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Honeybees
Honeybees M. D. Breed, University of Colorado, Boulder, CO, USA ã 2010 Elsevier Ltd. All rights reserved.
Background The honeybees, all members of the genus Apis, are one of the most familiar flying animals of terrestrial habitats. The center of diversity of the genus is Southeast Asia, where several species are found. Most of these species are limited in range to tropical and montane zones in Southeast and South Asia, but two species have far broader ranges. Apis cerana, sometimes called the Eastern hive bee, occurs as far north as Japan and into the Middle East. Apis mellifera, or the Western hive bee, is native to Africa. It expanded its range into Europe and Asia as the ice-age glaciers retreated, and has been spread by humans to the Americas, Australia, and Hawaii (Figure 1). A. mellifera has also been introduced through much of the range occupied by A. cerana, including Japan and mainland China. In this article, I review the basic biology of the genus Apis, with a focus behavior. Human associations with honeybees are deeply rooted in prehistory. Honey hunting was likely an important source of food for early humans living in Asia, Africa, and Europe. Cave paintings in Spain record prehistoric honey hunting by humans, and honey remains an important human food source. An image of the honeybee forms a key element in the ancient Egyptian hieroglyph symbolizing Lower Egypt. Roman ruins sometimes feature niches in walls that were designed to hold honeybee colonies, and numerous such walls constructed in the seventeenth and eighteenth centuries are found in the French and British countryside. Currently, honeybees are highly important pollinators, providing pollination services in manipulated agroecosystems in which native bee populations are reduced and for nonnative crop plants. Most of our scientific knowledge of honeybees comes from studies of A. mellifera. Scientists’ fascination with the honeybee dates back at least to Aristotle, and the maintenance of bee colonies by medieval religious communities fostered knowledge of bee management and behavior. Early publications, such as Charles Bulter’s Feminine Monarchie (1609) held a great amount of detail about honeybee biology, some correct and some incorrect, and form the foundation for modern knowledge of honeybees. The discovery by Jan Dzierzon in 1845 that male honeybees arise from unfertilized (haploid) eggs and females from fertilized (diploid) eggs is an excellent example of how the tradition of beekeeping by educated clergymen led to intellectual explorations of bee biology and behavior. Haplodiploidy, the system of sex determination discovered by Dzierzon and known as Dzierzon’s
rule, is now understood to be a characteristic of nearly all Hymenoptera. Twentieth century studies of honeybees are rooted in the work of Karl von Frisch (1886–1982), who shared the 1973 Nobel Prize in Physiology or Medicine with Niko Tinbergen and Konrad Lorenz. Von Frisch’s discoveries of color vision in bees, the dance language of the honeybee, and the ability of bees to use the polarization of light in their orientation were key to the development of sensory physiology and animal behavior as scientific fields. Generations of scientists have followed in von Frisch’s footsteps, refining and further developing concepts first proposed by von Frisch and his students.
The Apis Family Tree Honeybees lie in the subfamily Apinae of the family Apidae (Figure 2) although it should be noted that there has been considerable controversy over the phylogeny of these bees. Their branch of the apine family tree includes other eusocial taxa, the bumblebees and the stingless bees. In addition to eusociality, honeybees share the use of wax in nest construction with bumblebees and stingless bees, although honeybees are the only taxa to use wax as the sole construction element of their combs. Two major sets of differences align with the evolution of species in Apis – size and nesting habit. The genus divides among dwarf bees, giant bees, and bees that we would regard as more ‘normal’ in size, like A. mellifera. The overall appearance of all Apis species is quite similar, but size varies manyfold between the dwarf species, like A. florea, and giant species like A. dorsata. The dwarf honeybees, subgenus Micrapis, which includes A. florea (Figure 3) and A. andreniformis, are generally considered the basal, or most primitive, group within Apis. The giant honeybees are first derived from the dwarf honeybees and then the cavity-nesting honeybees are derived. The giant honeybees, subgenus Macrapis, include A. dorsata (Figure 4) and A. laboriosa. Micrapis and Macrapis species build nests of a single exposed comb suspended from a branch, cave roof or cliff. Bees in the subgenus Apis–Apis mellifera, A. cerana, A. nigrocincta, A. nuluensis, and A. koschevnikovi – all nest in cavities, such as hollow trees, and build nests of multiple combs. What features are held in common among all species in the genus? While the level of documentation varies among species, from the very well-known A. mellifera to the almost entirely unknown A. nuluensis, some generalizations about
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Figure 1 Western honeybee, Apis mellifera, colony in a small cave. The use of multiple combs is typical of cavity nesting honeybees, subgenus Apis. Photo by Thomas Ranker.
the genus are widely accepted. All Apis species are highly eusocial, meaning that queens and their daughter workers live together in colonies, there is a strong morphological differentiation between queens and workers, and the workers cooperate to rear additional workers, males (drones), and new queens from among their sibs. All members of the genus build nests of wax combs, have workers with barbed, autotomous stings, and have queens that, after multiple matings, store sperm for use throughout their life. Workers in all honeybee species communicate about food resources using a dance language and release alarm pheromones to alert nestmates to threats. Honeybees reproduce by swarming, with the queen in a colony leaving the nest with about half the workers and establishing a new nest; she is replaced in the old nest by one of her daughter queens. As with other eusocial Hymenoptera (ants, some wasps, as well as some other types of bee), all honeybee workers are female. Apis workers are highly differentiated from queens, with larger eyes, hairier bodies, small ovaries, no capacity to mate, and autotomous stings. Drones have yet stouter bodies and even larger eyes, probably adaptations for both flight and spotting potential mates.
