Trapline foraging by pollinators: its ontogeny, economics and possible consequences for plants

Background

Trapline foraging (repeated sequential visits to a series of feeding locations) has been often observed in pollinators collecting nectar or pollen from flowers. Although field studies on bumble-bees and hummingbirds have clarified fundamental aspects of this behaviour, trapline foraging still poses several difficult questions from the perspectives of both animals and plants. These questions include whether and how traplining improves foraging performance, how animals develop traplines with accumulating foraging experience, and how traplining affects pollen flow or plant reproduction.

Scope

First, we review our previous work performed by using computer simulations and indoor flight-cage experiments with bumble-bees foraging from arrays of automated feeders. Our findings include the following: (1) traplining benefits foragers that are competing for resources that replenish in a decelerating way, (2) traplining is a learned behaviour that develops over a period of hours and (3) the establishment of traplines could be hampered by spatial configuration of plants such as zigzags. Second, using a simulation model linking pollinator movement and pollen transfer, we consider how service by pollinators with different foraging patterns (searchers or trapliners) would affect pollen flow. Traplining increases mating distance and mate diversity, and reduces ‘iterogamy’ (self-pollination caused by return visits) at the population level. Furthermore, increased visitation rates can have opposite effects on the reproductive success of a plant, depending on whether the visitors are traplining or searching. Finally, we discuss possible consequences of traplining for plants in the light of new experimental work and modelling.

Conclusions

We suggest that trapline foraging by pollinators increases variation among plant populations in genetic diversity, inbreeding depression and contributions of floral traits to plant fitness, which should in turn affect the rates and directions of floral evolution. More theoretical and empirical studies are needed to clarify possible outcomes of such a neglected side of pollination.Key words: Artificial flower, Bombus, competition, floral evolution, foraging experience, iterogamy, model, pollen flow, pollinator movement, renewing resource, spatial memory, trapline foraging     

REPRODUCTION IN POLEMONIUM: PATTERNS AND IMPLICATIONS OF FLORAL NECTAR PRODUCTION AND STANDING CROPS

Patterns of floral nectar production and standing crop were measured in four populations of the herbaceous perennial plant species Polemonium foliosissimum. Contrary to prediction (Pleasants, 1983), individual flowers in this mass-flowering species were found to produce equivalent nectar volumes every day of their lives. Alternative methods of increasing the reward variability presented to pollinators are evaluated for P. foliosissimum and the relationship between that variability and risk-aversive foraging by pollinators is discussed. Significant spatial and temporal variability in rate of nectar production was found. Populations separated by approximately 200 m exhibited different rates. Nectar production declined significantly as a function of time of the flowering season in two populations but not in a third. In spite of such variability, individual plants showed consistency in production both within a single blooming season and across successive seasons. Because of the variability found in the present study, care should be taken to design appropriate sampling protocols in future nectar studies. Patterns of standing nectar crop were consistent with those expected if pollinators were using an area-restricted searching pattern.     

Trade-off between travel distance and prioritization of high-reward sites in traplining bumblebees

1.Animals exploiting renewable resource patches are faced with complex multi-location routing problems. In many species, individuals visit foraging patches in predictable sequences called traplines. However, whether and how they optimize their routes remains poorly understood.2.In this study, we demonstrate that traplining bumblebees (Bombus terrestris) make a trade-off between minimizing travel distance and prioritizing the most rewarding feeding locations.3.Individual bees trained to forage on five artificial flowers of equal reward value selected the shortest possible route as a trapline. After introducing a single highly rewarding flower to the array, they re-adjusted their routes visiting the most rewarding flower first provided the departure distance from the shortest possible route remained small (18%). When routes optimizing the initial rate of reward intake were much longer (42%), bees prioritized short travel distances.4.Under natural conditions, in which individual flowers vary in nectar productivity and replenish continuously, it might pay bees to prioritize highly rewarding locations, both to minimize the overall number of flowers to visit and to beat competitors.5.We discuss how combined memories of location and quality of resource patches could allow bees and other traplining animals to optimize their routing decisions in heterogeneous environments.     

