Pollination Ecology: Plant and Bee Interactions

By Paula Westmoreland

Statement of the Problem

Pollination ecology is the study of the ecological and evolutionary relationships involved in the pollination process. Pollination is one of the most vital processes linking plants and animals and is the basis for much of the biological diversity we see today. The dependable movement of pollen from one plant to others of its own species is a precondition for seed set and the development of fruit in most plants.

The earliest plant life was limited in its diversity due to reliance on abiotic or wind pollination. For wind-dispersed pollen to result in seed set, plants must be in close proximity to others of their own kind. In the early Cretaceous period, roughly 144 million years ago, an explosion in diversity occurred among angiosperms as species increased from an estimated 3000 to over 250,000 species of flowering plants. While many factors contributed to this explosion, pollination biologists now believe the most important factor may have been pollination by insects which allowed outcrossing of highly dispersed populations with relatively few individuals (Crepet, 1983, 30). The diversity in pollinator species also increased as pollinators adapted and coevolved with the expanding variety of plant life. In today’s diverse tropical rainforests less than 3 percent of all plant species rely on the wind for pollination. Vertebrates pollinate 5% of the canopy and 20-25% of the subcanopy. Bees and other insects pollinate 95% of the canopy and 75% of the subcanopy (Buchmann, 1996, 43).

It is widely accepted that a massive loss of biodiversity is occurring worldwide. It is less well known that a pollination crisis is occurring right in our own backyard. Native pollinators, including many stingless bee species, have declined in the Americas since the introduction of the European honeybee in the 1600s. The European honeybee is now facing threats to its own survival due to the arrival of Africanized honeybees and the spread of parasitic mites and diseases. Since 1990 beekeepers in the United States have lost 20% of all domestic managed bee colonies and if current rates continue over 50% of colonies may be lost in the northern United States and 100% in the southern United States. If native pollinators are not found to replace the European honeybees annual economic losses could top $5.7 billion (Buchmann, 1996, 192).

Habitat loss, the introduction of exotic species, expansion in the use of pesticides and herbicides, and the introduction of genetically-modified organisms (GMOs) into agricultural environments pose the greatest threats to the survival of a diverse pollinator population. Chemical and physical destruction of habitat has created fragmented landscapes that mirror isolated island environments. According to botanists Sudodh Jain and J.M. Oelsen, habitat fragmentation is as much a "life and death issue" for cross-pollinating plants as pesticide accumulation is for insectivorous birds (Buchmann, 1996, 25). Plants in many fragmented habitats are beginning to show the effects of pollinator limitation on seed set. Recent studies in Iowa’s tallgrass prairies and Argentina’s "Chaco Serrano" scrublands show evidence of natural pollinator limitation. In Argentina, 62% of 258 plant species studied suffered from lack of pollinator visits. In Iowa, the smallest and most isolated fragments of the remaining prairie have been abandoned since they are too small to sustain pollinator populations (Buchmann, 1996, 24). David Tillman at the University of Minnesota has developed computer models to simulate the effect of habitat fragmentation on species extinction. In the latest simulations, a 30% reduction in tropical rain forest triggered the extinction of 35% of species in the area within 400 years. A 30% reduction in temperate forest eliminated 5% of species within 40-60 years. These models appear to accurately reflect observations in the field (Tilman, 1994, 66).

The introduction of exotic species, such as the Africanized honeybees, has accelerated the decline of endemic or native bees. Africanized honeybees now inhabit 20 million square kilometers from northern Argentina to the southern United States. David Roubik has studied the impact of introduced bees on native bees for over twenty years. Africanized honeybees are a disturbance-loving species. They are preadapted to fragmented habitats due to their large foraging units, large flight range and broad floral diet (Roubik, 1996, 169). Roubik’s research has led him to suggest that competition from Africanized bees could cause the local extinction of Melipona and Trigona stingless bees within 10 years after moving into an area (Roubik, 1996, 179).

The application of herbicides and pesticides is growing rapidly in countries harboring the richest biological diversity. Pesticide sales to Ecuadorian farmers have more than doubled since 1980. Of the pesticides imported in 1990, over 20% of the chemicals have been shown to cause reproductive abnormalities in humans and other animals (Buchmann, 1996, 140). In 1993 over 165 million tons of pesticides were applied in Mexico. This increased another 50% in the first six months after the North American Free Trade Agreement (NAFTA) went into effect. In Brazil, pesticide use has more than tripled since 1980 to over $2 billion in 1990 (Buchmann, 1996, 141).

