Adaptive Foraging Behavior Research Articles

Emergence of structure in plant–pollinator networks: low floral resource constrains network specialisation

Specialisation enhances the efficiency of plant–pollinator networks through the exchange of conspecific pollen transfer for floral resources. Floral resources form the currency of plant–pollinator interactions, but the understanding of how floral resources affect the structure of plant–pollinator networks remains modest. Previous theory predicts that optimally foraging animal species will specialise to improve resource acquisition under high resource availability. Although floral resource availability depends on both the plant production and animal consumption of the resources, previous work has assumed that production and availability are equivalent. This potentially may have led to erroneous inferences on the effect of resource availability on specialisation. We develop a mutualistic Lotka–Volterra consumer‐resource model to investigate the influence of floral resource availability on plant–pollinator network structure. The model incorporates animal adaptive foraging behaviour, floral resource dynamics, and density‐dependent dynamics. Specialisation, nestedness and modularity of simulated networks generated from the model under a wide range of parameters were explained using the generalised linear model. We found that the distinction between floral resource dynamics and plant density dynamics was necessary for partial specialisation of plant–pollinator networks. This is because floral resource dynamics constrained animal preference due to its depletion by animal species. Floral resource abundance had a positive effect on network specialisation, but animal density had a negative effect on network specialisation. Floral resource dynamics thus play key roles in the structure of plant–pollinator networks, distinctive from plant species density dynamics.

Top-down effects of foraging decisions on local, landscape and regional biodiversity of resources (DivGUD).

Foraging by consumers acts as a biotic filtering mechanism for biodiversity at the trophic level of resources. Variation in foraging behaviour has cascading effects on abundance, diversity, and functional trait composition of the community of resource species. Here we propose diversity at giving-up density (DivGUD), i.e. when foragers quit exploiting a patch, as a novel concept and simple measure quantifying cascading effects at multiple spatial scales. In experimental landscapes with an assemblage of plant seeds, patch residency of wild rodents decreased local α-DivGUD (via elevated mortality of species with large seeds) and regional γ-DivGUD, while dissimilarity among patches in a landscape (ß-DivGUD) increased. By linking theories of adaptive foraging behaviour with community ecology, DivGUD allows to investigate cascading indirect predation effects, e.g. the ecology-of-fear framework, feedbacks between functional trait composition of resource species and consumer communities, and effects of inter-individual differences among foragers on the biodiversity of resource communities.

D-Serine and d-Alanine Regulate Adaptive Foraging Behavior in Caenorhabditis elegans via the NMDA Receptor.

d-Serine (d-Ser) is a coagonist for NMDA-type glutamate receptors and is thus important for higher brain function. d-Ser is synthesized by serine racemase and degraded by d-amino acid oxidase. However, the significance of these enzymes and the relevant functions of d-amino acids remain unclear. Here, we show that in the nematode Caenorhabditis elegans, the serine racemase homolog SERR-1 and d-amino acid oxidase DAAO-1 control an adaptive foraging behavior. Similar to many organisms, C. elegans immediately initiates local search for food when transferred to a new environment. With prolonged food deprivation, the worms exhibit a long-range dispersal behavior as the adaptive foraging strategy. We found that serr-1 deletion mutants did not display this behavior, whereas daao-1 deletion mutants immediately engaged in long-range dispersal after food removal. A quantitative analysis of d-amino acids indicated that d-Ser and d-alanine (d-Ala) are both synthesized and suppressed during food deprivation. A behavioral pharmacological analysis showed that the long-range dispersal behavior requires NMDA receptor desensitization. Long-term pretreatment with d-Ala, as well as with an NMDA receptor agonist, expanded the area searched by wild-type worms immediately after food removal, whereas pretreatment with d-Ser did not. We propose that d-Ser and d-Ala are endogenous regulators that cooperatively induce the long-range dispersal behavior in C. elegans through actions on the NMDA receptor.SIGNIFICANCE STATEMENT In mammals, d-serine (d-Ser) functions as an important neuromodulator of the NMDA-type glutamate receptor, which regulates higher brain functions. In Caenorhabditis elegans, previous studies failed to clearly define the physiological significance of d-Ser, d-alanine (d-Ala), and their metabolic enzymes. In this study, we found that these d-amino acids and their associated enzymes are active during food deprivation, leading to an adaptive foraging behavior. We also found that this behavior involved NMDA receptor desensitization.

