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.     

Effects of partitioning allochthonous and autochthonous resources on food web stability

The flux of energetic and nutrient resources across habitat boundaries can exert major impacts on the dynamics of the recipient food web. Competition for these resources can be a key factor structuring many ecological communities. Competition theory suggests that competing species should exhibit some partitioning to minimize competitive interactions. Species should partition both in situ (autochthonous) resources and (allochthonous) resources that enter the food web from outside sources. Allochthonous resources are important sources of energy and nutrients in many low productivity systems and can significantly influence community structure. The focus of this paper is on: (i) the influence of resource partitioning on food web stability, but concurrently we examine the compound effects of; (ii) the trophic level(s) that has access to allochthonous resources; (iii) the amount of allochthonous resource input; and (iv) the strength of the consumer–resource interactions. We start with a three trophic level food chain model (resource–consumer–predator) and separate the higher two trophic levels into two trophospecies. In the model, allochthonous resources are either one type available to both consumers and predators or two distinct types, one for consumers and one for predators. The feeding preferences of the consumer and predator trophospecies were varied so that they could either be generalists or specialists on allochthonous and/or autochthonous resources. The degree of specialization influenced system persistence by altering the structure and, therefore, the indirect effects of the food web. With regard to the trophic level(s) that has access to allochthonous resources, we found that a single allochthonous resource available to both consumers and predators is more unstable than two allochthonous resources. The results demonstrate that species populating food webs that experience low to moderate allochthonous resources are more persistent. The results also support the notion that strong links destabilize food web dynamics, but that weak to moderate strength links stabilize food web dynamics. These results are consistent with the idea that the particular structure, resource availability, and relative strength of links of food webs (such as degree of specialization) can influence the stability of communities. Given that allochthonous resources are important resources in many ecosystems, we argue that the influence of such resources on species and community persistence needs to be examined more thoroughly to provide a clearer understanding of food web dynamics.     

Scale-dependent foraging and patch choice in fractal environments

Many spatially complex environments are fractal, and consumers in these environments face scale-dependent trade-offs between encountering high densities of small resource patches versus low densities of large resource patches. I address the effects of these trade-offs on foraging by incorporating scale-dependent encounter of resources in fractal landscapes into classical optimal foraging theory. This model is then used to predict optimal scales of perception (foraging scale) and patch choice in response to spatial features of landscapes. The model predicts that, for a given density of resources, landscapes with greater extent and fractal dimension and that contain patchy (low fractal dimension) resources favour large foraging scales and specialization on a small proportion of resource patches. Fragmented (low fractal dimension) landscapes of small extent with dispersed (high fractal dimension) resources favour smaller foraging scales and generalists that use a large proportion of available resource patches. These predictions synthesize the results of other spatially explicit consumer–resource models into a simple framework and agree reasonably well with results of several empirical studies. This study thus places optimal foraging theory in a spatial context and suggests evolutionary mechanisms of consumers' responses to important spatial phenomena (e.g. habitat fragmentation, resource aggregation). This revised version was published online in July 2006 with corrections to the Cover Date.     

Signal verification can promote reliable signalling

The central question in communication theory is whether communication is reliable, and if so, which mechanisms select for reliability. The primary approach in the past has been to attribute reliability to strategic costs associated with signalling as predicted by the handicap principle. Yet, reliability can arise through other mechanisms, such as signal verification; but the theoretical understanding of such mechanisms has received relatively little attention. Here, we model whether verification can lead to reliability in repeated interactions that typically characterize mutualisms. Specifically, we model whether fruit consumers that discriminate among poor- and good-quality fruits within a population can select for reliable fruit signals. In our model, plants either signal or they do not; costs associated with signalling are fixed and independent of plant quality. We find parameter combinations where discriminating fruit consumers can select for signal reliability by abandoning unprofitable plants more quickly. This self-serving behaviour imposes costs upon plants as a by-product, rendering it unprofitable for unrewarding plants to signal. Thus, strategic costs to signalling are not a prerequisite for reliable communication. We expect verification to more generally explain signal reliability in repeated consumer–resource interactions that typify mutualisms but also in antagonistic interactions such as mimicry and aposematism.     

