Coordinating a group departure: who produces the piping signals on honeybee swarms?

A swarm of honeybees provides a striking example of an animal group performing a synchronized departure for a new location; in this case, thousands of bees taking off at once to fly to a new home. However, the means by which this is achieved remain unclear. Shortly before takeoff, one hears a crescendo of a high-pitched mechanical signal—worker piping—so we explored the role of this signal in coordinating a swarm’s mass takeoff. Specifically, we examined whether exclusively nest site scouts produce the worker piping signal or whether it is produced in a relay or chain reaction fashion. We found no evidence that bees other than the scouts that have visited the swarm’s chosen nest site produce piping signals. This absence of relay communication in piping suggests that it is a signal that only primes swarms for takeoff and that the release of takeoff is triggered by some other signal or cue; perhaps the takeoff of bees on the swarm periphery as they reach flight temperature in response to piping.     

Moving home: nest-site selection in the Red Dwarf honeybee (<Emphasis Type="Italic">Apis florea</Emphasis>)

The Red Dwarf honeybee (Apis florea) is one of two basal species in the genus Apis. A. florea differs from the well-studied Western Hive bee (Apis mellifera) in that it nests in the open rather than in cavities. This fundamental difference in nesting biology is likely to have implications for nest-site selection, the process by which a reproductive swarm selects a new site to live in. In A. mellifera, workers show a series of characteristic behaviors that allow the swarm to select the best nest site possible. Here, we describe the behavior of individual A. florea workers during the process of nest-site selection and show that it differs from that seen in A. mellifera. We analyzed a total of 1,459 waggle dances performed by 197 scouts in five separate swarms. Our results suggest that two fundamental aspects of the behavior of A. mellifera scouts—the process of dance decay and the process of repeated nest site evaluation—do not occur in A. florea. We also found that the piping signal used by A. mellifera scouts to signal that a quorum has been reached at the chosen site, is performed by both dancing and non-dancing bees in A. florea. Thus, the piping signal appears to serve a different purpose in A. florea. Our results illustrate how differences in nesting biology affect the behavior of individual bees during the nest-site selection process.     

Extra-pair paternity in alpine marmots, <Emphasis Type="Italic">Marmota marmota</Emphasis>: genetic quality and genetic diversity effects

Assuming that a male’s genetic characteristics affect those of his offspring, extra-pair copulation has been hypothesized to increase heterozygosity of the progeny—the “genetic compatibility” hypothesis—and the genetic diversity within litters—the “genetic diversity” hypothesis. We tested these two hypotheses in the alpine marmot (Marmota marmota), a socially monogamous mammal showing a high rate of extra-pair paternity (EPP). In a first step, we tested the assumption that a male’s genetic characteristics (heterozygosity and genetic similarity to the female) affect those of his offspring. Genetic similarity between parents influenced offspring heterozygosity, offspring genetic similarity to their mother, and litter genetic diversity. The father’s heterozygosity also influenced litter genetic diversity but did not affect offspring heterozygosity. Hence, heterozygosity seems not to be heritable in the alpine marmot. In a second step, we compared genetic characteristics of extra-pair young (EPY) and within-pair young (WPY). EPY were less genetically similar to their mother but not more heterozygous than WPY. EPY siblings were also less genetically similar than their WPY half siblings. Finally, the presence of EPY promoted genetic diversity within the litter. Thus, our data support both the “genetic compatibility” and the “genetic diversity” hypotheses. We discuss further investigations needed to determine the primary causes of EPP in this species.     

Do bumble bee queens choose nest sites to maximize foraging rate? Testing models of nest site selection

We proposed “foundress-max” hypothesis that a bumble bee foundress chooses her nest site to maximize her energy intake rate from nectar. To examine the hypothesis, we estimated the maximum energy intake rate at each site in the study area and compared the distribution of the maximum energy intake rates with those of actual nest sites. We also calculated rank correlations of the maximum energy intake rate with the number of nest-searching foundresses at 54 sites. The nest locations supported the foundress-max hypothesis, but the number of nest-searching foundresses did not. This could be attributed to the density of food sites: many food sites may attract many foundresses. Therefore, we subsequently proposed “foundress-sum” hypothesis that a foundress chooses her nest site to maximize the sum of energy intake rates. The nest locations supported the foundress-max hypothesis more than the foundress-sum hypothesis. A profitable food site would affect foundresses’ nest site selection.     

