Contrasting bee foraging in response to resource scale and local habitat management

It is hypothesized that two main factors drive the foraging patterns of native and exotic species: food resource availability and habitat composition. These factors are particularly relevant for native bees and exotic honeybees, essential crop pollinators that are sensitive to floral resources and habitat management, and that have recently exhibited alarming population declines. Mechanisms driving native and exotic bee foraging patterns may critically depend on floral resource availability and habitat composition, yet the impacts of these factors on bee foraging have never been simultaneously analyzed. In a coffee producing region in southern Mexico, we investigated the influence of coffee floral resource levels and habitat management on native and exotic bee foraging. We measured the amount of flowering coffee available at multiple spatial scales within two distinct agroforestry habitat types (high-shade and low-shade coffee) and recorded visits to coffee flowers, documenting bee species, visit duration and visit frequency. We observed a significantly greater number of visits in high-shade coffee habitats than in low-shade coffee habitats for both native and exotic bees. In high-shade coffee habitats, native solitary bee and native social bee visitation decreased significantly in response to increasing floral resource availability, exhibiting a 'dilution effect' at the smallest spatial scale. In contrast, in low-shade coffee habitats, Africanized honeybees exhibited a 'concentration effect', increasing visitation significantly in response to increasing floral resource availability at the largest spatial scale. This study is the first to show that foraging patterns of native bees and exotic honeybees contrast in response to floral resource level and scale and that this response is mediated by the vegetation management of the local habitat.     

Reef fishes foraging facilitation behavior: increasing the access to a food resource

Fishes associated in schools acquire adaptive advantages by grouping together, e.g., access to a larger variety of food resources, foraging sites, and protection against potential predators. This work presents the first record of a feeding association between the bucktooth parrotfish, Sparisoma radians and the sailor’s grunt Haemulon parra, on Tamandaré reefs, Southwestern Atlantic. Through this association, S. radians gained access to otherwise unavailable food resources to be found inside territorial damselfish domain, thus characterizing an event of foraging facilitation.     

A trade-off between scale and precision in resource foraging

Summary There is widespread uncertainty about the nature and role of morphological plasticity in resource competition in plant communities. We have assayed the foraging characteristics of leaf canopies and root systems of eight herbaceous plants of contrasted ecology using new techniques to create controlled patchiness in light and mineral nutrient supply. The results are compared with those of a conventional competition experiment. Measurements of dry matter partitioning and growth in patchy conditions indicate a consistent positive association between the foraging characteristics of roots and shoots, supporting the hypothesis of strong interdependence of competitive abilities for light and mineral nutrients. Differences are identified in the abilities of dominant and subordinate plants to forage on coarse and fine scalcs. It is suggested that a trade-off exists in the scale (“high” in dominants) and precision (high in subordinates) with which resources are intercepted and that this trade-off contributes to diversity in communities of competing plants.     

Ant foraging strategies vary along a natural resource gradient

Food selection by foragers is sensitive to the availability of resources, which may vary along geographical gradients. Hence, selectivity of food types by foragers is expected to track these resource gradients. Here we addressed this hypothesis and asked if foraging decisions of seed-eating ants differ along a geographic gradient of habitat productivity. The study was carried out for two years at five sites along a natural climatic gradient, ranging from arid to Mediterranean, where plant productivity varies six-fold across a short geographic distance of 250 km. We found that in ant colonies of the genus Messor, collective foraging decisions differed along the gradient. Specifically, at the high-productivity sites, a stronger association was found between plant seed availability and selectivity, suggesting that colonies respond more accurately to within-patch variation in food amounts. In contrast, colonies in low-productivity sites foraged in patches with higher concentration of seeds, suggesting that they respond more accurately to among-patch variation in food amounts. Moreover, at the high-productivity sites, colonies were more discriminating in their choice of food and preferred bigger seeds, while in the low-productivity sites, where smaller seeds were relatively more abundant, food collection depended mostly on seed availability. An experiment with artificial seed patches performed along the same climatic gradient, revealed no difference in food selectivity across sites when food type and availability were similar, and a general preference for bigger over medium-sized seeds. Overall, our findings suggest that resource availability is an important factor explaining food choice along a climatic gradient and imply that in low-productivity regions small-seeded species incur high predation pressure, whereas in high-productivity regions, large-seeded species suffer higher predation. This could have important consequences for plant species composition, particularly at the face of climate change, which could dramatically alter the foraging decisions of granivores.     