Honeybees, Agriculture, and Ecosystems Services A. mellifera is the champion honey producer in the genus. While all Apis species store some concentrated nectar (honey) in their combs, most honeybee species abscond
from nests if conditions are poor and seek out a more favorable nesting site, or are seasonally migratory, moving to accommodate variation in rain and temperature. A. mellifera is the only species which is successful across a vast expanse of the northern temperate zone (in Europe and Asia, and introduced into temperate North America). Escaping temperate winters is beyond the migratory ability of honeybees and it is likely that storage of large amounts (50 kg or more) of honey evolved as a way of having food stores for overwintering. Temperatures inside A. mellifera nests (and to the extent A. cerana lives in temperate climates, in cerana nests) are maintained near 30 C through the unfavorable season. Storing food creates an attractive resource for animals like skunks, raccoons, bears, and, obviously, humans. Additionally, the larvae and pupae, which are reared in cells in the comb, have high nutritional value. It is no surprise that honeybees have intense defensive methods available to them, and these defenses are highly effective against vertebrate predators. In many human cultures, bee larvae or pupae are consumed in addition to honey. Beeswax is regarded as a high-grade base for cosmetics and candles. Propolis (plant resins collected by bees to seal cracks and supplement wax as a structural material) was used as a base for varnishes prior to the development of petroleum-based wood finishes. Propolis was reputedly a key ingredient in finishes used on fine violins, such as those made by Stradivarius. Recently, hive products such as pollen, royal jelly, and propolis have been touted for their medicinal properties. Globally, most agriculturally managed honeybees are A. mellifera, but A. cerana colonies are maintained in parts of Asia. The techniques used to keep these two species are similar. Until the nineteenth century, bees were typically maintained in sections of hollow logs (Figure 5) or in woven straw hives, called ‘skeps.’ The skep is a state symbol for Utah, appearing on highway signs and at the center of the state seal. These arrangements had the disadvantage of not allowing inspection and management of the combs, and required at least partial destruction of the colony when honey was harvested. Early honeyhunters and beekeepers learned that smoke seemed to pacify bees, allowing for collection of honey with less risk of stinging. Much of beekeeping is based in the management of bee behavior. Beekeeping underwent a major advancement with the invention of moveable frames; these wooden (or now, plastic) supports hold the comb and allow for removal of individual combs from a hive. Also important in artificial hive construction is the concept of ‘bee space’; if the right-sized gaps – about 1.0 cm – are left between frames, and between the frames and the hive box, the bees use the spaces as passages, rather than filling them with wax and propolis. Keeping bee space means that frames are not cemented into place, facilitating their easy removal. The American beekeeper, Lorenzo Langstroth,
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Xylocopa Anthophora Centris Eulaema Eufriesea Euglossa Bombus Genus A Genus B Genus C Genus D Apis Genus E Genus F Genus G Genus H Genus I Kelneriapis Melipona Liotrigona Figure 2 A cladogram of the bee subfamily Apinae places the genus Apis on a branch with other eusocial bees, Bombus (the bumblebees) and the stingless bees (Melipona /Liotrigona). Genera labeled in green are extinct. Bombus, labeled in yellow, is primitively eusocial, with relatively little morphological differentiation between queens and workers. The genera labeled in red, including Apis and the stingless bees, are highly eusocial, with strong morphological differentiation between queens and workers. Reproduced with permission from Engel M S (2001) Monophyly and extensive extinction of advanced eusocial bees: Insights from an unexpected Eocene diversity. Proceedings of the National Academy of Sciences USA 1661–1664. Copyright 2001 National Academy of Sciences, USA.
is generally credited with developing the concept of bee space and linking it with moveable frames in the 1850s, resulting in the basis for modern beekeeping. The perfection of techniques for artificial insemination of honeybee queens, particularly by Harry Laidlaw, has allowed beekeepers and scientists to make controlled crosses among honeybees to enhance honeybee agricultural performance and for experimental purposes.
Diseases and Parasites of Honeybees Honeybees have attracted their share of diseases and parasites. Because of the commercial value of honeybees,
more is probably known about honeybee diseases than diseases afflicting any other insect. Viruses, such as bee paralysis viruses (BPV), bacteria, including the sporeforming American foulbrood, Paenibacillus larvae, protists such as Nosema apis, and the chalkbrood fungus, Pericystis apis, can all impair or kill workers (larvae in the cases of foulbrood and chalkbrood, adults for BPVs and Nosema). Mites, such as the tracheal mite, Acarapis woodi, and the Varroa mite, Varroa destructor, are also significant threats to honeybees. For most of these diseases and parasites, it is not clear in which species of Apis they originated, although all are now problems for A. mellifera populations. The Varroa mite evolved as a pest of A. cerana in Southeast Asia and its recent switch to A. mellifera, facilitated by
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Figure 3 An Apis florea colony. This dwarf honeybee nests lower in the vegetation and on slimmer branches than giant honeybees (see Figure 4). The comb, which is obscured by the bees, extends over the branch and a flattened portion of comb above the branch serves as a platform for dances in this species. Photo by Xiaobao Deng.
Figure 4 An Apis dorsata colony. Note that the comb does not extend up and over the tree branch. Apis dorsata often nests in aggregations, with many colonies occupying a large tree. Photo by Michael Breed.
global commerce in honeybees, has been disastrous for A. mellifera populations, whose natural defenses are only weakly developed. Recent public attention has focused on colony collapse disorder (CCD), a disease or complex of diseases that has greatly impacted global A. mellifera populations. Colony losses have exceeded 90% in some locations and loss of pollination services have had major impacts on some growers of fruits and vegetables. A variety of diseases have been suggested as causes of CCD, including paralysis viruses and Nosema ceranae, which has switched hosts from A. cerana to A. mellifera, but other factors, such as use of the neonicotinoid insecticide imadocloprid and global climate change have also been implicated. Resolution of
Figure 5 An Apis cerana colony maintained in a log hive in southern China (Yunnan province). The ends are removable for access to the combs. Photo by Michael Breed.
the cause or causes of CCD is a matter of extreme urgency, given the importance of ecosystem services provided by honeybees. Hygienic behavior is very much a part of honeybee responses to disease and parasites. Bees may respond to diseased or dying larvae and pupae by removing them from their colony. Carl Rothenbuhler’s famous studies in the 1960s of hygienic behavior in response to brood infections stood for many years as classic examples in behavioral genetics of how simple Mendelian models could explain behavioral variation. While we now understand that the genetics underlying hygienic behavior are more complex than what Rothenbuhler proposed, his basic finding of genetic variation for hygienic behavior should be recognized as a key stimulus for the development of the field of behavioral genetics. Genetic lines of A. mellifera selected for hygienic behavior have good levels of resistance to Varroa mites because infested larvae are removed from the colony before the mites reproduce. Bees may also groom themselves or their nestmates (allogrooming) to remove ectoparasites; this behavior is not genetically related to classic hygienic behavior but may enhance resistance to Varroa mites, as well.
The Honeybee Life Cycle Honeybees have no solitary phase in their life cycle. This differentiates them many, perhaps most, other eusocial insects. Queens depend completely on workers for their survival, and workers are nearly completely dependent on queens for reproduction. (Workers may occasionally lay a male egg.) New colonies are started by swarms, which consist of the reigning queen from a colony and a large number of her workers. Swarms settle usually on a tree
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limb or fence, but sometimes at inconvenient spots like a parked car, and scouts from the swarm search for appropriate nest sites. Returning scouts dance to indicate possible nest locations and within a few hours or days, the colony arrives at a consensus and moves to the new site, where they initiated comb construction and the queen, once comb is available, starts to lay. In temperate habitats, spring is the most promising time to swarm, as the colony will then have ample time to provision its new nest for the upcoming winter. Hence the Mother Goose rhyme: A swarm of bees in May Is worth a load of hay; A swarm of bees in June Is worth a silver spoon; A swarm of bees in July Is not worth a fly.
