Context dependence in foraging behaviour of Achillea millefolium

Context-dependent foraging behaviour is acknowledged and well documented for a diversity of animals and conditions. The contextual determinants of plant foraging behaviour, however, are poorly understood. Plant roots encounter patchy distributions of nutrients and soil fungi. Both of these features affect root form and function, but how they interact to affect foraging behaviour is unknown. We extend the use of the marginal value theorem to make predictions about the foraging behaviour of roots, and test our predictions by manipulating soil resource distribution and inoculation by soil fungi. We measured plant movement as both distance roots travelled and time taken to grow through nutrient patches of varied quality. To do this, we grew Achillea millefolium in the centers of modified pots with a high-nutrient patch and a low-nutrient patch on either side of the plant (heterogeneous) or patch-free conditions (homogeneous). Fungal inoculation, but not resource distribution, altered the time it took roots to reach nutrient patches. When in nutrient patches, root growth decreased relative to homogeneous soils. However, this change in foraging behaviour was not contingent upon patch quality or fungal inoculation. Root system breadth was larger in homogeneous than in heterogeneous soils, until measures were influenced by pot edges. Overall, we find that root foraging behaviour is modified by resource heterogeneity but not fungal inoculation. We find support for predictions of the marginal value theorem that organisms travel faster through low-quality than through high-quality environments, with the caveat that roots respond to nutrient patches per se rather than the quality of those patches.     

Importance of plasticity and decision-making strategies for plant resource acquisition in spatio-temporally variable environments

* Plants must cope with environmental variation in space and time. Phenotypic plasticity allows them to adjust their form and function to small-scale variations in habitat quality. Empirical studies have shown that stoloniferous plants can exploit heterogeneous habitats through plastic ramet specialization and internal resource exchange (division of labour). * Here we present a spatially explicit simulation model to explore costs and benefits of plasticity in spatio-temporally heterogeneous environments. We investigated the performance of three plant strategies in pairwise competition. The nonplastic strategy was unable to specialize. The autonomous plastic strategy displayed localized responses to external resource signals. In the coordinated plastic strategy, localized responses could be modified by internal demand signals from connected modules. * Plasticity in resource uptake proved beneficial in a broad range of environments. Modular coordination was beneficial under virtually all realistic conditions, especially if resource supplies did not closely match resource needs. * The benefits of division of labour extend considerably beyond the parameter combination covered by empirical studies. Our model provides a general framework for evaluating the benefits, costs and limits of plasticity in spatio-temporally heterogeneous habitats.     

The effects of environmental heterogeneity on root growth and root/shoot partitioning

AIMS: The purpose of this Botanical Briefing is to stimulate reappraisal of root growth, root/shoot partitioning, and analysis of other aspects of plant growth under heterogeneous conditions. SCOPE: Until recently, most knowledge of plant growth was based upon experimental studies carried out under homogeneous conditions. Natural environments are heterogeneous at scales relevant to plants and in forms to which they can respond. Responses to environmental heterogeneity are often localized rather than plant-wide, and not always predictable from traditional optimization arguments or from knowledge of the ontogenetic trends of plants growing under homogeneous conditions. These responses can have substantial impacts, both locally and plant-wide, on patterns of resource allocation, and significant effects on whole-plant growth. Results from recent studies are presented to illustrate responses of plants, plant populations and plant communities to nutritionally heterogeneous conditions. CONCLUSIONS: Environmental heterogeneity is a constant presence in the natural world that significantly influences plant behaviour at a variety of levels of complexity. Failure to understand its effects on plants prevents us from fully exploiting aspects of plant behaviour that are only revealed under patchy conditions. More effort should be invested into analysis of the behaviour of plants under heterogeneous conditions.     

Rapid systemic signaling during abiotic and biotic stresses: is the ROS wave master of all trades?

