Interactions with Combined Chemical Cues Inform Harvester Ant Foragers' Decisions to Leave the Nest in Search of Food

Social insect colonies operate without central control or any global assessment of what needs to be done by workers. Colony organization arises from the responses of individuals to local cues. Red harvester ants (Pogonomyrmex barbatus) regulate foraging using interactions between returning and outgoing foragers. The rate at which foragers return with seeds, a measure of food availability, sets the rate at which outgoing foragers leave the nest on foraging trips. We used mimics to test whether outgoing foragers inside the nest respond to the odor of food, oleic acid, the odor of the forager itself, cuticular hydrocarbons, or a combination of both with increased foraging activity. We compared foraging activity, the rate at which foragers passed a line on a trail, before and after the addition of mimics. The combination of both odors, those of food and of foragers, is required to stimulate foraging. The addition of blank mimics, mimics coated with food odor alone, or mimics coated with forager odor alone did not increase foraging activity. We compared the rates at which foragers inside the nest interacted with other ants, blank mimics, and mimics coated with a combination of food and forager odor. Foragers inside the nest interacted more with mimics coated with combined forager/seed odors than with blank mimics, and these interactions had the same effect as those with other foragers. Outgoing foragers inside the nest entrance are stimulated to leave the nest in search of food by interacting with foragers returning with seeds. By using the combined odors of forager cuticular hydrocarbons and of seeds, the colony captures precise information, on the timescale of seconds, about the current availability of food.     

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.     

How long will honey bees (<Emphasis Type="Italic">Apis mellifera</Emphasis> L.) be stimulated by scent to revisit past-profitable forage sites?

Honey bees utilise floral food sources that vary temporally in their relative and absolute quality. Via a sophisticated colony organisation, a honey bee colony allocates its foragers such that the colony focuses on the most profitable forage sites while keeping track of changes within its foraging environment. One important mechanism of the allocation of foragers is the ability of experienced foragers to revisit past-profitable forage sites after a period of temporary dearth caused by, for example, inclement weather. The scent of past-profitable forage within the colony brought back by other foragers is sufficient to reactivate these experienced foragers. Here I determine for how long bees react to the scent of a past-profitable forage site. I show that the ability of foragers to revisit the location of a past-profitable food source diminishes rapidly over a period of 10 days, until no forager reacts to the cue (scent). I discuss the implications of these findings with respect to the colony’s ability to react rapidly to changing foraging conditions.     

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.     

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.     

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.     

Does group foraging promote efficient exploitation of resources?

Increased avoidance of food patches previously exploited by other companions has been proposed as one adaptive benefit of group foraging. However, does group foraging really represent the most efficient way to exploit non- or slowly-renewing resources? Here, I used simulations to explore the costs and benefits of exploiting non-renewing resources by foragers searching for food patches independently or in groups in habitats with different types of resource distribution. Group foragers exploited resources in a patch more quickly and therefore spent proportionately more time locating new patches. Reduced avoidance of areas already exploited by others failed to overcome the increased time cost of searching for new food patches and group foragers thus obtained food at a lower rate than solitary foragers. Group foraging provided one advantage in terms of a reduction in the variance of food intake rate. On its own, reduced avoidance of exploitation competition through group foraging appears unlikely to increase mean food intake rate when exploiting non-renewing patches but may provide a way to reduce the risk of an energy shortfall.     

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.     

The Regulation of Ant Colony Foraging Activity without Spatial Information

Many dynamical networks, such as the ones that produce the collective behavior of social insects, operate without any central control, instead arising from local interactions among individuals. A well-studied example is the formation of recruitment trails in ant colonies, but many ant species do not use pheromone trails. We present a model of the regulation of foraging by harvester ant (Pogonomyrmex barbatus) colonies. This species forages for scattered seeds that one ant can retrieve on its own, so there is no need for spatial information such as pheromone trails that lead ants to specific locations. Previous work shows that colony foraging activity, the rate at which ants go out to search individually for seeds, is regulated in response to current food availability throughout the colony's foraging area. Ants use the rate of brief antennal contacts inside the nest between foragers returning with food and outgoing foragers available to leave the nest on the next foraging trip. Here we present a feedback-based algorithm that captures the main features of data from field experiments in which the rate of returning foragers was manipulated. The algorithm draws on our finding that the distribution of intervals between successive ants returning to the nest is a Poisson process. We fitted the parameter that estimates the effect of each returning forager on the rate at which outgoing foragers leave the nest. We found that correlations between observed rates of returning foragers and simulated rates of outgoing foragers, using our model, were similar to those in the data. Our simple stochastic model shows how the regulation of ant colony foraging can operate without spatial information, describing a process at the level of individual ants that predicts the overall foraging activity of the colony.     