Individual differences in nest defense in the colonial breeding Black-tailed Gulls

Often in colonial seabirds, all colony members are believed to defend against nest predators and experience equal nest predation risk. However, the variation of defense behavior among members and its reproductive consequences are largely unknown. We investigated (1) individual variation in the nest defense of breeding Black-tailed Gulls Larus crassirostris against a natural egg predator, the Jungle Crow Corvus macrorhynchos and (2) how this behavioral variation affects an individual’s own nest predation risk and that of their neighbors. Results were compared between 2 years where crow attack levels were manipulated to average 5 and 22 times normal rates (“low” and “high” predation risk years, respectively) by the placement of varying numbers of artificial nests containing unguarded eggs at the perimeter of the gull colony. In both years, 23–38% of parents, mostly males, showed “aggressive” defense behavior (strikes or chases) against crows and decoys. Other “non-aggressive” gulls showed no defense. In the year of low predation risk, intrusion rates by crows (landing within 0.5 m of an individual gull’s nest) were similar for aggressive and non-aggressive gulls. In the year of high predation risk, however, the rates of intrusion for aggressive gulls (4%) and for non-aggressive gulls with an aggressive neighbor (37%) were significantly lower than for non-aggressive gulls without an aggressive neighbor (76%). These results indicate that aggressive individuals reduce nest predation risk for themselves and conspecific neighbors in a colonially breeding species.     

Nest site selection in the open-nesting honeybee Apis florea

We studied nest site selection by swarms of the red dwarf honeybee, Apis florea. By video recording and decoding all dances of four swarms, we were able to determine the direction and distances indicated by 1,239 dances performed by the bees. The bees also performed a total of 715 nondirectional dances; dances that were so brief that no directional information could be extracted. Even though dances converged over time to a smaller number of areas, in none of the swarms did dances converge to one site. As a result, even prior to lift off, bees performed dances indicating nest sites in several different directions. Two of four swarms traveled directly in what seemed to be the general direction indicated by the majority of dances in the half hour prior to swarm lift off. The other two traveled along circuitous routes in the general direction indicated by the dances. We suggest that nest site selection in A. florea has similar elements to nest site selection in the better-studied Apis mellifera. However, the observation that many more locations are indicated by dances prior to lift off also shows that there are fundamental differences between the two species.     

Co-occurrence of three types of egg policing in the Norwegian wasp <Emphasis Type="Italic">Dolichovespula norwegica</Emphasis>

In insect societies, workers often try to challenge the reproductive monopoly of the queen by laying their own eggs. Successful worker reproduction, however, is frequently prevented by queen policing or worker policing, whereby either the mother queen or non-reproductive workers selectively kill worker-laid eggs. Recently, a third mechanism—“selfish” worker policing—has also been described in which the workers selectively police worker-laid eggs but also lay eggs themselves. Here, we present results from the monogynous wasp Dolichovespula norwegica, which show that all three kinds of policing—queen policing, worker policing and “selfish” worker policing—co-occur. The net effect of these three kinds of policing collectively favoured the queen’s reproduction, as within 1 day 44% of the worker-laid eggs versus only 8% of the queen-laid eggs were eaten. Of the worker-laid eggs that were killed by workers, approximately two thirds were eaten by the reproductive workers even though these made up only a small proportion, 8%, of the work force. This means that policing workers obtained both direct fitness benefits as well as indirect (inclusive) fitness. In addition, we show that worker policing was carried out by a limited, specialised set of workers that was estimated to constitute approximately one quarter of the whole colony and of which 66% were non-reproductive.     