Oceans of stimuli: an individual-based model to assess the role of olfactory cues and local enhancement in seabirds' foraging behaviour.

Oceans are extremely dynamic environments, which poses challenges for top-predators such as seabirds to find food resources. Yet, seabirds evolved sensorial abilities (olfactory senses) along with complex behaviours (social information transfer through local enhancement) to improve foraging efficiency. Using the Cory's shearwater (Calonectris borealis) as a model species, we developed an individual-based model to explore the complementary role of different searching mechanisms (olfactory foraging and local enhancement) for the optimal foraging behaviour of pelagic seabirds during 1-day foraging trips around breeding colonies. Model outputs were compared with observed patterns of Cory's shearwaters distribution during local foraging trips. Also, the foraging efficiency of virtual individuals was analysed considering hypothetical scenarios of foraging conditions and densities of foraging individuals around breeding colonies. The results support the use of a combination of searching strategies by Cory's shearwaters, which produced representative patterns of space use from tracked individuals, including spatial foraging segregation of neighbouring sub-colonies. Furthermore, while the mechanisms underpinning local enhancement played a key role in mitigating sub-optimal foraging conditions, the use of olfactory senses conferred great adaptive foraging advantages over a wide range of environmental conditions. Our results also indicate a synergistic effect between the two strategies, which suggests that a multimodal foraging strategy is useful to forage in extremely dynamic environments. The developed model provides a basis for further investigation regarding the role of foraging mechanisms in the population dynamics of colonial animals, including the adaptive foraging behaviour of marine top predators to dynamic environmental conditions.

Relationship between morphometrics and trophic levels in deep-sea fishes

Marine food webs are structured, in part, by predator gape size. Species found in deep-sea environments may have evolved such that they can consume prey of a wide range of sizes, to maximise resource intake in a low-productivity ecosystem. Estimates of gape size are central to some types of ecosystem model that determine which prey are available to predators, but cannot always be measured directly. Deep-sea species are hypothesized to have larger gape sizes than shallower-water species relative to their body size and, because of pronounced adaptive foraging behaviour, show only a weak relationship between gape size and trophic level. Here we present new data describing selective morphological measurements and gape sizes of 134 osteichthyan and chondrichthyan species from the deep sea (200-1300 m) off New Zealand. We describe how gape size (height, width and area) varied with factors including fish size, taxonomy (class and order within a class) and trophic level estimated from stable isotopes. For deep-sea species, there was a strong relationship between gape size and fish size, better predicted by body mass than total length, which varied by taxonomic group. Results show that predictions of gape size can be made from commonly measured morphological variables. No relationship between gape size and trophic level was found, likely a reflection of using trophic level estimates from stable isotopes as opposed to the commonly used estimates from FishBase. These results support the hypothesis that deep-sea fish are generalists within their environment, including suspected scavenging, even at the highest trophic levels.

Alternative prey impedes the efficacy of a natural enemy of mosquitoes

Adaptive foraging behaviour in the presence of multiple prey types may mediate stability to predator-prey relationships. For biological control agents, the presence of alternative prey may thus reduce ecological impacts towards target organisms, presenting a key challenge to the derivation of agent efficacies. Quantifications of non-target effects are especially important for generalist biocontrol agents in their regulation of pests, vectors and invasive species. We examined the predatory impact of the notonectid Anisops debilis towards larvae of the vector mosquito complex Culex pipiens in the presence of varying densities of alternative daphniid prey. Experimentally, we quantified functional responses of A. debilis towards target mosquito prey under different background daphniid compositions, and also tested for prey switching propensities by the notonectid predator. Increasing background densities of daphniids significantly reduced the predatory impact of notonectids on mosquitoes, characterised by reductions in attack rates, lengthening of handling times and lessening of maximum feeding rates. Furthermore, notonectids displayed a significant selective preference in favour of daphniid prey over mosquitoes, irrespective of prey proportions in aquatic environments. Accordingly, notonectids did not display a prey switching pattern. We thus demonstrate that the presence of alternative prey can dampen predatory impacts of notonectids towards mosquitoes, as compared to more simplistic pairwise systems with singular prey choice. Accordingly, the effects of stabilising mechanisms, such as adaptive foraging, should be further integrated in biocontrol agent assessments.

