Thomas D. Seeley

Adaptive significance of the age polyethism schedule in honeybee colonies

SummaryThe adaptive origins of the honeybees age polyethism schedule were studied by testing whether the schedule for labor inside the nest reflects a compromise between efficiency in locating tasks and efficiency in performing tasks. I checked two predictions of this hypothesis: (1) at each age a worker handles a set of tasks (rather than one task), and (2) the elements of each ages task-set co-occur spatially in the nest (rather than being spatially segregated). Most observations match these predictions, once workers reach the age of 2 days. The unpredicted specialization of 0 to 2-day-old workers on the single task of cell cleaning may reflect an unusual ease in locating work sites for this particular task. There are 5 female castes in honeybee colonies: the queen (reproductive caste), plus 4 age subcastes among the workers (cell cleaning caste, broodnest caste, food storage caste, and forager caste).

Collective decision-making in honey bees: how colonies choose among nectar sources

SummaryA honey bee colony can skillfully choose among nectar sources. It will selectively exploit the most profitable source in an array and will rapidly shift its foraging efforts following changes in the array. How does this colony-level ability emerge from the behavior of individual bees? The answer lies in understanding how bees modulate their colonys rates of recruitment and abandonment for nectar sources in accordance with the profitability of each source. A forager modulates its behavior in relation to nectar source profitability: as profitability increases, the tempo of foraging increases, the intensity of dancing increases, and the probability of abandoning the source decreases. How does a forager assess the profitability of its nectar source? Bees accomplish this without making comparisons among nectar sources. Neither do the foragers compare different nectar sources to determine the relative profitability of any one source, nor do the food storers compare different nectar loads and indicate the relative profitability of each load to the foragers. Instead, each forager knows only about its particular nectar source and independently calculates the absolute profitability of its source. Even though each of a colonys foragers operates with extremely limited information about the colonys food sources, together they will generate a coherent colonylevel response to different food sources in which better ones are heavily exploited and poorer ones are abandoned. This is shown by a computer simulation of nectar-source selection by a colony in which foragers behave as described above. Nectar-source selection by honey bee colonies is a process of natural selection among alternative nectar sources as foragers from more profitable sources “survive” (continue visiting their source) longer and “reproduce” (recruit other foragers) better than do foragers from less profitable sources. Hence this colonial decision-making is based on decentralized control. We suggest that honey bee colonies possess decentralized decision-making because it combines effectiveness with simplicity of communication and computation within a colony.

Foraging Strategy of Honeybee Colonies in a Temperate Deciduous Forest

To understand the foraging strategy of honeybee colonies, we measured certain tem- poral and spatial patterns in the foraging activities of a colony living in a temperate deciduous forest. We monitored foraging activities by housing the colony in an observation hive and reading its re- cruitment dances to map its food source patches. We found that the colony routinely foraged several kilometres from its nest (median 1.7 km, 95% of foraging within 6.0 km), frequently (at least daily) adjusted its distribution of foragers on its patches, and worked relatively few patches each day (mean of 9.7 patches accounted for 90% of each days forage). These foraging patterns, together with prior studies on the mechanisms of honeybee recruitment communication, indicate that the foraging strategy of a honeybee colony involves surveying the food source patches within a vast area around its nest, pooling the reconnaissance of its many foragers, and using this information to focus its forager force on a few high-quality patches within its foraging area.

Parasites, Pathogens, and Polyandry in Social Hymenoptera

Multiple mating by females with different males is widespread among insects, both solitary and social species (reviews in Walker 1980; Page and Metcalf 1982; Cole 1983; Starr 1984). Such polyandry creates opportunities for sperm competition (Parker 1984), a frequent outcome of which is multiple paternity within broods (e.g., in wasps, Metcalf and Whitt 1977, Muralidharan etal. 1986, Ross 1986; in ants, Pamilo 1982). Because multiple mating can thus reduce the average genetic relationship among female nest mates, polyandry represents an intriguing paradox for the original kin-selection explanations for the evolution of hymenopteran eusociality (Hamilton 1964, 1972; Starr 1979). Moreover, mating multiply may expose queens to increased chances of being preyed on or of contracting venereal diseases. Not surprisingly, therefore, considerable interest has recently been focused on the causes and consequences of multiple mating in insects generally (Thornhill and Alcock 1983, pp. 449-471) and social insects particularly (Page 1980, 1986). In one extreme but well-documented case, honeybee queens (Apis mellifera) may mate 17 or more times (Adams et al. 1977). Because the sperm from different males mix extensively rather than clumping separately, workers from many patrilines are simultaneously present in each colony (data in Taber 1955; Kerr et al. 1980; Laidlaw and Page 1984). Evidence is rapidly accumulating that worker honeybees can distinguish between closely and distantly related larvae (Page and Erickson 1984; Visscher 1986) and between fulland half-sibling adults (Getz and Smith 1983), using learned cues of genetic origin (Breed et al. 1985; Getz and Smith 1986). In the hive, such discrimination is manifested as nepotism and differential aggression: workers rear, feed, and groom a disproportionately large number of their full sisters (in colonies with or without queens; Noonan 1986; Frumhoff and Schneider 1987) and attack and bite an inordinate proportion of half sisters (in queenless colonies; Evers and Seeley 1986). It seems likely that such discrimination among patrilines may sometimes compromise colony-level efficiency and thus the queens reproductive output. Regardless, evidence of intra-nest kin-recognition mechanisms implies a long evolutionary history of discrepant reproductive interests among colony members resulting from multiple mating. In view of the potential disadvantages stemming from polyandry and the fact