Better the nest site you know: decision-making during nest migrations by the Pharaoh’s ant

Animals frequently have to decide between alternative resources and in social insects these individual choices produce a colony-level decision. The choice of nest site is a particularly critical decision for a social insect colony to make, but the decision making process has still only been studied in a few species. In this study, we investigated nest selection by the Pharaoh’s ant, Monomorium pharaonis, a species renowned for its propensity to migrate and its use of multi-component trail pheromones to organise decision-making in other contexts. When presented with the choice of familiar and novel nests of equal quality in a Y set-up, colonies preferentially migrated towards the familiar nest, suggesting a form of colony-level ‘memory’ of potential nest sites. However, if the novel nest was superior to the familiar nest, then colonies began migrating initially to the familiar nest, but then redirected their migration to the superior quality novel nest. This may be an effective method of reducing colony exposure while searching for an optimum nest site. Branches that had previously led to a selected nest were attractive to ants in subsequent migrations, suggesting that trail pheromones mediate the decision making process. The adaptive, pheromone-based organisation of nest-site selection by Pharaoh’s ants matches their ephemeral environment and is likely to contribute to their success as a 'tramp' species.     

Risk-prone hunting by chimpanzees (<Emphasis Type="Italic">Pan troglodytes schweinfurthii</Emphasis>) increases during periods of high diet quality

Most studies suggest that during times of nutritional stress, an animal faced with two foraging choices should follow a risk-prone strategy, choosing the option with highest payoff variance. This “scarcity/risk” hypothesis was developed to account for the foraging patterns of small animals with high metabolic rates susceptible to the threat of starvation. In this paper, we propose that animals should also be risk-prone when their diet quality is particularly high, far exceeding that which is needed to survive. Under these circumstances, the costs of experiencing a low or negative payoff can easily be recouped. We suggest that large-bodied omnivores are most likely to adopt this “abundance/risk” strategy. We investigate this question among wild chimpanzees (Pan troglodytes) that choose between a risk-averse strategy of feeding on plant material and a risk-prone strategy of hunting red colobus monkeys. Using 14 years of data on the Kanyawara chimpanzees of Kibale National Park, Uganda, we find strong evidence that chimpanzees follow the “abundance/risk” strategy. Both hunting rate (hunts/100 observation hours) and the probability of hunting upon encountering red colobus monkeys were positively correlated with seasonal consumption of ripe drupe fruits, a class of preferred food associated with elevated reproductive performance by females. Critically, these results remained statistically significant after controlling for the potentially confounding effects of male chimpanzee party size and the presence of sexually receptive females. These findings suggest that the relationship between risk-sensitive foraging and diet quality depends upon the daily probability of starvation, the number of alternative foraging strategies, and the degree to which diet quality satisfies an animal’s nutritional requirements.     

An oligarchy of nest-site scouts triggers a honeybee swarm’s departure from the hive

Animals that travel in groups must synchronize the timing of their departures to assure cohesion of the group. While most activities in large colonies of social insects have decentralized control, certain activities (e.g., colony migration) can have centralized control, with only a special subset of well-informed individuals making a decision that affects the entire colony. We recently discovered that a small minority of individuals in a honeybee colony—an oligarchy—decides when to trigger the departure of a swarm from its hive. The departure process begins with some bees producing the worker-piping signal (the primer for departure) and is followed by these bees producing the buzz-run signal (the releaser for departure). In this study, we determined the identity of these signalers. We found that a swarm’s nest-site scouts search for potential nest cavities prior to the departure of the swarm from its hive. Furthermore, we found that the predeparture nest-site scouts are the sole producers of the worker-piping signal and that they are the first producers of the buzz-run signal. The control of the departure of a honeybee swarm from its hive shows how a small minority of well-informed individuals in a large social insect colony can make important decisions about when a colony should take action.     

The role of the queen mandibular gland pheromone in honeybees (<Emphasis Type="Italic">Apis mellifera</Emphasis>): honest signal or suppressive agent?