Behavioral Tracking and Neuromast Imaging of Mexican Cavefish.

Cave-dwelling animals have evolved a series of morphological and behavioral traits to adapt to their perpetually dark and food-sparse environments. Among these traits, foraging behavior is one of the useful windows into functional advantages of behavioral trait evolution. Presented herein are updated methods for analyzing vibration attraction behavior (VAB: an adaptive foraging behavior) and imaging of associated mechanosensors of cave-adapted tetra, Astyanax mexicanus. In addition, methods are presented for high-throughput tracking of a series of additional cavefish behaviors including hyperactivity and sleep-loss. Cavefish also show asociality, repetitive behavior and higher anxiety. Therefore, cavefish serve as an animal model for evolved behaviors. These methods use free-software and custom-made scripts that can be applied to other types of behavior. These methods provide practical and cost-effective alternatives to commercially available tracking software.

Evolution of the developmental plasticity and a coupling between left mechanosensory neuromasts and an adaptive foraging behavior

Many animal species exhibit laterality in sensation and behavioral responses, namely, the preference for using either the left or right side of the sensory system. For example, some fish use their left eye when observing social stimuli, whereas they use their right eye to observe novel objects. However, it is largely unknown whether such laterality in sensory-behavior coupling evolves during rapid adaptation processes. Here, in the Mexican tetra, Astyanax mexicanus, we investigate the laterality in the relationship between an evolved adaptive behavior, vibration attraction behavior (VAB), and its main sensors, mechanosensory neuromasts. A. mexicanus has a surface-dwelling form and cave-dwelling forms (cavefish), whereby a surface fish ancestor colonized the new environment of a cave, eventually evolving cave-type morphologies such as increased numbers of neuromasts at the cranium. These neuromasts are known to regulate VAB, and it is known that, in teleosts, the budding (increasing) process of neuromasts is accompanied with dermal bone formation. This bone formation is largely regulated by endothelin signaling. To assess the evolutionary relationship between bone formation, neuromast budding, and VAB, we treated 1–3 month old juvenile fish with endothelin receptor antagonists. This treatment significantly increased cranial neuromasts in both surface and cavefish, and the effect was significantly more pronounced in cavefish. Antagonist treatment also increased the size of dermal bones in cavefish, but neuromast enhancement was observed earlier than dermal bone formation, suggesting that endothelin signaling may independently regulate neuromast development and bone formation. In addition, although we did not detect a major change in VAB level under this antagonist treatment, cavefish did show a positive correlation of VAB with the number of neuromasts on their left side but not their right. This laterality in correlation was observed when VAB emerged during cavefish development, but it was not seen in surface fish under any conditions tested, suggesting this laterality emerged through an evolutionary process. Above all, cavefish showed higher developmental plasticity in neuromast number and bone formation, and they showed an asymmetric correlation between the number of left-right neuromasts and VAB.

Robustness of rigid and adaptive networks to species loss.

Controversies in the complexity-stability debate have been attributed to the methodologies used such as topological vs. dynamical approaches or rigid vs. adaptive foraging behaviour of species. Here, we use a bipartite network model that incorporates both topological and population dynamics to investigate the robustness of 60 real ecological networks to the loss of generalist and specialist species. We compare the response in both adaptive and rigid networks. Our results show that the removal of generalists leads to the most secondary extinctions, implying that conservation strategies should aim to protect generalist species in the ecosystem. We also show that adaptive behaviour renders networks vulnerable to species loss at initial stages but enhances long term stability of the system. However, whether adaptive networks are more robust to species loss than rigid ones depends on the structure of the network. Specifically, adaptive networks with modularity < 0.3 are more robust than rigid networks of the same modularity. Interestingly, the more modular a network is, the less robust it is to external perturbations.