Body size and species coexistence in consumer–resource interactions: A comparison of two alternative theoretical frameworks

Species coexistence involving trophic interactions has been investigated under two theoretical frameworks—partitioning shared resources and accessing exclusive resources. The influence of body size on coexistence is well studied under the exclusive resources framework, but has received less attention under the shared-resources framework. We investigate body-size-dependent allometric extensions of a classical MacArthur-type model where two consumers compete for two shared resources. The equilibrium coexistence criteria are compared against the general predictions of the alternative framework over exclusive resources. From the asymmetry in body size allometry of resource encounter versus demand our model shows, counterintuitively, and contrary to the exclusive resource framework, that a smaller consumer should be competitively superior across a wide range of supplies of the two resource types. Experimental studies are reviewed to resolve this difference among the two frameworks that arise from their respective assumptions over resource distribution. Another prediction is that the smaller consumer may have relatively stronger control over equilibrium resource abundance, and the loss of smaller consumers from a community may induce relatively stronger trophic cascades. Finally, from satiating consumers’ functional response, our model predicts that greater difference among resource sizes can allow a broader range of consumer body sizes to coexist, and this is consistent with the predictions of the alternative framework over exclusive resources. Overall, this analysis provides an objective comparison of the two alternative approaches to understand species coexistence that have heretofore developed in relative isolation. It advances classical consumer–resource theory to show how body size can be an important factor in resource competition and coexistence.     

On the influence of food quality in consumer–resource interactions

While nutrients are an important regulating factor in food webs, no theoretical studies have examined limits to consumer growth imposed by nutrient concentrations (i.e. food quality) of their prey. Empirical studies have suggested that nutrients may play a role in limiting assimilation efficiencies of herbivores. Using a simple food chain model, I find that prey nutrient concentration does directly influence the growth rate of consumers and potentially increase the stability of consumer–resource interactions. This suggests that the strength of trophic cascades and the relative importance of top–down versus bottom–up control in food webs is significantly influenced by nutrient availability in food resources of consumers. Additionally, the results imply that increases in resource input may cause a change in which resource is limiting and thereby negate any potential "paradox of enrichment".     

Emergence of spatially structured populations by area‐concentrated search

The idea that populations are spatially structured has become a very powerful concept in ecology, raising interest in many research areas. However, despite dispersal being a core component of the concept, it typically does not consider the movement behavior underlying any dispersal. Using individual‐based simulations in continuous space, we explored the emergence of a spatially structured population in landscapes with spatially heterogeneous resource distribution and with organisms following simple area‐concentrated search (ACS); individuals do not, however, perceive or respond to any habitat attributes per se but only to their foraging success. We investigated the effects of different resource clustering pattern in landscapes (single large cluster vs. many small clusters) and different resource density on the spatial structure of populations and movement between resource clusters of individuals. As results, we found that foraging success increased with increasing resource density and decreasing number of resource clusters. In a wide parameter space, the system exhibited attributes of a spatially structured populations with individuals concentrated in areas of high resource density, searching within areas of resources, and “dispersing” in straight line between resource patches. “Emigration” was more likely from patches that were small or of low quality (low resource density), but we observed an interaction effect between these two parameters. With the ACS implemented, individuals tended to move deeper into a resource cluster in scenarios with moderate resource density than in scenarios with high resource density. “Looping” from patches was more likely if patches were large and of high quality. Our simulations demonstrate that spatial structure in populations may emerge if critical resources are heterogeneously distributed and if individuals follow simple movement rules (such as ACS). Neither the perception of habitat nor an explicit decision to emigrate from a patch on the side of acting individuals is necessary for the emergence of such spatial structure.     

