Consequences of adaptive foraging in diverse communities

1.  Selective pressures acting on foraging activities constrain the strength of interaction, hence the stability and energetic availability in food webs.
2.  Because such selective pressures are usually measured at the individual level and because most experimental and theoretical works focus on simple settings, linking adaptive foraging with community scale patterns is still a far stretch.
3.  Some recent models incorporate foraging adaptation in diverse communities. The models vary in the way they incorporate adaptation, via evolutionary or behavioural changes, and define individual fitness in various ways.
4.  In spite of these differences, some general results linking adaptation to community structure and functioning emerge. In the present article, I introduce these different models and highlight their common results.
5.  Adaptive foraging provides stability to large food web models and predicts successfully interaction patterns within food webs as well as other topological features such as food chain length.
6.  The relationships between adaptive foraging and other structuring factors particularly depend on how well connected the local community is with surrounding communities (metacommunity aspect).     

Weaving animal temperament into food webs: implications for biodiversity

Recent studies into community level dynamics are revealing processes and patterns that underpin the biodiversity and complexity of natural ecosystems. Theoretical food webs have suggested that species‐rich and highly complex communities are inherently unstable, but incorporating certain characteristics of empirical communities, such as allometric body size scaling and non‐random interaction distributions, have been shown to enhance stability and facilitate species coexistence. Incorporating individual level traits and variability into food web theory is seen as a future pathway for this research and our growing knowledge of individual behaviours, in the form of temperament (or personality) traits, can inform the direction of this research. Temperament traits are consistent differences in behaviour between individuals, which are repeatable across time and/or across ecological contexts, such as aggressive or boldness behaviours that commonly differ between individuals of the same species. These traits, under the framework of behavioural reaction norms, show both individual consistency as well as contextual and phenotypic plasticity. This is likely to contribute significantly to the effects of individual trait variability and adaptive trophic behaviour on the structure and dynamics of food webs, which are apparently stabilizing. Exploring the role of temperament in the context of community ecology is a unique opportunity for cross‐pollination between ecological fields, and can provide new insights into community stability and biodiversity.     

Scaling from individuals to networks in food webs

1.  Food webs, the set of predator–prey interactions in an ecosystem, are a prototypical complex system. Much research to date has concentrated on the use of models to identify and explain the key structural features which characterize food webs.
2.  These models often fall into two general categories: (i) phenomenological models which are built upon a set of heuristic rules in order to explain some empirical observation and (ii) population-level models in which interactions between individuals result in emergent properties for the food web. Both types of models have helped to uncover how food-web structure is a product of factors such as foraging behaviour, prey selection and species' body sizes.
3.  Historically, the two types of models have followed rather different approaches to the problem. Despite the apparent differences, the overlap between the two styles of models is substantial. Examples are highlighted here.
4.  By paying greater attention to both the similarities and differences between the two, we will be better able to demonstrate the ecological insights offered by phenomenological models. This will help us, for example, design experiments which could validate or refute underlying assumptions of the models. By linking models to data, scaling from individuals to networks, we will be closer to understanding the true origins of food-web structure.     

When should we expect early bursts of trait evolution in comparative data? Predictions from an evolutionary food web model

Conceptual models of adaptive radiation predict that competitive interactions among species will result in an early burst of speciation and trait evolution followed by a slowdown in diversification rates. Empirical studies often show early accumulation of lineages in phylogenetic trees, but usually fail to detect early bursts of phenotypic evolution. We use an evolutionary simulation model to assemble food webs through adaptive radiation, and examine patterns in the resulting phylogenetic trees and species' traits (body size and trophic position). We find that when foraging trade-offs result in food webs where all species occupy integer trophic levels, lineage diversity and trait disparity are concentrated early in the tree, consistent with the early burst model. In contrast, in food webs in which many omnivorous species feed at multiple trophic levels, high levels of turnover of species' identities and traits tend to eliminate the early burst signal. These results suggest testable predictions about how the niche structure of ecological communities may be reflected by macroevolutionary patterns.     

