Global optimization from suboptimal parts: foraging sensu lato by leaf-cutting ants

Central-place foraging theory has been unable to explain the load selection behavior of leaf-cutting ants (Atta spp., Attini: Formicidae). We suggest that this is due to incomplete consideration of the sequence of behaviors involved in resource acquisition by these ants. Unlike most central-place foragers, leaf-cutting ants do not return to their nests with food. Instead, the leaf fragments they gather must be processed within the nest to convert them to substrate for fungal gardens. We have shown previously that leaf fragment size affects the rate of distribution and processing of leaf tissue inside laboratory nests of Atta colombica. Including these tasks in the calculation of foraging rate may help explain load selection and other features of central-place foraging by Atta colonies. Here we develop a mathematical model of the complete sequence of external and internal tasks that lead to addition of substrate to fungal gardens. Using realistic parameter values, the leaf fragment sizes predicted to maximize a colony's rate of foraging in this broad sense correspond well with the mean fragment sizes actually collected by Atta colonies in the field. The optimal fragment size for global performance in the model is below the size that would maximize the delivery rate by above-ground foragers. The globally optimal size also fails to maximize the rate of either fragment distribution or fragment processing within the nest. Our results show how maximum collective performance of an ensemble of linked tasks may require behavior that would appear suboptimal in a piecemeal analysis of tasks.     

Imperfectly optimal animals

Summary We consider models of behavior that apply to two different problems: when a predator should leave a foraging site and how a female should choose the best available male. In each case we derive rules for an optimal solution to the problem. We also derive models based on very simple, plausible rules of behavior that we suspect animals may actually use. Although the expected payoffs from optimality models always exceed the expected payoffs from our simpler behavioral models, under certain conditions the difference is not large. When good foraging sites last but a short time and when females' mobility in their habitat is limited, the results of simple models and optimal models are very close indeed.Because of the difficulty of distinguishing between the results of each type of model and because natural selection will presumably provide a best mix of solutions to a range of problems rather than a best solution to any one problem, we suggest that behavioral ecologists expend more effort on simple, plausible models of animal behavior. Such models provide ready-made testable hypotheses about the animal's approximation to optimality and about the actual mechanisms of behavior.     

Individual experience-based foraging can generate community territorial structure for competing ant species

To gain additional territory while defending existing territory, animals must acquire and use information regarding resource characteristics and competitive pressure. For social organisms like ants, individual workers have experiences to acquire information, but territory establishment is a colony level behavior. Colony behavior, in turn, affects community structure. Here, I investigate how an individual ant’s previous experience affects its future foraging behavior and how individual behaviors can scale up to community territorial structure for two coexisting Formica species. To do this, I combine a field survey, a multi-agent computer simulation, and a manipulation experiment. The field survey shows that workers of both species co-occur on many trees early in the season, but ants on trees become segregated by species as the season progresses. The simulation demonstrates how this segregated spatial distribution can result from ants using a foraging strategy in which individuals show a preference for foraging sites based on previous experience. The experiment suggests that these ants are indeed capable of experience-based foraging behavior; ants preferentially return to sites where they have had positive experiences and avoid sites where they have had negative experiences. Results from this study suggest that spatially explicit information can be collected and stored by individuals to facilitate colony territorial structure, and that future investigations of community territory formation should include effects of individual previous experience.     

Individual energetic state can prevail over social regulation of foraging in honeybees

The energetic state of an individual is a fundamental driver of its behavior. However, an individual in a eusocial group such as the honeybees is subject to the influence of both the individual and the colony energetic states. As these two states are normally coupled, it has led to the predominant view that behaviors, such as foraging, are dictated by the colony state acting through social regulatory mechanisms. Uncoupling the energetic state of an individual honeybee from its colony by feeding it with a non-nutritious sugar, we show that energetically stressed bees in a colony with full food stores do not consume this food to meet their energetic shortfall but instead compensate by first reducing their activity level and then by increasing their foraging rate. This suggests that foraging in eusocial groups is still partly under the regulatory control of the energetic state of the individual and supports the notion that regulatory mechanisms in solitary insects have been co-opted to drive altruistic behavior in eusocial insects. The observation that energetically stressed bees also experience higher mortality during foraging also suggests that energetic stress mediated by a variety of factors can be a common mechanism that underlies the recent observation of bees disappearing from their colonies. We also discuss how nutritional imbalance in a social insect individual can alter its behavior to influence colony life history.     