Measuring changes in consumer resource availability to riverine pulsing in Breton Sound, Louisiana, USA

Resource pulses are thought to structure communities and food webs through the assembly of consumers. Aggregated consumers represent a high quality resource subsidy that becomes available for trophic transfer during and after the pulse. In estuarine systems, riverine flood pulses deliver large quantities of basal resources and make high quality habitat available for exploitation by consumers. These consumers represent a change in resources that may be available for trophic transfer. We quantified this increased consumer resource availability (nekton density, biomass, energy density) provided by riverine flood pulsing in Breton Sound, Louisiana, USA. We used water level differences between an area subject to two experimental riverine flood pulses (inflow) and a reference area not receiving inflow to identify the percentage of nekton standing stock and energy density that may be attributable solely to riverine pulsing and may represent a consumer resource subsidy. Riverine pulsing accounted for more than 60% of resident nekton density (ind m(-2)), biomass (g m(-2)), and energy density (cal m(-2)) on the flooded marsh surface during two experimental pulse events in 2005. Our results document the potential subsidy of resident nekton standing stock from a riverine flood pulse available for export to subtidal habitats. Given predicted large scale changes in river discharge globally, this approach could provide a useful tool for quantifying the effects of changes in riverine discharge on consumer resource availability.     

Intraguild predation with spatially structured interactions

Consumer–resource interactions with intraguild predation (IGP) were studied in a spatial setting (i.e., predators catch prey and individuals reproduce within local neighborhoods only). Pair approximation (a method for deriving ordinary differential equations that approximate the dynamics of a community that interacts in a lattice environment) was used to study the effect of spatially structured species interactions. An individual-based computer simulation was used to extend the study to a case with spatially variable resource densities. The qualitative results of the pair approximation model were similar to those of the corresponding non-spatial model. However, the spatial model predicted coex((istence over a wider range of parameters than the non-spatial model when intraguild prey are nutritionally valuable to intraguild predators. Spatially heterogeneous resource distributions and spatially structured interaction could overturn the qualitative predictions of non-spatial models.     

Mantled Howler (<Emphasis Type="Italic">Alouatta palliata</Emphasis>) Arboreal Pathway Networks: Relative Impacts of Resource Availability and Forest Structure

Numerous studies have concluded that primates move about their environments in a nonrandom manner, frequently traveling between consecutive foraging sites along relatively straight-line paths. However, primates do not always take the most direct path between resources, and a number of species have been observed to travel repeatedly along a network of the same arboreal pathways. In this study, I used spatially explicit techniques to examine quantitatively what mantled howler monkey groups on Barro Colorado Island, Panama, accomplish by selecting nonlinear paths between resources and by repeatedly using the same paths within an arboreal network. Results show that chosen arboreal paths between sites where foraging occurred have higher levels of resource availability and canopy connectivity than comparable straight-line paths between the same sites. When comparing the relative importance of these factors, autologistic models of pathway choice indicate that though canopy connectivity is related to the location of repeatedly used arboreal pathway networks, the most statistically significant predictor is resource availability (both on a path and within a visual detection distance of a path). These results provide support for the hypothesis that repeated use of arboreal pathway networks aids in resource monitoring and acquisition. In addition, statistical models developed from 1 primary focal group’s travel patterns had high predictive value when employed to generate likely locations for arboreal pathways in the home ranges of 3 neighboring groups. This finding has important implications for studies of primate habitat use and seed dispersal, as it suggests that different groups consistently use similar characteristics when deciding on travel paths.     

Metaphysiological and evolutionary dynamics of populations exploiting constant and interactive resources:R—K selection revisited

Summary I begin by reviewing the derivation of continuous logistic growth and dynamic consumer—resource interaction equations in terms of specific resource extraction and biomass conversion functions that are considered to hold at a population level. Evolutionary stable strategy (ESS) methods are discussed for analysing populations modelled by these equations. The question of selection trade-offs is then considered, particularly in the context of populations being efficient at extracting resources versus converting resources to their own biomass. Questions relating to single populations with high versus low conversion rates and interacting populations with high versus low self-interference rates are also considered. The models discussed here demonstrate conclusively that self-interference is an essential part of any consumption process: without it population growth and interaction processes do not make any sense. The analysis clarifies concepts relating to the somewhat discredited notion ofr—K selection.     

