Honeybee recruitment to scented food sources: correlations between in-hive social interactions and foraging decisions

Information exchange of environmental cues facilitates decision-making processes among members of insect societies. In honeybee foraging, it is unknown how the odor cues of a resource are relayed to inactive nest mates to enable resource exploitation at specific scented sources. It is presumed that bees need to follow the dance or to be involved in trophallaxis with a successful forager to obtain the discovered floral scent. With this in mind, we evaluated the influence of food scent relayed through in-hive interactions and the subsequent food choices. Results obtained from five colonies demonstrated that bees arriving at a feeding area preferred to land at a feeder carrying the odor currently exploited by the trained forager. The bees that landed at this feeder also showed more in-hive encounters with the trained forager than the individuals that landed at the alternative scented feeder. The most frequent interactions before landing at the correct feeder were body contacts with the active forager, a behavior that involves neither dance following nor trophallaxis. In addition, a reasonable proportion of successful newcomers showed no conspicuous interactions with the active forager. Results suggest that different sources of information can be integrated inside the hive to establish an odor-rewarded association useful to direct honeybees to a feeding site. For example, simple contacts with foragers or food exchanges with non-active foragers seem to be enough to choose a feeding site that carries the same scent collected by the focal forager.     

Plasticity in echolocation signals of European pipistrelle bats in search flight: implications for habitat use and prey detection

We studied the echolocation and hunting behavior of three aerial insectivorous species of bats (Vespertilionidae: Pipistrellus) in the field in order to characterize the signals used by the bats and to determine how call structure varies in relation to habitat structure (uncluttered versus cluttered space). We documented free-flying, naturally foraging wild pipistrelles in various habitats using multiflash stereophotography combined with simultaneous sound recordings. Then we reconstructed the bat's flight position in three-dimensional space and correlated it with the corresponding echolocation sequences. In all three species of pipistrelles, signal structure varied substantially. In echolocation sequences of the search phase we found a consistent association of signal types with habitat types. In uncluttered habitats (obstacles more than 5 m from the bat) pipistrelles emitted almost exclusively narrowband signals with bandwidths less than 15 kHz. In cluttered habitats (obstacles less than 5 m from the bat) they switched to signals with bandwidths of more than 15 kHz. Wideband signals were also used when the bats were turning in cluttered and uncluttered spaces and for an instant after turning away from obstacles. Prey detection occured only when the outgoing signal did not overlap with the returning echo from potential prey. The bats also avoided overlap of echoes from potential prey and obstacles. Based on the results of this study, we propose an overlap-free window within which pipistrelles may detect potential prey and which allows predictions of minimum distances to prey and clutter-producing objects. Correspondence to: E.K.V. Kalko     

Innate movement rules in foraging bees: flight distances are affected by recent rewards and are correlated with choice of flower type

The non-random movement patterns of foraging bees are believed to increase their search efficiency. These patterns may be innate, or they may be learned through the bees’ early foraging experience. To identify the innate components of foraging rules, we characterized the flight of naive bumblebees, foraging on a non-patchy “field” of randomly scattered artificial flowers with three color displays. The flowers were randomly mixed and all three flower types offered equal nectar volumes. Visited flowers were refilled with probability 0.5. Flight distances, flight durations and nectar probing durations were determined and related to the bees’ recent experiences. The naive bees exhibited area-restricted search behavior, i.e., flew shorter distances following visits to rewarding flowers than after visits to empty flowers. Additionally, flight distances during flower-type transitions were longer than flight distances between flowers of the same type. The two movement rules operated together: flight distances were longest for flights between flower types following non-rewarding visits, shortest for within-type flights following rewarding visits. An increase in flight displacement during flower-type shifts was also observed in a second experiment, in which all three types were always rewarding. In this experiment, flower-type shifts were also accompanied by an increase in flight duration. Possible relationships between flight distances, flight durations and flower-type choice are discussed. Received: 20 November 1995/Accepted after revision: 10 May 1996     

Timing of the evening emergence from day roosts of the grey-headed flying fox, Pteropus poliocephalus: the effects of predation risk, foraging needs, and social context

