Population and community consequences of spatial subsidies derived from central-place foraging

Central-place foragers, such as ants, beavers, and colonial seabirds, can act as biological conduits, subsidizing local communities with allochthonous resources. To explore the consequences of such biologically vectored resource redistribution, we draw on an example from cave ecology and develop a population-level model of central-place foraging based on the dispersal kernel framework. We explore how the size of the patch in which central-place foraging occurs and the spatial distribution of foragers within that patch feed back to influence the population dynamics of the central-place forager and the species richness of the associated recipient community. We demonstrate that the particular way in which a population of central-place foragers uses space has two important effects. First, space use determines the stability of the forager population and establishes patch size thresholds for persistence, stable equilibria, and limit cycles. Second, alternative foraging kernels lead to qualitatively different scaling relationships between the size of the foraging patch and species richness back at the central place. These analyses provide a new link among elements of ecology related to animal behavior, population dynamics, and species diversity while also providing a novel perspective on the utility of integrodifference equations for problems in spatial ecology.     

Dynamic matching of forager size to resources in the continuously polymorphic leaf-cutter ant, Atta colombica (Hymenoptera, Formicidae)

Abstract.  1. Ergonomic optimisation theory proposes that by increasing variation in worker morphology, social insect colonies may increase their dietary breadth; however, little is known about how this relationship operates at the colony level. This study examines the colony-level pattern of forager size allocation to resource sites in a natural setting.
2. Using a biologically relevant measure of toughness, it is shown that leaf-cutter ant colonies exploit a variety of plant resources that vary significantly in toughness at any given time.
3. Forager size is shown to be matched to the toughness of plant material, with larger ants harvesting tougher material.
4. Furthermore, outbound foragers travelling to a harvest site are matched in size to the toughness of plant material contained within the site and are not a random selection of available foragers. The match between forager size and plant toughness may reduce the number of wasted trips and ill-matched foragers.
5. The observed colony-level pattern of forager allocation could be the result of learning by individual foragers, or the result of information shared at the colony level.     

The short-term regulation of foraging in harvester ants

In the seed-eating ant Pogonomyrmex barbatus, the return ofsuccessful foragers stimulates inactive foragers to leave thenest. The rate at which successful foragers return to the nestdepends on food availability; the more food available, the morequickly foragers will find it and bring it back. Field experimentsexamined how quickly a colony can adjust to a decline in therate of forager return, and thus to a decline in food availability,by slowing down foraging activity. In response to a brief, 3-to 5-min reduction in the forager return rate, foraging activityusually decreased within 2–3 min and then recovered within5 min. This indicates that whether an inactive forager leavesthe nest on its next trip depends on its very recent experienceof the rate of forager return. On some days, colonies respondedmore to a change in forager return rate. The rapid colony responseto fluctuations in forager return rate, enabling colonies toact as risk-averse foragers, may arise from the limited intervalover which an ant can track its encounters with returning foragers.     

Socially stable territories: the negotiation of space by interacting foragers

This article presents a theory of territoriality that integrates optimal foraging and conflict resolution through negotiation. Using a spatially explicit model of a sit-and-wait forager, we show that when resources are scarce, there is a conflict between foragers: there is not enough space for all individuals to have optimal home ranges. We propose that a division of space that solves this conflict over resources is the outcome of a negotiation between foragers. We name this outcome the socially stable territories (SST). Using game theory we show that in a homogenous patch occupied by two interacting foragers, both individuals receive identical energy yields at the socially stable territories; that is, there is economic equity. Economic inequity can arise in a heterogeneous patch or from asymmetries in fighting abilities between the foragers. Opportunity costs play a role in reducing economic inequity. When the asymmetry in fighting abilities is very large, a negotiated division of space is not possible and the forager with lowest fighting ability may be evicted from the habitat patch. A comparison between territories and overlapping home ranges shows that energy yields from territories are generally higher. We discuss why there are instances in which individuals nevertheless overlap home ranges.     