In the days prior to swarming, colonies rear several new queens in larger than typical cells that extend from the bottom edges of the comb. Queen larvae receive a diet of royal jelly that apparently stimulates development of the queen morphology but all female eggs have the potential to develop into either queens or workers. While typically only one new queen is needed, the extra queens provide a degree of insurance. The first queen emerging from her cocoon may kill the other queens; sometimes, large colonies produce secondary swarms headed by new queens. Colonies also produce drones, beginning in the spring and extending well into the summer. Drones fly in aggregations several meters in the air, and queens on mating flights seek those aggregations, with drones then engaging in a chase to actually mate with the queen. Drone genitalia are ripped out and left in the queen’s reproductive tract when a drone mates, providing an ineffective block against subsequent matings by the queen.
The Comb and Behavior One of the most unique and intriguing aspects of honeybee biology is the use of wax for the construction of the nest (Figure 6). The mechanical and architectural properties of the comb are the result of an enchanting interplay between an outstanding construction material and perfect design. Honeybees produce wax from glands located in the intersegmental membranes on the sternal surface of the abdomen. Wax scales from the glands are chewed, secretions from glands in the head are added, and then wax is formed into comb. Wax is a metabolically costly product; 6–7 kg of honey are required to make 1 kg of wax. Wax consists of hundreds of compounds. Alkanes, like those found in petroleum-based waxes, are but a small component of beeswax. Wax esters, and, notably, fatty acids, which add strength and resilience, are
Figure 6 Apis mellifera comb, showing the beautiful symmetry and efficient use of materials by honeybees in comb construction. Photo by Michael Breed.
important parts of the blend. Even though beeswax has superficial similarities to paraffin wax, its unique properties have made it a preferred material for cosmetics, applications in art such as batik, and high-quality candles. Behaviorally, the fatty acids and alkenes (which are present in smaller amounts) serve as important cues for bees in the colony in social recognition. Under natural conditions the bees shape the comb. In managed colonies apiarists often give the bees a foundation, made of wax or plastic, that guides comb construction within moveable frames. The hexagonal cells (Figure 6) are a marvelous extraction of maximum strength and storage space from a minimum of material. The bees appear to be guided in their construction by innate knowledge and the ability to build new comb following the pattern of existing comb. The comb is a result of the collective behavior of many individual bees, each adding a few wax scales secreted from their wax glands. It may appear that complex guiding forces drive comb-building. Hexagonal construction is, however, not unique to honeybees; it appears in the paper nests of many eusocial wasps and in some parts of stingless bee nests, and may be a simple result of close packing of developing larvae. As the comb is used for rearing larvae, the silk larval cocoons are incorporated, and the old comb has a much darker color than the new comb. Details of construction, though, are remarkably consistent across species. The size of most of the cells in the comb matches the size of worker larvae; dwarf species produce the comb with small cells and giant bees have very large cells. Cells intended for rearing drones are slightly larger than worker cells, and tend to be located around the margins of the comb. As a unifying feature of the genus Apis, the use of the wax comb for nests is, indeed, a marvel of nature.
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Division of Labor All honeybee workers are alike, morphologically, and it seems that all are equally capable of contributing to tasks within the colony. Age is the most important variable in determining the behavior of a bee at any given moment, with the youngest adult workers performing tasks deep inside the colony, such as cleaning and nursing brood. Slightly older bees engage in comb construction. Between 10 and 20 days of adult age workers shift to the periphery of the colony, guarding (Figure 7), fanning to circulate air, and removing dead bees. Yet older bees forage or stand ready to fly in colony defense, serving as soldiers. In the summer, workers live roughly 4 weeks. This pattern of agerelated shifts in activity is termed as temporal polyethism. Physiologically, the picture is more complex, as workers vary in the likelihood that they will become nectar or pollen foragers. Genetic differences among workers, at least in part, underly fates of bees in becoming nectar or pollen foragers. The interactions between age, demand for task performance, and genetics in determining worker activities within colonies remain a fascinating topic for future study. The role of queens is simpler and much more easily defined. After emergence as adults, queens may enter a short phase of competition with other potential queens, which can include fights to the death. Queens then leave the colony for one or more mating flights, after which they return. Having mated 10–20 times (at least in A. mellifera), the queen soon begins laying eggs, her only task until she dies; queens may live 5–7 years. Egg-laying by the queen is interrupted only by unfavorable seasons – winter in the temperate zone, dry seasons in the tropics – and times when the colony is absconding (all bees leave the nest and
search for a new location) and swarming (the queen leaves with about half the workers). Male honeybees, drones, do not work within the colony. Their role is to fly and attempt to mate with queens. Late in summer, drones may be forcibly removed from colonies by the workers.
Queen Pheromones Queens release pheromones throughout their lives. 9-Oxodecenoic acid (9-ODA) serves as a sex pheromone in A. mellifera, attracting males to queens on their mating flight, and a related compound, 10-hydroxydecenoic acid (10-HDA) serves a similar function in A. florea. A mixture of compounds from the mandibular glands of queens (queen mandibular pheromone, or QMP) appears to inhibit production of new queens and to maintain some aspects of worker-like behavior. In A. mellifera, QMP includes 9-ODA, 9-HDA, methyl-p-hydroxybenzoate (HOB), and 4-hydroxy-3-methoxy phenylethanol (HVA). Queens continuously produce QMP; if the queen is removed or QMP production is blocked, workers begin rearing emergency replacement queens. QMP attracts a retinue of workers to surround the queen; QMP is transmitted via retinue workers throughout the colony, but it is volatile and disappears quickly from the colony if the queen is not present.
Other Pheromones Pheromones probably play a role in almost every aspect of honeybee behavior. Brood pheromone, for example, has received attention as a possible stimulant of foraging behavior. Nasonov pheromone, produced from the Nasonov glands on the dorsum of the abdomen, is composed of highly volatile oils, such as geraniol and citral, and serves as an assembly pheromone during swarming. Footprint pheromones may mark locations that foragers have visited. Alarm pheromones are discussed below. The rich chemical life of honeybees is only partly understood.
Colony Defense
Figure 7 A guard honeybee, Apis mellifera. Photo by Michael Breed.