In the United States rapid changes have occurred in industrial agriculture that may pose significant threats to pollinators. The biotechnology revolution has led to the widespread planting of genetically-modified crops during the last five years. In 1997 over 25% of the U.S. corn crop was genetically-modified, a large percentage modified to eliminate insect pests using a Bt-resistant gene. A 1998 Cornell University study documented that pollen from Bt-resistant corn that landed on milkweeds killed 56% of monarch butterflies that visited the effected milkweeds (Losey, 1999, 214). Entymologists are concerned that a gene introduced into canola to increase herbicide tolerance is impacting learning and orientation abilities of bees (Spivak, 1999). Other impacts of GMOs on pollinator populations are not yet known.

We, as humans, have a stake in the continued survival of a diverse plant and pollinator population. The survival of pollinators is crucial to the continued survival of diverse plant populations and maintenance of agricultural productivity. 80% of the species of food plants worldwide depend on pollination by animals, most of which are insects. In addition, one in every three mouthfuls of food we eat and beverages we drink are visited by pollinators (Buchmann, 1996, xiv). As humans we are not dependent on pollinators for the majority of our caloric intake (most cereals and grains are wind-pollinated) but we do rely on them for nutrition and variety in our diet (most fruits, vegetables and berries are insect-pollinated).

This series of papers will look at the nature and diversity of interactions between plants and pollinators, field research on rare plants, and the pollination crisis in agriculture.

The Pollination Process

Pollination Ecology

Peter Kevan, a Canadian ecologist, recently pointed out "the information available on pollinators’ interactions with plants is often the weakest link in our chain of understanding of how ecosystems function" (Buchmann, 1996, 133). Maintenance of a diverse system of pollination depends on developing our understanding of pollination ecology, its history and key concepts.

Interest in pollination ecology is as ancient as culture itself. Our earliest records come from a bas relief found in Layard at Nimrod in ancient Assyria, dating to about 1500 B.C., depicting the artificial cross-pollination of the data palm, Phoenix dactylifera, by winged divine creatures with human forms and eagles’ heads (Real, 1983, 1). From ancient times until the 1930s pollination ecology was primarily descriptive, anecdotal and observational with research focused primarily on the temperate zones. After the 1930s there was a growing emphasis on the tropics and the focus shifted to quantitative and experimental studies. Since the 1970s scientists have directed their attention to studying the ecological and evolutionary principles of breeding systems, animal energetics, phylogenetic relationships, ecosystem structure and function, and population structure and dynamics (Baker, 1983, 15).

Plant-Pollinator Relationships

Interactions between flowering plants and their pollinators are the result of a long and intimate coevolutionary relationship. Analysis of fossil records provides insights into the emergence of reproductive structures in certain plants and the selective powers of insect pollinators (Crepet, 1983, 47). Different types of plant-pollinator relationships have evolved from the highly specialized obligarate mutualists to the jack-of-all-trades generalists.

In obligarate mutualisms there is a one to one symbiosis between a single pollinator species and a single plant species. While these relationships are rare because of their high risk, they exert a disproportionately large influence in structuring plant and animal communities. In tropical forest environments, 750 fig species depend on different species of small wasps as their single pollinator. Up to 70 percent of vertebrate diets in certain forests are derived from figs (Buchmann, 1996, 58). Judith Bronstein of the University of Arizona observes:

Figs have been called keystone mutualists of tropical forests – a keystone is the one that holds the arch together. The idea here is that if you pulled out the keystones, it would be disastrous for many of the animals that rely on them…This would happen, for instance, due to the selective logging of the trees upon which strangler figs establish themselves. Or, by spraying insecticides, you wipe out wasps, which in turn will cause their fig tree hosts to decline or possibly go extinct since the trees won’t be able to rely upon any other local pollinators. Both mutualists are locked in an intricate evolutionary dance and cannot change partners…it is assumed that populations would crash if figs or their obligarate mutualistic pollinators were wiped out. If this happened, cascading extinctions would be expected. (Buchmann, 1996, 60).

The majority of mutualists, however, are products of diffuse coevolution. In this form of mutualism a guild of pollinators will show strong allegiances to a set of particular flowers with similar floral forms. The flowers may bloom sequentially or overlap in space and time. If a single plant or pollinator goes extinct, the remaining members of the guild will have other options.