Rapidly communicating the perception of an abiotic stress event, wounding or pathogen infection, from its initial site of occurrence to the entire plant, i.e. rapid systemic signaling, is essential for successful plant acclimation and defense. Recent studies highlighted an important role for several rapid whole‐plant systemic signals in mediating plant acclimation and defense during different abiotic and biotic stresses. These include calcium, reactive oxygen species (ROS), hydraulic and electric waves. Although the role of some of these signals in inducing and coordinating whole‐plant systemic responses was demonstrated, many questions related to their mode of action, routes of propagation and integration remain unanswered. In addition, it is unclear how these signals convey specificity to the systemic response, and how are they integrated under conditions of stress combination. Here we highlight many of these questions, as well as provide a proposed model for systemic signal integration, focusing on the ROS wave.     

Effects of Nutrient Heterogeneity and Competition on Root Architecture of Spruce Seedlings: Implications for an Essential Feature of Root Foraging

Background

We have limited understanding of root foraging responses when plants were simultaneously exposed to nutrient heterogeneity and competition, and our goal was to determine whether and how plants integrate information about nutrients and neighbors in root foraging processes.

Methodology/Principal Findings

The experiment was conducted in split-containers, wherein half of the roots of spruce (Picea asperata) seedlings were subjected to intraspecific root competition (the vegetated half), while the other half experienced no competition (the non-vegetated half). Experimental treatments included fertilization in the vegetated half (FV), the non-vegetated half (FNV), and both compartments (F), as well as no fertilization (NF). The root architecture indicators consisted of the number of root tips over the root surface (RTRS), the length percentage of diameter-based fine root subclasses to total fine root (SRLP), and the length percentage of each root order to total fine root (ROLP). The target plants used novel root foraging behaviors under different combinations of neighboring plant and localized fertilization. In addition, the significant increase in the RTRS of 0–0.2 mm fine roots after fertilization of the vegetated half alone and its significant decrease in fertilizer was applied throughout the plant clearly showed that plant root foraging behavior was regulated by local responses coupled with systemic control mechanisms.

Conclusions/Significance

We measured the root foraging ability for woody plants by means of root architecture indicators constructed by the roots possessing essential nutrient uptake ability (i.e., the first three root orders), and provided new evidence that plants integrate multiple forms of environmental information, such as nutrient status and neighboring competitors, in a non-additive manner during the root foraging process. The interplay between the responses of individual root modules (repetitive root units) to localized environmental signals and the systemic control of these responses may well account for the non-additive features of the root foraging process.     

Adaptive foraging behaviour of individual pollinators and the coexistence of co-flowering plants

Although pollinators can play a central role in determining the structure and stability of plant communities, little is known about how their adaptive foraging behaviours at the individual level, e.g. flower constancy, structure these interactions. Here, we construct a mathematical model that integrates individual adaptive foraging behaviour and population dynamics of a community consisting of two plant species and a pollinator species. We find that adaptive foraging at the individual level, as a complementary mechanism to adaptive foraging at the species level, can further enhance the coexistence of plant species through niche partitioning between conspecific pollinators. The stabilizing effect is stronger than that of unbiased generalists when there is also strong competition between plant species over other resources, but less so than that of multiple specialist species. This suggests that adaptive foraging in mutualistic interactions can have a very different impact on the plant community structure from that in predator–prey interactions. In addition, the adaptive behaviour of individual pollinators may cause a sharp regime shift for invading plant species. These results indicate the importance of integrating individual adaptive behaviour and population dynamics for the conservation of native plant communities.     

Invasive clonal plant species have a greater root-foraging plasticity than non-invasive ones

Clonality is frequently positively correlated with plant invasiveness, but which aspects of clonality make some clonal species more invasive than others is not known. Due to their spreading growth form, clonal plants are likely to experience spatial heterogeneity in nutrient availability. Plasticity in allocation of biomass to clonal growth organs and roots may allow these plants to forage for high-nutrient patches. We investigated whether this foraging response is stronger in species that have become invasive than in species that have not. We used six confamilial pairs of native European clonal plant species differing in invasion success in the USA. We grew all species in large pots under homogeneous or heterogeneous nutrient conditions in a greenhouse, and compared their nutrient-foraging response and performance. Neither invasive nor non-invasive species showed significant foraging responses to heterogeneity in clonal growth organ biomass or in aboveground biomass of clonal offspring. Invasive species had, however, a greater positive foraging response in terms of root and belowground biomass than non-invasive species. Invasive species also produced more total biomass. Our results suggest that the ability for strong root foraging is among the characteristics promoting invasiveness in clonal plants.     