Honeybee colony defense can be loosely divided into three categories of responses – defense against other bee colonies, defense against invertebrate predators and honey thieves, and defense against vertebrates. The primary weapon of the honeybee is the sting, which is supplemented by biting with the mandibles. The sting is autotomous, meaning the tissue attaching the sting to the bee’s body is weak and the sting pulls out of the bee easily. Barbs on the shaft of the sting catch in the skin of
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the victim, the sting pulls loose, and muscles remain with the sting pump venom into the skin. The queen has a sting, but it is not barbed. Alarm pheromones, highly volatile chemicals released from a gland associated with the sting, serve to alert other bees in the colony to threats. Honeybee nests have tempting concentrations of honey, and when nectar is low in availability, workers may turn to robbing other colonies. Robbing and defenses against robbing are best studied in A. mellifera, which, as pointed out above, tends to store large amounts of honey. The mixture of fatty acids in the comb of any given colony is unique to that colony, and gives the workers the means to discriminate colony mates from noncolony mates. Guard bees, which patrol near hive entrances, examine approaching bees with their antennae and bite and sting bees from other colonies. Guarding is more intense when nectar supplies are low. Less is known about this type of colony defense in other species of honeybee. Invertebrate predators on honeybee colonies have generated a set of interesting adaptations. In Asia and the Middle East, hornets feed on adult bees and can decimate colonies. Bees forming the blanket on the surface of A. florea and A. dorsata nests (Figures 3 and 4) ‘shimmer’ – move their wings to produce a wave-like effect radiating through the bees – in response to the presence of a hornet. A. cerana workers shimmer at the entrance of their nest. If the bees capture a hornet, large numbers may surround it; the bees then produce heat by shivering and can actually bake a hornet to death. For most people, the pain caused by the defensive abilities of honeybees against vertebrates determines their most immediate impression of bees. The sting of a single worker can cause local pain, itching, and, in hypersensitive individuals a catastrophic anaphylactic reaction. Honeybee venom consists of two nonenzyme proteins, apamin and melittin, an enzyme, hyalonuridase, and the biogenic amines, dopamine and histamine. Apamin is a neurotoxin which may associate with the pain that accompanies a bee sting. Melittin lyses cell walls, probably enhancing local inflammation. Hyalonuridase breaks down connective tissues, perhaps enhancing the spread of the venom, and dopamine and histamine probably increase circulation in the area of the sting, also improving venom spread. Apamin and melittin are hyperallergens, so vertebrates with repeated exposure may be at risk for developing strong immune reactions to bee venom. Major disturbances of a honeybee nest, by a human or other vertebrate, result in hundreds or thousands of bees flying near the nest. These bees orient to dark colors and movement, and tend to concentrate around the eyes and ankles of the victim. Alarm pheromone released from stings stimulates even more bees to fly. Defensive behavior against vertebrates is, again, best studied in A. mellifera, but the giant honeybees also have a
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reputation of being aggressive defenders of their nest and fierce stingers. Some ecotypes of A. mellifera, sometimes called ‘African’ or ‘Africanized’ bees, have particularly intense colony defense, with their defended area extending many meters from the nest and large numbers of bees responding to threats. Following the release of these more strongly defensive bees into Brazil, thousands of people have died in stinging events. ‘African’ bees are more successful in tropical climates than ‘European’ bees and have spread to their southern climatic limits in Argentina and near their northern limits in California, Arizona, and Texas. In addition to their defensiveness, ‘African’ bees are noted for their high likelihood of absconding under poor living conditions, production of large numbers of swarms, and long-distance movement of swarms. Beekeepers in North America attempt to genetically manage their bees to reduce the defensive characteristics of their colonies, while beekeepers in Central and South America have, over time, adapted to working with these more difficult bees.
Foraging Behavior Honeybees are usually thought of as floral generalists, exploiting a wide range of flowers for their nectar and pollen. Honeybees sometimes collect food from wind pollinated plants, like pollen cattails, or from extrafloral nectaries. Honeybees collecting sugary fluid from soda cans or from unscreened kitchens may be viewed as pests. Within this overall pattern of generalist foraging, though, individual worker bees can remain quite faithful to a given plant species. Here I highlight a few interesting points about the large topic of communication about food resources. A small subset of foragers work as scouts for a colony. The mechanism for determining which bees scout and how many bees scout is poorly understood. These bees, when they find nectar or pollen, dance upon return to the nest, and recruit other bees to the same food source. As noted above, some foragers specialize in pollen collection, others in nectar, and some collect both types of food. Another class of foragers collects water, which on hot days is brought into the colony and evaporated for cooling; without evaporative cooling extreme temperatures would quickly melt the comb wax. In times of severe forage shortage in the surrounding landscape, honeybee colonies send out few scouts; low activity may conserve food reserves. Honeybee foragers can range up to several kilometers from their nest, but most of the foraging activity from a given colony is concentrated within a few hundred meters of the nest. Honeybees are not territorial on flowers, so bees from many colonies can forage in the same area without direct aggression occurring at flowers.
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This contrasts with some stingless bees, which are highly territorial at flowers. Honeybees are efficient pollinators; the fidelity of a given bee to a plant species results in effective crosspollination. Flowers with open corollas and accessible nectaries, such as apples, are easily worked by honeybees, while honeybees have difficulty with deep, narrow corollas, such as honeysuckle, or complicated flowers, like alfalfa. The manipulability of honeybee behavior and their broad range of acceptable flowers makes them the prime agricultural pollinator in many ecosystems.
are required to evolutionarily move from the solitary ancestors of Apis to the sophisticated social behavior of this genus. See also: Ant, Bee and Wasp Social Evolution; Caste Determination in Arthropods; Collective Intelligence; Dance Language; Developmental Plasticity; Division of Labor; Queen–Queen Conflict in Eusocial Insect Colonies; Queen–Worker Conflicts Over Colony Sex Ratio; Social Recognition.
Further Reading Genomics and the Future of Honeybee Research The honeybee genome has been sequenced, with the first release of sequence data in 2003. The availability of genomic data opens important future pathways for learning how gene expression relates to eusocial behavior and caste differentiation. The basic groundplan for reproductive biology in insects, and in Hymenoptera in particular, has been modified in bees to support the existence of distinct reproductive and nonreproductive castes; genomic research may ultimately help to explain how animals with the same genes – queens and workers – can have such different morphology and behavior, and what genetic modifications
Buchwald R, Greenberg AR, and Breed MD (2005) A biomechanical perspective on beeswax. American Entomologist 51: 39–41. Engel MS (2001) Monophyly and extensive extinction of advanced eusocial bees: Insights from an unexpected Eocene diversity. Proceedings of the National Academy of Sciences USA 98: 1661–1664. Hepburn HR (1986) Honeybees and Wax, p. 205. Berlin: SpringerVerlag. Hepburn HR and Radloff SE (1998) Honeybees of Africa, p. 377. Berlin: Springer. Oldroyd BP and Wongsiri S (2006) Asian Honey Bees: Biology, Conservation, and Human Interactions, p. 360. Cambridge: Harvard University Press. Seeley TD (1996) The Wisdom of the Hive: The Social Physiology of Honey Bee Colonies, p. 318. Cambridge: Harvard University Press. Winston ML (1991) The Biology of the Honey Bee, p. 294. Cambridge: Harvard University Press.