Not all pollinators, however, specialize on a particular set of like-shaped flowers – some like the honeybee are generalists. Honeybees have the greatest pollen dietary range of any known pollinator. In addition to collecting pollen from flowering plants they even obtain pollen from normally wind-pollinated and nectarless flowers such as grasses and ragweeds.

Studies suggest there are long-term matches between sets of pollinators and particular flowers. These are referred to as plant-pollinator landscapes. Appendix A describes five of the most common landscapes and their features. While these matches provide a good starting point for understanding the interaction between plants and pollinators one needs to look at the entire landscape of ecological interactions revolving around pollen and nectar availability to identify the entire range of animals that may function as potential pollinators.

While obligarate mutualists may represent the most vulnerable plant-pollinator relationship other relationships can also be threatened by extinctions when habitats are fragmented. Sequential mutualisms are relatively common in a number of landscapes. Sequential mutualists may specialize in one particular plant at a specific time and shift to other plants throughout the season. In this plant-pollinator relationship a sequence of flowers must be available to support the pollinator for an entire season.

On the floodplains of western Colorado the Ute ladies’ tress orchid demonstrates the perils of sequential mutualisms. Bumblebees rely on this rare orchid only for nectar so a sequence of other flowers must be available to provide pollen during the entire season. Lacking these foraging resources in the area, not enough bumblebees will stay to cross-pollinate the orchid. Consequently, the presence of other plant species may be just as critical to the survival of the orchid as the pollinators themselves. (Buchmann, 1996, 79).

Migratory species, even thought they are generalists, depend on sequential flowering of several species along a nectar corridor. If one link in the floral chain is broken – through habitat destruction or selective removal of a plant forming the critical link – the pollinator may be unable to wait without food until other resources become available.

Nectarivorous bats switch through a variety of nectar-providing plants as they migrate from tropical to arid temperate environments. Even where there is only one nectar source available for a particular bat species, it usually flowers in sequence with other bat-loving plants to the north and south along a bat’s migratory route. Thus the bat may specialize on just one kind of flower in each local environment, but these are linked into a nectar corridor of successive flowering times along the bat’s migratory route. (Buchmann, 1996, 81).

The phenomena of disappearing bees and diminishing plant reproduction is known as the Allee effect. The effect occurs when a population’s size drops below a certain threshold when it can no longer support its ecological associates and will lose its viability (Buchmann, 1996, 109). Unless there is rapid selection for rare mutants that allow for other forms of reproduction, such as self-pollination, plant populations will die out once their pollinators are gone.

Plants and the Pollination Process

Two major processes are required for the successful production of progeny in flowering plants – the setting of seed and the development of fruit. Seed set is dependent on pollination and the availability of sufficient maternal resources to develop the seed after fertilization. In angiosperms the flower is the center of pollination activity. Typically a flower is made up of four parts - sepals, petals, stamens, and carpels. The sepals enclose and protect the developing bud. The petals may contain nectar to attract pollinators. The stamens contain anthers that release pollen. The carpels each contain a stigma with an ovary that, after fertilization, can develop into a seed.

Plants have evolved self-pollinating and cross-pollinating breeding systems to ensure fertilization. Breeding system variations have developed from a combination of evolutionary and ecological factors including genetic selection and pollinator availability (Wyatt, 1983, 85). Self-pollination occurs when the pollen used to fertilize comes from the same plant that produced the ovary. Cross-pollination occurs when the pollen used to fertilize comes from another plant in the same species. In general, cross-pollination is favored even if selfing is possible because of the increased genetic variability within the population that improves a plant’s ability to adapt to changing conditions. The lack of genetic variability in self-pollinating species often leads to inbreeding depression with depressed seed set and seed weight.

Plants avoid self-pollination through self-incompatibility i.e. physiological barriers that make it difficult or impossible to self-fertilize. These barriers may include self-sterility, different maturing times between the anther and stigma, or spatial arrangements that are impossible to bridge. Self-pollination is common in some species where pollinator populations fluctuate enormously, where competition for pollinators is intense, or where plants live a shorter life. In the United Kingdom, 2/3 of flowering plants are capable of self-pollination. Some species use self-pollination as a backup strategy - the violet produces showy flowers in spring to attract pollinators for cross-pollination and later in the year produces smaller flowers for self-pollination if its cross-pollination strategy fails (Proctor, 1996, 334).