Preference in patchy landscapes: the influence of scale-specific intake rates and variance in reward

Understanding the responses of foragers to patchy distributionsof resources has formed a fundamental challenge in behavioralecology. Two currencies have been used to assess the patch preferencesof herbivores—intake rate maximization and risk sensitivity.We wished to understand if small mammalian foragers, collaredlemmings (Dichrostonyx groenlandicus), choose patches to maximizefood intake rate or to reduce risk of starvation in "variable"environments. Moreover, we examined the possibility that maximizingintake rate depends on the spatial scale of patchiness. We designedan experiment offering two alternative patches of food, varyingthe predictability of food rewards and the "potential intakerate" at different spatial scales. Collared lemmings did notconsistently select patches that maximized their intake rateat either scale studied. Instead, they chose patches offeringthe least variation in food reward over the course of the experiment.Collared lemmings used prior knowledge gained from previousforaging bouts to assess food variability. We interpret theseresults as evidence for risk-averse foraging strategies, whichare predicted for continuous foragers aiming to minimize riskof starvation.     

Variability in nectar production and standing crop, and their relation to pollinator visits in a Mediterranean shrub

Nectar standing crops in flowers within an individual plant are often highly variable. This variability may be a by-product of the foraging activity of insect pollinators. Alternatively, plants may be selected to produce highly variable rewards to reduce consecutive visitation by risk-averse pollinators, thus diminishing within-plant pollen transfer. This study evaluated the roles of pollinator control vs. plant control over nectar variability in the bee-pollinated shrub Rosmarinus officinalis L. (Lamiaceae). We sampled nectar production, standing crop and pollinator visits in three shrubs of one population over 17 days during one blooming season. Nectar production rates were highly variable (CV = 1.48), and increased after rainy days. Nectar standing crops were even more variable (CV = 2.16), decreased with increasing temperatures, and increased with time since the last rain. Pollinator visit rates decreased with variability in nectar standing crops, increased with flower number per shrub, and were unaffected by variability in nectar production rates. Repeated sampling of marked flowers revealed no correlation between their nectar standing crops and production rates. These findings support the role of reward variance in reducing pollinator visits, but suggest that plants are not in complete control of this variability. Rather, plant-generated variability can be modified by intensive foraging activity of pollinators. Such pollinator control over nectar variability is likely to reduce the selective advantage of plant-generated reward variation. Handling Editor: Neal Williams.     

Optimal foraging: Random movement by pollen collecting bumblebees

Summary Two bumblebee species, Bombus bifarius and B. flavifrons, forage randomly with respect to direction when gathering pollen on Potentilla gracilis. Bees avoid revisiting flowers by being able to differentiate recently visited from unvisited flowers. This recognition occurs while bees are flying over open flowers and appears to be a response to the amount of available pollen within flowers. Random foraging with respect to direction is the optimal strategy when the probability of flower revisitation is low. Bumblebees appear to be moving preferentially between nearest neighbors, again as predicted by foraging theory. This behavior causes the establishment of pollen patches in the P. gracilis population. Unlike other pollinators studied in similar situations, bumblebees on P. gracilis do not forage utilizing an area-restricted searching behavior. Because floral reward quality can be assessed at low cost by bees foraging on P. gracilis, their tendency to move to nearby flowers even after encountering a poor quality blossom apparently yields a higher rate of net energy intake than does area-restricted searching. The data indicate that bumblebees exhibit great plasticity in foraging behavior and that they are able to forage efficiently under a wide range of environmental conditions.     