Examining the effects of chronic,lake-wide elevated temperatures on behavioural expression in largemouth bass,Micropterus salmoides

Many behaviours have differential fitness consequences across thermal and ecological contexts, indicating that both ecological shifts and warming temperatures induced by climatic change may alter how organisms behave. However, empirical evidence of temperature-driven behavioural selection in natural systems is lacking. We compared behaviours and behavioural syndromes related to activity, exploration, boldness and aggression in populations of largemouth bass (Micropterus salmoides) from ambient lakes to the those from artificially warmed, power plant cooling lakes to investigate changes in behaviours associated with warmer environments. Activity, exploration, boldness and aggression of juvenile largemouth bass were assessed in laboratory conditions using a novel environment assay and a risky situation assay. We found that activity and exploratory behaviours were higher and decreased through first year ontogeny in populations from heated lakes, whereas these behaviours were lower and showed no relationship through ontogeny in populations from ambient lakes. We attribute these differences to the changes in food source availability in heated lakes associated with temperature-driven ecological effects. Bold and aggressive behaviours tended to differ between populations, as did correlations between behaviours, but did not differ between ambient and heated lakes. The findings of this work identify that large ecological changes associated with warming environments, such as food availability, may drive changes in some aspects of behavioural expression in largemouth bass but that other aspects of behavioural expression may be driven by lake-specific factors not related to warming.     

Niche partitioning due to adaptive foraging reverses effects of nestedness and connectance on pollination network stability

Much research debates whether properties of ecological networks such as nestedness and connectance stabilise biological communities while ignoring key behavioural aspects of organisms within these networks. Here, we computationally assess how adaptive foraging (AF) behaviour interacts with network architecture to determine the stability of plant–pollinator networks. We find that AF reverses negative effects of nestedness and positive effects of connectance on the stability of the networks by partitioning the niches among species within guilds. This behaviour enables generalist pollinators to preferentially forage on the most specialised of their plant partners which increases the pollination services to specialist plants and cedes the resources of generalist plants to specialist pollinators. We corroborate these behavioural preferences with intensive field observations of bee foraging. Our results show that incorporating key organismal behaviours with well‐known biological mechanisms such as consumer‐resource interactions into the analysis of ecological networks may greatly improve our understanding of complex ecosystems.     

Pollen feeding in Heliconius butterflies: the singular evolution of an adaptive suite

Major evolutionary transitions can be triggered by behavioural novelty, and are often associated with ‘adaptive suites’, which involve shifts in multiple co-adapted traits subject to complex interactions. Heliconius butterflies represent one such example, actively feeding on pollen, a behaviour unique among butterflies. Pollen feeding permits a prolonged reproductive lifespan, and co-occurs with a constellation of behavioural, neuroanatomical, life history, morphological and physiological traits that are absent in closely related, non-pollen-feeding genera. As a highly tractable system, supported by considerable ecological and genomic data, Heliconius are an excellent model for investigating how behavioural innovation can trigger a cascade of adaptive shifts in multiple diverse, but interrelated, traits. Here, we synthesize current knowledge of pollen feeding in Heliconius, and explore potential interactions between associated, putatively adaptive, traits. Currently, no physiological, morphological or molecular innovation has been explicitly linked to the origin of pollen feeding, and several hypothesized links between different aspects of Heliconius biology remain poorly tested. However, resolving these uncertainties will contribute to our understanding of how behavioural innovations evolve and subsequently alter the evolutionary trajectories of diverse traits impacting resource acquisition, life history, senescence and cognition.     

Food web structure in riverine landscapes

1. Most research on freshwater (and other) food webs has focused on apparently discrete communities, in well-defined habitats at small spatial and temporal scales, whereas in reality food webs are embedded in complex landscapes, such as river corridors. Food web linkages across such landscapes may be crucial for ecological pattern and process, however. Here, we consider the importance of large scale influences upon lotic food webs across the three spatial dimensions and through time.
2. We assess the roles of biotic factors (e.g. predation, competition) and physical habitat features (e.g. geology, land-use, habitat fragmentation) in moulding food web structure at the landscape scale. As examples, external subsidies to lotic communities of nutrients, detritus and prey vary along the river corridor, and food web links are made and broken across the land–water interface with the rise and fall of the flood.
3. We identify several avenues of potentially fruitful research, particularly the need to quantify energy flow and population dynamics. Stoichiometric analysis of changes in C : N : P nutrient ratios over large spatial gradients (e.g. from river source to mouth, in forested versus agricultural catchments), offers a novel method of uniting energy flow and population dynamics to provide a more holistic view of riverine food webs from a landscape perspective. Macroecological approaches can be used to examine large-scale patterns in riverine food webs (e.g. trophic rank and species–area relationships). New multivariate statistical techniques can be used to examine community responses to environmental gradients and to assign traits to individual species (e.g. body-size, functional feeding group), to unravel the organisation and trophic structure of riverine food webs.     