Cross-pollination is accomplished through a variety of abiotic (wind and water) and biotic (bees, butterflies and moths, bats, beetles, birds, etc) vectors. Appendix B identifies the classes of pollinators for flowering plants. The earliest form of pollination was pollination by wind. This strategy involves producing masses of low-cost gametes. For wind pollination to be successful, plants must grow in fairly dense stands to ensure "pollen rain" will land on target stigma. Pollen blown by wind can travel to a distance of 15 meters and is most effective in conditions of low air turbulence, low humidity and low rainfall. It is characteristic of temperate deciduous and boreal forests and relatively rare in tropical environments (Whitehead, 1983, 98).

Pollination by biotic vectors requires plants to make significant investments in high-priced showy flowers to attract pollinators. The chance of reproductive success may be greatly enhanced by relying on biotic vectors. In order to attract pollinators, plants must offer rewards. Floral rewards may include shelter from storms, protection from predators, safe refuges for mating, strategic stakeouts for territorial defense, locations for ambushing prey, delectable sources of nectar and pollen, resins, oils, perfumes, and other chemicals.

Nectar supplies pollinators with energy in the form of carbohydrates and is the primary food source for most adult winged insects. Nectar production places relatively light demands on plant resources since water, carbon dioxide and sunlight are generally in abundant supply. Nectar concentrations vary from 15-75% sugar. The nectar produced is targeted to attract specific pollinators. Some plants produce sucrose-type nectars to attract long-tongued bees, butterflies, moths, and birds. Other plants produce hexose-type nectars to attract short-tongued bees, flies and bats (Procter, 1996, 40). Nectar production is usually timed to pollinator activity. In dry desert areas where most pollinators are nocturnal nectar production occurs at night.

Pollen is ‘expensive’ for the plant to produce. It is rich in nitrogen and phosphorous, two elements often in growth limiting short supply. Pollen contains 16-30% protein, 1-7% starch, 0-15% sugar, and 3-10% fat (Procter, 1996, 39). Bees, unlike other insects, collect pollen for their young who require protein for their growth, creating a demand for the protein-rich food. In order to feed their young as well as themselves bees make far more visits to flowers than other pollinators, enhancing their effectiveness. As a result, many plants have evolved as high pollen-producers in spite of the fact that nectar production is more economical (Procter, 1996, 38).

The high costs of advertising and rewards associated with successful animal pollination and fruit production may take their toll on the growth of some plants. In spite of this investment, some plants still fail to attract sufficient pollinators.

Boston University’s Richard Primack and Pamela Hall have tracked the growth and reproductive success of the pink lady slipper orchid, Cypripedium acaule, for several years in eastern Massachusetts. The single, nectarless, pink flower that is produced amounts to 18 percent of the plant’s total dry weight. One successful flowering and fruiting episode can tax the entire plant for up to four subsequent years. And yet there may be good reason to make that investment. At the present time, there is an apparent scarcity of bumblebees in the eastern Massachusetts forests. Only 2 percent of the pink lady slippers are visited by bumblebees in a way that results in pollination and seed set (Buchmann, 1996, 45).

From a plant’s standpoint, not all pollinators are equal. Some pollinators are nectar robbers, who pierce the plant to steal nectar, ignoring pollen completely. Some pollinators are more effective than others.

Near Mexico City two researchers have been studying Manfreda brachystachya, a relative to mescal-producing century plants. The lesser long-nosed bat remains its constant pollinator even though other bats, hawkmoths and hummingbirds pay visits. From 1982 to 1985 seed set dropped by 75% in the plants. Researchers went on to show that declines in seed set directly reflected declines in bat visitation rates even though other floral visitors were present. When bats visited the plants frequently, seed set was high; when they were nearly absent, seed set was low (Buchmann, 1996, 23).

Flower constancy is the tendency of an animal to restrict its visits to flowers of a single species, even when they are intermixed with other equally accessible and rewarding flowers (Waser, 1983, 255). Floral constancy demands pollinator faithfulness, which varies greatly among pollinators. In a extensive study of individual bumblebees, which normally show high fidelity, scientists calculated that an average of 57% of pollen loads were pure, 32% were mixtures of two species, 13% mixtures of three species, and 5% mixtures of four species (Rathcke, 1983, 319).

This behavior may be induced by an insufficient abundance of a single plant species rather than pollinator preference. In another case, a hive contained pollen from 55 flowering species or 25% of all flowering plants within reach of the hive (Proctor, 1996, 141).