Foraging preferences: Response to reward skew

Recent theoretical and empirical work on foraging behaviour suggests that animals may respond to both the means and variances in benefits associated with available resources. We attempt to extend this analysis by asking if reward skew (third moment about the mean) might influence preference when two options have equal means and equal variances. We examine how minimizing the probability of starvation might induce response to skew. In the Appendix we develop an expected ‘fitness’ model which follows from economic theory and indicates more general conditions concerning responses to skew. We also report experiments involving foraging white-crowned sparrows (Zonotrichia leucophrys). Under conditions where positive skew should be favoured, the birds' behaviour supports the prediction. However, their response to skew is not as strong as responses to variance noted in the same individuals.     

Individual differences in searching behaviour and spatial foraging consistency in a central place marine predator

Consistent intra‐population variability in foraging behaviour is found among a wide range of taxa. Such foraging specialisations are common among marine vertebrates, yet it is not clear how individuals repeatedly locate prey or foraging sites at ocean‐wide scales. Using GPS and time‐depth loggers we studied the fine‐scale foraging behaviour of central‐place northern gannets Morus bassanus at two large colonies. First, we estimated the degree of consistency in individual foraging routes and sites across repeated trips. Second, we tested for individual differences in searching behaviour in response to environmental covariates using reaction norms, estimated from mixed effect models. Adult gannets tracked over multiple foraging trips showed repeatable between‐individual differences in terminal points and departure angles of foraging trips, but low repeatability in trip duration and trip length. Importantly, individual birds showed highly repeatable dive locations, with consistently different environmental conditions (such as copepod abundance), suggesting a high degree of foraging site specialisation. Gannets also showed between‐individual differences in searching behaviour along environmental gradients, such that individuals intensified searching under different conditions. Together these results suggest that widespread individual foraging consistency may represent specialisation and be linked with individual responses to environmental conditions. Such divergent searching behaviour could provide a mechanism by which consistent foraging behaviour arises and is maintained among animals that forage across large spatial scales.     

A biochemically semi-detailed model of auxin-mediated vein formation in plant leaves

We present here a model intended to capture the biochemistry of vein formation in plant leaves. The model consists of three modules. Two of these modules, those describing auxin signaling and transport in plant cells, are biochemically detailed. We couple these modules to a simple model for PIN (auxin efflux carrier) protein localization based on an extracellular auxin sensor. We study the single-cell responses of this combined model in order to verify proper functioning of the modeled biochemical network. We then assemble a multicellular model from the single-cell building blocks. We find that the model can, under some conditions, generate files of polarized cells, but not true veins.     

Long-distance stress and developmental signals associated with abscisic acid signaling in environmental responses

Flowering plants consist of highly differentiated organs, including roots, leaves, shoots and flowers, which have specific roles: root system for water and nutrient uptake, leaves for photosynthesis and gas exchange and reproductive organs for seed production. The communication between organs through the vascular system, by which water, nutrient and signaling molecules are transported, is essential for coordinated growth and development of the whole plant, particularly under adverse conditions. Here, we highlight recent progress in understanding how signaling pathways of plant hormones are associated with long-distance stress and developmental signals, with particular focus on environmental stress responses. In addition to the root-to-shoot peptide signal that induces abscisic acid accumulation in leaves under drought stress conditions, we summarize the diverse stress-responsive peptide signals reported to date to play a role in environmental responses.     

Chemical Alarm Signals Enhance Survival of Brook Charr (Salvelinus fontinalis) During Encounters with Predatory Chain Pickerel (Esox niger)