Obtaining Specimens with Slowed,Accelerated and Reversed Aging in the Honey Bee Model

Societies of highly social animals feature vast lifespan differences between closely related individuals. Among social insects, the honey bee is the best established model to study how plasticity in lifespan and aging is explained by social factors.The worker caste of honey bees includes nurse bees, which tend the brood, and forager bees, which collect nectar and pollen. Previous work has shown that brain functions and flight performance senesce more rapidly in foragers than in nurses. However, brain functions can recover, when foragers revert back to nursing tasks. Such patterns of accelerated and reversed functional senescence are linked to changed metabolic resource levels, to alterations in protein abundance and to immune function. Vitellogenin, a yolk protein with adapted functions in hormonal control and cellular defense, may serve as a major regulatory element in a network that controls the different aging dynamics in workers.Here we describe how the emergence of nurses and foragers can be monitored, and manipulated, including the reversal from typically short-lived foragers into longer-lived nurses. Our representative results show how individuals with similar chronological age differentiate into foragers and nurse bees under experimental conditions. We exemplify how behavioral reversal from foragers back to nurses can be validated. Last, we show how different cellular senescence can be assessed by measuring the accumulation of lipofuscin, a universal biomarker of senescence.For studying mechanisms that may link social influences and aging plasticity, this protocol provides a standardized tool set to acquire relevant sample material, and to improve data comparability among future studies.     

Using spatially explicit models to characterize foraging performance in heterogeneous landscapes

ABSTRACT The success of most foragers is constrained by limits to their sensory perception, memory, and locomotion. However, a general and quantitative understanding of how these constraints affect foraging benefits, and the trade-offs they imply for foraging strategies, is difficult to achieve. This article develops foraging performance statistics to assess constraints and define trade-offs for foragers using biased random walk behaviors, a widespread class of foraging strategies that includes area-restricted searches, kineses, and taxes. The statistics are expected payoff and expected travel time and assess two components of foraging performance: how effectively foragers distinguish between resource-poor and resourcerich parts of their environments and how quickly foragers in poor parts of the environment locate resource concentrations. These statistics provide a link between mechanistic models of individuals' movement and functional responses, population-level models of forager distributions in space and time, and foraging theory predictions of optimal forager distributions and criteria for abandoning resource patches. Application of the analysis to area-restricted search in coccinellid beetles suggests that the most essential aspect of these predators's foraging strategy is the "turning threshold," the prey density at which ladybirds switch from slow to rapid turning. This threshold effectively determines whether a forager exploits or abandons a resource concentration. Foraging is most effective when the threshold is tuned to match physiological or energetic requirements. These performance statistics also help anticipate and interpret the dynamics of complex spatially and temporally varying forager-resource systems.     

Integrating the roles of information and competitive ability on the spatial distribution of social foragers

Understanding and predicting the spatial distribution of social foragers among patchily distributed resources is a problem that has been addressed with numerous approaches over the 30 yr since the ideal free distribution (IFD) was first introduced. The two main approaches involve perceptual constraints and unequal competitors. Here we present a model of social foragers choosing among resource patches. Each forager makes a probabilistic choice on the basis of the information acquired through past foraging experiences. Food acquisition is determined by the forager's competitive ability. This model predicts that perceptual constraints have a greater influence on the spatial distribution of foragers than unequal competitive abilities but that competitive ability plays an important role in determining an individual's information state and behavior. Better competitors have access to more information; consequently, we find that competitive abilities and perceptual constraints are integrated through the social environment occupied by individual foragers. Relative competitive abilities influence the forager's information state, and the ability to use information determines the resulting spatial distribution.     