Opposing organizing forces of deposit-feeding marine communities

We contend that a range of phenomena characterizing temperate deposit-feeding communities in low-energy environments is strongly organized by two principal opposing forces: (1) spatially localized inputs of detritus or new recruits, leading to a mosaic of initial patches, with subsequent impacts on spatio-temporal variation of species with limited mobility; and (2) the impact of mobile consumers, which move to spatially localized resources and thereby exert major controls over comparatively larger spatial scales. Surface deposit feeders react differently from deep feeders, in terms of spatio-temporal population change. The two opposing community control forces, combined with responses of deposit feeder functional groups, have potentially different effects on community structure. Mobile consumers, often acting as keystone species, may move to localized patches created by the bottom-up force of food input or by localized recruitment of prey. Their mobility, combined with predicted optimal foraging behavior, would usually produce a spatially homogenizing force, leading to reduced spatial variation in community composition. By contrast, spatially localized inputs of resources, if dominant, would always lead to strong spatial heterogeneity. Dominance of complex space–time variation in detrital enrichment would lead to strong spatio-temporal complexity in macrofauna if the response of recruiting larvae and rapidly growing small invertebrate populations was immediate and keyed to localized food input. The ability of mobile consumers to locate detritus, combined with the spatial distribution and overall input rate of detritus, should determine the balance of surface and deep-feeding deposit feeders. The opposing force approach can be applied to communities generally.     

The roles of history: age and prior exploitation in aquatic container habitats have immediate and carry‐over effects on mosquito life history

1. Per‐capita resource availability in aquatic habitats is influenced directly by consumer density via resource competition and indirectly via delayed resource competition when temporally non‐overlapping cohorts of larvae exploit the same resources. In detritus‐based systems, resources are likely to be influenced by the age of the aquatic habitat, as detritus changes in quality over time and may be replenished by new inputs. 2. For aquatic insects that exploit detritus‐based habitats, feeding conditions experienced during immature stages can influence fitness directly via effects on development and survivorship, but also indirectly by influencing adult traits such as fecundity and longevity. 3. Larval habitat age and prior resource exploitation were manipulated in a field experiment using the container mosquito Aedes triseriatus. 4. It was found that A. triseriatus from older habitats had greater larval survival, faster development and greater adult longevity. Exploitation of larval habitats by a prior cohort of larvae had a significant negative effect on subsequent cohorts of larvae by delaying development. 5. It is suggested that extended conditioning of detritus probably resulted in conversion of recalcitrant resources to more available forms which improved the quality of the habitat. 6. In a parallel study, evidence was found of carry‐over effects of habitat age and prior exploitation on adult longevity for A. triseriatus and Aedes japonicus collected from unmanipulated aquatic habitats. 7. These results indicate the importance of detritus dynamics and the discontinuous nature of resource competition in these mosquito‐dominated aquatic systems.     

Consumer–resource matching in a food chain when both predators and prey are free to move

The classical theory of the ideal free distribution (IFD) predicts that the spatial distribution of consumers should follow the distribution of the resources they depend on. Here, we study consumer–resource matching in a community context. Our model for the community is a food chain with three levels. We study whether the primary consumers are able to match resources both under predation risk and in its absence. Both prey and predators have varying degrees of knowledge of the global and local resource distribution. We present two versions of the model. In the "resource maximising" model, the consumers consider the availability of their resource only. In the "balancing" model, individual consumers minimise predation risk per unit of resource that they can gain access to. We show that both models can lead to perfect matching of consumers on resources and predators on consumers, assuming that individuals have full knowledge of the whole environment. However, when the consumers' information and freedom of movement are greater than those of the predators, then the predators generally undermatch the consumers. In the opposite case, we observe overmatching and high consumer movement rates. Furthermore, undermatching of predators on consumers tends to induce overmatching of consumers on resources.     