Group decision making in swarms of honey bees

Abstract This study renews the analysis of honey bee swarms as decision-making units. We repeated Lindauers observations of swarms choosing future home sites but used modern videorecording and bee-labelling techniques to produce a finer-grained description of the decision-making process than was possible 40 years ago. Our results both confirm Lindauers findings and reveal several new features of the decision-making process. Viewing the process at the group level, we found: (1) the scout bees in a swarm find potential nest sites in all directions and at distances of up to several kilometers; (2) initially, the scouts advertise a dozen or more sites with their dances on the swarm, but eventually they advertise just one site; (3) within about an hour of the appearance of unanimity among the dancers, the swarm lifts off to fly to the chosen site; (4) there is a crescendo of dancing just before liftoff, and (5) the chosen site is not necessarily the one that is first advertised on the swarm. Viewing the process at the individual level, we found: (1) the dances of individual scout bees tend to taper off and eventually cease, so that many dancers drop out each day; (2) some scout bees switch their allegiance from one site to another, and (3) the principal means of consensus building among the dancing bees is for bees that dance initially for a non-chosen site to cease their dancing altogether, not to switch their dancing to the chosen site. We hypothesize that scout bees are programmed to gradually quit dancing and that this reduces the possibility of the decision-making process coming to a standstill with groups of unyielding dancers deadlocked over two or more sites. We point out that a swarms overall strategy of decision making is a “weighted additive strategy.” This strategy is the most accurate but also the most demanding in terms of information processing, because it takes account of all of the information relevant to a decision problem. Despite being composed of small-brained bees, swarms are able to use the weighted additive strategy by distributing among many bees both the task of evaluating the alternative sites and the task of identifying the best of these sites.

Social foraging in honey bees: how nectar foragers assess their colony's nutritional status

SummaryA honey bee colony operates as a tightly integrated unit of behavioral action. One manifestation of this in the context of foraging is a colonys ability to adjust its selectivity among nectar sources in relation to its nutritional status. When a colonys food situation is good, it exploits only highly profitable patches of flowers, but when its situation is poor, a colonys foragers will exploit both highly profitable and less profitable flower patches. The nectar foragers in a colony acquire information about their colonys nutritional status by noting the difficulty of finding food storer bees to receive their nectar, rather than by evaluating directly the variables determining their colonys food situation: rate of nectar intake and amount of empty storage comb. (The food storer bees in a colony are the bees that collect nectar from returning foragers and store it in the honey combs. They are the age group (generally 12–18 day old bees) that is older than the nurse bees but younger than the foragers. Food storers make up approximately 20% of a colony members.) The mathematical theory for the behavior of queues indicates that the waiting time experienced by nectar foragers before unloading to food storers (queue length) is a reliable and sensitive indicator of a colonys nutritional status. Queue length is automatically determined by the ratio of two rates which are directly related to a colonys nutritional condition: the rate of arrival of loaded nectar foragers at the hive (arrival rate) and the rate of arrival of empty food storers at the nectar delivery area (service rate). These two rates are a function of the colonys nectar intake rate and its empty comb area, respectively. Although waiting time conveys crucial information about the colonys nutritional status, it has not been molded by natural selection to serve this purpose. Unlike “signals”, which are evolved specifically to convey information, this “cue” conveys information as an automatic by-product. Such cues may prove more important than signals in colony integration.