Host-dependent differences in prey acquisition between populations of a kleptoparasitic spider Argyrodes kumadai (Araneae: Theridiidae)

Abstract.  1. A kleptoparasitic spider, Argyrodes kumadai , is known to use phylogenetically unrelated host species in different regions – Cyrtophora moluccensis (Araneidae) in south-west Japan and Agelena silvatica (Agelenidae) in north-east Japan. The work reported here examined whether differences in host characters affect prey acquisition of A. kumadai .
2. Field surveys showed that prey-biomass capture rate of Argyrodes was significantly higher in populations parasitising Cyrtophora than in populations parasitising Agelena . Although Argyrodes appeared to catch fewer prey within Cyrtophora webs, they were able to feed upon substantially larger prey.
3. Differences in prey-biomass capture rate were found to reflect differences in host traits rather than regional differences in potential prey availability. Individuals in populations parasitising Cyrtophora were observed to acquire prey via a number of foraging tactics that included stealing wrapped food bundles, feeding upon prey remains and, in the case of large prey items, feeding together with the host. In contrast, individuals in populations parasitising Agelena were only ever observed to feed upon small prey items ignored by its host.
4. This variability in prey acquisition between kleptoparasite populations reflected different opportunities for feeding within their respective host webs – opportunities that were primarily determined by the foraging behaviour of the host. One key trait associated with host foraging behaviour was host-web structure, namely the presence/absence of a retreat.     

Interactive effects of body-size structure and adaptive foraging on food-web stability

Body-size structure of food webs and adaptive foraging of consumers are two of the dominant concepts of our understanding how natural ecosystems maintain their stability and diversity. The interplay of these two processes, however, is a critically important yet unresolved issue. To fill this gap in our knowledge of ecosystem stability, we investigate dynamic random and niche model food webs to evaluate the proportion of persistent species. We show that stronger body-size structures and faster adaptation stabilise these food webs. Body-size structures yield stabilising configurations of interaction strength distributions across food webs, and adaptive foraging emphasises links to resources closer to the base. Moreover, both mechanisms combined have a cumulative effect. Most importantly, unstructured random webs evolve via adaptive foraging into stable size-structured food webs. This offers a mechanistic explanation of how size structure adaptively emerges in complex food webs, thus building a novel bridge between these two important stabilising mechanisms.     

Shift in predation regime mediates diversification of foraging behaviour in a dragonfly genus

1. Behavioural adaptations to avoid and evade predators are common. Many studies have investigated population divergence in response to changes in predation regime within species, but studies exploring interspecific patterns are scant. Studies on interspecific divergence can infer common outcomes from evolutionary processes and highlight the role of environmental constraints in shaping species traits. 2. Species of the dragonfly genus Leucorrhinia underwent well‐studied shifts from habitats being dominated by predatory fish (fish lakes) to habitat being dominated by predatory invertebrates (dragonfly lakes). This change in top predators resulted in a set of adaptive trait modifications in response to the different hunting styles of both predator types: whereas predatory fish actively search and pursue prey, invertebrate predator follow a sit‐and‐wait strategy, not pursuing prey. 3. Here it is shown that the habitat shift‐related change in selection regime on larval Leucorrhinia caused species in dragonfly lakes to evolve increased larval foraging and activity, and results suggest that they lost the ability to recognise predatory fish. 4. The results of the present study highlight the impact of predators on behavioural trait diversification with habitat‐specific predation regimes selecting for distinct behavioural expression.     