Smart,smarter, smartest: foraging information states and coexistence

Animals possess different abilities to gain and use information about the foraging patches they exploit. When ignorant of the qualities of encountered patches, a smart forager should leave all patches after the same amount of fixed search time. A smarter forager can be Bayesian by using information on cumulative harvest and time spent searching a patch to better inform its patch‐departure decision. The smartest forager has immediate and continuous knowledge about patch quality, and can make a perfect decision about when to leave each patch. Here we let each of these three strategies harvest resources from a slowly regenerating environment. Eventually a steady‐state distribution of prey among patches arises where the environment‐wide resource renewal just balances the environment‐wide harvest of the foragers. The fixed time forager creates a distribution with the highest mean and highest variance of patch qualities, followed by the Bayesian and the prescient in that order. The less informed strategies promote distributions with both more resources and more exploitable information than the more informed strategies. While it is true that a better‐informed strategy will always out‐perform a less well‐informed, its increase in performance may not compensate it for any costs associated with being better informed. We imagine that the fixed time strategy may be least expensive and the prescient strategy most expensive in terms of sensory organs and associated assess and respond capabilities. To consider competition between such strategies with varying costs, we introduced a single individual of each of the strategies into the environments created by populations of the other strategies. There are threshold costs associated with the better‐informed strategy such that it can or cannot outcompete a less‐informed strategy. However, over a relatively narrow range of foraging costs, less‐informed and better‐informed strategies will coexist. Furthermore, for the prescient and the Bayesian strategies, some combinations of foraging costs produce alternate stable states – whichever strategy establishes first remains safe from invasion by the other.     

Remembering the good and the bad: memory-based mediation of the food–safety trade-off in dynamic landscapes

Predator–prey interactions are central to fitness as animals simultaneously avoid death and consume resources to ensure growth and reproduction. Along with direct effects, predators can also exert strong non-consumptive effects. For example, prey shift habitat use in the presence of predators, a potentially learned behavior. The impact of cognition on movement and predator interactions is largely unexplored despite evidence of learned responses to predation threat. We explore how learning and spatial memory influence predator–prey dynamics by introducing predators into a memory-driven movement modeling framework. To model various aspects of risk, we vary predator behavior: their persistence and spatial correlation with the prey’s resources. Memory outperforms simpler movement processes most in patchy environments with more predictable predators that are more easily avoided once learned. In these cases, memory aids foragers in managing the food–safety trade-off. For example, particular parameterizations of the predation memory reduce encounters while maintaining consumption. We found that non-consumptive effects are highest in landscapes of concentrated, patchy resources. These effects are intensified when predators are highly correlated with the forager’s resources. Smooth landscapes provide more opportunities for foragers to simultaneously consume resources and avoid predators. Predators are able to effectively guard all resources in very patchy landscapes. These non-consumptive effects are also seen with the shift away from the best quality habitat compared to foraging in a predator-free environment.     

Bumble bee olfactory information flow and contact-based foraging activation

Nestmate foraging activation and interspecific variation in foraging activation is poorly understood in bumble bees, as compared to honey bees and stingless bees. We therefore investigated olfactory information flow and foraging activation in the New World bumble bee species, Bombus impatiens. We (1) tested the ability of foragers to associate forager-deposited odor marks with rewarding food, (2) determined whether potential foragers will seek out the food odor brought back by a successful forager, and (3) examined the role of intranidal tactile contacts in foraging activation. Bees learned to associate forager-deposited odor marks with rewarding food. They were significantly more attracted to an empty previously rewarding feeder presented at a random position within an array of eight previously non-rewarding feeders. However, foragers did not exhibit overall odor specificity for short-term, daily floral shifts. For two out of three tested scents, activated foragers did not significantly prefer the feeder providing the same scent as that brought back by a successful forager. Finally, bees contacted by the successful forager inside the nest were significantly more likely to leave the nest to forage (38.6% increase in attempts to feed from empty feeders) than were non-contacted bees. This is the first demonstration that tactile contact, a hypothesized evolutionary basal communication mechanism in the social corbiculate bees, is involved in bumble bee foraging activation. Received 4 September 2007; revised 30 May 2008; accepted 15 July 2008.     