Testing dynamic variance-sensitive foraging using individual differences in basal metabolic rates of zebra finches

Social foragers can alternate between searching for food (producer tactic), and searching for other individuals that have located food in order to join them (scrounger tactic). Both tactics yield equal rewards on average, but the rewards generated by producer are more variable. A dynamic variance-sensitive foraging model predicts that social foragers should increase their use of scrounger with increasing energy requirements and/or decreased food availability early in the foraging period. We tested whether natural variation in minimum energy requirements (basal metabolic rate or BMR) is associated with differences in the use of producer–scrounger foraging tactics in female zebra finches Taeniopygia guttata . As predicted by the dynamic variance-sensitive model, high BMR individuals had significantly greater use of the scrounger tactic compared with low BMR individuals. However, we observed no effect of food availability on tactic use, indicating that female zebra finches were not variance-sensitive foragers under our experimental conditions. This study is the first to report that variation in BMR within a species is associated with differences in foraging behaviour. BMR-related differences in scrounger tactic use are consistent with phenotype-dependent tactic use decisions. We suggest that BMR is correlated with another phenotypic trait which itself influences tactic use decisions.     

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.     

Resource characteristics and competition affect colony and individual foraging strategies of the wood ant Formica integroides

Abstract.  1. Resource characteristics and competitive pressure can affect an ant colony's foraging strategy. This study examined the ability of the wood ant Formica integroides to respond, at both the colony and individual levels, to changes in competitive pressure for access to terrestrial and arboreal resources.
2. Because foraging behaviours depend on resource characteristics, foraging for different resource types (e.g. terrestrial and arboreal habitats) produces different spatial or territorial arrangements. In this study, terrestrial contests for resources followed an interference-exploitation tradeoff, while arboreal foragers defended entire trees as absolute territories.
3. Competitive pressure for access to arboreal resources was shown to increase with distance from F. integroides nests.
4. In this study, the ability of F. integroides to defend a resource varied with body size. Large foragers were better defenders than small foragers. For groups of foragers, the ability to defend a resource increased with the ratio of large to small foragers.
5. In response to competitive pressure, F. integroides colonies altered the size distribution of arboreal, but not terrestrial, foragers. An increase in competitive pressure was matched by an increase in the number of large foragers allocated to trees. This response to competition affected the relationship between body size and distance from the nest for arboreal foragers.
6. Foraging behaviours for individual arboreal foragers also varied with competitive pressure. As competition increased, large arboreal foragers spent more time in direct contact with the resource rather than standing between resource patches.     

Eavesdropping foragers use level of collective commotion as public information to target high quality patches

Public information offers a valuable means for social foragers to determine the relative quality of foraging patches. Despite much evidence that foragers use public information based on others’ feeding behavior, no experiments have examined whether foragers might use public information based on others’ competitive behavior, particularly the collective commotion that can be generated by aggregations. Such commotion could potentially provide a rich source of public information: as foragers compete in a patch with an especially high value resource, their heightened competition intensity could enable eavesdropping foragers to target this superior patch, based simply on its higher level of collective commotion. To test the hypothesis that the level of collective commotion is used as public information by eavesdropping foragers I conducted field experiments on terrestrial hermit crabs Coenobita compressus. These animals engage in collective competitive interactions in foraging patches for food and shells, generating variable levels of commotion across different quality patches. By experimentally manipulating the level of collective commotion in sham aggregations in the wild I show that a higher level of commotion is exploited by eavesdropping foragers to differentially target more valuable patches. Broadly, these results highlight an underappreciated significance of competitive by‐products and higher‐ order collective pheno mena as forms of public information for foragers.     

Depletion of seed patches by Merriam’s kangaroo rats: are GUD assumptions met?