This study addresses the functional question of how variation in foraging strategy, predation risk, and social context influence the timing of the evening emergence from day roosts of the grey-headed flying fox, Pteropus poliocephalus. The onset of evening emergence was expected to vary according to the relative costs and benefits of emerging early and should, therefore, reflect an optimal trade-off between predation risks and foraging needs. The onset of the colony-wide emergence was closely correlated with the time of sunset and cloud cover. However, as expected, the onset of the colony-wide emergence was delayed when a diurnal avian predator was present, whereas the onset was advanced during lactation when presumably energetic demands are higher. The trade-off between predation risks and foraging needs was further reflected in the emergence times of individual bats: adult females emerged earlier when they had higher foraging needs as indicated by their body condition; young emerged later when they were smaller and likely to be more at risk from predation due to their less developed flying skills. However, the emergence time of adult males depended on their social status: smaller bachelor males emerged from the colony earlier than larger harem-holding males who guard their harems until the last female had left. Thus, whereas the colony-wide emergence time reflected the outcome of a trade-off between predation risks and general foraging needs, on an individual level, the outcome of this trade-off depended on sex, age, body condition, and structural size and was modified by social context.     

Vigilance and foraging substrate: anti-predatory considerations in a non-standard environment

Summary The commonly studied standard anti-predatory environment presents animals with spatially-distinct feeding sites and refuges from attack, neither of which necessarily obstructs predator detection. In contrast, tree-trunks provide animals with a markedly non-standard environment in which the foraging substrate itself may be a refuge from attack that unavoidably obstructs predator detection. Thus anti-predatory behavior in this environment should be influenced not only by a perceived risk of attack, but also by the nature of the refuge/foraging substrate itself. Downy woodpeckers (Picoides pubescens) are a common tree-trunk foraging animal, and an experimental analysis of their behavior suggests that they respond appropriately to their non-standard anti-predatory environment. In particular, anti-predatory vigilance varies strongly with changes in tree trunk diameter. Two modes of vigilance were apparent. In stationary vigilance, woodpeckers maintained the position of their feet while rotating their bodies side-to-side to peer around the trunk; mobile vigilance involved movement around the trunk itself. Both the frequency and angle of rotation of stationary vigilance increased with trunk diameter, as did the frequency of mobile vigilance. The woodpeckers also held their heads farther away from the trunk surface as diameter increased. All of these measures of vigilance increased under a greater perceived risk of predation. As might be expected given these results, downy woodpeckers avoided thick trunks; they did not, however, prefer the thinnest (least obstructive) available trunks. These preferences may reflect the influence of trunk diameter on thermo-ecological and/or anti-predator considerations not related to vigilance. Overall, this arboreal environment provides an unusual perspective on anti-predator decision-making with several implications for tree-trunk foraging animals in general.     

Social foraging and dominance relationships: the effects of socially mediated interference

In socially foraging animals, it is widely acknowledged that the position of an individual within the dominance hierarchy of the group has a large effect upon its foraging behaviour and energetic intake, where the intake of subordinates can be reduced through socially mediated interference. In this paper, we explore the effects of interference upon group dynamics and individual behaviour, using a spatially explicit individual-based model. Each individual follows a simple behavioural rule based upon its energetic reserves and the actions of its neighbours (where the rule is derived from game theory models). We show that dominant individuals should have larger energetic reserves than their subordinates, and the size of this difference increases when either food is scarce, the intensity of interference suffered by the subordinates increases, or the distance over which dominant individuals affect subordinates increases. Unlike previous models, the results presented in this paper about differences in reserves are not based upon prior assumptions of the effects of social hierarchy and energetic reserves upon predation risk, and emerge through nothing more than a reduction in energetic intake by the subordinates when dominants are present. Furthermore, we show that increasing interference intensity, food availability or the distance over which dominants have an effect also causes the difference in movement between ranks to increase (where subordinates move more than dominants), and the distance over which dominants have an effect changes the size of the groups that the different ranks are found in. These results are discussed in relation to previous studies of intra- and interspecific dominance hierarchies.     

Maternal energy expenditure does not change with flight costs or food availability in the pied flycatcher (Ficedula hypoleuca): costs and benefits for nestlings

We manipulated parental work load without changing brood size in a population of pied flycatchers Ficedula hypoleuca by removing two primaries (7 and 9) from each wing of females, thus reducing wing area and increasing flight costs. At other nests, we offered supplementary food in the form of live mealworms (10–20 g daily from hatching) to reduce brood demand and thus parental foraging costs. Other nests were left as controls. The daily energy expenditure of females feeding 12-day-old nestlings was measured with doubly labelled water D₂ ¹⁸O. Females in both treatments expended the same amount of energy, fed at the same rate and had similar body masses to birds in the control group. No effect of treatment on male mass and feeding effort was detected. More nestlings, however, died in nests of handicapped females. Nestlings of handicapped females had significantly lower body mass and haematocrit values than nestlings in food-supplemented nests, with nestlings in control nests occupying an intermediate position. The effects of both treatments on nestling mass, haematocrit values and mortality rates were only noticeable in nests infested with mites. Maternal energy expenditure is apparently constrained and offspring pay the costs imposed by reduced provisioning rate or increased demand caused by ectoparasites, while receiving benefits when food supply improves. The presumption that avian reproductive costs derive from changes in a flexible energy output may not be met in many cases. Received: 24 October 1998 / Received in revised form: 15 March 1999 / Accepted: 26 April 1999     