Matching consumer feeding behaviours and resource traits: a fourth‐corner problem in food‐web theory

For decades, food web theory has proposed phenomenological models for the underlying structure of ecological networks. Generally, these models rely on latent niche variables that match the feeding behaviour of consumers with their resource traits. In this paper, we used a comprehensive database to evaluate different hypotheses on the best dependency structure of trait‐matching patterns between consumers and resource traits. We found that consumer feeding behaviours had complex interactions with resource traits; however, few dimensions (i.e. latent variables) could reproduce the trait‐matching patterns. We discuss our findings in the light of three food web models designed to reproduce the multidimensionality of food web data; additionally, we discuss how using species traits clarify food webs beyond species pairwise interactions and enable studies to infer ecological generality at larger scales, despite potential taxonomic differences, variations in ecological conditions and differences in species abundance between communities.     

Adaptive foraging does not always lead to more complex food webs

Recent modeling studies exploring the effect of consumers’ adaptivity in diet composition on food web complexity invariably suggest that adaptivity in foraging decisions of consumers makes food webs more complex. That is, it allows for survival of a higher number of species when compared with non-adaptive food webs. Population-dynamical models in these studies share two features: parameters are chosen uniformly for all species, i.e. they are species-independent, and adaptive foraging is described by the search image model. In this article, we relax both these assumptions. Specifically, we allow parameters to vary among the species and consider the diet choice model as an alternative model of adaptive foraging. Our analysis leads to three important predictions. First, for species-independent parameter values for which the search image model demonstrates a significant effect of adaptive foraging on food web complexity, the diet choice model produces no such effect. Second, the effect of adaptive foraging through the search image model attenuates when parameter values cease to be species-independent. Finally, for the diet choice model we observe no (significant) effect of adaptive foraging on food web complexity. All these observations suggest that adaptive foraging does not always lead to more complex food webs. As a corollary, future studies of food web dynamics should pay careful attention to the choice of type of adaptive foraging model as well as of parameter values.     

Predicting the effects of temperature on food web connectance

Few models concern how environmental variables such as temperature affect community structure. Here, we develop a model of how temperature affects food web connectance, a powerful driver of population dynamics and community structure. We use the Arrhenius equation to add temperature dependence of foraging traits to an existing model of food web structure. The model predicts potentially large temperature effects on connectance. Temperature-sensitive food webs exhibit slopes of up to 0.01 units of connectance per 1°C change in temperature. This corresponds to changes in diet breadth of one resource item per 2°C (assuming a food web containing 50 species). Less sensitive food webs exhibit slopes down to 0.0005, which corresponds to about one resource item per 40°C. Relative sizes of the activation energies of attack rate and handling time determine whether warming increases or decreases connectance. Differences in temperature sensitivity are explained by differences between empirical food webs in the body size distributions of organisms. We conclude that models of temperature effects on community structure and dynamics urgently require considerable development, and also more and better empirical data to parameterize and test them.     

Foraging ecology and patterns of diversification in dipteran parasitoids of fire ants in south Brazil

1. At least sixteen species of parasitoid flies in the genus Pseudacteon (family Phoridae) attack fire ants in the Solenopsis saevissima subcomplex in South America. Little is known of behavioural or ecological differences among Pseudacteon parasitoids of fire ants, although their coexistence in multispecies communities would suggest that important differences exist. Seven Pseudacteon species in two separate communities were studied in south-east Brazil. The way in which hosts detect and respond to the presence of parasitoids, attack rates of the parasitoids, and host location behaviour of the parasitoids were examined.
2. Reductions in fire ant recruitment were more closely related to the number of ants attacked along a foraging trail than to the amount of time that a phorid was present.
3. Pseudacteon solenopsidis differed from other phorid species by flying backwards while pursuing ants, by attacking at lower rates than other phorids, and by spending longer around fire ant foraging trails than other phorids before departing. Fire ant recruitment to food often rebounded in the continued presence of P. solenopsidis.
4. In each of the two communities, certain Pseudacteon species appeared frequently at Solenopsis foraging trails, whereas others appeared predominantly at mound disturbances. Two distinct size classes of phorids were present in each community, and the community with the larger ant host species also had a third and larger phorid species. No phorid species from the same community had similar body sizes and similar host location behaviours, although numerous species from different communities shared both of these traits.
5. Heterogeneity in host size and in the ecological circumstances under which hosts are vulnerable to attack appears to have influenced the evolution and perhaps maintenance of diverse Pseudacteon communities.     