A diversity of aquatic organisms release chemical alarm signals when attacked or captured by a predator. These alarm signals are thought to warn other conspecifics of danger and, consequently, may benefit receivers by increasing their survival. Here we experimentally investigated the differences in behaviour and survival of hatchery-reared juvenile brook charr Salvelinus fontinalis that had been exposed to either brook charr skin extract (experimental treatment) or a control of swordtail skin extract (control treatment). Charr exposed to conspecific skin extract exhibited a significant reduction in movement and/or altered their foraging behaviour in the laboratory when compared with charr exposed to swordtail skin extract. We also exposed charr to either water conditioned by a single brook charr disturbed by a predatory bird model or water conditioned by a single undisturbed brook charr. Charr exposed to disturbance signals reduced activity significantly more than charr exposed to chemical stimuli from undisturbed charr. These results demonstrate the existence of both damage-released alarm signals and disturbance signals in brook charr. Wild brook charr also responded to damage-released alarm cues under natural conditions. Charr avoided areas of a stream with minnow traps labelled with conspecific alarm cues vs. control cues. During staged encounters with chain pickerel Esox niger in the laboratory, predator-naive charr fry were better able to evade the predator if they were previously warned by an alarm signal, thus suggesting a survival benefit to receivers. Collectively, these results demonstrate that the presence of alarm signals in brook charr has important implications for understanding predator–prey interactions.     

Chromatic signals control proboscis movements during hovering flight in the hummingbird hawkmoth Macroglossum stellatarum

Most visual systems are more sensitive to luminance than to colour signals. Animals resolve finer spatial detail and temporal changes through achromatic signals than through chromatic ones. Probably, this explains that detection of small, distant, or moving objects is typically mediated through achromatic signals. Macroglossum stellatarum are fast flying nectarivorous hawkmoths that inspect flowers with their long proboscis while hovering. They can visually control this behaviour using floral markings known as nectar guides. Here, we investigate whether this is mediated by chromatic or achromatic cues. We evaluated proboscis placement, foraging efficiency, and inspection learning of naïve moths foraging on flower models with coloured markings that offered either chromatic, achromatic or both contrasts. Hummingbird hawkmoths could use either achromatic or chromatic signals to inspect models while hovering. We identified three, apparently independent, components controlling proboscis placement: After initial contact, 1) moths directed their probing towards the yellow colour irrespectively of luminance signals, suggesting a dominant role of chromatic signals; and 2) moths tended to probe mainly on the brighter areas of models that offered only achromatic signals. 3) During the establishment of the first contact, naïve moths showed a tendency to direct their proboscis towards the small floral marks independent of their colour or luminance. Moths learned to find nectar faster, but their foraging efficiency depended on the flower model they foraged on. Our results imply that M. stellatarum can perceive small patterns through colour vision. We discuss how the different informational contents of chromatic and luminance signals can be significant for the control of flower inspection, and visually guided behaviours in general.     

The dilemma of foraging herbivores: dealing with food and fear

For foraging herbivores, both food quality and predation risk vary across the landscape. Animals should avoid low-quality food patches in favour of high-quality ones, and seek safe patches while avoiding risky ones. Herbivores often face the foraging dilemma, however, of choosing between high-quality food in risky places or low-quality food in safe places. Here, we explore how and why the interaction between food quality and predation risk affects foraging decisions of mammalian herbivores, focusing on browsers confronting plant toxins in a landscape of fear. We draw together themes of plant–herbivore and predator–prey interactions, and the roles of animal ecophysiology, behaviour and personality. The response of herbivores to the dual costs of food and fear depends on the interplay of physiology and behaviour. We discuss detoxification physiology in dealing with plant toxins, and stress physiology associated with perceived predation risk. We argue that behaviour is the interface enabling herbivores to stay or quit food patches in response to their physiological tolerance to these risks. We hypothesise that generalist and specialist herbivores perceive the relative costs of plant defence and predation risk differently and intra-specifically, individuals with different personalities and physiologies should do so too, creating individualised landscapes of food and fear. We explore the ecological significance and emergent impacts of these individual-based foraging outcomes on populations and communities, and offer predictions that can be clearly tested. In doing so, we provide an integrated platform advancing herbivore foraging theory with food quality and predation risk at its core.     