Recycling food and agriculture by-products to mitigate climate change: a review

Food loss and waste is a major issue affecting food security, environmental pollution, producer profitability, consumer prices, and climate change. About 1.3 billion tons of food products are yearly lost globally, with China producing approximately 20 million tons of soybean dregs annually. Here, we review food and agricultural byproducts with emphasis on the strategies to convert this waste into valuable materials. Byproducts can be used for animal and plant nutrition, biogas production, food, extraction of oils and bioactive substances, and production of vinegar, wine, edible coatings and organic fertilizers. For instance, bioactive compounds represent approximately 8–20% of apple pomace, 5–17% of orange peel, 10–25% of grape seeds, 3–15% of pomegranate peel, and 2–13% of date palm seeds. Similarly, the pharmaceutical industry uses approximately 6.5% of the total output of gelatin derived from fish bones and animal skin. Animals fed with pomegranate peel and olive pomace improved the concentration of deoxyribonucleic acid and protein, the litter size, the milk yield, and nest characteristics. Biogas production amounts to 57.1% using soybean residue, 53.7% using papaya peel, and 49.1% using sugarcane bagasse.

     

Predator foraging behavior in response to perception and learning by its prey: interactions between orb-spinning spiders and stingless bees

Although rewarded bees learn and remember colors and patterns, they have difficulty in learning to avoid negative stimuli such as decorated spider webs spun by Argiope argentata. A. argentata decorates its web with silk patterns that vary unpredictably (Fig. 1) and thus foraging insects that return to sites where spiders are found encounter new visual cues daily. Stingless bees can learn to avoid spider webs but avoidance-learning is slowed or inhibited by daily variation in web decorations (Figs. 3,4; Tables 1,2). In addition, even if bees learn to avoid decorated webs found in one location, they are unable to generalize learned-avoidance responses to similarly decorated webs found at other sites. A. argentata seems to have evolved a foraging behavior that is tied to the ways insects perceive and process information about their environment. Because of the evolutionary importance of bee-flower interdependence, the predatory behavior of web-decorating spiders may be difficult for natural selection to act against.     

Low roost-site fidelity in pallid bats: associated factors and effect on group stability

Despite potential costs of changing roost or densites, many animals frequently move between roosts or dens. Pallid bats (Antrozous pallidus) change diurnal roost sites frequently and also reportedly have a variety of cooperative social behaviors, many of which are associated with the care of developing offspring. Roost switching is likely to increase the costs of maintaining the group stability expected with social cooperation. Pallid bats roosting in rock crevices in central Oregon were studied with radiotelemetry to (1) examine characteristics of day roosts, (2) determine what ecological factors were correlated with low roost fidelity, and (3) examine the temporal stability of roosting groups of pregnant and lactating bats. Pallid bats changed roosts an average of once every 1.4 days throughout the summer. The bats exhibited seasonal shifts in roost use, occupying roosts behind thin slabs of rock in cool weather and roosts in deep rock crevices in warm weather. Roost switching was not correlated with daily variations in weather conditions or with structural characteristics of the diurnal roosts, although switching may have allowed bats to maintain familiarity with several roosts that vary in microclimate. Roost switching was positively correlated with ectoparasite load. High ectoparasite levels were correlated with lower body weights in lactating females (Fig. 3), suggesting that parasites may be costly to the bats. Roost switching may be a strategy to decrease ectoparasite loads by interrupting the reproductive cycles of those parasites that spend at least part of their life cycle on the walls of the roost. Both pregnant and lactating pallid bats frequently changed their diurnal roost location, but lactating bats tended to travel shorter distances between consecutive roosts. Lactating bats were more likely to continue to associate with particular roostmates despite changes in the location of the diurnal roost (Fig. 4) and were less likely to roost alone. Although the stability of groups of lactating bats was not absolute, evidence supported the prediction that such groups are more cohesive than are those of pregnant bats. Received: 20 June 1995/Accepted after revision: 13 July 1996     