Available nitrogen: A time-based study of manipulated resource islands

Spatial and temporal heterogeneity of available nitrogen are critical determinants of the distribution and abundance of plants and animals in ecosystems. Evidence for the resource island theory suggests that soils below tree and shrub canopies contain higher amounts of resources, including available nitrogen, than are present in interspace areas. Disturbances, such as prescribed fire and tree removal, are common management practices in shrub-woodland ecosystems, but it is not known if these practices affect resource islands. We examined temporal variation in resource islands of available nitrogen and their retention after fire and woody plant removal. From August 1997 to October 1998, soil nitrate (NO₃^–) and ammonium (NH₄⁺) were measured monthly from canopy and interspace plots within four juniper-sagebrush sites along a precipitation gradient in central Oregon, USA. At each site, soil samples were collected from untreated plots, plots in which woody plants were removed, and those treated with prescribed fire in fall 1997. In burned treatments, canopy concentrations were significantly higher than interspace concentrations throughout the measurement period. Canopy NO₃^– and NH₄⁺ concentrations were significantly higher on burned vs. unburned treatments for four months after fire. After woody plant removal, NO₃^– and NH₄⁺ concentrations did not differ from the controls. Untreated control areas had higher NO₃^– and NH₄⁺ concentrations under juniper canopies for nearly all months. Wetter sites had smaller differences between canopy and interspace concentrations through time than did the two drier sites. In relation to NO₃^– and NH₄⁺ in this ecosystem, resource islands appear to be more ephemeral in wetter sites, and more pronounced following fire disturbances than in controls or those treated by woody plant removal.     

Plasticity in R/S ratio, morphology and fitness-related traits in response to reciprocal patchiness of light and nutrients in the stoloniferous herb, Glechoma longituba L

Clonal fragments of the stoloniferous herb Glechoma longituba were subjected to a complementary patchiness of light and soil nutrients including two spatially homogeneous treatments (SR–SR and IP–IP) and two spatially heterogeneous treatments (IP–SR and SR–IP). SR and IP indicate patches (shaded, rich) with low light intensity (shaded, S), high nutrient availability (rich, R) and patches (illuminated, poor) with high light intensity (illuminated, I) and low nutrient availability (poor, P), respectively. Plasticity of the species in root–shoot ratio, fitness-related traits (biomass, number of ramets and dry weight per ramet) and clonal morphological traits (length and specific length of stolon internodes, area and specific area of laminae, length and specific length of petioles) were experimentally examined. The aim is to understand adaptation of G. longituba to the environment with reciprocal patches of light and soil nutrients by plasticities both in root–shoot ratio and in (clonal) morphology. Our experiment revealed performance of the clonal fragments growing from patches with high light intensity and low soil nutrient availability into the adjacent opposite patches was increased in terms of the fitness-related characters. R/S ratio and clonal morphology were plastic. Meanwhile, the capture of light resource from the light-rich patches was enhanced while the capture of soil nutrients from either the nutrient-rich or the nutrient-poor patches was not. Analysis of cost and benefit disclosed positive effects of clonal integration on biomass production of ramets in the patches with low light intensity and high soil nutrient availability. These results suggest an existence of reciprocal translocation of assimilates and nutrients between the interconnected ramets. The reinforced performance of the clonal fragments seems to be related with specialization of clonal morphology in the species.     