Constraints on foraging success due to resource ecology limit colony productivity in social insects

The benefit of group living is a fundamental question in social evolution. For sociality to evolve, each individual must gain in terms of some fitness component by living in larger groups. However, in social insects, a decrease in per capita success in brood production has been observed in larger groups. While it has been proposed that this decrease could be outweighed by an increase in the predictability of success, a functional basis to this hypothesis has so far never been demonstrated. In this paper, using foraging economics as a functional proxy to colony productivity, we construct a model to explore how number of foragers in the colony interacts with the ecology of resources to influence per capita foraging success and its predictability. The results of the model show that there is no increase in per capita foraging success in larger colonies under most circumstances, though there is an increase in its predictability. We then test the model with empirical data on the foraging behavior of the primitively eusocial wasp, Ropalidia marginata. The consistency between the data and the model suggests that foraging economics could provide a robust functional basis in explaining the relationship between colony size and productivity.     

A systematic survey of the integration of animal behavior into conservation

The role of behavioral ecology in improving wildlife conservation and management has been the subject of much recent debate. We sought to answer 2 foundational questions about the current use of behavioral knowledge in conservation: To what extent is behavioral knowledge used in wildlife conservation and management, and how does the use of animal behavior differ among conservation fields in both frequency and types of use? We searched the literature for intersections between key fields of animal behavior and conservation and created a systematic heat map (i.e., graphical representation of data where values are represented as colors) to visualize relative efforts. Some behaviors, such as dispersal and foraging, were commonly considered (mean [SE] of 1147.38 [353.11] and 439.44 [108.85] papers per cell, respectively). In contrast, other behaviors, such as learning, social, and antipredatory behaviors were rarely considered (mean [SE] of 33.88 [7.62], 44.81 [10.65], and 22.69 [6.37] papers per cell, respectively). In many cases, awareness of the importance of behavior did not translate into applicable management tools. Our results challenge previous suggestions that there is little association between the fields of behavioral ecology and conservation and reveals tremendous variation in the use of different behaviors in conservation. We recommend that researchers focus on examining underutilized intersections of behavior and conservation themes for which preliminary work shows a potential for improving conservation and management, translating behavioral theory into applicable and testable predictions, and creating systematic reviews to summarize the behavioral evidence within the behavior‐conservation intersections for which many studies exist.     

Pattern-oriented modeling of bird foraging and pest control in coffee farms

We develop a model of how land use and habitat diversity affect migratory bird populations and their ability to suppress an insect pest on Jamaican coffee farms. Bird foraging—choosing which habitat patch and prey to use as prey abundance changes over space and time—is the key process driving this system. Following the “pattern-oriented” modeling strategy, we identified nine observed patterns that characterize the real system's dynamics. The model was designed so that these patterns could potentially emerge from it. The resulting model is individual-based, has fine spatial and temporal resolutions, represents very simply the supply of the pest insect and other arthropod food in six habitat types, and includes foraging habitat selection as the only adaptive behavior of birds. Although there is an extensive heritage of bird foraging theory in ecology, most of it addresses only the individual level and is too simple for our context. We used pattern-oriented modeling to develop and test foraging theory for this across-scale problem: rules for individual bird foraging that cause the model to reproduce a variety of patterns observed at the system level. Four alternative foraging theories were contrasted by how well they caused the model to reproduce the nine characteristic patterns. Four of these patterns were clearly reproduced with the “null” theory that birds select habitat randomly. A version of classical theory in which birds stay in a patch until food is depleted to some threshold caused the model to reproduce five patterns; this theory caused lower, not higher, use of habitat experiencing an outbreak of prey insects. Assuming that birds select the nearby patch providing highest intake rate caused the model to reproduce all but one pattern, whereas assuming birds select the highest-intake patch over a large radius produced an unrealistic distribution of movement distances. The pattern reproduced under none of the theories, a negative relation between bird density and distance to trees, appears to result from a process not in the model: birds return to trees at night to roost. We conclude that a foraging model for small insectivorous birds in diverse habitat should assume birds can sense higher food supply but over short, not long, distances.     

