The causes of the tremble dance of the honeybee,Apis mellifera

Tremble dances are sometimes performed by returning forager bees instead of waggle dances. Recent studies by Seeley (1992) and Kirchner (1993) have revealed that this behaviour is part of the recruitment communication system of bees. The ultimate cause of tremble dances is, according to Seeley (1992), an imbalance between the nectar intake rate and the nectar processing capacity of the colony. This imbalance is correlated with a long initial search time of returning foragers to find bees to unload them. However, it remained unclear whether a long search time is the direct proximate cause of tremble dancing. Here we report that a variety of experimental conditions can elicit tremble dances. All of them have in common that the total search time that foragers spend searching for unloaders, until they are fully unloaded, is prolonged. This finding supports and extends the hypothesis that a long search time is the proximate cause of tremble dancing. The results also confirm the previous reports of Lindauer (1948) and others about factors eliciting tremble dancing.     

Physiological correlates of genetic variation for rate of behavioral development in the honeybee, Apis mellifera

Two factors that influence age at onset of foraging in honeybees are juvenile hormone (JH) and colony age demography (older bees inhibit behavioral development of younger bees). We tested the hypothesis that genetic variation among bees for these factors influences genetic variation in behavioral development. Pairs of colonies showing genetic differences in rates of behavioral development were identified in a screening experiment and bees from these colonies were used for physiological and behavioral assays. Six pairs were assayed, three with European bees only and three with both European and Africanized bees. There was genetic variation for the following four components: (1) production of JH in four pairs (experiment 1); (2) sensitivity to JH in three pairs (experiment 2); (3) sensitivity to social inhibition in three pairs (experiment 3), and (4) potency of social inhibition in four pairs (experiment 4). Cross-fostering assays (experiment 5), which allowed all four components to be evaluated simultaneously, revealed genetic variation for production of JH, sensitivity to JH, or sensitivity to social inhibition in five of six pairs, and potency of social inhibition in five of six pairs. There was often evidence for genotypic differences in more than one component, and no consistent pattern of association among any of the components. Africanized bees had faster rates of behavioral development than European bees, but there were no racial differences in patterns of variation among the four components. These results indicate that there are at least several, apparently distinct, physiological processes associated with JH and colony age demography upon which natural selection can act to alter the rate of behavioral development in honeybees. Received: 8 December 1998 / Received in revised form: 29 July 1999 / Accepted: 8 August 1999     

MORPH—An individual-based model to predict the effect of environmental change on foraging animal populations

This paper describes an individual-based model, MORPH, that has been designed to predict the effect of environmental change on foraging animal populations. The key assumptions of MORPH are that individuals within populations behave in order to maximise their perceived fitness, but that perceived fitness may not always be positively related to the actual chances of survival and reproduction. MORPH has been parameterised for coastal birds on several European sites and predicted the effect of environmental change, caused by factors such as habitat loss, disturbance from humans and sea-level rise, on the survival and body condition of these species. However, MORPH contains a basic framework to describe animal physiology and foraging behaviour, and the distribution and abundance of the resources required by these animals. Therefore, MORPH is not restricted to coastal birds, and is potentially applicable to a wider range of systems. To be applied to a forager system, MORPH requires parameters describing (i) the distribution of the food supply and how food quality and abundance changes through time; (ii) the rate at which foragers consume food given the abundance of food and competitors; (iii) the amount of food the forager must consume each day to survive; (iv) the distribution and seasonal changes in other factors which influence the foraging behaviour and survival of foragers. The purpose of this paper is to (i) describe MORPH, (ii) give examples of its application, (iii) describe the types of systems to which MORPH can be applied, and (iv) publish its source code and a user guide.     

Antipredator strategies of house finches: are urban habitats safe spots from predators even when humans are around?

Urbanization decreases species diversity, but it increases the abundance of certain species with high tolerance to human activities. The safe-habitat hypothesis explains this pattern through a decrease in the abundance of native predators, which reduces predation risk in urban habitats. However, this hypothesis does not consider the potential negative effects of human-associated disturbance (e.g., pedestrians, dogs, cats). Our goal was to assess the degree of perceived predation risk in house finches (Carpodacus mexicanus) through field studies and semi-natural experiments in areas with different levels of urbanization using multiple indicators of risk (flock size, flight initiation distance, vigilance, and foraging behavior). Field studies showed that house finches in more urbanized habitats had a greater tendency to flock with an increase in population density and flushed at larger distances than in less urbanized habitats. In the semi-natural experiment, we found that individuals spent a greater proportion of time in the refuge patch and increased the instantaneous pecking rate in the more urbanized habitat with pedestrians probably to compensate for the lower amount of foraging time. Vigilance parameters were influenced in different ways depending on habitat type and distance to flock mates. Our results suggest that house finches may perceive highly urbanized habitats as more dangerous, despite the lower number of native predators. This could be due to the presence of human activities, which could increase risk or modify the ability to detect predators. House finches seem to adapt to the urban environment through different behavioral strategies that minimize risk.     

What currency do scatter-hoarding gray jays maximize?