Effect of local spatial plant distribution and conspecific density on bumble bee foraging behaviour

1. Size variations in pollinator populations may modify competitive interactions among foragers. Competition among pollinators has been shown to lead to one of two contrasting behaviours: either specialisation to the most profitable plant species or generalisation to several species. When foraging, pollinators are also confronted with heterogeneity in the spatial distribution of plant resources. Because variations in both the forager density and plant spatial distribution can affect pollinator behaviour, focus was on the interactive effect of these two factors. 2. Bumble bee (Bombus terrestris L.) individuals were trained on a focal species (Lotus corniculatus L.) and experimentally tested whether variations in the forager density (two or six bumble bees foraging together), plant community spatial distribution (two plant species: L. corniculatus and Medicago sativa, which were either patchily or randomly distributed), and their interaction modified bumble bee foraging behaviour. 3. It was shown that when confronted with a high forager density, bumble bees focused their visits towards the most familiar species, especially when foraging under a random plant distribution. These modifications affected the fruiting of the focal plant species, with a significantly lower reproductive success under low density/patchy conditions. 4. This study demonstrates that the foraging decisions of bumble bees are influenced by variations in both the conspecific density and plant spatial distribution. Given the increasing impact of human activities on plant‐pollinator communities, this raises the question of the potential implications of these results for plant communities in natural conditions when confronted with variations in the pollinator density and spatial distribution of plants.     

Spatial models of foraging in clonal plant species

Ramets of some clonal plant species alter their internode lengths or their frequency of lateral branching in response to their immediate microenvironment. Such “plant foraging” responses are thought to allow clones to concentrate in favorable portions of their environment. Despite widespread interest among ecologists in plant foraging, few realistic models have been developed to examine conditions under which plant foraging responses are likely to provide clones with ecological benefit. In this paper, we develop spatially explicit, stochastic simulation models to examine consequences of both empirical and hypothetical plant foraging responses. We construct a hierarchical series of models in which we incorporate effects of resource heterogeneity on spacer lengths, angles of growth, and lateral branch production. We also vary the number, size, and arrangement of patches, and the presence or absence of ramet mortality. Simulations based on hypothetical data demonstrated the potential importance of shortening spacer lengths in favorable habitat. In these simulations, ramet crowding increased significantly, implying a potential cost to plant foraging responses whose magnitude is large enough to cause ramets to concentrate in favorable patches. Models calibrated with empirical data suggest that when clonal plants were able to concentrate in favorable habitat, this was usually caused by increased daughter ramet production in the favorable habitat. Variation in clonal growth angles had little impact on the ability of ramets or clones to locate favorable patches, but did increase the ability of clones to remain in favorable patches once found. Alterations in the number and size of patches strongly influenced the effectiveness of the foraging response. The spatial arrangement of patches also was important: clumped distributions of patches decreased the success with which plants located favorable patches, especially at the genet level and when the number of patches was low. Finally, when ramet mortality varied with patch quality, there was an increase in the percentage of ramets located in favorable patches; differential ramet mortality also lessened the impact of other effects, such as the decreased success of clones when patches are clumped. Overall, our models indicate that the effectiveness of plant foraging responses is variable and is likely to depend on a suite of environmental conditions.     

光照强度和基质养分对匍匐茎草本金戴戴克隆生长和克隆形态的影响

在深度遮光(光照强度为高光条件的6.25%,约为自然光照的5.3%)或低养分条件下,金戴戴(Halerpestes ruthenica Ovcz.)生物量、初级分株叶面积、分株总数、匍匐茎总数和总长度均显著减小,而比节间长和比叶柄长显著增加.在低养分条件下,金戴戴匍匐茎平均节间长显著增加,而匍匐茎分枝强度和分株数显著减小.这些结果与克隆植物觅食模型相符合,表明当生长于异质性生境中,金戴戴可能通过以克隆生长和克隆形态的可塑性实现的觅养行为来增加对养分资源的摄取.在深度遮光条件下,金戴戴平均间隔子长度(即平均节间长和平均叶柄长)均显著减小.这一结果与以往实验中匍匐茎草本间隔子对中度和轻度遮光(光照强度为高光条件的13%～75%,>10%的自然光照)的反应不同.这表明,在深度遮光条件下匍匐茎克隆植物可能不发生通过间隔子可塑性实现的觅光行为.光照强度和基质养分条件的交互作用对许多性状如总生物量、匍匐茎总数和总长度、二级和三级分株数、分株总数、初级分株叶面积以及分枝强度均有十分显著的效应.在高光条件下,基质养分对这些性状有十分显著的影响;而在低光条件下,基质养分条件对这些性状不产生影响或影响较小.这表明,光照强度影响金戴戴对基质养分的可塑性反应.在深度遮光或低养分条件下,金戴戴可能通过减小匍匐茎节间粗度(增加比节间长)来增加或维持其相对长度,从而更有机会逃离资源丰度低的斑块.     