Self-organization in collective honeybee foraging: emergence of symmetry breaking,cross inhibition and equal harvest-rate distribution

De Vries and Biesmeijer described in 1998 an individual-oriented model that simulates the collective foraging behaviour of a colony of honeybees. Here we report how this model has been expanded and show how, through self-organization, three colony-level phenomena can emerge: symmetry breaking, cross inhibition and the equal harvest-rate distribution. Symmetry breaking is the phenomenon that the numbers of foragers visiting two equally profitable food sources will diverge after some time. Cross inhibition is the phenomenon that, by increasing the profitability of one of two equal food sources, the number of foragers visiting the other source will decrease. In some circumstances, the bees foraging on two sources of different profitabilities will be distributed between these sources such that the two average energy harvest rates are equal. We will refer to this phenomenon as the equal harvest-rate distribution. For each of these three phenomena, we show what the necessary behavioural rules to be followed by the individual forager bees are, and what the necessary circumstances are (that is, what values the model parameters should take) in order for these phenomena to arise. It seems that patch size and forager group size largely determine when each of these phenomena will arise. Experimenting with two types of currency, net gain rate and net gain efficiency, revealed that only gain rate may result in an equal harvest-rate distribution of foragers visiting different food sources.     

Energy gains predict the distribution of plains bison across populations and ecosystems

Developing tools that help predict animal distribution in the face of environmental change is central to understanding ecosystem function, but it remains a significant ecological challenge. We tested whether a single foraging currency could explain bison (Bison bison) distribution in dissimilar environments: a largely forested environment in Prince Albert National Park (Saskatchewan, Canada) and a prairie environment in Grasslands National Park (Saskatchewan, Canada). We blended extensive behavioral observations, relocations of radio-collared bison, vegetation surveys, and laboratory analyses to spatially link bison distribution in the two parks and expected gains for different nutritional currencies. In Prince Albert National Park, bison were more closely associated with the distribution of plants that maximized their instantaneous energy intake rate (IDE) than their daily intake of digestible energy. This result reflected both bison's intensity of use of individual meadows and their selection of foraging sites within meadows. On this basis, we tested whether IDE could explain the spatial dynamics of bison reintroduced to Grasslands National Park. As predicted, bison distribution in this park best matched spatial patterns of plants offering rapid IDE rather than rapid sodium intake, phosphorus intake, or daily intake of digestible energy. Because the two study areas have very different plant communities, a phenomenological model of resource selection developed in one area could not be used to predict animal distribution in the other. We were able, however, to successfully infer the distribution of bison from their foraging objective. This consistency in foraging currency across ecosystems and populations provides a strong basis for forecasting animal distributions in novel and dynamic environments.     

Behavioral and life-history components of division of labor in honey bees (Apis mellifera L.)

Variability exists among worker honey bees for components of division of labor. These components are of two types, those that affect foraging behavior and those that affect life-history characteristics of workers. Variable foraging behavior components are: the probability that foraging workers collect (1) pollen only; (2) nectar only; and (3) pollen and nectar on the same trip. Life history components are: (1) the age the workers initiate foraging behavior; (2) the length of the foraging life of a worker; and (3) worker length of life. We show how these components may interact to change the social organization of honey bee colonies and the lifetime foraging productivity of individual workers. Selection acting on foraging behavior components may result in changes in the proportion of workers collecting pollen and nectar. Selection acting on life-history components may affect the size of the foraging population and the distribution of workers between within nest and foraging activities. We suggest that these components define possible sociogenic pathways through which colony-level natural selection can change social organization. These pathways may be analogous to developmental pathways in the morphogenesis of individual organisms because small changes in behavioral or life history components of individual workers may lead to major changes in the organizational structure of colonies. Correspondence to: R.E. Page, Jr.     

Why is competition more intense if food is supplied more slowly?