Predicting resource utilization: the utility of optimal foraging models

Predicting how predation changes communities is an important challenge for ecologists. One view assumes that predictions can be made in terms of behavioural phenomena. Static optimality methods have been used to devise models of prey choice and are thought to have performed well. Two examples from the literature show that models of diet choice have either been applied without first testing them at the individual level, or have been tested in a way that does not fulfil all their assumptions. A discussion of the nature of mathematical models shows why it is dangerous to translate theories into natural language and how important it is to appreciate the limitations on the mathematical functions describing behaviour. A final section discusses behavioural phenomena such as satiation and learning, which are likely to limit the predictive capacities of static optimization models. It is likely that dynamic models are the way forward although they may be harder to apply at the ecological level.     

Social foraging and the behavioral ecology of intragroup resource transfers

Two chimpanzees stalk, isolate, and kill a red colobus monkey. An attendant primatologist notes that parts of the prey are relinquished selectively to onlooking scroungers (Fig. 1). A human forager returns to camp mid-afternoon with a freshly killed, medium-sized ungulate. Later in the day, an ethnographer observes that shared portions of the animal have found their way into the cooking pots of most or all of those in the small band. Examining a prehistoric scatter of food residues, an ethnoarcheologist wonders when early hominids began to scrounge or share food, and with what consequences for our evolution. All of these settings represent one problem: the analysis of intragroup resource transfers among social foragers. New studies in the behavioral ecology of transfers show them to be more commonplace in nature, more complicated and variable, and more subject to comparative analysis than has been appreciated.     

Optimal resource allocation to survival and reproduction in parasitic wasps foraging in fragmented habitats

Expansion and intensification of human land use represents the major cause of habitat fragmentation. Such fragmentation can have dramatic consequences on species richness and trophic interactions within food webs. Although the associated ecological consequences have been studied by several authors, the evolutionary effects on interacting species have received little research attention. Using a genetic algorithm, we quantified how habitat fragmentation and environmental variability affect the optimal reproductive strategies of parasitic wasps foraging for hosts. As observed in real animal species, the model is based on the existence of a negative trade-off between survival and reproduction resulting from competitive allocation of resources to either somatic maintenance or egg production. We also asked to what degree plasticity along this trade-off would be optimal, when plasticity is costly. We found that habitat fragmentation can indeed have strong effects on the reproductive strategies adopted by parasitoids. With increasing habitat fragmentation animals should invest in greater longevity with lower fecundity; yet, especially in unpredictable environments, some level of phenotypic plasticity should be selected for. Other consequences in terms of learning ability of foraging animals were also observed. The evolutionary consequences of these results are discussed.     

Quantifying dynamic resource allocation illuminates foraging strategy in Phanerochaete velutina

Saprotrophic woodland fungi forage for mineral nutrients and woody resources by extension of a mycelial network across the forest floor. Different species explore at different rates and establish networks with qualitatively differing architecture. However, detailed understanding of fungal foraging behaviour has been hampered by the absence of tools to quantify resource allocation and growth accurately and non-invasively. To solve this problem, we have used photon-counting scintillation imaging (PCSI) to map and quantify nutrient allocation and localised growth simultaneously in heterogeneous resource environments. We show that colonies spontaneously shift to an asymmetric growth pattern, even in the absence of added resources, often with a distinct transition between the two growth phases. However, the extent of polarisation was much more pronounced and focussed in the presence of an additional cellulose resource. In this case, there was highly localised growth, often at the expense of growth elsewhere in the colony, and marked accumulation of ¹⁴C-AIB in the sector of the colony with the added resource. The magnitude of the response was greatest when resource was added around the time of the endogenous developmental transition. The focussed response required a metabolisable resource, as only limited changes were seen with glass fibre discs used to mimic the osmotic and thigmotropic stimuli upon resource addition. Overall the behaviour is consistent with an adaptive foraging strategy, both to exploit new resources and also to redirect subsequent foraging effort to this region, presumably with an expectation that the probability of finding additional resources is increased.     