Queen promiscuity lowers disease within honeybee colonies

Most species of social insects have singly mated queens, but in some species each queen mates with numerous males to create a colony with a genetically diverse worker force. The adaptive significance of polyandry by social insect queens remains an evolutionary puzzle. Using the honeybee (Apis mellifera), we tested the hypothesis that polyandry improves a colonys resistance to disease. We established colonies headed by queens that had been artificially inseminated by either one or 10 drones. Later, we inoculated these colonies with spores of Paenibacillus larvae, the bacterium that causes a highly virulent disease of honeybee larvae (American foulbrood). We found that, on average, colonies headed by multiple-drone inseminated queens had markedly lower disease intensity and higher colony strength at the end of the summer relative to colonies headed by single-drone inseminated queens. These findings support the hypothesis that polyandry by social insect queens is an adaptation to counter disease within their colonies.

Social foraging by honeybees: how colonies allocate foragers among patches of flowers

SummaryTo understand how a colony of honeybees keeps its forager force focussed on rich sources of food, and analysis was made of how the individual foragers within a colony decide to abandon or continue working (and perhaps even recruit to) patches of flowers. A nectar forager grades her behavior toward a patch in response to both the nectar intake rate of her colony and the quality of her patch. This results in the threshold in patch quality for acceptance of a patch being higher when the colonial intake rate of nectar is high than when it is low. Thus colonies can adjust their patch selectivity so that they focus on rich sources when forage is abundant, but spread their workers among a wider range of sources when forage is scarce. Foragers assess their colonys rate of nectar intake while in the nest, unloading nectar to receiver bees. The ease of unloading varies inversely with the colonial intake rate of nectar. Foragers assess patch quality while in the field, collecting nectar. By grading their behavior steeply in relation to such patch variables as distance from the nest and nectar sweetness, foragers give their colony high sensitivity to differences in profitability among patches. When a patchs quality declines, its foragers reduce their rate of visits to the patch. This diminishes the flow of nectar from the poor patch which in turn stimulates recruitment to rich patches. Thus a colony can swiftly redistribute its forager force following changes in the spatial distribution of rich food sources. The fundamental currency of nectar patch quality is not net rate of energy intake, (Gain-Cost)/Time, but may be net energy efficiency, (Gain-Cost)/Cost.

Honey bee foragers as sensory units of their colonies

Forager honey bees function not only as gatherers of food for their colonies, but also as sensory units shaped by natural selection to gather information regarding the location and profitability of forage sites. They transmit this information to colony members by means of waggle dances. To investigate the way bees transduce the stimulus of nectar-source profitability into the response of number of waggle runs, I performed experiments in which bees were stimulated with a sucrose solution feeder of known profitability and their dance responses were videorecorded. The results suggest that several attributes of this transduction process are adaptations to enhance a bees effectiveness in reporting on a forage site. (1) Bees register the profitability of a nectar source not by sensing the energy gain per foraging trip or the rate of energy gain per trip, but evidently by sensing the energetic efficiency of their foraging. Perhaps this criterion of nectar-source profitability has been favored by natural selection because the foraging gains of honey bees are typically limited by energy expenditure rather than time availability. (2) There is a linear relationship between the stimulus of energetic efficiency of foraging and the response of number of waggle runs per dance. Such a simple stimulus-response function appears adequate because the range of suprathreshold stimuli (max/min ratio of about 10) is far smaller than the range of responses (max/min ratio of about 100). Although all bees show a linear stimulus-response function, there are large differences among individuals in both the response threshold and the slope of the stimulus-response function. This variation gives the colony a broader dynamic range in responding to food sources than if all bees had identical thresholds of dance response. (3) There is little or no adaptation in the dance response to a strong stimulus (tonic response). Thus each dancing bee reports on the current level of profitability of her forage site rather than the changes in its profitability. This seems appropriate since presumably it is the current profitability of a forage site, not the change in its profitability, which determines a sites attractiveness to other bees. (4) The level of forage-site quality that is the threshold for dancing is tuned by the bees in relation to forage availability. Bees operate with a lower dance threshold when forage is sparse than when it is abundant. Thus a colony utilizes input about a wide range of forage sites when food is scarce, but filters out input about low-reward sites when food is plentiful. (5) A dancing bee does not present her information in one spot within the hive but instead distributes it over much of the dance floor. Consequently, the dances for different forage sites are mixed together on the dance floor. This helps each bee following the dances to take a random sample of the dance information, which is appropriate for the foraging strategy of a honey bee colony since it is evidently designed to allocate foragers among forage sites in proportion to their profitability.

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

Abstract. 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.