Assessment of food source profitability in honeybees (<Emphasis Type="Italic">Apis mellifera</Emphasis>): how does disturbance of foraging activity affect trophallactic behaviour?

When forager honeybees (Apis mellifera) return to the hive after a successful foraging trip, they unload the collected liquid to recipient hive mates through mouth-to-mouth contacts (trophallaxis). The speed at which the liquid is transferred (unloading rate) from donor to recipient is related to the profitability of the recently visited food source. Two main characteristics that define this profitability are the flow of solution delivered by the feeder and the time invested by the forager at the source (visit time). To investigate the effect of visit time on trophallactic behaviour, donor foragers were trained to a rate feeder that could deliver different flows of solution. We dissociated visit time and flow of solution by introducing pauses in the solution's deliverance at different moments of the foraging visit. We analysed whether timing of the non-deliverance period within the visit is important for the forager's assessment of resource profitability. During the subsequent trophallactic encounter with a hive mate, unloading rate was related to the total time invested by the forager at the food source only if the ingestion process had already been started. These results together with previous ones suggest that foragers integrate an overall flow rate of solution of the feeder throughout the entire foraging visit.     

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

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

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.     

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.     

Effects of experience on food-searching behavior in the antFormica schaufussi (Hymenoptera: Formicidae)

Foragers of the ant Formica schaufussitend to return to and search at a site of a previous food find. The search tactic employed by a forager on its return trip is related to the type of food previously encountered: search is more persistent in response to carbohydrate than to protein food. Using different reinforcement schedules with carbohydrate and protein food rewards, we show that, on a short-term as well as on a long-term basis, the basic pattern of search observed in naive foragers is only slightly modified through foraging experience. Foragers do not increase their search effort or adjust their search pattern when either type of food is systematically renewed on a fixed reward schedule and thus do not seem to be able to learn to assess the food predictability. Collective responses that could compensate for this lack of individual flexibility and increase foraging efficiency at the colony level are discussed.     

Beyond diffusion: Modelling local and long-distance dispersal for organisms exhibiting intensive and extensive search modes

The distribution of foragers on the landscape has important consequences to, for example, the spread rate of an invasive species or the outcrossing levels between neighbouring crops. Since forager distribution can be difficult to measure directly, mathematical models are often used to predict the population density of dispersing foragers on the landscape. We model organism movement using a diffusion framework in which the foraging population is divided into two subpopulations engaged in intensive and extensive search modes respectively. Movement in the intensive search mode (ISM) is modeled by diffusion, and movement in the extensive search mode (ESM) is modeled by advection. We show that our model provides a superior fit to organism movement data than more traditional diffusion or diffusion-advection models in which the forager population is considered homogeneous. Our results have implications for the understanding of dispersal in a wide variety of applications.     

Prior knowledge about spatial pattern affects patch assessment rather than movement between patches in tactile-feeding mallard

1. Heterogeneity in food abundance allows a forager to concentrate foraging effort in patches that are rich in food. This might be problematic when food is cryptic, as the content of patches is unknown prior to foraging. In such case knowledge about the spatial pattern in the distribution of food might be beneficial as this enables a forager to estimate the content of surrounding patches. A forager can benefit from this pre-harvest information about the food distribution by regulating time in patches and/or movement between patches. 2. We conducted an experiment with mallard Anas platyrhynchos foraging in environments with random, regular, and clumped spatial configurations of full and empty patches. An assessment model was used to predict the time in patches for different spatial distributions, in which a mallard is predicted to remain in a patch until its potential intake rate drops to the average intake rate that can be achieved in the environment. A movement model was used to predict lengths of interpatch movements for different spatial distributions, in which a mallard is predicted to travel to the patch where it expects the highest intake rate. 3. Consistent with predictions, in the clumped distribution mallard spent less time in an empty patch when the previously visited neighbouring patch had been empty than when it had been full. This effect was not observed for the random distribution. This shows that mallard use pre-harvest information on spatial pattern to improve patch assessment. Patch assessment could not be evaluated for the regular distribution. 4. Movements that started in an empty patch were longer than movements that started in a full patch. Contrary to model predictions this effect was observed for all spatial distributions, rather than for the clumped distribution only. In this experiment mallard did not regulate movement in relation to pattern. 5. An explanation for the result that pre-harvest information on spatial pattern affected patch assessment rather than movement is that mallard move to the nearest patch where the expected intake rate is higher than the critical value, rather than to the patch where the highest intake rate is expected.     