Queen pheromones interfere with worker reproduction in social insects. However, there is still an unresolved question as to whether this pheromone acts as an “honest” signal for workers, giving a reliable indication of the queen’s reproductive value, or as a suppressive agent, inhibiting worker reproduction independent of the queen’s reproductive capacity. In honeybees (Apis mellifera), the queen’s mandibular gland secretion, a mix of fatty acids and some aromatic compounds, is crucial for regulating the reproductive division of labor in the colony inhibiting ovary development in workers. We quantified the mandibular gland secretions of virgin, drone-laying, and naturally mated queens using gas chromatography to test whether the queens’ mating, ovary activation, or the reproductive value for workers correlated with the composition of the secretion. Although the absolute amounts of the “queen substance” 9-oxo-2(E)-decenoic acid (9-ODA) were similar among the three groups, the proportions of 9-ODA decreased with increasing reproductive quality. Furthermore, the ratios of queen to worker compounds were similar in all three treatment groups, irrespective of the reproductive capacity. A multivariate analysis including all six compounds could not separate drone-laying queens from naturally mated ones, both with active ovaries but only the latter ensuring colony survival. We suggest that the mandibular gland pheromones are unlikely to function as reliable indicators of queen reproductive value and rather operate as an agent to suppress worker reproduction. This does not exclude the possibility that other “honest” pheromone signals exist in the honeybee colony, but these would have to arise from other semiochemicals, which could be produced by both the queen and the brood.     

Nest-site selection in honey bees: how well do swarms implement the "best-of-N" decision rule?

This study views a honey bee swarm as a supraorganismal entity which has been shaped by natural selection to be skilled at choosing a future home site. Prior studies of this decision-making process indicate that swarms attempt to use the best-of-N decision rule: sample some number (N) of alternatives and then select the best one. We tested how well swarms implement this decision rule by presenting them with an array of five nest boxes, only one of which was a high-quality (desirable) nest site; the other four were medium-quality (acceptable) sites. We found that swarms are reasonably good at carrying out the best-of-N decision rule: in four out of five trials, swarms selected the best site. In addition, we gained insights into how a swarm implements this decision rule. We found that when a scout bee returns to the swarm cluster and advertises a potential nest site with a waggle dance, she tunes the strength of her dance in relation to the quality of her site: the better the site, the stronger the dance. A dancing bee tunes her dance strength by adjusting the number of waggle-runs/dance, and she adjusts the number of waggle-runs/dance by changing both the duration and the rate of her waggle-run production. Moreover, we found that a dancing bee changes the rate of her waggle-run production by changing the mean duration of the return-phase portion of her dance circuits. Differences in return-phase duration underlie the impression that dances differ in liveliness. Although a honey bee swarm has bounded rationality (e.g., it lacks complete knowledge of the possible nesting sites), through its capacity for parallel processing it can choose a nest site without greatly reducing either the breadth or depth of its consideration of the alternative sites. Such thoroughness of information gathering and processing no doubt helps a swarm implement the best-of-N decision rule.     

Individual- and condition-dependent effects on habitat choice and choosiness

Research on consistent individual differences in behavior, or “behavioral syndromes”, continues to grow rapidly, and yet, the aspects of behavior under consideration have remained remarkably limited. Here, we consider individual variation in consistency of choice (termed here “choosiness”), as expressed during habitat choice. We repeatedly tested the responses of female Western Black Widows, Latrodectus hesperus, to two cues of habitat quality: prey chemical cues and variation in web site illuminance. We estimated females’ response by the distance they positioned themselves from (1) the source of prey chemical cues and (2) the darkest edge of our test arena. Individuals with low variance in their responses are deemed more “choosy”, whereas individuals with high variance are deemed less “choosy”. Generally, most females initiated web construction near the source of the prey chemical cues and tended to place themselves in low-light conditions. However, we detected strong, repeatable differences in females’ intensity of response, and within-individual variance of response (i.e., choosiness) was correlated across situations: females with highly consistent responses towards cricket chemical cues also exhibited highly consistent responses towards variation in light conditions. When deprived of food for extended periods, females were indistinguishable in their responses towards prey chemical cues, but tended to initiate web construction in brighter lighting conditions. Food-deprived females universally exhibited higher variance and diminished consistency in their responses (i.e., they were less choosy). Additionally, higher choosiness was associated with greater mass loss during choice trials, suggesting choosiness is energetically costly. Our results demonstrate that consistency of response to environmental cues is yet another element of behavior that varies among individuals and variation in choosiness could beget speed/quality trade-offs during animal decision making.     