Adaptive evolution of foraging-related trait in intraguild predation system

This paper considers a tri-trophic food chain in which the top predator (intraguild predator) also feeds on the basal resource. We refer to the model as intraguild predation. We analyze its dynamics from an evolutionary perspective. The attack rate or foraging effort of the middle species (intraguild prey) for the basal resources is assumed to be evolvable and is also assumed to be traded off with the vulnerability to being attacked by the top predator. We focus on the analysis of the evolutionary dynamics of the attack rate using the adaptive dynamics approximation of mutation limited evolution. In particular, the critical function analysis is applied. This study reveals that the evolutionary dynamics of the intraguild predation system is completely characterized by the concavity of the trade-off function and admits trichotomous dynamic scenarios: (1) when the trade-off function is more concave than the critical function, an evolutionary singular strategy exists and is a repeller; (2) when the trade-off function is less concave than the critical function, the evolutionary singular strategy is convergence stable and turns into an evolutionary branching point, in which case the monomorphic intraguild prey will split into two different types; (3) when the trade-off function is convex, the evolutionary singular strategy turns into a continuous stable strategy and is uninvadable. Our theoretical analysis suggests that the adaptive foraging behavior may strongly influence the community stability. Consequently, it may promote the diversity of intraguild prey and the persistence of the system on the evolutionary timescale, which highlight a more comprehensive mechanistic understanding of the intricate interplay between ecological and evolutionary force. This modeling approach provides a venue for research on indirect effects from an evolutionary perspective.

Botanical Preferences of Africanized Bees (Apis mellifera) on the Coast and in the Atlantic Forest of Sergipe, Brazil

Pollen analysis in honey can be used as an alternative method to researchinto flowers visited by bees in an area. This study aimed to indentify the mainfloral families in honey from apiaries in the Atlantic Forest and Sergipe statecoast. Honey samples from these apiaries were studied, as well as plants thatgrow around them, which can be used as a source of foraging for bees. Thepalynological technique was used to compare the pollen content of honeysamples with the pollen grains from leaves of plants found in the vicinityof the apiaries to assess whether they had been visited by bees. The resultsof studies in both sites were similar in terms of incompatibility of familiesfound in the apiary vicinity and honey. Thus, it was possible to observe thatin honey samples from the coast and in the remaining Atlantic forest, thenumber of families was greater than the number of families found in theapiary vicinity, which highlights the diversity of plants visited by bees and apossible expansion of the visited area for food search. This diversity suggestsan adaptive foraging behavior to plant resources available in the environment,which may facilitate the pollination of these botanical families andconsequently improve their genetic quality.

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.

Beavers and lilies: selective herbivory and adaptive foraging behaviour

Summary With the global population of beavers (Castor spp.) increasing, and reintroductions widespread, it is crucial to be able to predict potential impacts on flora and fauna based on defined foraging behaviours. Nymphaea alba (white water lily) is regularly consumed by beavers and provides a model system to test selective foraging behaviour and quantify potential impacts on aquatic resources in standing‐water habitats. Using biometric relationships within N. alba pads, we accurately reconstructed the size and weight of consumed pads, demonstrating that beavers (Castor fiber) selected pads that were significantly larger and heavier than unselected pads. By selecting larger leaves, beavers may also avoid chemical defences associated with anthocyanin pigments that dominate in smaller leaves. Grazing was concentrated in shallow depths (55.7 ± 10.7 cm) close to the shore (2.95 ± 0.62 m) relative to ungrazed plots (100.5 ± 9.2 cm; 4.79 ± 0.68 m). The level of selectivity was unchanged with increasing distance from a central feeding place. Beavers removed 24–50% of pads within grazed areas, but relative to the whole N. alba leaf pad resource, the impact of this foraging was low (0.38–1.23% loss). Plant species diversity was unaffected by foraging, and there was no evidence of indirect effects on non‐targeted N. alba pads or flowers. When foraging in the aquatic environment, beavers are highly selective and can have a minor effect on food resources whilst feeding optimally and opportunistically. Since beavers demonstrate adaptive foraging strategies depending on their foraging environment, this knowledge should be incorporated into future decisions on further reintroduction or habitat restoration programmes.