Background The honeybees, all members of the genus Apis, are one of the most familiar flying animals of terrestrial habitats. The center of diversity of the genus is Southeast Asia, where several species are found. Most of these species are limited in range to tropical and montane zones in Southeast and South Asia, but two species have far broader ranges. Apis cerana, sometimes called the Eastern hive bee, occurs as far north as Japan and into the Middle East. Apis mellifera, or the Western hive bee, is native to Africa. It expanded its range into Europe and Asia as the ice-age glaciers retreated, and has been spread by humans to the Americas, Australia, and Hawaii (Figure 1). A. mellifera has also been introduced through much of the range occupied by A. cerana, including Japan and mainland China. In this article, I review the basic biology of the genus Apis, with a focus behavior. Human associations with honeybees are deeply rooted in prehistory. Honey hunting was likely an important source of food for early humans living in Asia, Africa, and Europe. Cave paintings in Spain record prehistoric honey hunting by humans, and honey remains an important human food source. An image of the honeybee forms a key element in the ancient Egyptian hieroglyph symbolizing Lower Egypt. Roman ruins sometimes feature niches in walls that were designed to hold honeybee colonies, and numerous such walls constructed in the seventeenth and eighteenth centuries are found in the French and British countryside. Currently, honeybees are highly important pollinators, providing pollination services in manipulated agroecosystems in which native bee populations are reduced and for nonnative crop plants. Most of our scientific knowledge of honeybees comes from studies of A. mellifera. Scientists’ fascination with the honeybee dates back at least to Aristotle, and the maintenance of bee colonies by medieval religious communities fostered knowledge of bee management and behavior. Early publications, such as Charles Bulter’s Feminine Monarchie (1609) held a great amount of detail about honeybee biology, some correct and some incorrect, and form the foundation for modern knowledge of honeybees. The discovery by Jan Dzierzon in 1845 that male honeybees arise from unfertilized (haploid) eggs and females from fertilized (diploid) eggs is an excellent example of how the tradition of beekeeping by educated clergymen led to intellectual explorations of bee biology and behavior. Haplodiploidy, the system of sex determination discovered by Dzierzon and known as Dzierzon’s
rule, is now understood to be a characteristic of nearly all Hymenoptera. Twentieth century studies of honeybees are rooted in the work of Karl von Frisch (1886–1982), who shared the 1973 Nobel Prize in Physiology or Medicine with Niko Tinbergen and Konrad Lorenz. Von Frisch’s discoveries of color vision in bees, the dance language of the honeybee, and the ability of bees to use the polarization of light in their orientation were key to the development of sensory physiology and animal behavior as scientific fields. Generations of scientists have followed in von Frisch’s footsteps, refining and further developing concepts first proposed by von Frisch and his students.
The Apis Family Tree Honeybees lie in the subfamily Apinae of the family Apidae (Figure 2) although it should be noted that there has been considerable controversy over the phylogeny of these bees. Their branch of the apine family tree includes other eusocial taxa, the bumblebees and the stingless bees. In addition to eusociality, honeybees share the use of wax in nest construction with bumblebees and stingless bees, although honeybees are the only taxa to use wax as the sole construction element of their combs. Two major sets of differences align with the evolution of species in Apis – size and nesting habit. The genus divides among dwarf bees, giant bees, and bees that we would regard as more ‘normal’ in size, like A. mellifera. The overall appearance of all Apis species is quite similar, but size varies manyfold between the dwarf species, like A. florea, and giant species like A. dorsata. The dwarf honeybees, subgenus Micrapis, which includes A. florea (Figure 3) and A. andreniformis, are generally considered the basal, or most primitive, group within Apis. The giant honeybees are first derived from the dwarf honeybees and then the cavity-nesting honeybees are derived. The giant honeybees, subgenus Macrapis, include A. dorsata (Figure 4) and A. laboriosa. Micrapis and Macrapis species build nests of a single exposed comb suspended from a branch, cave roof or cliff. Bees in the subgenus Apis–Apis mellifera, A. cerana, A. nigrocincta, A. nuluensis, and A. koschevnikovi – all nest in cavities, such as hollow trees, and build nests of multiple combs. What features are held in common among all species in the genus? While the level of documentation varies among species, from the very well-known A. mellifera to the almost entirely unknown A. nuluensis, some generalizations about
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Figure 1 Western honeybee, Apis mellifera, colony in a small cave. The use of multiple combs is typical of cavity nesting honeybees, subgenus Apis. Photo by Thomas Ranker.
the genus are widely accepted. All Apis species are highly eusocial, meaning that queens and their daughter workers live together in colonies, there is a strong morphological differentiation between queens and workers, and the workers cooperate to rear additional workers, males (drones), and new queens from among their sibs. All members of the genus build nests of wax combs, have workers with barbed, autotomous stings, and have queens that, after multiple matings, store sperm for use throughout their life. Workers in all honeybee species communicate about food resources using a dance language and release alarm pheromones to alert nestmates to threats. Honeybees reproduce by swarming, with the queen in a colony leaving the nest with about half the workers and establishing a new nest; she is replaced in the old nest by one of her daughter queens. As with other eusocial Hymenoptera (ants, some wasps, as well as some other types of bee), all honeybee workers are female. Apis workers are highly differentiated from queens, with larger eyes, hairier bodies, small ovaries, no capacity to mate, and autotomous stings. Drones have yet stouter bodies and even larger eyes, probably adaptations for both flight and spotting potential mates.