Crab regulation of cross-ecosystem resource transfer by marine foraging fire ants

Permeability of boundaries in biological systems is regulated by biotic and/or abiotic factors. Despite this knowledge, the role of biotic factors in regulating resource transfer across ecosystem boundaries has received little study. Additionally, little is known about how cross-ecosystem resource transfer affects source populations. We used experiments, observations and stable isotopes, to evaluate: (1) the proportion of intertidal-foraging black fire ant (Solenopsis richteri) diet derived from marine sources, (2) how black fire ant cross-ecosystem resource transfer is altered by the dominant bioengineer in the intertidal, a burrowing crab (Neohelice granulata), (3) the top-down impact of these terrestrial ants on a marine resource, and (4) the effect of marine resources on recipient black fire ants. We found that more than 85% of the black fire ant diet is derived from marine sources, the number of intertidal foraging ants doubles in the absence of crab burrows, and that ants cause a 50% reduction in intertidal polychaetes. Also, ant mound density is three times greater adjacent to marine systems. This study reveals that cross-ecosystem foraging terrestrial ants can clearly have strong impacts on marine resources. Furthermore, ecosystem engineers that modify and occupy habitat in these ecosystem boundaries can strongly regulate the degree of cross-ecosystem resource transfer and resultant top down impacts.     

A model of resource partitioning between foraging bees based on learning

Central place foraging pollinators tend to develop multi-destination routes (traplines) to exploit patchily distributed plant resources. While the formation of traplines by individual pollinators has been studied in detail, how populations of foragers use resources in a common area is an open question, difficult to address experimentally. We explored conditions for the emergence of resource partitioning among traplining bees using agent-based models built from experimental data of bumblebees foraging on artificial flowers. In the models, bees learn to develop routes as a consequence of feedback loops that change their probabilities of moving between flowers. While a positive reinforcement of movements leading to rewarding flowers is sufficient for the emergence of resource partitioning when flowers are evenly distributed, the addition of a negative reinforcement of movements leading to unrewarding flowers is necessary when flowers are patchily distributed. In environments with more complex spatial structures, the negative experiences of individual bees on flowers favour spatial segregation and efficient collective foraging. Our study fills a major gap in modelling pollinator behaviour and constitutes a unique tool to guide future experimental programs.     

Behavioral mechanisms underlying ants' density-dependent deterrence of aphid-eating predators

Density-dependent mutualisms have been well documented, but the behavioral mechanisms that can produce such interactions are not as well understood. We investigated interactions between predatory ladybirds and the ant Lasius neoniger, which engages in a facultative association with the aphid Aphis fabae . We found that ants disrupted predator aggregation and deterred foraging, but that this effect varied with aphid density. In the field, smaller aphid colonies had higher numbers of ants per aphid (higher relative ant density), whereas plants with larger aphid colonies had lower relative ant density. Ants deterred ladybird foraging when relative ant density was high, but when relative ant density was low, ladybirds aggregated to aphids and foraged more successfully. This difference in ladybird foraging success appeared to be driven by variation in the ants' distribution on the plant and the ladybirds' reaction to ants. When relative ant density was high, ants moved around the perimeter of the aphid colonies, which resulted in faster detection of predators and a greater likelihood of ladybirds leaving. However, when relative ant density was low, ants moved only in the midst of the aphid colonies and rarely around the perimeter, which allowed predators to approach the aphid colony from the perimeter and feed without detection. Such predators were less likely to leave the aphid colony when subsequently detected by ants. We suggest that differences in relative ant numbers, ant distribution, and predator reaction to detection by ants could lead to complex population-level consequences including density-dependent mutualisms and the possibility that predators act as prudent predators.     