An integrated look at decision-making in bees as they abandon a depleted food source

While there has been considerable research on the behavioral processes that underlie animals’ ability respond to shifting rewards, it remains unclear how animals coordinate multiple processes over time. To investigate this, we compared the behavior of honeybees (Apis mellifera) and bumblebees (Bombus impatiens), in an open-ended search task. Bees were given brief access to a high-quality food source, which then became non-rewarding. Then, over an extended period, we examined (1) bees’ tendency to persist at the depleted site, (2) their tendency to return to a different low-quality food source where they had been foraging previously, (3) their tendency to return to the hive, and (4) how previous reward history influenced their tendency to shift among these options. Compared to bumblebees, honeybees were much slower to abandon the depleted site and were much more likely to make trips to the hive while bumblebees were much more likely to return to the familiar low-quality site. These observed species differences are interpreted in terms of evolved individual and social differences between these species. We show evidence of well-studied behavioral processes such as extinction, negative contrast effects, and reliance on a social group, and provide, for the first time, a picture of how these processes interact with one another as part of a common sequential decision-making process.     

Costs of delayed dispersal and alloparental care in the fungus-cultivating ambrosia beetle <Emphasis Type="Italic">Xyleborus affinis</Emphasis> Eichhoff (Scolytinae: Curculionidae)

Body reserves may determine the reproductive output of animals, depending on their resource allocation strategy. In insects, an accumulation of reserves for reproduction is often obtained before dispersal by pre-emergence (or maturation) feeding. This has been assumed to be an important cause of delayed dispersal from the natal nest in scolytine beetles. In the cooperatively breeding ambrosia beetles, this is of special interest because in this group delayed dispersal could serve two alternative purposes: “selfish” maturation feeding or “altruistic” alloparental care. To distinguish between these two possibilities, we have experimentally studied the effect of delayed dispersal on future reproductive output in the xyleborine ambrosia beetle Xyleborus affinis. Females experimentally induced to disperse and delayed dispersing females did not differ in their body condition at dispersal and in their founding success afterwards, which indicates that females disperse independently of condition, and staying adult females are fully mature and would be able to breed. However, induced dispersers produced more offspring than delayed dispersers within a test period of 40 days. This suggests that delayed dispersal comes at a cost to females, which may result primarily from alloparental care and leads to a reduced reproductive output. Alternatively, females might have reproduced prior to dispersal. This is unlikely, however, for the majority of dispersing females because of the small numbers of offspring present in the gallery when females dispersed, suggesting that mainly the foundress had reproduced. In addition, “gallery of origin” was a strong predictor of the reproductive success of females, which may reflect variation in the microbial complex transmitted vertically from the natal nest to the daughter colony, or variation of genetic quality. These results have important implications for the understanding of proximate mechanisms selecting for philopatry and alloparental care in highly social ambrosia beetles and other cooperatively breeding arthropods.     

The role of the vibration signal in the house-hunting process of honey bee (<Emphasis Type="Italic">Apis mellifera</Emphasis>) swarms

The function of the vibration signal of the honey bee (Apis mellifera) during house hunting was investigated by removing vibrating bees from swarms and examining the effects on waggle dancing for nest sites, liftoff preparations and swarm movement. We compared house hunting among three swarm types: (1) test swarms (from which vibrating bees were removed), (2) manipulated control (MC) swarms (from which randomly selected workers and some waggle dancers were removed), and (3) unmanipulated control (UC) swarms (from which no bees were removed). The removal of vibrating bees had pronounced effects on liftoff preparations and swarm movement. Compared to the MC and UC swarms, the test swarms had significantly greater liftoff-preparation periods, were more likely to abort liftoff attempts, and in some cases were unable to move to the chosen site after the swarm became airborne. However, the three swarm types did not differ in overall levels of waggle dance activity, the time required to achieve consensus for a nest site, the rate at which new waggle dancers were recruited for the chosen site, or the ability to maintain levels of worker piping necessary to prepare for flight. The removal of vibrating bees may therefore have altered liftoff behavior because of a direct effect on vibration signal activity. A primary function of the signal during house hunting may be to generate a level of activity in workers that enhances and coordinates responses to other signals that stimulate departure and movement to a new location.Communicated by R. Page     

Do newborn domestic rabbits Oryctolagus cuniculus compete for thermally advantageous positions in the litter huddle?