Colony foraging allocation is finely tuned to food distance and sweetness even close to a bee colony

Social bee colonies can allocate their foraging resources over a large spatial scale, but how they allocate foraging on a small scale near the colony is unclear and can have implications for understanding colony decision‐making and the pollination services provided. Using a mass‐foraging stingless bee, Scaptotrigona pectoralis (Dalla Torre) (Hymenoptera: Apidae: Meliponini), we show that colonies will forage near their nests and allocate their foraging labor on a very fine spatial scale at an array of food sources placed close to the colony. We counted the foragers that a colony allocated to each of nine feeders containing 1.0, 1.5, or 2.0 M sucrose solution [31, 43, and 55% sucrose (wt/wt), respectively] at distances of 10, 15, and 20 m from the nest. A significantly greater number of foragers (2.6–5.3 fold greater) visited feeders placed 10 vs. 20 m away from the colony. Foraging allocation also corresponded to food quality. At the 10‐m feeders, 4.9‐fold more foragers visited 2.0 M as compared to 1.0 M sucrose feeders. Colony forager allocation thus responded to both differences in food distance and quality even when the travel cost was negligible compared to normal colony foraging distances (10 m vs. an estimated 800–1 710 m). For a nearby floral patch, this could result in unequal floral visitation and pollination.     

An Adaptive Difference in the Relationship between Foraging Mode and Responses to Prey Chemicals in two Congeneric Scincid Lizards

Sensory abilities must allow efficient detection of prey, but the senses used and their relative importance may vary with hunting methods. In lizards, ambush foragers locate prey visually and active foragers use a combination of vision and vomerolfaction, the chemical sense associated with the vomeronasal system. Active foragers, but not ambush foragers, discriminate between prey chemicals and other chemical stimuli sampled by tongue-flicking. In active foragers, features of the tongue that may improve chemical sampling, such as elongation and forking are more pronounced and density of vomeronasal chemoreceptors is greater, than in ambush foragers. Foraging mode is fixed in most lizard families, and correlated evolution has been demonstrated among foraging mode, discrimination of prey chemicals, and lingual-vomeronasal morphology by interfamilial comparisons. Here I present information on a rare case of an intrageneric difference in foraging mode in the genus Mabuya . Laboratory experiments on the discrimination of prey chemicals showed that the active forager M . striata sparsa exhibits prey chemical discrimination, but the ambush forager M . acutilabris does not. The active forager also has a slightly more elongated tongue with deeper notching at the tip than the ambush forager, which might be a response to a change in foraging behavior or a reflection of unrelated differences in head shape. These findings confirm predictions based on correlated evolution between the hunting method and use of the chemical sense to locate food. They further show that chemosensory behavior is adjusted to change in foraging mode more rapidly than was previously known and suggest that behavioral changes may occur more rapidly than associated modifications of chemosensory morphology.     

Quantifying the effect of colony size and food distribution on harvester ant foraging

Desert seed-harvester ants, genus Pogonomyrmex, are central place foragers that search for resources collectively. We quantify how seed harvesters exploit the spatial distribution of seeds to improve their rate of seed collection. We find that foraging rates are significantly influenced by the clumpiness of experimental seed baits. Colonies collected seeds from larger piles faster than randomly distributed seeds. We developed a method to compare foraging rates on clumped versus random seeds across three Pogonomyrmex species that differ substantially in forager population size. The increase in foraging rate when food was clumped in larger piles was indistinguishable across the three species, suggesting that species with larger colonies are no better than species with smaller colonies at collecting clumped seeds. These findings contradict the theoretical expectation that larger groups are more efficient at exploiting clumped resources, thus contributing to our understanding of the importance of the spatial distribution of food sources and colony size for communication and organization in social insects.     

The allocation of foragers in red wood ants

Abstract. 1. We studied how colonies of the red wood ant, Formica polyctena , adjust the numbers of foragers allocated to different foraging trails. In a series of field experiments, foragers were marked and transferred from one nest to another, related nest, where they joined the foraging force. Transferred workers acted as a reserve of uncommitted, available foragers.
2. Previous work shows that each individual forager habitually uses one trail. We found that for an uncommitted forager, the influence of recruitment initially is stronger than that of directional fidelity. Transferred workers were likely to use trails leading to new food sources. When transferred to a new nest, foragers were not likely to use a trail in the same direction as their original trail in the donor nest.
3. After a week, transferred foragers tended to develop route fidelity. Even after bait was no longer present, they continued to use the trail that had formerly led to a bait source.
4. We examined how colonies adjust numbers on a trail by experimentally depleting some trails. Colonies usually did not compensate for depletion: foragers were not recruited to depleted trails.
5. In general, the dynamics of foraging in this species facilitate a consistent foraging effort rather than rapid adjustments of forager allocation.