Pollinator faithfulness is an important factor in plant fitness (Waser, 1983, 256). Improper pollen transfer will mean pollen loss for the donating flower and may result in the accumulation of improper pollen on floral stigmas of the receiving flower. Research has shown that foreign pollen can lower seed set through stigma clogging, chemical or physical interference with plant processes, or though production of sterile hybrids (Rathcke, 1983, 307). Many flowers have evolved structures to regulate the behavior of particular visitors with precision and to exclude others with a high degree of effectiveness.

Orchids have developed ways of ensuring their pollinia get transferred only to another flower of their own species and are not "wasted" by being left in flowers of an altogether different species. Every orchid genus-and sometimes species as well-has a predetermined "map" of locations on the body of its bee visitors on which to glue its precious pollen cargo. During each subsequent encounter with a flower of the same kind, the particular shape of the flower forces the bee to twist and turn in a way that increases the probability that the properly placed pollen package is effectively transferred (Buchmann, 1996, 52).

Current research strongly suggests that pollination limitation does occur in natural populations and is not a rare phenomena (Rathcke, 1983, 319). Given this there may be strong selection pressures that enable plants to self-pollinate similar to what happens in small, island habitats where pollinators are too scarce to ensure cross-pollination.

Bees and the Pollination Process

While beetles far outnumber bee species in the global pollination trade, bees are the most abundant taxonomic group of pollinators outside the tropics. Bees are now thought to have originated during the Cretaceous period at a time when there was an explosion in the diversity of flowering plants (Crepet, 1983, 43). They are in the order of Hymenoptera, the suborder Apocrita and the family Apidae. Globally 25,000 bees have been named and catalogued with estimates of 40,000 species alive today or 1 in every 10 species on earth. In the continental United States, entymologists have estimated 4000-5000 ground-nesting and twig-nesting bees (Buchmann, 1996, 89).

Bees have reached their greatest diversity in the deserts and savannas of the world due to the patchiness of floral resources. Most bees are ground-nesters and deserts provide a mosaic of habitats that help trigger the adaptive radiation of small pollinators. Tucson, for example, is one of the richest bee real estates in the world with 580 species of plants and over 1000 species of native bees (Buchmann, 1996, 88). While most native bees in the Americas are solitary, the majority of research has been done on the social bees, Apis (honeybee) and Bombus (bumblebee).

Lifecycle and foraging habits differ significantly among bee species. Honeybees are perennial and have the longest flying season of any bee. Their territory extends to about 60 degrees North latitude. They are the first bees to emerge in the spring because of their broad floral diet (Williams, 1996, 68). Fertilized queens start new colonies and may produce 2-3 broods of "worker bees" each year. "Scout bees" are the first to emerge from the hive. Their job is to explore for new food sources. The "worker bees" are the next to emerge. They collect the majority of pollen and nectar used by the colony.

Bumblebees are annual bees and are scarce early in the year. The first bees to emerge in the spring are the "worker bees." Males and queens are produced at the climax of the colonies development. Colony size may vary from 40 bees to 200 bees. The range of the bumblebee is much broader than the honeybee. Because of their size, insulation and ability to warm up, they have lower temperature thresholds than honeybees and are the first to forage each morning (Williams, 1996, 69). Solitary bees are annual bees and have a short flying season of 3-4 weeks.

Bees are frequently classified as long-tongued and short-tongued bees. They use their tongue to slurp nectar and as a trowel for plastering saliva to the walls of their hives to protect them from moisture, fungi and collapse (Proctor, 1996, 115). Nearly all bees are vegetarians. They have an almost total dependence on flower food for their survival. This makes them efficient pollinators but also means they will leave an area when the flower population is insufficient to feed them.

Nectar provides the bee with their fuel for flight and pollen provides them with their daily bread.

Bees usually collect nectar early in the day for their own energy reserves and collect pollen later in the day for feeding their young. Any surplus nectar is carried to the nest. The nectar is regurgitated repeatedly and thickens as it is exposed to the warm air. The resulting honey is stored in the comb and used for later consumption by the collective. A large honeybee colony can produce 520 pounds of honey in a year (Buchmann, 1996, 173). Honey production is an extremely labor-intensive enterprise.

One pound of clover honey represents approximately 17,330 foraging trips. Each bee visits 500 flowers in a single trip of 25 minutes. This pound of honey represents the food rewards from 8.7 million flowers and 7221 hours of bee labor (Procter, 1996, 42).