Competition among mammalian siblings for scarce resources can be severe. Whereas research to date has focused on competition for the mother’s milk, the young of many (particularly altricial) species might also be expected to compete for thermally favorable positions within the nest, den, or litter huddle. We investigated this in newborn pups of the European rabbit Oryctolagus cuniculus, a species in which the altricial young are not brooded by the mother, and in which competition for milk is severe. In eight unculled litters (N = 86 pups) of a domestic chinchilla strain, we calculated huddling indexes for individual pups on postnatal days 2–5 as a measure of the degree of insulation they received from littermates. Pups maintained almost constant physical contact with the litter huddle. They performed brief but frequent rooting and climbing behaviors, which usually improved their huddling index, interspersed with longer periods of quiescence during which their huddling index declined. As expected, we found a significant positive relation between pups’ mean huddling index and body temperature. Unexpectedly, however, we did not find a relation between huddling index and pups’ birth weight, survival, milk intake, or efficiency of converting milk to body mass. We conclude that rather than competing for thermally advantageous positions within the huddle newborn rabbits share out thermally advantageous positions as they move in a continual dynamic flow through it. Thus, in newborn rabbits, competition for the mother’s milk exists alongside mutual “cooperative” benefits of littermate presence. This contribution is part of the special issue “Sibling competition and cooperation in mammals” (guest editors: Robyn Hudson and Fritz Trillmich).     

The early bee catches the flower - circadian rhythmicity influences learning performance in honey bees, <Emphasis Type="Italic">Apis mellifera</Emphasis>

Circadian rhythmicity plays an important role for many aspects of honey bees’ lives. However, the question whether it also affects learning and memory remained unanswered. To address this question, we studied the effect of circadian timing on olfactory learning and memory in honey bees Apis mellifera using the olfactory conditioning of the proboscis extension reflex paradigm. Bees were differentially conditioned to odours and tested for their odour learning at four different “Zeitgeber” time points. We show that learning behaviour is influenced by circadian timing. Honey bees perform best in the morning compared to the other times of day. Additionally, we found influences of the light condition bees were trained at on the olfactory learning. This circadian-mediated learning is independent from feeding times bees were entrained to, indicating an inherited and not acquired mechanism. We hypothesise that a co-evolutionary mechanism between the honey bee as a pollinator and plants might be the driving force for the evolution of the time-dependent learning abilities of bees.     

Echolocation behavior of the bat <Emphasis Type="Italic">Vespertilio murinus</Emphasis> reveals the border between the habitat types “edge” and “open space”

We test the hypothesis that echolocation behavior can be used to find the border between bat habitats. Assuming that bats react to background targets in “edge space” but not in “open space”, we determined the border between these two habitat types for commuting individuals of the parti-colored bat Vespertilio murinus. We recorded sequences of bats’ echolocation signals while they flew parallel to the walls of large buildings and to the ground and determined the signals’ average bandwidth, duration, and pulse interval. These parameters varied systematically with the estimated horizontal and vertical distances between the bats and the background. A distinct effect of horizontal distance to the background on echolocation behavior was found for horizontal distances of less than 6 m, thus indicating the border between edge and open space. Only a few bats flew at vertical distances below 5 m. However, enough passages at vertical distances of 5 m and above indicated that the vertical border is somewhere below a distance of 5 m. Within edge space, V. murinus reacted to the background by reducing signal duration, increasing bandwidth at closer distances, and often emitting one signal per wing beat. In open space, signal parameters did not vary as a function of distance to the background. There, V. murinus emitted the longest signals with the narrowest bandwidth and often made one or two wing beats without emitting a pulse. With our data we support with statistical methods the hypothesis that echolocation behavior reveals the border between the habitat types “edge” and “open space”.