A jellyfish diet for the herbivorous green turtle Chelonia mydas in the temperate SW Atlantic

Feeding ecology of juvenile green turtles (Chelonia mydas) was studied from 2008 to 2011 at Samborombon Bay (35°30′–36°30′S, Argentina), combining data on digestive tract examination and stable isotope analysis through a Bayesian mixing model. We found that animal matter, in particular gelatinous plankton, was consumed in large proportions compared to herbivorous food items such as terrestrial plants and macroalgae. This diet is facilitated by the high abundance of gelatinous plankton in the region, thus confirming the adaptive foraging behaviour of the juveniles according to prey abundance in the SW Atlantic. To our knowledge, this is the first study to employ this combination of techniques and to conclusively demonstrate that animal matter, in particular gelatinous plankton, is important in the diet of the neritic green sea turtles.

Can bees simultaneously engage in adaptive foraging behaviour and attend to cryptic predators?

Bees foraging for nectar often have to discriminate between flowers with similar appearance but different nectar rewards. At the same time, they must be vigilant for ambush predators, such as crab spiders, which can camouflage themselves on flowers. We investigated whether bees, Bombus terrestris, can efficiently discriminate similar flower colours while exposed to predation threat from cryptic predators. Bees were individually tested in tightly controlled laboratory experiments using artificial flowers whose nectar supply was administered with precision pumps. Predation risk was simulated by automated crab spider ‘robots’ that captured bees for a limited duration without injuring them. Bees’ behaviour was monitored by a 3D video tracking system. We experimented with both cryptic and conspicuous spiders, finding that bees had no difficulty avoiding conspicuous spiders while still foraging adaptively. Conversely, they prioritized predator avoidance at the expense of maximizing energy intake when faced with detecting cryptic predators and a difficult colour discrimination task. This difference in behaviour was not due to cognitive limitations: bees were able to discriminate between similar flower types under predation risk from cryptic spiders when choosing the safe flower type incurred a gustatory punishment in the form of bitter quinine solution. However, this resulted in bees incurring substantially higher costs in terms of floral inspection times. We conclude that bees have the capacity to attend to difficult foraging tasks while simultaneously avoiding cryptic predators, but only do so when avoidance of gustatory punishment justifies the increased costs.

Elephant seal foraging dives track prey distribution, not temperature: Comment on McIntyre et al. (2011)

McIntyre et al. (2011; Mar Ecol Prog Ser 441:257?272) concluded that climate change-related ocean warming may lead to deeper foraging dives by southern elephant seals as their prey is forced into deeper depths. They further assert that fitness for the seals will be reduced because of greater physiological costs for deep dives and the assumption that deep foraging is less successful. Their conclusions are based on an observed correlation between a temperature index and elephant seal diving depth but do not include any observations of prey. We recently observed pronounced differences in the vertical distribution of pelagic biota—biota that may well include elephant seal prey—across the same frontal zone considered by McIntyre et al. (2011) and believe that their suggested link between temperature and diving depth is actually a link between predators and distinct prey fields—a reflection of adaptive foraging behaviour in a complex and dynamic pelagic system. As such, the analysis of McIntyre et al. (2011) is uninformative about likely impacts of ocean warming.

Adapting foraging to habitat heterogeneity and climate change: an individual-based model for wading birds