Overestimations of food abundance: predator responses to prey aggregation

Understanding and predicting the consequences of trophic interactions for community processes requires knowledge of the role of food availability, which is often wrongly conflated with prey abundance. For prey animals in groups, this is not fully understood. Previous work has shown that oystercatchers more frequently attack solitary rather than aggregated limpets and are more successful in predation attempts on singletons. It has also been demonstrated that an attack on one limpet in a group alerts the entire group, all of which then clamp down and become unavailable. I show that Eurasian Oystercatchers (Haematopus ostralegus L.) attack only one limpet in a group and then move on to attack another individual limpet, and I also demonstrate that the distance they move is greater than the distance at which groups of limpets have been known to detect attacks. Thus in the oystercatcher-limpet predator-prey system on rocky shores, groups of limpets are actually one prey item independently of the number of limpets in the group. This has implications for assessment of food supply for avian predators on rocky shores, with consequences for our understanding of previously documented trophic cascades.     

Differences in sensory ecology contribute to resource partitioning in the bats Myotis bechsteinii and Myotis nattereri (Chiroptera: Vespertilionidae)

Coexisting animal species frequently differ in resource use in at least one niche dimension and thus avoid competition. While a range of morphological differences that lead to differentiation in animals' mechanical access to food have been identified, the role of sensory differences in within-guild niche differentiation has received less attention. We tested the hypothesis that differences in sensory access to prey contribute to resource partitioning between potentially competing species using two sympatric, similar-sized, congeneric bat species as a model system. Nursery colonies of Natterer's bat (Myotis nattereri) and Bechstein's bat (Myotis bechsteinii) roost in bat boxes in the same orchard and forage in forests and orchards nearby. In observations and behavioural experiments with freshly captured M. bechsteinii, we showed that individuals are able to hunt using prey-generated sound alone. In contrast, M. nattereri rarely uses prey-generated sound, but instead is able to find prey by echolocation very close to vegetation. In accordance with these behavioural data, we showed that M. bechsteinii has significantly larger ears than M. nattereri, providing it with superior detection and localization abilities for relatively low-frequency prey rustling sounds. We hypothesized that these differences in sensory ecology of the two syntopic, congeneric species would contribute to resource partitioning, so that M. bechsteinii would find more noisy prey taxa, possibly hidden in vegetation, by listening for prey sounds, while M. nattereri would have better access to still prey using echolocation or associative learning. Analysis of faecal samples collected on the same nights from bat boxes occupied by each species corroborated this prediction. The diets of the two species differed significantly, reflecting their different prey perception techniques and thereby supporting the hypothesis that differences in sensory ecology contribute to niche differentiation. Electronic supplementary material Supplementary material is available for this article at and accessible for authorised users. B.M. Siemers and S.M. Swift contributed equally to this work.     

Fruit detection and discrimination by small fruit-eating bats (Phyllostomidae): echolocation call design and olfaction

We studied the role of echolocation and other sensory cues in two small frugivorous New World leaf-nosed bats (Phyllostomidae: Artibeus watsoni and Vampyressa pusilla) feeding on different types of fig fruit. To test which cues the bats need to find these fruit, we conducted behavioral experiments in a flight cage with ripe and similar-sized figs where we selectively excluded vision, olfaction, and echolocation cues from the bats. In another series of experiments, we tested the discrimination abilities of the bats and presented sets of fruits that differed in ripeness (ripe, unripe), size (small, large), and quality (intact(infested with caterpillars). We monitored the bats' foraging and echolocation behavior simultaneously. In flight, both bat species continuously emitted short (<2 ms), multi-harmonic, and steep frequency-modulated (FM) calls of high frequencies, large bandwidth, and very low amplitude. Foraging behavior of bats was composed of two distinct stages: search or orienting flight followed by approach behavior consisting of exploration flights, multiple approaches of a selected fruit, and final acquisition of ripe figs in flight or in a brief landing. Both bat species continuously emitted echolocation calls. Structure and pattern of signals changed predictably when the bats switched from search or orienting calls to approach calls. We did not record a terminal phase before final acquisition of a fruit, as it is typical for aerial insectivorous bats prior to capture. Both bat species selected ripe over unripe fruit and non-infested over infested fruit. Artibeus watsoni preferred larger over smaller fruit. We conclude from our experiments, that the bats used a combination of odor-guided detection together with echolocation for localization in order to find ripe fruit and to discriminate among them.