Cortical Network Models of Firing Rates in the Resting and Active States Predict BOLD Responses

Measurements of blood oxygenation level dependent (BOLD) signals have produced some surprising observations. One is that their amplitude is proportional to the entire activity in a region of interest and not just the fluctuations in this activity. Another is that during sleep and anesthesia the average BOLD correlations between regions of interest decline as the activity declines. Mechanistic explanations of these phenomena are described here using a cortical network model consisting of modules with excitatory and inhibitory neurons, taken as regions of cortical interest, each receiving excitatory inputs from outside the network, taken as subcortical driving inputs in addition to extrinsic (intermodular) connections, such as provided by associational fibers. The model shows that the standard deviation of the firing rate is proportional to the mean frequency of the firing when the extrinsic connections are decreased, so that the mean BOLD signal is proportional to both as is observed experimentally. The model also shows that if these extrinsic connections are decreased or the frequency of firing reaching the network from the subcortical driving inputs is decreased, or both decline, there is a decrease in the mean firing rate in the modules accompanied by decreases in the mean BOLD correlations between the modules, consistent with the observed changes during NREM sleep and under anesthesia. Finally, the model explains why a transient increase in the BOLD signal in a cortical area, due to a transient subcortical input, gives rises to responses throughout the cortex as observed, with these responses mediated by the extrinsic (intermodular) connections.     

Pollinator parasites and the evolution of floral traits

The main selective force driving floral evolution and diversity is plant–pollinator interactions. Pollinators use floral signals and indirect cues to assess flower reward, and the ensuing flower choice has major implications for plant fitness. While many pollinator behaviors have been described, the impact of parasites on pollinator foraging decisions and plant–pollinator interactions have been largely overlooked. Growing evidence of the transmission of parasites through the shared‐use of flowers by pollinators demonstrate the importance of behavioral immunity (altered behaviors that enhance parasite resistance) to pollinator health. During foraging bouts, pollinators can protect themselves against parasites through self‐medication, disease avoidance, and grooming. Recent studies have documented immune behaviors in foraging pollinators, as well as the impacts of such behaviors on flower visitation. Because pollinator parasites can affect flower choice and pollen dispersal, they may ultimately impact flower fitness. Here, we discuss how pollinator immune behaviors and floral traits may affect the presence and transmission of pollinator parasites, as well as how pollinator parasites, through these immune behaviors, can impact plant–pollinator interactions. We further discuss how pollinator immune behaviors can impact plant fitness, and how floral traits may adapt to optimize plant fitness in response to pollinator parasites. We propose future research directions to assess the role of pollinator parasites in plant–pollinator interactions and evolution, and we propose better integration of the role of pollinator parasites into research related to pollinator optimal foraging theory, floral diversity and agricultural practices.     

Exploration or exploitation: life expectancy changes the value of learning in foraging strategies

The acquisition of information is a fundamental part of individual foraging behaviour in heterogeneous and changing environments. We examine how foragers may benefit from utilizing a simple learning rule to update estimates of temporal changes in resource levels. In the model, initial expectation of resource conditions and rate of replacing past information by new experiences are genetically inherited traits. Patch-time allocation differs between learners and foragers that use a fixed patch-leaving threshold throughout the foraging season. It also deviates from foragers that obtain information about the environment at no cost. At the start of a foraging season, learners sample the environment by frequent movements between patches, sacrificing current resource intake for information acquisition. This is done to obtain more precise and accurate estimates of resource levels, resulting in increased intake rates later in season. Risk of mortality may alter the trade-off between exploration and exploitation and thus change patch sampling effort. As lifetime expectancy decreases, learners invest less in information acquisition and show lower foraging performance when resource level changes through time.