depends on the identity or diversity of neighboring plants. Effects of neighbors on consumer-resource interactions (“associational effects”) occur in many systems, including plant-herbivore interactions, predator-prey interactions (mimicry), and plant-pollinator interactions. Unfortunately, we know little about how ecologically or evolutionarily important these effects are because we lack appropriate models and data to determine how neighbor effects on individuals contribute to net interactions at population and community levels. Here we supply a general definition of associational effects, review relevant theory, and suggest strategies for future theoretical and empirical work. We find that mathematical models from a variety of fields suggest that individual-level associational effects will influence population and community dynamics when associational effects create local frequency dependence. However, there is little data on how local frequency dependence in associational effects is generated, or on the form or spatial scale of that frequency dependence. Similarly, existing theory lacks consideration of nonlinear and spatially explicit frequency dependence. We outline an experimental approach for producing data that can be related to models to advance our understanding of how associational effects contribute to population and community processes.

Effects of plant neighborhoods on plant–herbivore interactions: resource dilution and associational effects

Effects of neighboring plants on herbivore damage to a focal plant (associational effects) have been documented in many systems and can lead to either increased or decreased herbivore attack. Mechanistic models that explain the observed variety of herbivore responses to local plant community composition have, however, been lacking. We present a model of herbivore responses to patches that consist of two plant types, where herbivore densities on a focal plant are determined by a combination of patch-finding, within-patch redistribution, and patch-leaving. Our analyses show that the effect of plant neighborhood on herbivores depends both on how plant and herbivore traits combine to affect herbivore movement and on how experimental designs reveal the effects of plant density and plant relative frequency. Associational susceptibility should be the dominant pattern when herbivores have biased landing rates within patches. Other behavioral decision rules lead to mixed responses, but a common pattern is that in mixed patches, one plant type experiences associational resistance while the other plant experiences associational susceptibility. In some cases, the associational effect may shift sign along a gradient of plant frequency, suggesting that future empirical studies should include more than two plant frequencies to detect nonlinearities. Finally, we find that associational susceptibility should be commonly observed in experiments using replacement designs, whereas associational resistance will be the dominant pattern when using additive designs. Consequently, outcomes from one experimental design cannot be directly compared to studies with other designs. Our model can also be translated to other systems with foragers searching for multiple resource types.

Habitat specialization, body size, and family identity explain lepidopteran density–area relationships in a cross-continental comparison

Habitat fragmentation may strongly affect species density, species interactions, and the rate of ecosystem processes. It is therefore important to understand the observed variability among species responses to fragmentation and the underlying mechanisms. In this study, we compare density–area relationships (DARs) for 344 lepidopteran species belonging to 22 families (butterflies and moths). This analysis suggested that the DARslope is generally positive for moths and negative for butterflies. The differences are suggested to occur because moths are largely olfactory searchers, whereas most butterflies are visual searchers. The analysis also suggests that DARs vary as a function of habitat specialization and body size. In butterflies, generalist species had a more negative DARslope than specialist species because of a lower patch size threshold. In moths, the differences in DARslope between forest and open habitat species were large for small species but absent for large species. This difference is argued to occur because the DARslope in large species mainly reflects their search mode, which does not necessarily vary between moth groups, whereas the slope in small species reflects population growth rates.

Population Fluctuations of Voles in North Fennoscandian Tundra: Contrasting Dynamics in Adjacent Areas with Different Habitat Composition

During 1991-1996. we studied population fluctuations of microtine rodents (primarily Clethrionomys rufocanus). of their winter food plants, and of their predators in a low arctic habitat complex, dominated by unproductive lichen dwarf-birch tundra. More productive habitats occurred patchwise throughout the landscape. On a south-facing slope, productive scrubland habitats prevailed, and luxuriant habitats were locally abundant. Our main method was live-trapping on 14 grids, representing typical lowland tundra (5 replicates), the productive slope (4 replicates) and barren high-altitude tundra (5 replicates). Within the slope vole populations were cyclic. In the lowland tundra. vole fluctuations were primarily seasonal, but the vole erash on the productive slope coincided with a phase of relatively low vole densities in the lowland. The highland was characterised by low vole densities. During the phase of rapid population growth, long-range dispersal occurred within the slope and from the slope to surrounding areas. Moreover, small mustelids which had initially been present only on the slope, started to move elsewhere, along natural dispersal corridors. Shoot mortalities of the main winter food plant. Vaccinium myrtillus. remained low. The observed scenario is consistent with the hypothesis that vole cycles represent a mustelid-microtine limit cycle, because cycles created by this mechanism should disappear when the productive habitats, capable of supporting resident predators, become fragmented and embedded in a vast unsuitable area.