Honeybees, Agriculture, and Ecosystems Services A. mellifera is the champion honey producer in the genus. While all Apis species store some concentrated nectar (honey) in their combs, most honeybee species abscond
from nests if conditions are poor and seek out a more favorable nesting site, or are seasonally migratory, moving to accommodate variation in rain and temperature. A. mellifera is the only species which is successful across a vast expanse of the northern temperate zone (in Europe and Asia, and introduced into temperate North America). Escaping temperate winters is beyond the migratory ability of honeybees and it is likely that storage of large amounts (50 kg or more) of honey evolved as a way of having food stores for overwintering. Temperatures inside A. mellifera nests (and to the extent A. cerana lives in temperate climates, in cerana nests) are maintained near 30 C through the unfavorable season. Storing food creates an attractive resource for animals like skunks, raccoons, bears, and, obviously, humans. Additionally, the larvae and pupae, which are reared in cells in the comb, have high nutritional value. It is no surprise that honeybees have intense defensive methods available to them, and these defenses are highly effective against vertebrate predators. In many human cultures, bee larvae or pupae are consumed in addition to honey. Beeswax is regarded as a high-grade base for cosmetics and candles. Propolis (plant resins collected by bees to seal cracks and supplement wax as a structural material) was used as a base for varnishes prior to the development of petroleum-based wood finishes. Propolis was reputedly a key ingredient in finishes used on fine violins, such as those made by Stradivarius. Recently, hive products such as pollen, royal jelly, and propolis have been touted for their medicinal properties. Globally, most agriculturally managed honeybees are A. mellifera, but A. cerana colonies are maintained in parts of Asia. The techniques used to keep these two species are similar. Until the nineteenth century, bees were typically maintained in sections of hollow logs (Figure 5) or in woven straw hives, called ‘skeps.’ The skep is a state symbol for Utah, appearing on highway signs and at the center of the state seal. These arrangements had the disadvantage of not allowing inspection and management of the combs, and required at least partial destruction of the colony when honey was harvested. Early honeyhunters and beekeepers learned that smoke seemed to pacify bees, allowing for collection of honey with less risk of stinging. Much of beekeeping is based in the management of bee behavior. Beekeeping underwent a major advancement with the invention of moveable frames; these wooden (or now, plastic) supports hold the comb and allow for removal of individual combs from a hive. Also important in artificial hive construction is the concept of ‘bee space’; if the right-sized gaps – about 1.0 cm – are left between frames, and between the frames and the hive box, the bees use the spaces as passages, rather than filling them with wax and propolis. Keeping bee space means that frames are not cemented into place, facilitating their easy removal. The American beekeeper, Lorenzo Langstroth,
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Xylocopa Anthophora Centris Eulaema Eufriesea Euglossa Bombus Genus A Genus B Genus C Genus D Apis Genus E Genus F Genus G Genus H Genus I Kelneriapis Melipona Liotrigona Figure 2 A cladogram of the bee subfamily Apinae places the genus Apis on a branch with other eusocial bees, Bombus (the bumblebees) and the stingless bees (Melipona /Liotrigona). Genera labeled in green are extinct. Bombus, labeled in yellow, is primitively eusocial, with relatively little morphological differentiation between queens and workers. The genera labeled in red, including Apis and the stingless bees, are highly eusocial, with strong morphological differentiation between queens and workers. Reproduced with permission from Engel M S (2001) Monophyly and extensive extinction of advanced eusocial bees: Insights from an unexpected Eocene diversity. Proceedings of the National Academy of Sciences USA 1661–1664. Copyright 2001 National Academy of Sciences, USA.
is generally credited with developing the concept of bee space and linking it with moveable frames in the 1850s, resulting in the basis for modern beekeeping. The perfection of techniques for artificial insemination of honeybee queens, particularly by Harry Laidlaw, has allowed beekeepers and scientists to make controlled crosses among honeybees to enhance honeybee agricultural performance and for experimental purposes.
Diseases and Parasites of Honeybees Honeybees have attracted their share of diseases and parasites. Because of the commercial value of honeybees,
more is probably known about honeybee diseases than diseases afflicting any other insect. Viruses, such as bee paralysis viruses (BPV), bacteria, including the sporeforming American foulbrood, Paenibacillus larvae, protists such as Nosema apis, and the chalkbrood fungus, Pericystis apis, can all impair or kill workers (larvae in the cases of foulbrood and chalkbrood, adults for BPVs and Nosema). Mites, such as the tracheal mite, Acarapis woodi, and the Varroa mite, Varroa destructor, are also significant threats to honeybees. For most of these diseases and parasites, it is not clear in which species of Apis they originated, although all are now problems for A. mellifera populations. The Varroa mite evolved as a pest of A. cerana in Southeast Asia and its recent switch to A. mellifera, facilitated by
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Figure 3 An Apis florea colony. This dwarf honeybee nests lower in the vegetation and on slimmer branches than giant honeybees (see Figure 4). The comb, which is obscured by the bees, extends over the branch and a flattened portion of comb above the branch serves as a platform for dances in this species. Photo by Xiaobao Deng.
Figure 4 An Apis dorsata colony. Note that the comb does not extend up and over the tree branch. Apis dorsata often nests in aggregations, with many colonies occupying a large tree. Photo by Michael Breed.
global commerce in honeybees, has been disastrous for A. mellifera populations, whose natural defenses are only weakly developed. Recent public attention has focused on colony collapse disorder (CCD), a disease or complex of diseases that has greatly impacted global A. mellifera populations. Colony losses have exceeded 90% in some locations and loss of pollination services have had major impacts on some growers of fruits and vegetables. A variety of diseases have been suggested as causes of CCD, including paralysis viruses and Nosema ceranae, which has switched hosts from A. cerana to A. mellifera, but other factors, such as use of the neonicotinoid insecticide imadocloprid and global climate change have also been implicated. Resolution of
Figure 5 An Apis cerana colony maintained in a log hive in southern China (Yunnan province). The ends are removable for access to the combs. Photo by Michael Breed.
the cause or causes of CCD is a matter of extreme urgency, given the importance of ecosystem services provided by honeybees. Hygienic behavior is very much a part of honeybee responses to disease and parasites. Bees may respond to diseased or dying larvae and pupae by removing them from their colony. Carl Rothenbuhler’s famous studies in the 1960s of hygienic behavior in response to brood infections stood for many years as classic examples in behavioral genetics of how simple Mendelian models could explain behavioral variation. While we now understand that the genetics underlying hygienic behavior are more complex than what Rothenbuhler proposed, his basic finding of genetic variation for hygienic behavior should be recognized as a key stimulus for the development of the field of behavioral genetics. Genetic lines of A. mellifera selected for hygienic behavior have good levels of resistance to Varroa mites because infested larvae are removed from the colony before the mites reproduce. Bees may also groom themselves or their nestmates (allogrooming) to remove ectoparasites; this behavior is not genetically related to classic hygienic behavior but may enhance resistance to Varroa mites, as well.
The Honeybee Life Cycle Honeybees have no solitary phase in their life cycle. This differentiates them many, perhaps most, other eusocial insects. Queens depend completely on workers for their survival, and workers are nearly completely dependent on queens for reproduction. (Workers may occasionally lay a male egg.) New colonies are started by swarms, which consist of the reigning queen from a colony and a large number of her workers. Swarms settle usually on a tree
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limb or fence, but sometimes at inconvenient spots like a parked car, and scouts from the swarm search for appropriate nest sites. Returning scouts dance to indicate possible nest locations and within a few hours or days, the colony arrives at a consensus and moves to the new site, where they initiated comb construction and the queen, once comb is available, starts to lay. In temperate habitats, spring is the most promising time to swarm, as the colony will then have ample time to provision its new nest for the upcoming winter. Hence the Mother Goose rhyme: A swarm of bees in May Is worth a load of hay; A swarm of bees in June Is worth a silver spoon; A swarm of bees in July Is not worth a fly.