Fast food in ant communities: how competing species find resources

An understanding of foraging behavior is crucial to understanding higher level community dynamics; in particular, there is a lack of information about how different species discover food resources. We examined the effect of forager number and forager discovery capacity on food discovery in two disparate temperate ant communities, located in Texas and Arizona. We defined forager discovery capacity as the per capita rate of resource discovery, or how quickly individual ants arrived at resources. In general, resources were discovered more quickly when more foragers were present; this was true both within communities, where species identity was ignored, as well as within species. This pattern suggests that resource discovery is a matter of random processes, with ants essentially bumping into resources at a rate mediated by their abundance. In contrast, species that were better discoverers, as defined by the proportion of resources discovered first, did not have higher numbers of mean foragers. Instead, both mean forager number and mean forager discovery capacity determined discovery success. The Texas species used both forager number and capacity, whereas the Arizona species used only forager capacity. There was a negative correlation between a species’ prevalence in the environment and the discovery capacity of its foragers, suggesting that a given species cannot exploit both high numbers and high discovery capacity as a strategy. These results highlight that while forager number is crucial to determining time to discovery at the community level and within species, individual forager characteristics influence the outcome of exploitative competition in ant communities.     

Combining Perturbations and Parameter Variation to Influence Mean First Passage Times

Perturbations are relatively large shocks to state variables that can drive transitions between stable states, while drift in parameter values gradually alters equilibrium magnitudes. This latter effect can lead to equilibrium bifurcation, the generation, or annihilation of equilibria. Equilibrium annihilations reduce the number of equilibria and so are associated with catastrophic population collapse. We study the combination of perturbations and parameter drift, using a two-species intraguild predation (IGP) model. For example, we use bifurcation analysis to understand how parameter drift affects equilibrium number, showing that both competition and predation rates in this model are bifurcating parameters. We then introduce a stochastic process to model the effects of population perturbations. We demonstrate how to evaluate the joint effects of perturbations and drift using the common currency of mean first passage time to transitions between stable states. Our methods and results are quite general, and for example, can relate to issues in both pest control and sustainable harvest. Our results show that parameter drift (1) does not importantly change the expected time to reach target points within a basin of attraction, but (2) can dramatically change the expected time to shift between basins of attraction, through its effects on equilibrium resilience.     

A search theory model of patch-to-patch forager movement with application to pollinator-mediated gene flow

We present a spatially implicit analytical model of forager movement, designed to address a simple scenario common in nature. We assume minimal depression of patch resources, and discrete foraging bouts, during which foragers fill to capacity. The model is particularly suitable for foragers that search systematically, foragers that deplete resources in a patch only incrementally, and for sit-and-wait foragers, where harvesting does not affect the rate of arrival of forage. Drawing on the theory of job search from microeconomics, we estimate the expected number of patches visited as a function of just two variables: the coefficient of variation of the rate of energy gain among patches, and the ratio of the expected time exploiting a randomly chosen patch and the expected time travelling between patches. We then consider the forager as a pollinator and apply our model to estimate gene flow. Under model assumptions, an upper bound for animal-mediated gene flow between natural plant populations is approximately proportional to the probability that the animal rejects a plant population. In addition, an upper bound for animal-mediated gene flow in any animal-pollinated agricultural crop from a genetically modified (GM) to a non-GM field is approximately proportional to the proportion of fields that are GM and the probability that the animal rejects a field.     

The role of recombination and selection in the modifier theory of sex-ratio distortion

The equilibrium configurations for a two-locus multialle model of sex-linked meiotic drive are studied with regard to the recombination fraction:limit cycles can occur in the case of small recombination while stable equilibrium points associated with linkage equilibrium can exist for an intermediate range of recombination values depending on the equilibrium sex ratio, linkage disequilibrium at nearby equilibrium points taking turn with loser linkage. The evolutionary dynamics in two-locus sex-ratio distortion systems is enlightened: while equilibria with a sex ratio closer to 1/2 are more likely to be stable with respect to perturbations on the frequencies of sex-ratio distorters that are represented at equilibrium, such equilibria are also more vulnerable to the invasion of mutant distorters when there is some degree of linkage with the sex-determining locus. For X-linked multimodifier systems of sex-ratio distortion, differential fertilities and viabilities are incorporated and a maximum principle is suggested.     