Depletion of experimental seed patches by granivorous animals often is used as a qualitative assay of foraging activity. An optimal foraging model suggests that seed amounts remaining when foragers leave patches ("giving-up-density", GUD) also provide quantitative measures of foraging economics, diet strategies and foraging abilities. Such quantitative uses of GUDs rest on several largely untested assumptions. We tested two of these with Merriam's kangaroo rats: that gain curves are smoothly decelerating, and that foragers leave patches at a constant harvest rate. Harvest rates indeed declined with patch residence time, but in the piecewise linear fashion expected of systematic search. Animals also revisited areas within patches less frequently than expected with random search. In the field, they depleted patches in multiple visits and did not use a constant-rate leaving rule. These deviations from model assumptions cast doubt on inferences about foraging ecology that have been based on quantitative GUD theory.     

Host frass as arrestant chemicals in locating host Mythimna separata by the tachinid fly Exorista japonica

We investigated the response of the tachinid fly, Exorista japonica (Townsend), to host frass or its extracts in order to clarify the host location mechanisms of female flies in a potential host habitat. Host searching time in a patch and the number of patch visits were analyzed by using a frass-containing patch which was excreted by host larvae, Mythimna separata (Walker) (Lepidoptera: Noctuidae), and patches to which host frass extracts were applied. E. japonica females were arrested in response to the host-frass-containing patch after contacting the frass with their front tarsi, thereby spending most of the time to search the patch and to revisit the host-frass patch. While host-searching time in the patch by the females was longest at their first visit of a patch with host frass, searching time decreased with successive visits. The female flies also exhibited area-restricted searching with methanol extracts of the host frass. Area-restricted searching activity increased with the concentration of host-frass extract, i.e., total searching time in the patch and the number of patch visits varied in a dose-dependent manner. E. japonica females likely employ chemicals in host frass as arrestants in host location.     

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.     

Assessing Targets for the Restoration of Herbaceous Vegetation in Ponderosa Pine Forests

A restoration project is considered a success when the initial target is met, but many targets are plausible. We evaluated the success of a restoration project in its 11th year since treatment in a southwestern ponderosa pine–bunchgrass community and the appropriateness of several targets. We measured the responses of (1) total standing crop; (2) standing crop of five functional groups (C₃ and C₄ graminoids, leguminous forbs, and nonleguminous perennial and annual forbs); (3) graminoid community composition; and (4) standing crop of five common graminoid species (Festuca arizonica, Muhlenbergia montana, Elymus elymoides, Carex geophila, and Poa fendleriana). Targets were quantified in remnant grass patches, which provided the standards for these targets, and were assessed in three other forest patch types (pre‐settlement tree patches, post‐settlement tree patches, and patches where all post‐settlement trees were removed). Patches where all post‐settlement trees were removed reached target levels for total standing crop, C₃ and C₄ graminoid standing crop, graminoid community composition, and M. montana, E. elymoides, and C. geophila standing crops. Standing crop of legumes and of F. arizonica did not increase over time in any patch type. Targets were not met in pre‐settlement patches or in patches where some post‐settlement trees were left standing, suggesting that it is unrealistic to expect equal responses across all patch types. If increasing herbaceous standing crop is a major goal, practitioners should create gaps within the pine forest canopy.     

Foraging behaviour and dispersion of eastern grey kangaroos (Macropus giganteus) in an ideal free framework

Ideal free distribution (IFD) theory predicts that animals in competitive situations should distribute themselves among available habitat patches according to the density of conspecifics and its regulatory effect on resources. To investigate the applicability of IFD models to free-ranging herbivores, we quantified the dispersion and foraging behaviour of eastern grey kangaroos Macropus giganteus among habitat patches of differing suitability, within and outside a reservoir catchment in southern Victoria, Australia. Kangaroo densities within the catchment had a regulatory effect on resource density, while surrounding farmland maintained a higher standing crop despite higher densities of competitors. This difference was slight in autumn, however, when the system was apparently close to equilibrium. Gross bite rates of individuals foraging in farmland were lower than for individuals foraging within the catchment, and vigilance behaviour occurred more frequently in farmland habitat than any other, decreasing time devoted to feeding. Interference competition occurred in only 1.9% of focal samples, although competitive differences based on phenotype were observed. Although resource gains by individual kangaroos are likely to be influenced by other factors, including resource dynamics, predation risk and phenotypic differences, IFD theory provides a valuable analytical framework for this herbivore foraging system.     