In an effort to assess the role of adaptive foraging behaviour to the spatial and temporal heterogeneity as a factor determining the success of the colony, we used single-colony individual-based spatial models for a visual foraging, the Great Blue Heron and a tactile foraging bird, the Wood Stork. The model followed simultaneously daily activities of individuals, their spatial movements, foraging efficiency, bioenergetics and growth of the nestlings during a nesting season. For each colony we used two scenarios; in the first, that depicted a normal nesting season, the extent and distribution of feeding sites led to successful reproduction for both species. In the second, we simulated increased precipitation regimes resulting in reversals in water depth (i.e. increases in depth during the dry season when water levels are normally falling). The results reveal that Wood Storks were significantly more adversely affected than Great Blue Herons by the prey dilution caused by the reversals in water depth. In the latter scenario where resources became scarce, resource predictability decreased. The foraging birds that foraged in groups exhibited low foraging success, resulting in poor reproductive performance. This result was more pronounced in the case of storks that foraged in groups than for herons foraging in groups. Concluding, increased variance in precipitation regimes is more likely to affect tactile rather than visual foraging bird species. Further, in harsh climatic conditions (increased precipitation and water level regimes) solitary foraging was more beneficial for wading birds than group foraging.

Adaptive behaviour, tri-trophic food-web stability and damping of chaos

We examine the effect of adaptive foraging behaviour within a tri-trophic food web with intra-guild predation. The intra-guild prey is allowed to adjust its foraging effort so as to achieve an optimal per capita growth rate in the face of realized feeding, predation risk and foraging cost. Adaptive fitness-seeking behaviour of the intra-guild prey has a stabilizing effect on the tri-trophic food-web dynamics provided that (i) a finite optimal foraging effort exists and (ii) the trophic transfer efficiency from resource to predator via the intra-guild prey is greater than that from the resource directly. The latter condition is a general criterion for the feasibility of intra-guild predation as a trophic mode. Under these conditions, we demonstrate rigorously that adaptive behaviour will always promote stability of community dynamics in the sense that the region of parameter space in which stability is achieved is larger than for the non-adaptive counterpart of the system.

Variance‐Sensitive Green Woodhoopoes: A New Explanation for Sex Differences in Foraging?

AbstractStudies of cooperatively breeding birds rarely benefit from the extensive research on adaptive foraging behaviour, despite the potential for concepts such as state‐dependent foraging to explain many aspects of behaviour in social groups. For example, sex differences in preferred foraging techniques used by green woodhoopoes, Phoeniculus purpureus, have previously been explained by sexual dimorphism in bill length and the benefits afforded by foraging specialization and niche differentiation within cooperative groups. Contrary to this argument, there were no sex differences in mean foraging success and/or prey size captured when males and females used the same foraging techniques. Subordinates of both sexes did experience lower and more varied foraging success compared with dominants, but probably only as a consequence of competition or inexperience. However, dominant males experienced greater variance in individual foraging success compared with dominant females, and dominant males also experienced greater variances in prey size when using their preferred foraging techniques. Dominant males therefore appeared to specialize in foraging techniques that provided more variable rewards, whilst dominant females consistently chose to minimize variation in reward. Dominant females also experienced less variance in foraging returns when using the same techniques as males, suggesting a possible link with sexual dimorphism in bill length. Partitioning of foraging niches in dominant green woodhoopoes therefore appears to be better explained by sex differences in variance (risk) sensitivity to foraging rewards. We suggest that this kind of detailed analysis of state‐dependent foraging has the potential to explain many of the crucial age and sex differences in behaviour within cooperative groups.

Effects of evolutionary changes in prey use on the relationship between food web complexity and stability

AbstractThe relationship between food web complexity and stability has been the subject of a long‐standing debate in ecology. Although rapid changes in the food web structure through adaptive foraging behavior can confer stability to complex food webs, as reported by Kondoh (Science 299:1388–1391, 2003), the exact mechanisms behind this adaptation have not been specified in previous studies; thus, the applicability of such predictions to real ecosystems remains unclear. One mechanism of adaptive foraging is evolutionary change in genetically determined prey use. We constructed individual‐based models of evolution of prey use by predators assuming explicit population genetics processes, and examined how this evolution affects the stability (i.e., the proportion of species that persist) of the food web and whether the complexity of the food web increased the stability of the prey–predator system. The analysis showed that the stability of food webs decreased with increasing complexity regardless of evolution of prey use by predators. The effects of evolution on stability differed depending on the assumptions made regarding genetic control of prey use. The probabilities of species extinctions were associated with the establishment or loss of trophic interactions via evolution of the predator, indicating a clear link between structural changes in the food web and community stability.