Effects of nitrogen supply and elevated carbon dioxide on construction cost in leaves of Pinus taeda (L.) seedlings

Seedlings of loblolly pine (Pinus taeda L.) were grown under varying conditions of soil nitrogen and atmospheric carbon dioxide availability to investigate the interactive effects of these resources on the energetic requirements for leaf growth. Increasing the ambient CO₂ partial pressure from 35 to 65 Pa increased seedling growth only when soil nitrogen was high. Biomass increased by 55% and photosynthesis increased by 13% after 100 days of CO₂ enrichment. Leaves from seedlings grown in high soil nitrogen were 7.0% more expensive on a g glucose g^–1 dry mass basis to produce than those grown in low nitrogen, while elevated CO₂ decreased leaf cost by 3.5%. Nitrogen and CO₂ availability had an interactive effect on leaf construction cost expressed on an area basis, reflecting source-sink interactions. When both resources were abundant, leaf construction cost on an area basis was relatively high (81.8±3.0 g glucose m^–2) compared to leaves from high nitrogen, low CO₂ seedlings (56.3±3.0 g glucose m^–2) and low nitrogen, low CO₂ seedlings (67.1±2.7 g glucose m^–2). Leaf construction cost appears to respond to alterations in the utilization of photoassimilates mediated by resource availability.     

Network analyses reveal the role of large snakes in connecting feeding guilds in a species‐rich Amazonian snake community

In ecological communities, interactions between consumers and resources lead to the emergence of ecological networks and a fundamental problem to solve is to understand which factors shape network structure. Empirical and theoretical studies on ecological networks suggest predator body size is a key factor structuring patterns of interaction. Because larger predators consume a wider resource range, including the prey consumed by smaller predators, we hypothesized that variation in body size favors the rise of nestedness. In contrast, if resource consumption requires specific adaptations, predators are expected to consume distinct sets of resources, thus favoring modularity. We investigate these predictions by characterizing the trophic network of a species‐rich Amazonian snake community (62 species). Our results revealed an intricate network pattern resulting from larger species feeding on higher diversity of prey and therefore promoting nestedness, whereas snakes with specific lifestyles and feeding on distinct resources, promoting modularity. Species removal simulations indicated that the nested structure is favored mainly by the presence of five species of the family Boidae, which because of their body size and generalist lifestyles connect modules in the network. Our study highlights the particular ways traits affect the structure of interactions among consumers and resources at the community level.     

Resource-use-related traits correlate with population turnover rates, but not stem diameter growth rates, in 29 subtropical montane tree species

The relationships between species’ functional traits and their demographic life histories are central to understanding the causes of life-history diversity. A previous study identified three independent demographic axes amongst 29 broadleaved tree species: a light-demand axis, a population turnover rate (r–K) axis, and one discriminating substrate requirements for recruitment. This study evaluates the basis of life-history variation amongst the 29 species by assessing the correlation between the three demographic axes above and 14 morphological, phenological, architectural and biomass-partitioning traits. A principal components analysis of the 14 traits revealed two main axes: (1) a ‘resource capture versus conservation’ axis separated species with large and thin leaf laminas, high leaf K, P and N concentrations, light wood and small seeds from species with opposite attributes, and (2) a ‘physiognomic’ axis separated species with compound leaves, high leaf/above-ground mass ratio, and tall first branch in saplings from species with opposite attributes. Subsequent paired correlations and a Procrustes superimposition analysis showed that species with attributes typical of high capture and low conservation of resources, small seeds and short stature had faster population turnover rates (short longevity, and high mortality and recruitment rates) than species with opposite attributes. Species with compound leaves, high leaf/above-ground mass ratio, and tall first branch as saplings (physiognomic axis) tended to be more light-demanding and to have fast diameter growth rates of stems 10 cm diameter. The independence between attributes typical of resource capture or conservation and stem diameter growth rate is noteworthy; it differs from correlations often reported for saplings and could be attributed to ontogenetic changes in plant function. In addition, the clear link between attributes typical of resource capture or conservation and plant recruitment, survivorship and longevity is consistent with r–K theory and brings to light an important connection between a leading axis of plant evolutionary diversification (resource capture versus conservation) and rates of population turnover.