We investigated competition for food among two groups of six clone amagos (salmonids), Oncorhynchusmasoumacrostomus, in a laboratory experiment with different rates of food input. We examined the effect of temporal clumping of food resources on the inequality of food sharing between competitors. Monopolization of food by dominants was greater at a low input rate (one food item per 10 s) than at a high input rate (1 food item per 1 s). Aggressive behavior by dominants was more frequent at the low input rate than at the high input rate; its purpose was presumably to interfere with the feeding behavior of subordinates. We assessed the relative importance of three foraging factors (the number of approaches to food items, the chance per approach and the gain per chance) in enhancing inequality in food gain between individuals. Dominants had a disproportionately high chance per approach and gain per chance at the low input rate, but not at the high input rate. The chance of obtaining a food item per approach depended on how many competitors approached simultaneously. The gain per chance depended on the competitive ability of the approaching fish. There was an interaction between these components, such that the number of approaches affected the chance per approach and gain per chance. We evaluated the independent effect of the chance per approach, and showed that it was higher for dominants than for subordinates at the low input rate, but not at the high input rate. This implies that subordinates changed their behavior and became more likely to avoid approaching food at the same time as dominants at the low input rate. Received: 13 August 1996 / Accepted after revision: 30 November 1996     

High social density increases foraging and scouting rates and induces polydomy in Temnothorax ants

Many organisms live in crowded groups where social density affects behavior and fitness. Social insects inhabit nests that contain many individuals where physical interactions facilitate information flow and organize collective behaviors such as foraging, colony defense, and nest emigration. Changes in nest space and intranidal crowding can alter social interactions and affect worker behavior. Here, I examined the effects of social density on foraging, scouting, and polydomy behavior in ant colonies—using the species Temnothorax rugatulus. First, I analyzed field colonies and determined that nest area scaled isometrically with colony mass—this indicates that nest area changes proportionally with colony size and suggests that ants actively control intranidal density. Second, laboratory experiments showed that colonies maintained under crowded conditions had greater foraging and scouting activities compared to the same colonies maintained at a lower density. Moreover, crowded colonies were significantly more likely to become polydomous. Polydomous colonies divided evenly based on mass between two nests but distributed fewer, heavier workers and brood to the new nests. Polydomous colonies also showed different foraging and scouting rates compared to the same colonies under monodomous conditions. Combined, the results indicate that social density is an important colony phenotype that affects individual and collective behavior in ants. I discuss the function of social density in affecting communication and the organization of labor in social insects and hypothesize that the collective management of social density is a group level adaptation in social insects.     

Colony energy requirements affect the foraging currency of bumble bees

Summary This study examines whether the foraging behavior of worker bumble bees (Bombus: Apidae) collecting nectar on inflorescences of seablush (Plectritis congesta: Valerianaceae) is affected by colony energetic requirements, which were experimentally manipulated either by adding sucrose solution to honey pots or by removing virtually all available nectar from the pots. The competing hypotheses tested were: (1) no change; energetic requirements do not affect behavior, since there is a single best way to collect food in a given environment; (2) energetic currency; the energetic currency maximized by foragers changes according to colony energetic condition, with nectar-depletion causing a shift from maximizing long-term productivity to maximizing immediate energetic gain, thereby de-emphasizing energetic costs; and (3) predation; foragers devalue risk of predation as risk of starvation increaes, with colony nectar-depletion causing foragers to be less predation riskaverse in order to increase immediate energetic gain. Relative to when their colony energy reserves were enhanced, foragers from nectar-depleted colonies selected smaller inflorescences, visited fewer flowers per inflorescence, probed flowers at a higher rate while on each inflorescence, and walked between inflorescences less often, thereby spending a greater proportion of their foraging trip in flight. These behaviors increased a bee's energetic costs while foraging, and should also have increased its immediate energetic gains, allowing rejection of the no change hypothesis. Predictions of the predation hypothesis were generally not supported, and our results best support the energetic currency hypothesis. Foraging currency of bumble bees therefore appears to be a function of colony energetic state. Offprint requests to: R.V. Cartar     

Habitat structure helps guide the emergence of colony-level personality in social spiders