Optimal foraging in nonpatchy habitats. I. Bounded one-dimensional resource

We present a model of optimal foraging in habitats where the food has an arbitrary density distribution (continuous or not). The classical models of foraging strategies assume that the food is distributed in patches and that the animal divides its time between the two distinct behaviors of patch exploitation and interpatch travel. This assumption is hard to accept in instances where the food distribution is continuous in space, and where travel and feeding cannot be sharply distinguished. In this paper, the habitat is assumed to be one-dimensional and bounded, and the animal is assumed to have a limited foraging time available. The problem is treated mathematically in the context of the calculus of variations. The optimal solution is to divide the habitat in two subsets according to the food density. In the richer subset, the animal equalizes the density distribution; in the poorer subset, it travels as fast as possible.     

Dietary similarity and foraging range of two seed-harvester ants during resource fluctuations

Summary Diets of desert seed-harvester ants Veromessor pergandei and Pogonomyrmex rugosus were studied for 3 years at two habitats where they are common and sympatric. Diets of the two species were similar, consisting mainly (87% of 23,913 seeds) of three annual plant species (Schismus arabicus, Plantago insularis, and Pectocarya recurvata). Diets converged following a drought in Winter/Spring 1984 which reduced seed production during this time. Foraging range of P. rugosus almost doubled following the drought while foraging range of V. pergandei remained constant. Neither ant species move their nests once established rendering them effectively sessile granivores. This limits the dietary options of a given colony and may explain interspecific dietary convergence.     

Short‐term foraging responses of a generalist predator to management‐driven resource pulses

Generalist predators characteristically switch prey in response to resource pulses. Ungulate population reinforcement through translocation provides stressed and vulnerable prey, and apex predator reintroduction provides carrion, both resources that can be exploited by generalist predators. We investigated the dietary response of black‐backed jackal to two management interventions in the Karoo National Park, South Africa, namely the reinforcement of the springbok population, and then the reintroduction of lions. By analysing jackal diets from scats collected before and after each management intervention, we show that the relative per cent occurrence and biomass consumed of springbok increased in the diet following the population reinforcement of springbok. In contrast, large ungulates were more prevalent in the diet following apex predator reintroduction. These results suggest that jackals took advantage of a potentially vulnerable abundant springbok population following their population reinforcement, and then switched to foraging on carrion provided by reintroduced lions. These results provide insights into the dietary response of a generalist mesopredator to management interventions. A key lesson from the study is that the diet of generalist predators is context‐dependent and should be interpreted in that light.     

Predation risk and resource abundance mediate foraging behaviour and intraspecific resource partitioning among consumers in dominance hierarchies

Dominance hierarchies and the resulting unequal resource partitioning among individuals are key mechanisms of population regulation. The strength of dominance hierarchies can be influenced by size‐dependent tradeoffs between foraging and predator avoidance whereby competitively inferior subdominants can access a larger proportion of limiting resources by accepting higher predation risk. Foraging‐predation risk tradeoffs also depend on resource abundance. Yet, few studies have manipulated predation risk and resource abundance simultaneously; consequently, their joint effect on resource partitioning within dominance hierarchies are not well understood. We addressed this gap by measuring behavioural responses of masu salmon Oncorhynchus masou ishikawae to experimental manipulations of predation risk and resource abundance in a natural temperate forest stream. Responses to predation risk depended on body size and social status such that larger fish (often social dominants) exhibited more risk‐averse behaviour (e.g. lower foraging and appearance rates) than smaller subdominants after exposure to a simulated predator. The magnitude of this effect was lower when resources were elevated, indicating that dominant fish accepted a higher predation risk to forage on abundant resources. However, the influence of resource abundance did not extend to the population level, where predation risk altered the distribution of foraging attempts (a proxy for energy intake) from being skewed towards large individuals to being skewed towards small individuals after predator exposure. Our results imply that size‐dependent foraging–predation risk tradeoffs can weaken the strength of dominance hierarchies by allowing competitively inferior subdominants to access resources that would otherwise be monopolized.     