Differential learning and memory by co-occurring ant species

Foragers of the antsMessor pergandei andPogonomyrmex rugosus experience differing levels of variability in the distribution of seeds they harvest due to species-specific differences in foraging behavior.Messor pergandei foragers experience more variable seed distributions and densities, learn to recognize a novel seed faster but forget this information faster thanP. rugosus, which experiences more constant seed distributions even in the same habitat. Rate of learning to recognize a novel seed species was negatively associated with measures of seed species diversity for both ants.Messor pergandei foragers respond to variation in seed density by varying number of seeds handled per seed harvested, whileP. rugosus foragers do not. Memory of a novel seed exceeds forager longevity, due perhaps to use of seed caches as a type of information center.     

Temperature and forager body size affect carbohydrate collection in German yellowjackets, Vespula germanica (Hymenoptera, Vespidae)

The classic formulation of optimal foraging theory predicts that a central-place forager will gather more food if it is required to travel farther from the nest to find that food. We examined the foraging behavior of German yellowjackets (Vespula germanica) to determine whether carbohydrate foragers follow this pattern. We trained foragers to collect 2 M fructose solution at 5 or 50 m from the nest and measured the time spent feeding, load size, and the rate of delivery. We show that as a forager’s crop fills during a foraging bout, the amount of solution ingested per second decreased. However, load size did not change as wasps collected food up to 50 m from the nest. Instead, temperature and body size were better predictors of the volume of fructose a forager carried. Finally, the rate of fructose delivered to the nest was higher at warmer temperatures. Due to the fact that wasps gather more food but feed for shorter periods of time at warmer temperatures, we found an overall negative relationship between feeding time and load size. We conclude that the strong effects temperature had on the behavior of V. germanica foragers imply that feeding time may not always be an accurate predictor of the size of the load an individual carries back to the nest. Results from this study suggest that in yellowjacket colonies, foragers can collect and bring disproportionately more food back to the nest during the warmest days of the summer, a time of year when this pest species reaches peak population size during its annual colony cycle.     

Foragers versus farmers: contrasting effects of two behavioural groups of herbivores on coral reefs

Herbivorous fishes have been attributed a central role in structuring benthic communities on coral reefs. However, the relative importance of different behavioural groups of herbivores may differ and their interactions may be complex. This study focuses on an experiment that discriminates between two groups of herbivorous fish: (1) “Foragers” (relatively mobile, schooling grazers, including parrotfishes and surgeonfishes) and (2) “Farmers” (highly site-attached, territorial species, primarily damselfishes). Preliminary observations at Kimbe Bay (Papua New Guinea) showed that both groups were common, and that farmers defended areas from foragers and maintained algal communities that were distinct from the surrounding undefended substratum. An orthogonal combination of a farmer removal treatment and a forager exclusion treatment was applied to isolate their separate effects on algae and corals, and to determine whether farmer territory composition results from forager exclusion or algal cultivation. The experiment showed that foragers had quantitatively greater and qualitatively different effects on sessile benthic community structure than farmers. Where foragers were excluded, there were substantial increases in the cover and biomass of macro-algae and a decline in some corals, regardless of the presence of farmers. Where farmers were removed there was a moderate decline in the cover of some food algal species, regardless of whether foragers had access. No effect of the exclusion of foragers by farmers could be detected. Our results support prevailing views that foragers have a major impact on coral reefs and farmers cultivate selected algae, but challenge the hypothesis that damselfish influence habitat structure by moderating forager disturbance.     