Studying the environmental factors that guide the emergence of collective behaviors is instrumental to understanding the ecology and evolution of animal societies. Although recent work has provided insights into the demographic factors that influence inter-colony variation in collective behavior (i.e., colony-level personality or collective personality), relatively few studies have investigated how the physical environment (e.g., habitat structure) affects colony-level personality. Here, we study the emergence of collective personality in prey capture behavior in the social spider, Stegodyphus dumicola. We measured collective prey capture behavior four times over 36 days in a classic repeated measures design. We used four different artificial habitat (web support) structures in three different treatments: habitat structure was either (1) fixed and undisturbed, (2) disturbed with a complete removal of webbing between each measurement, or (3) disturbed with changes of habitat structure between each measurement. Our results revealed that repeatability in colony-level personality was retained as long as habitat structure was not altered. However, the repeatability of colony-level personality declined precipitously when groups were forced to build their webs on novel habitat structures. Furthermore, habitat structure affected collective capture behavior, that is, latency to attack and the number of attackers differed among colonies on different habitat structures. Collectively, our data demonstrate that habitat structure is instrumental in shaping both the mean and repeatability of the collective behavior of colonies and may influence overall foraging success.     

Exploring the effects of individual traits and within-colony variation on task differentiation and collective behavior in a desert social spider

Social animals are extraordinarily diverse and ecologically abundant. In understanding the success of complex animal societies, task differentiation has been identified as a central mechanism underlying the emergence and performance of adaptive collective behaviors. In this study, we explore how individual differences in behavior and body size determine task allocation in the social spider Stegodyphus dumicola. We found that individuals with high body condition indices were less likely to participate in prey capture, and individuals’ tendency to engage in prey capture was not associated with either their behavioral traits or body size. No traits were associated with individuals’ propensity to participation in web repair, but small individuals were more likely to engage in standard web-building. We also discovered consistent, differences among colonies in their collective behavior (i.e., colony-level personality). At the colony level, within-colony variation in behavior (aggressiveness) and body size were positively associated with aggressive foraging behavior. Together, our findings reveal a subtly complex relationship between individual variation and collective behavior in this species. We close by comparing the relationship between individual variation and social organization in nine species of social spider. We conclude that intraspecific variation is a major force behind the social organization of multiple independently derived lineages of social spider.     

Mate quality,not aggressive spillover,explains sexual cannibalism in a size-dimorphic spider

Sexual cannibalism particularly before mating is costly for the male victim but also for the female aggressor if she risks remaining unmated. The aggressive spillover hypothesis explains the persistence of this behavior as a maladaptive side effect of positive selection on aggressiveness in a foraging context. The hypothesis predicts that the occurrence of sexual cannibalism is explained by female aggressiveness but is not related to male phenotype or behavioral type. An alternative hypothesis invokes sexual selection and makes the opposite prediction namely that sexual cannibalism is an expression of female choice and should hence mainly target males of low quality. We tested the above hypotheses on a sexually dimorphic nephilid spider Nephilengys livida, known for male monopolization of females via genital damage, female genital plugging, and mate guarding, by staging mating trials during which we recorded mating behaviors and occurrences of pre- and postcopulatory cannibalism. We did not restrict assessment of aggressiveness to the mating and foraging context but also included aggression against same sex conspecifics. To assess female personalities, i.e., consistent individual differences in behavior including aggressiveness, we repeatedly tested them for intra-sex aggression, voracity towards prey, locomotory activity, and boldness. Females exhibited consistent differences in intra-sex aggressiveness, latency to attack prey, and boldness. Aggressive females had shorter latencies to attack prey and were more active than non-aggressive ones. In contrast to the predictions of the aggressive spillover hypothesis, females that were aggressive towards prey and towards other females were not more likely to attack a male than non-aggressive females. In support of the mate choice hypothesis, less aggressive males were more likely attacked and cannibalized than more aggressive ones. This hints at sexual selection for aggressiveness in males and raises the question of mechanisms that maintain variation in male aggressiveness.     

Selection on social traits in greater spear-nosed bats, Phyllostomus hastatus

Many studies assume that selection molds social traits and have investigated the manner in which this occurs, yet very few studies have measured the strength of selection on social traits in natural populations. In this paper, I report results of phenotypic selection analyses on two social traits – the size of social groups and the frequency of group foraging – in Phyllostomus hastatus, the greater spear-nosed bat. I found significant positive directional selection on individual group foraging frequency, but no directional selection on individuals in different-sized social groups. These results have implications for the structure of social groups, cooperative behavior among group mates, and maternal investment strategies. I argue that combining studies of natural selection on wild populations with experiments to identify the agents and mechanisms of selection can do much to increase our understanding of social evolution.     