In the days prior to swarming, colonies rear several new queens in larger than typical cells that extend from the bottom edges of the comb. Queen larvae receive a diet of royal jelly that apparently stimulates development of the queen morphology but all female eggs have the potential to develop into either queens or workers. While typically only one new queen is needed, the extra queens provide a degree of insurance. The first queen emerging from her cocoon may kill the other queens; sometimes, large colonies produce secondary swarms headed by new queens. Colonies also produce drones, beginning in the spring and extending well into the summer. Drones fly in aggregations several meters in the air, and queens on mating flights seek those aggregations, with drones then engaging in a chase to actually mate with the queen. Drone genitalia are ripped out and left in the queen’s reproductive tract when a drone mates, providing an ineffective block against subsequent matings by the queen.
The Comb and Behavior One of the most unique and intriguing aspects of honeybee biology is the use of wax for the construction of the nest (Figure 6). The mechanical and architectural properties of the comb are the result of an enchanting interplay between an outstanding construction material and perfect design. Honeybees produce wax from glands located in the intersegmental membranes on the sternal surface of the abdomen. Wax scales from the glands are chewed, secretions from glands in the head are added, and then wax is formed into comb. Wax is a metabolically costly product; 6–7 kg of honey are required to make 1 kg of wax. Wax consists of hundreds of compounds. Alkanes, like those found in petroleum-based waxes, are but a small component of beeswax. Wax esters, and, notably, fatty acids, which add strength and resilience, are
Figure 6 Apis mellifera comb, showing the beautiful symmetry and efficient use of materials by honeybees in comb construction. Photo by Michael Breed.
important parts of the blend. Even though beeswax has superficial similarities to paraffin wax, its unique properties have made it a preferred material for cosmetics, applications in art such as batik, and high-quality candles. Behaviorally, the fatty acids and alkenes (which are present in smaller amounts) serve as important cues for bees in the colony in social recognition. Under natural conditions the bees shape the comb. In managed colonies apiarists often give the bees a foundation, made of wax or plastic, that guides comb construction within moveable frames. The hexagonal cells (Figure 6) are a marvelous extraction of maximum strength and storage space from a minimum of material. The bees appear to be guided in their construction by innate knowledge and the ability to build new comb following the pattern of existing comb. The comb is a result of the collective behavior of many individual bees, each adding a few wax scales secreted from their wax glands. It may appear that complex guiding forces drive comb-building. Hexagonal construction is, however, not unique to honeybees; it appears in the paper nests of many eusocial wasps and in some parts of stingless bee nests, and may be a simple result of close packing of developing larvae. As the comb is used for rearing larvae, the silk larval cocoons are incorporated, and the old comb has a much darker color than the new comb. Details of construction, though, are remarkably consistent across species. The size of most of the cells in the comb matches the size of worker larvae; dwarf species produce the comb with small cells and giant bees have very large cells. Cells intended for rearing drones are slightly larger than worker cells, and tend to be located around the margins of the comb. As a unifying feature of the genus Apis, the use of the wax comb for nests is, indeed, a marvel of nature.
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Division of Labor All honeybee workers are alike, morphologically, and it seems that all are equally capable of contributing to tasks within the colony. Age is the most important variable in determining the behavior of a bee at any given moment, with the youngest adult workers performing tasks deep inside the colony, such as cleaning and nursing brood. Slightly older bees engage in comb construction. Between 10 and 20 days of adult age workers shift to the periphery of the colony, guarding (Figure 7), fanning to circulate air, and removing dead bees. Yet older bees forage or stand ready to fly in colony defense, serving as soldiers. In the summer, workers live roughly 4 weeks. This pattern of agerelated shifts in activity is termed as temporal polyethism. Physiologically, the picture is more complex, as workers vary in the likelihood that they will become nectar or pollen foragers. Genetic differences among workers, at least in part, underly fates of bees in becoming nectar or pollen foragers. The interactions between age, demand for task performance, and genetics in determining worker activities within colonies remain a fascinating topic for future study. The role of queens is simpler and much more easily defined. After emergence as adults, queens may enter a short phase of competition with other potential queens, which can include fights to the death. Queens then leave the colony for one or more mating flights, after which they return. Having mated 10–20 times (at least in A. mellifera), the queen soon begins laying eggs, her only task until she dies; queens may live 5–7 years. Egg-laying by the queen is interrupted only by unfavorable seasons – winter in the temperate zone, dry seasons in the tropics – and times when the colony is absconding (all bees leave the nest and
search for a new location) and swarming (the queen leaves with about half the workers). Male honeybees, drones, do not work within the colony. Their role is to fly and attempt to mate with queens. Late in summer, drones may be forcibly removed from colonies by the workers.
Queen Pheromones Queens release pheromones throughout their lives. 9-Oxodecenoic acid (9-ODA) serves as a sex pheromone in A. mellifera, attracting males to queens on their mating flight, and a related compound, 10-hydroxydecenoic acid (10-HDA) serves a similar function in A. florea. A mixture of compounds from the mandibular glands of queens (queen mandibular pheromone, or QMP) appears to inhibit production of new queens and to maintain some aspects of worker-like behavior. In A. mellifera, QMP includes 9-ODA, 9-HDA, methyl-p-hydroxybenzoate (HOB), and 4-hydroxy-3-methoxy phenylethanol (HVA). Queens continuously produce QMP; if the queen is removed or QMP production is blocked, workers begin rearing emergency replacement queens. QMP attracts a retinue of workers to surround the queen; QMP is transmitted via retinue workers throughout the colony, but it is volatile and disappears quickly from the colony if the queen is not present.
Other Pheromones Pheromones probably play a role in almost every aspect of honeybee behavior. Brood pheromone, for example, has received attention as a possible stimulant of foraging behavior. Nasonov pheromone, produced from the Nasonov glands on the dorsum of the abdomen, is composed of highly volatile oils, such as geraniol and citral, and serves as an assembly pheromone during swarming. Footprint pheromones may mark locations that foragers have visited. Alarm pheromones are discussed below. The rich chemical life of honeybees is only partly understood.
Colony Defense
Figure 7 A guard honeybee, Apis mellifera. Photo by Michael Breed.