Optimal movement between patches under incomplete information about the spatial distribution of food items

If the food distribution contains spatial pattern, the food density in a particular patch provides a forager with information about nearby patches. Foragers might use this information to exploit patchily distributed resources profitably. We model the decision on how far to move to the next patch in linear environments with different spatial patterns in the food distribution (clumped, random, and regular) for foragers that differ in their degree of information. An ignorant forager is uninformed and therefore always moves to the nearest patch (be it empty or filled). In contrast, a prescient forager is fully informed and only exploits filled patches, skipping all empty patches. A Bayesian assessor has prior knowledge about the content of patches (i.e. it knows the characteristics of the spatial pattern) and may skip neighbouring patches accordingly by moving to the patch where the highest gain rate is expected. In most clumped and regular distributions there is a benefit of assessment, i.e. Bayesian assessors achieve substantially higher long-term gain rates than ignorant foragers. However, this is not the case in distributions with less strong spatial pattern, despite the fact that there is a large potential benefit from a sophisticated movement rule (i.e. a large penalty of ignorance). Bayesian assessors do also not achieve substantially higher gain rates in environments that are relatively rich or poor in food. These results underline that an incompletely informed forager that is sensitive to spatial pattern should not always respond to existing pattern. Furthermore, we show that an assessing forager can enhance its long-term gain rate in highly clumped and some specific near-regular food distributions, by sampling the environment in slightly larger spatial units.     

Harvesting resources in groups or alone: the case of renewing patches

Group foraging has been proposed to be the most efficient mannerwith which to exploit habitats with renewing patches as individualsin groups are less likely to revisit patches that have alreadybeen exploited recently by others. However, to avoid a group-selectionargument, it is necessary to compare the success of solitaryand group foraging tactics when each competes with the other.We used a genetic algorithm approach to examine the costs andbenefits of exploiting renewing resources in a spatially andtemporally explicit habitat, thus controlling the time courseof resource renewal and including the time cost of travelingbetween patches, which may be a significant factor for groupforagers that deplete patches more quickly. Results indicatethat group foragers fare more poorly than an equivalent numberof solitary foragers in the same habitat unless the rate ofresource renewal is very low. The low revisitation rate by groupforagers allows resources to replenish more fully, thus maintainingthe resource level across the habitat at a higher level. Incontrast, solitary foragers, who revisit previously exploitedpatches more often, maintain the same resources at a lower level.Nevertheless, a pure population of group foragers can be readilyinvaded by solitary foragers even when the rate of renewal isat low levels. We conclude that while group foraging may bean efficient tactic to exploit renewing resources, it is nota stable strategy under the circumstances examined in this model.     

Optimal movement between patches under incomplete information about the spatial distribution of food items

If the food distribution contains spatial pattern, the food density in a particular patch provides a forager with information about nearby patches. Foragers might use this information to exploit patchily distributed resources profitably. We model the decision on how far to move to the next patch in linear environments with different spatial patterns in the food distribution (clumped, random, and regular) for foragers that differ in their degree of information. An ignorant forager is uninformed and therefore always moves to the nearest patch (be it empty or filled). In contrast, a prescient forager is fully informed and only exploits filled patches, skipping all empty patches. A Bayesian assessor has prior knowledge about the content of patches (i.e. it knows the characteristics of the spatial pattern) and may skip neighbouring patches accordingly by moving to the patch where the highest gain rate is expected. In most clumped and regular distributions there is a benefit of assessment, i.e. Bayesian assessors achieve substantially higher long-term gain rates than ignorant foragers. However, this is not the case in distributions with less strong spatial pattern, despite the fact that there is a large potential benefit from a sophisticated movement rule (i.e. a large penalty of ignorance). Bayesian assessors do also not achieve substantially higher gain rates in environments that are relatively rich or poor in food. These results underline that an incompletely informed forager that is sensitive to spatial pattern should not always respond to existing pattern. Furthermore, we show that an assessing forager can enhance its long-term gain rate in highly clumped and some specific near-regular food distributions, by sampling the environment in slightly larger spatial units.