Ancient behaviors of larval amphibians in response to an emerging fungal pathogen, <Emphasis Type="Italic">Batrachochytrium dendrobatidis</Emphasis>

Behaviors have evolved in response to various selection pressures over evolutionary time. However, not all behaviors are adaptive. Some presumably “ancient” behaviors, persistent for millions of years, may be detrimental in the face of novel selection pressures in modern times. These pressures include a multitude of emerging infectious diseases which may be stimulated by environmental changes. We examined how a globally emerging amphibian pathogen, Batrachochytrium dendrobatidis (BD), affected two key evolutionarily persistent behaviors displayed by amphibian larvae: aggregation and thermoregulation. Larval aggregation behavior is often essential for foraging, thermoregulation, and antipredator defense, but varies among species. Thermoregulatory behavior speeds larval development in ephemeral habitats. Specifically, we examined whether aggregation and thermoregulatory behaviors changed when exposed to the BD pathogen in two species (Bufo boreas and Rana cascadae) whose larvae aggregate in nature. In laboratory choice tests, larvae of neither species avoided infected conspecifics. BD-exposed B. boreas larvae aggregated, while unexposed R. cascadae larvae associated more frequently with BD-exposed conspecifics. There was no evidence of behavioral fever or altered thermoregulation in larvae of four species we examined (Pseudacris regilla, Rana aurora, B. boreas, R. cascadae). The absence of behavioral fever may suggest an inability of the larvae of some host species to mediate infection risk by this pathogen. Thermoregulatory behaviors may exhibit a high degree of evolutionary inertia in amphibian hosts because they are linked with host physiology and developmental rates, while altered aggregation behaviors could potentially elevate pathogen transmission rates, leading to increased infection risk in social amphibian species.     

Costs and benefits of pocket gopher foraging: linking behavior and physiology

Animals can attain fitness benefits by maintaining a positive net energy balance, including costs of movement during resource acquisition and the profits from foraging. Subterranean rodent burrowing provides an excellent system in which to examine the effects of movement costs on foraging behavior because it is energetically expensive to excavate burrows. We used an individual-based modeling approach to study pocket gopher foraging and its relationship to digging cost, food abundance, and food distribution. We used a unique combination of an individual-based foraging-behavior model and an energetic model to assess survival, body mass dynamics, and burrow configurations. Our model revealed that even the extreme cost of digging is not as costly as it appears when compared to metabolic costs. Concentrating digging in the area where food was found, or area-restricted search (ARS), was the most energetically efficient digging strategy compared to a random strategy. Field data show that natural burrow configurations were more closely approximated by the animals we modeled using ARS compared to random diggers. By using behavior and simple physiological principles in our model, we were able to observe realistic body mass dynamics and recreate natural movement patterns.     

Female mate choice in the gray treefrog (Hyla versicolor) in three experimental environments

We studied female mate choice by Hyla versicolor in three venues to examine how acoustic and spatial complexity, background noise, and the calling behavior of males might influence preferences manifest in previous laboratory two-stimulus choice tests. Our laboratory-based two-stimulus choice tests with and without broadcasts of chorus noise demonstrated that females prefer long calls relative to short calls when calling efforts of alternatives are equivalent. Background noise impaired the ability of females to discriminate in favor of longer over shorter calls, but the magnitude of the effect was small. Captures of females at eight speakers broadcasting 6- to 27-pulse calls at the edge of a pond revealed strong discrimination against only the shortest call variant. In natural choruses, females may only rarely encounter males using such unattractive vocalizations. Female phonotaxis at an artificial pond with caged and electronically monitored calling males also indicated that consequences of female preferences for temporal aspects of calling observed in two-stimulus choice tests are much attenuated in choruses and explain only small portions (<10%) of the variation in male mating success. Nevertheless, relatively high call duration and calling effort increased male attractiveness. Acoustic interference emerged as another significant factor influencing male mating success and possibly the differences in female choice observed in laboratory and chorus settings. We suggest that the bias of females against both overlapped and very short calls may help explain why males lengthen their calls but lower their rate of delivery in response to increases in chorus size.