Gray jays (Perisoreus canadensis) cache thousands of food items during each summer for use during the subsequent winter. Previous work on the economics of gray jay scatter-hoarding behavior was based on the assumption that the jays maximize the rate at which they store food energy; alternative currencies were not considered. Here we develop and test models based on two currencies, net rate (net recoverable energy stored per unit time) and efficiency (recoverable energy stored per unit energy expended). Our experiment involved providing gray jays with two options. After collecting a single food item upon arrival at a feeding apparatus, a jay could wait for two additional food items to become (simultaneously) available and then transport all three items for storage in scattered arboreal sites. Alternatively, the jay could immediately transport the single item to a storage site and return to the source repeatedly for additional single-item loads. By incrementally increasing the amount of time jays were required to wait for multipleitem loads, we were able to determine how long jays would wait before switching from multiple- to single-item caching trips. In contrast with the finding in a variety of species that efficiency-maximization models provide a better account of foraging behavior, the net rate-maximization model was a better predictor of the jays' switching point than was the efficiency-maximization model (Figs. 2 and 3). We discuss these conflicting results in the context of recent theory that describes the conditions favoring rate- versus efficiency-maximizing behavior (Ydenberg et al. 1994). Offprint requests to: T.A. Waite     

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     

Evidence of behavioral co-option from context-dependent variation in mandible use in trap-jaw ants (Odontomachus spp.)

Evolutionary co-option of existing structures for new functions is a powerful yet understudied mechanism for generating novelty. Trap-jaw ants of the predatory genus Odontomachus are capable of some of the fastest self-propelled appendage movements ever recorded; their devastating strikes are not only used to disable and capture prey, but produce enough force to launch the ants into the air. We tested four Odontomachus species in a variety of behavioral contexts to examine if their mandibles have been co-opted for an escape mechanism through ballistic propulsion. We found that nest proximity makes no difference in interactions with prey, but that prey size has a strong influence on the suite of behaviors employed by the ants. In trials involving a potential threat (another trap-jaw ant species), vertical jumps were significantly more common in ants acting as intruders than in residents (i.e. a dangerous context), while horizontal jumps occurred at the same rate in both contexts. Additionally, horizontal jump trajectories were heavily influenced by the angle at which the substrate was struck and appear to be under little control by the ant. We conclude that while horizontal jumps may be accidental side-effects of strikes against hard surfaces, vertical escape jumps are likely intentional defensive behaviors that have been co-opted from the original prey-gathering and food-processing functions of Odontomachus jaws.     

How floral odours are learned inside the bumblebee (Bombus terrestris) nest

Recruitment in social insects often involves not only inducing nestmates to leave the nest, but also communicating crucial information about finding profitable food sources. Although bumblebees transmit chemosensory information (floral scent), the transmission mechanism is unknown as mouth-to-mouth fluid transfer (as in honeybees) does not occur. Because recruiting bumblebees release a pheromone in the nest that triggers foraging in previously inactive workers, we tested whether this pheromone helps workers learn currently rewarding floral odours, as found in food social learning in rats. We exposed colonies to artificial recruitment pheromone, paired with anise scent. The pheromone did not facilitate learning of floral scent. However, we found that releasing floral scent in the air of the colony was sufficient to trigger learning and that learning performance was improved when the chemosensory cue was provided in the nectar in honeypots; probably because it guarantees a tighter link between scent and reward, and possibly because gustatory cues are involved in addition to olfaction. Scent learning was maximal when anise-scented nectar was brought into the nest by demonstrator foragers, suggesting that previously unidentified cues provided by successful foragers play an important role in nestmates learning new floral odours.     

Behavioral genomics of honeybee foraging and nest defense

The honeybee has been the most important insect species for study of social behavior. The recently released draft genomic sequence for the bee will accelerate honeybee behavioral genetics. Although we lack sufficient tools to manipulate this genome easily, quantitative trait loci (QTLs) that influence natural variation in behavior have been identified and tested for their effects on correlated behavioral traits. We review what is known about the genetics and physiology of two behavioral traits in honeybees, foraging specialization (pollen versus nectar), and defensive behavior, and present evidence that map-based cloning of genes is more feasible in the bee than in other metazoans. We also present bioinformatic analyses of candidate genes within QTL confidence intervals (CIs). The high recombination rate of the bee made it possible to narrow the search to regions containing only 17–61 predicted peptides for each QTL, although CIs covered large genetic distances. Knowledge of correlated behavioral traits, comparative bioinformatics, and expression assays facilitated evaluation of candidate genes. An overrepresentation of genes involved in ovarian development and insulin-like signaling components within pollen foraging QTL regions suggests that an ancestral reproductive gene network was co-opted during the evolution of foraging specialization. The major QTL influencing defensive/aggressive behavior contains orthologs of genes involved in central nervous system activity and neurogenesis. Candidates at the other two defensive-behavior QTLs include modulators of sensory signaling (Am5HT ₇ serotonin receptor, AmArr4 arrestin, and GABA-B-R1 receptor). These studies are the first step in linking natural variation in honeybee social behavior to the identification of underlying genes.     

Prey detection without successful capture affects spider’s orb-web building behaviour

Animals obtain information from past foraging experience to adjust their foraging activity according to their environment. The ability of spiders to obtain information from unsuccessful predation experiences was investigated by examining the effects on web building, a significant foraging investment, of prey detection without successful capture in the orb-web spider Cyclosa octotuberculata. Four treatments were employed: (1) successful capture and feeding: one syrphid fly was allowed to be captured and consumed by the spider on the web; (2) single prey-item detection: a syrphid fly was placed on the web to lure the spider, but was removed before capture; (3) five prey-item detection: above prey-item detection stimulus was given five times; and, (4) control: neither prey nor feeding on the web. While control spiders decreased the total thread length and capture area of their webs, prey-item detection spiders in both conditions increased them, indicating that the spider obtained information from unsuccessful predation experience to adjust their foraging investment. The fed spiders exhibited a significantly greater increase than the prey-detection-only spiders, suggesting that prey detection alone and prey detection with consumption had different informational effects. Total thread length did not differ between single and five prey-item detection spiders, but distance between two adjacent sticky spirals increased only in the former spiders, possibly because five times unsuccessful predations prevented spiders to reduce web stickiness. It suggests that the spider changed web morphology according to the number of prey detection.