Energy benefits and emergent space use patterns of an empirically parameterized model of memory‐based patch selection

Many species frequently return to previously visited foraging sites. This bias towards familiar areas suggests that remembering information from past experience is beneficial. Such a memory‐based foraging strategy has also been hypothesized to give rise to restricted space use (i.e. a home range). Nonetheless, the benefits of empirically derived memory‐based foraging tactics and the extent to which they give rise to restricted space use patterns are still relatively unknown. Using a combination of stochastic agent‐based simulations and deterministic integro‐difference equations, we developed an adaptive link (based on energy gains as a foraging currency) between memory‐based patch selection and its resulting spatial distribution. We used a memory‐based foraging model developed and parameterized with patch selection data of free‐ranging bison Bison bison in Prince Albert National Park, Canada. Relative to random use of food patches, simulated foragers using both spatial and attribute memory are more efficient, particularly in landscapes with clumped resources. However, a certain amount of random patch use is necessary to avoid frequent returns to relatively poor‐quality patches, or avoid being caught in a relatively poor quality area of the landscape. Notably, in landscapes with clumped resources, simulated foragers that kept a reference point of the quality of recently visited patches, and returned to previously visited patches when local patch quality was poorer than the reference point, experienced higher energy gains compared to random patch use. Furthermore, the model of memory‐based foraging resulted in restricted space use in simulated landscapes and replicated the restricted space use observed in free‐ranging bison reasonably well. Our work demonstrates the adaptive value of spatial and attribute memory in heterogeneous landscapes, and how home ranges can be a byproduct of non‐omniscient foragers using past experience to minimize temporal variation in energy gains.     

The advantage of alternative tactics of prey and predators depends on the spatial pattern of prey and social interactions among predators

Individual variation in behavioral strategies is ubiquitous in nature. Yet, explaining how this variation is being maintained remains a challenging task. We use a spatially-explicit individual-based simulation model to evaluate the extent to which the efficiency of an alternative spacing tactic of prey and an alternative search tactic of predators are influenced by the spatial pattern of prey, social interactions among predators (i.e., interference and information sharing) and predator density. In response to predation risk, prey individuals can either spread out or aggregate. We demonstrate that if prey is extremely clumped, spreading out may help when predators share information regarding prey locations and when predators shift to area-restricted search following an encounter with prey. However, dispersion is counter-selected when predators interact by interference, especially under high predator density. When predators search for more randomly distributed prey, interference and information sharing similarly affect the relative advantage of spreading out. Under a clumped prey spatial pattern, predators benefit from shifting their search tactic to an area-restricted search following an encounter with prey. This advantage is moderated as predator density increases and when predators interact either by interference or information sharing. Under a more random prey pattern, information sharing may deteriorate the inferior search tactic even more, compared to interference or no interaction among predators. Our simulation clarifies how interactions among searching predators may affect aggregation behavior of prey, the relative success of alternative search tactics and their potential to invade established populations using some other search or spacing tactics.     

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.     

Spatial learning and discrimination of food patches in the European badger (Meles meles L.)

Theories of foraging often assume that concentrations of prey (‘patches’) can be discriminated by a forager, but there have been few studies of how this is achieved when patches are not recognizable by means of an obvious proximal cue. We observed the search trajectories of two badgers (Meles meles L.) foraging for peanuts in artificial patches to see how efficiently they could map a new patch in the first place, and whether they would remember the location and extent of a previously visited patch. The results suggest that when a patch is encountered for the first time, a strategy of area-restricted searching keeps the animal's trajectory largely within the patch boundary. After a single exposure to a novel patch, however, badgers show evidence of being able to remember its location and extent, apparently with reference to distal landmarks.     

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.