Honeybee colony defense can be loosely divided into three categories of responses – defense against other bee colonies, defense against invertebrate predators and honey thieves, and defense against vertebrates. The primary weapon of the honeybee is the sting, which is supplemented by biting with the mandibles. The sting is autotomous, meaning the tissue attaching the sting to the bee’s body is weak and the sting pulls out of the bee easily. Barbs on the shaft of the sting catch in the skin of
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the victim, the sting pulls loose, and muscles remain with the sting pump venom into the skin. The queen has a sting, but it is not barbed. Alarm pheromones, highly volatile chemicals released from a gland associated with the sting, serve to alert other bees in the colony to threats. Honeybee nests have tempting concentrations of honey, and when nectar is low in availability, workers may turn to robbing other colonies. Robbing and defenses against robbing are best studied in A. mellifera, which, as pointed out above, tends to store large amounts of honey. The mixture of fatty acids in the comb of any given colony is unique to that colony, and gives the workers the means to discriminate colony mates from noncolony mates. Guard bees, which patrol near hive entrances, examine approaching bees with their antennae and bite and sting bees from other colonies. Guarding is more intense when nectar supplies are low. Less is known about this type of colony defense in other species of honeybee. Invertebrate predators on honeybee colonies have generated a set of interesting adaptations. In Asia and the Middle East, hornets feed on adult bees and can decimate colonies. Bees forming the blanket on the surface of A. florea and A. dorsata nests (Figures 3 and 4) ‘shimmer’ – move their wings to produce a wave-like effect radiating through the bees – in response to the presence of a hornet. A. cerana workers shimmer at the entrance of their nest. If the bees capture a hornet, large numbers may surround it; the bees then produce heat by shivering and can actually bake a hornet to death. For most people, the pain caused by the defensive abilities of honeybees against vertebrates determines their most immediate impression of bees. The sting of a single worker can cause local pain, itching, and, in hypersensitive individuals a catastrophic anaphylactic reaction. Honeybee venom consists of two nonenzyme proteins, apamin and melittin, an enzyme, hyalonuridase, and the biogenic amines, dopamine and histamine. Apamin is a neurotoxin which may associate with the pain that accompanies a bee sting. Melittin lyses cell walls, probably enhancing local inflammation. Hyalonuridase breaks down connective tissues, perhaps enhancing the spread of the venom, and dopamine and histamine probably increase circulation in the area of the sting, also improving venom spread. Apamin and melittin are hyperallergens, so vertebrates with repeated exposure may be at risk for developing strong immune reactions to bee venom. Major disturbances of a honeybee nest, by a human or other vertebrate, result in hundreds or thousands of bees flying near the nest. These bees orient to dark colors and movement, and tend to concentrate around the eyes and ankles of the victim. Alarm pheromone released from stings stimulates even more bees to fly. Defensive behavior against vertebrates is, again, best studied in A. mellifera, but the giant honeybees also have a
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reputation of being aggressive defenders of their nest and fierce stingers. Some ecotypes of A. mellifera, sometimes called ‘African’ or ‘Africanized’ bees, have particularly intense colony defense, with their defended area extending many meters from the nest and large numbers of bees responding to threats. Following the release of these more strongly defensive bees into Brazil, thousands of people have died in stinging events. ‘African’ bees are more successful in tropical climates than ‘European’ bees and have spread to their southern climatic limits in Argentina and near their northern limits in California, Arizona, and Texas. In addition to their defensiveness, ‘African’ bees are noted for their high likelihood of absconding under poor living conditions, production of large numbers of swarms, and long-distance movement of swarms. Beekeepers in North America attempt to genetically manage their bees to reduce the defensive characteristics of their colonies, while beekeepers in Central and South America have, over time, adapted to working with these more difficult bees.
Foraging Behavior Honeybees are usually thought of as floral generalists, exploiting a wide range of flowers for their nectar and pollen. Honeybees sometimes collect food from wind pollinated plants, like pollen cattails, or from extrafloral nectaries. Honeybees collecting sugary fluid from soda cans or from unscreened kitchens may be viewed as pests. Within this overall pattern of generalist foraging, though, individual worker bees can remain quite faithful to a given plant species. Here I highlight a few interesting points about the large topic of communication about food resources. A small subset of foragers work as scouts for a colony. The mechanism for determining which bees scout and how many bees scout is poorly understood. These bees, when they find nectar or pollen, dance upon return to the nest, and recruit other bees to the same food source. As noted above, some foragers specialize in pollen collection, others in nectar, and some collect both types of food. Another class of foragers collects water, which on hot days is brought into the colony and evaporated for cooling; without evaporative cooling extreme temperatures would quickly melt the comb wax. In times of severe forage shortage in the surrounding landscape, honeybee colonies send out few scouts; low activity may conserve food reserves. Honeybee foragers can range up to several kilometers from their nest, but most of the foraging activity from a given colony is concentrated within a few hundred meters of the nest. Honeybees are not territorial on flowers, so bees from many colonies can forage in the same area without direct aggression occurring at flowers.
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This contrasts with some stingless bees, which are highly territorial at flowers. Honeybees are efficient pollinators; the fidelity of a given bee to a plant species results in effective crosspollination. Flowers with open corollas and accessible nectaries, such as apples, are easily worked by honeybees, while honeybees have difficulty with deep, narrow corollas, such as honeysuckle, or complicated flowers, like alfalfa. The manipulability of honeybee behavior and their broad range of acceptable flowers makes them the prime agricultural pollinator in many ecosystems.
are required to evolutionarily move from the solitary ancestors of Apis to the sophisticated social behavior of this genus. See also: Ant, Bee and Wasp Social Evolution; Caste Determination in Arthropods; Collective Intelligence; Dance Language; Developmental Plasticity; Division of Labor; Queen–Queen Conflict in Eusocial Insect Colonies; Queen–Worker Conflicts Over Colony Sex Ratio; Social Recognition.
Further Reading Genomics and the Future of Honeybee Research The honeybee genome has been sequenced, with the first release of sequence data in 2003. The availability of genomic data opens important future pathways for learning how gene expression relates to eusocial behavior and caste differentiation. The basic groundplan for reproductive biology in insects, and in Hymenoptera in particular, has been modified in bees to support the existence of distinct reproductive and nonreproductive castes; genomic research may ultimately help to explain how animals with the same genes – queens and workers – can have such different morphology and behavior, and what genetic modifications
Buchwald R, Greenberg AR, and Breed MD (2005) A biomechanical perspective on beeswax. American Entomologist 51: 39–41. Engel MS (2001) Monophyly and extensive extinction of advanced eusocial bees: Insights from an unexpected Eocene diversity. Proceedings of the National Academy of Sciences USA 98: 1661–1664. Hepburn HR (1986) Honeybees and Wax, p. 205. Berlin: SpringerVerlag. Hepburn HR and Radloff SE (1998) Honeybees of Africa, p. 377. Berlin: Springer. Oldroyd BP and Wongsiri S (2006) Asian Honey Bees: Biology, Conservation, and Human Interactions, p. 360. Cambridge: Harvard University Press. Seeley TD (1996) The Wisdom of the Hive: The Social Physiology of Honey Bee Colonies, p. 318. Cambridge: Harvard University Press. Winston ML (1991) The Biology of the Honey Bee, p. 294. Cambridge: Harvard University Press.