Detritivory: stoichiometry of a neglected trophic level

Previous syntheses have identified the key roles that phylogeny, body size, and trophic level play in determining arthropod stoichiometry. To date, however, detritivores have been largely omitted from such syntheses, despite their importance in nutrient cycling, biodiversity, and food web interactions. Here, we report on a compiled database of the allometry and nutritional stoichiometry (N and P) of detritivorous arthropods. Overall, both N and P content for detritivores varied among major phylogenetic lineages. Detritivore N content was similar to the N content of herbivores, but below that of predators. By contrast, detritivore P content was independent of trophic level. Contrary to previous reports, neither nutrient varied with body size. This analysis places detritivores in the context of related herbivores and predators, and as such, sets the stage for future investigations into the causes and consequences of elemental (mis)matches between detritivores and their detrital resources.

The Impact of Cormorants on Plant–Arthropod Food Webs on Their Nesting Islands

This study investigated the effects of cormorant colonies on plant–arthropod island food webs, the consequences of nutrient-rich runoff on marine communities, and feedback loops from marine to terrestrial ecosystems. Terrestrial plant responses were as expected, with the highest plant biomass on islands with low nest density and the highest nitrogen (N) content on islands with high nest density. In contrast to our hypothesis, we found no uniform density response across guilds. Among herbivores, the variable responses may depend on the relative importance of plant quality or quantity. As expected, nutrient-rich runoff entered water bodies surrounding cormorant nesting islands, but only at high nest density, and increased the density of emerging insects. This created a potential feed-back loop to spiders (major terrestrial predators), where stable isotope analyses suggested great use of chironomids. Contrary to our expectation, this potential feed-back did not result in the highest spider density on islands with a high cormorant nest density. Web spiders showed no changes in density on active cormorant islands, and lycosids were actually less abundant on active cormorant islands compared to reference islands. The variable response of spiders despite increased dipteran densities, and also in other consumer groups, may be due to direct negative effects of cormorants on soil chemistry, vegetation cover, and other density regulating forces (for example, top–down forces) not studied here. This study highlights the importance of including processes in the surrounding marine ecosystem to understand the impacts of seabirds on the food web structures of their nesting islands.

Linking Land and Sea: Different Pathways for Marine Subsidies

Nutrients and energy derived from marine autotrophs subsidize shore ecosystems, increasing productivity and affecting food web dynamics and structure. In this study we examined how the inland reach of such inflow effects depends on vectors carrying the marine inflow inland and on landscape structure. We used stable isotopes of carbon and nitrogen to examine the roles of arthropod vectors in carrying marine-derived nutrients inland in two very different shore ecosystems: shore meadows in Sweden with marine inflows of algae and emerging chironomid midges; and sandy beaches and shore dunes in south-western Australia with marine inflows of algae and seagrass. In a colonization experiment, we found that deposited wrack on the beach is quickly colonized by both grazers and predators. However, in both systems we found a larger inland reach of the marine subsidy than could be accounted for by deposited macrophytes on shores alone, and that dipterans and spiders potentially functioned as vectors for the inflow. Our results indicate that marine inflows are important for near-shore terrestrial ecosystems well above the water’s edge, and that this effect is largely due to arthropod vectors (mainly dipterans and spiders) in both low-productivity sandy beach ecosystems at the Indian Ocean coast of Australia, and more productive shore meadows on the Baltic Sea coast of Sweden. Our findings also suggest that the type of vector transporting marine material inland may be as important as the productivity contrast between ecosystems for explaining the degree of marine influence on the terrestrial system.

Mechanisms of apparent competition in seasonal environments : an example with vole herbivory

Mechanisms of apparent competition in seasonal environments: an example with vole herbivory