Adaptive foraging of leaf‐cutter ants to spatiotemporal changes in resource availability in Neotropical savannas

1. Generalist herbivores feed on a wide and diverse set of species, but fine‐scale foraging patterns may be affected by the interplay between the quality, quantity and spatial distribution of host plants. 2. The foraging patterns of a prevalent Neotropical herbivore, the leaf‐cutter ant Atta laevigata, in the Brazilian Cerrado savannas were examined in order to determine if patterns observed are in concert with central‐place foraging predictions. 3. The results showed that A. laevigata acts as a polyphagous but highly selective herbivore, with ant attacks often resulting in partial defoliation of less‐preferred species and full defoliation of preferred ones. It was found, for the first time, that there is a strong and positive relationship between the relative attack frequency on plants from preferred species and foraging distance to the nest. This suggests a balance between the quality of plant resources harvested and costs involved in their transportation. It was also observed that colonies focused their harvest on preferred species in months with low availability of young leaves. Consequently, high herbivory rate was more frequent in plants attacked far away from the nest and in dry months. 4. These assessments highlight the fact that Atta colonies may become more selective as foraging distance to the nest increases and in response to fluctuations in the availability of palatable resources throughout the year. The results also show some dissimilarities in the foraging behaviours of A. laevigata when compared with other locations, suggesting that widely distributed herbivores may modify foraging strategies across their geographic range.     

The scale-precision trade-off in spacial resource foraging by plants: restoring perspective

BACKGROUND AND AIMS: From the results of a comparative study using quantitative standardized assays of the scale and precision of responses of root and shoot systems to resource patchiness, Campbell et al. (1991; Oecologia 87: 532-538) proposed a mechanism of species coexistence in herbaceous communities involving a dynamic equilibrium between, respectively, the coarse- and fine-scale foraging of dominant and subordinate species. The purpose of this paper is to reject a recent assertion that with respect to root systems the scale-precision hypothesis has been falsified. DISCUSSION AND CONCLUSION: Reference to the original papers confirms that the scope of the hypothesis was confined to circumstances (eg. mown meadows) where the vigour of potential dominants is restricted by intermittent removal of biomass. This qualification in the original hypothesis is a crucial omission from the meta-analysis conducted by Kembel and Cahill (2005; American Naturalist 166: 216-230). The original papers also contain examples that illustrate the operation of forms of selection that prevent the development of precise foraging below ground; these also appear to have escaped the attention of recent participants in this field of research.     

Lifelong foraging and individual specialisation are influenced by temporal changes of resource availability

Resource availability largely determines the distribution and behaviour of organisms. In plant–pollinator communities, availability of floral resources may change so rapidly that pollinator individuals can benefit from switching between multiple resources, i.e. different flowering plant species. Insect pollinator individuals of a given generation often occur in different time windows during the reproductive season. This temporal variation in individual occurrences, together with the rapidly changing resource availability, may lead individuals of the same population to encounter and use different resources, resulting in an apparent individual specialisation. We hypothesized, that 1) individual pollinators change their resource use (flower visitation) during their lifetime according to the changing availability of floral resources, and that 2) temporal variation in individual occurrences of pollinators and in resource availability will partly explain individual specialisation. To test these hypotheses, we observed flower visitations of individually marked clouded Apollo butterflies Parnassius mnemosyne during one reproductive season. We found temporal changes in lifetime individual resource use that followed the changes in resource availability, indicating that butterflies can adjust foraging to varying resource availability. Individuals differed considerably in their resource use. This variation was partly explained by temporal variation in both floral resource availability and temporal occurrence of individual butterflies. We suggest the butterfly as a sequential specialist, i.e. short‐term specialist and long‐term generalist. This foraging plasticity can be essential for short‐living insect pollinators in rapidly changing environments. Although flowering dynamics do not fully explain the variability in foraging, our results highlight the importance of temporal dimension in resource use studies. Ultimately, the relative pace of environmental change compared to individual lifespan may be a key factor in resource use plasticity.