Scaling laws of ambush predator ‘waiting’ behaviour are tuned to a common ecology

The decisions animals make about how long to wait between activities can determine the success of diverse behaviours such as foraging, group formation or risk avoidance. Remarkably, for diverse animal species, including humans, spontaneous patterns of waiting times show random ‘burstiness’ that appears scale-invariant across a broad set of scales. However, a general theory linking this phenomenon across the animal kingdom currently lacks an ecological basis. Here, we demonstrate from tracking the activities of 15 sympatric predator species (cephalopods, sharks, skates and teleosts) under natural and controlled conditions that bursty waiting times are an intrinsic spontaneous behaviour well approximated by heavy-tailed (power-law) models over data ranges up to four orders of magnitude. Scaling exponents quantifying ratios of frequent short to rare very long waits are species-specific, being determined by traits such as foraging mode (active versus ambush predation), body size and prey preference. A stochastic–deterministic decision model reproduced the empirical waiting time scaling and species-specific exponents, indicating that apparently complex scaling can emerge from simple decisions. Results indicate temporal power-law scaling is a behavioural ‘rule of thumb’ that is tuned to species’ ecological traits, implying a common pattern may have naturally evolved that optimizes move–wait decisions in less predictable natural environments.     

Behavioural responses of invasive American mink Neovison vison to an eradication campaign, revealed by stable isotope analysis

1.  The detrimental impacts of invasive, non-native species on islands are widely acknowledged and it is often best to act rapidly against such species, even where uncertainty exists over the best way to proceed. If management actions are evaluated and refined, using information learnt from the biology of culled animals, this uncertainty can be gradually reduced, increasing the likelihood of a successful outcome.
2.  American mink Neovison vison carcasses were collected as part of an eradication campaign on several islands of the Outer Hebrides, Scotland, and stable isotope analysis was used to describe ecological variation in this invasive non-native predator.
3.  Isotope profiles from individual mink whiskers demonstrated how behaviour at a population level changed markedly over time. As the eradication campaign progressed, mink increased their reliance on marine food sources and focused their activity on the coastline. Stable isotope analyses also demonstrated sex-related changes in foraging and ranging behaviour in relation to food resource availability on the two main island complexes.
4.   Synthesis and applications. Our findings contribute to the refinement of a campaign to extend the successful eradication of mink from Uist and Harris, to the whole of the Outer Hebrides archipelago, UK. They also highlight the potential for stable isotope approaches to provide more detailed postmortem information that can inform adaptive management of wildlife populations for conservation objectives.     

Foraging mode of the chameleon,Bradypodion pumilum: a challenge to the sit‐and‐wait versus active forager paradigm?

Foraging mode is an important aspect of life history, often associated with traits such as locomotor mode, energy budget, risk of predation and reproductive effort. Because of these life-history associations, classification of foraging mode can be conceptually useful. Lizards figured prominently in the historical development of foraging mode concepts, yet our current understanding is dominated by only two lizard families which are good examples of the two extreme modes, sit-and-wait vs. active foraging. A great deal of lizard phylogenetic diversity remains unrepresented. Chameleons are a highly derived lizard taxon for which we have very little behavioural or ecological data, and no foraging mode data. Because chameleons are so unusual, it is not possible to predict where they will fit within the bimodal paradigm. I studied time budget and foraging mode in the Cape dwarf chameleon, Bradypodion pumilum , in Stellenbosch, South Africa. Several approaches were taken to assess foraging behaviour. First, lag-sequential analysis was applied to compare rates behaviours associated with observed eating events, which did not support a sit-and-wait foraging mode. Second, the number of moves per minute (MPM) and per cent time moving (%TM) were compared with those of other lizard taxa from the literature. Foraging in B. pumilum was found to be most consistent with an active foraging mode, although the MPM is unusually low. Thus I propose classification of B. pumilum as a cruise forager. Sufficient data are available to define a discriminant function for active vs. sit-and-wait modes among lizard speries, which classifys B. pumilum as active and additionally lends statistical support for good separation between foraging modes. These findings are discussed in relation to the evolution of foraging modes in chameleons and other lizard families.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 84 , 797–808.