Bees have evolved complex morphological and behavioral adaptations for collecting and transporting pollen. Insects that collect pollen are usually covered with dense coats of hair. Each hair has a large set of teeth and hooks to which the pollen adheres. As the bee leaves a flower, a series of brushes and combs gather the pollen and place in into the pollen basket. One load after another is pushed into the basket until it is full. A basket can contain as much as ten milligrams and as many as a million pollen grains. The pollen load is then transported back to the hive and deposited in a storage cell where younger bees break it up. Eventually the nurse bees will eat the pollen and convert it to "mother’s milk" for feeding the larvae. Many solitary bees, including mason and leafcutters, have brushes on their abdomen and are known as abdominal collectors. Other bees are known as crop collectors. Crop collectors scrape pollen from plants using their mouth, swallow it for transport, and spit it out when they return to their nesting site. The honeybee, bumblebee and stingless bees of the tropics, Meliponae, are the most important pollen collectors (Barth, 1985, 60). Honeybee colonies have been known to collect 50-85 pounds of pollen per year (Buchmann, 1996, 63).

Pollination services are provided at a cost to the pollinators. These costs include the calories expended in moving from plant to plant and subsequent investments in gathering, transporting and processing the floral rewards. Travel costs can be exceedingly high as in the case of the hermit hummingbird, the pollinator of Heliconia or "bird of paradise" flowers. The hummingbird often flies more than a mile through forest before reaching the next Heliconia plant (Buchmann, 1996, 53). Pollinators also incur evolutionary costs by investing in specialized morphological and chemical adaptations that often limit their ability to use other floral resources.

To obtain the nectar of one Heliconia species hummingbirds must rotate their heads at an angle of more than 90 degrees – almost upside-down to allow their bills to reach the hidden nectaries. The Heliconia offers copious quantities of energy-rich nectar to hummers that can achieve this acrobatic feat. In doing so, pollen is placed on the chin and base of the bill thereby reducing the possibility that the flower’s pollen will later be deposited on the wrong kind of flower (Buchmann, 1996, 53).

The foraging behavior of pollinators is a force shaping plant populations and their communities. Floral morphology and plant architecture, phenological patterns of flowering, diversity of gene systems, gene flow and population structures all depend in part on foraging behavior (Waddington, 1983, 213). The foraging behavior of bees can vary dramatically. Bees specializing in plants at low density use a technique called traplining. They visit each plant in a set route and take up to 50 minutes to collect a load before they return to the nest (Procter, 1996, 135).

Bees frequently use orientation flights to allow them to fix the exact position of plants after only a few flights. During an orientation flight, a bee will fly around the objects they are interested in using gradually increasing circles as they fix the object’s position in relation to other objects in the landscape. Using these techniques, bees are able to maintain approximate knowledge of plants in central areas and exact knowledge of distant plants (Procter, 1996, 137).

In the tropics, some non-social bees forage in groups of 300 or more. Other long-lived quasi-social tropical bees forage over long distances to locate food sources. One recorded bee flew 20 kilometers from its nest during a 60-minute period (Procter, 1996, 135).

Honeybees navigate by the sun and orient themselves by light polarization in order to navigate in cloudy weather. They have a very extensive and extremely focused foraging behavior. Groups of bees will continue to work new sets of flowers after one patch is exhausted for the day while others return to the hive until their favorite crop is productive again. A honeybee colony may forage within a 60 square mile radius of its hive. E.O. Wilson once said "if bees were the size of humans and their flight distances similarly scaled up, a single bee colony placed in the middle of Texas would collect pollen and nectar from wildflowers in about one half the state" (Buchmann, 1996, 61).

Scent plays an important role in the communication of the nature of food sources. Returning foragers carry the scent of flowers into the hive and this scent is used to help other bees find the same kind of flower (Procter, 1996, 128). Honeybees use dances to communicate the remainder of information about valuable food sources. Their dances describe the direction, distance, abundance, and nature of a valuable food source. Melipona, social stingless bees, use a pulsed beating of the wings to indicate distance to a food source. They communicate the direction to the food source by a complex leadership ritual outside the nest (Procter, 1996, 133).

The organization of a honeybee colony makes for ruthless exploitation of every food source within an area. Their social life makes possible communication, cooperative effort and division of labor. Social bees live in colonies some numbering as many as 50,000 individuals. Honeybee colonies are superorganisms weighing 5 kilograms or more, requiring massive amounts of pollen, nectar and water from the surrounding countryside (Buchmann, 1996, 127). By their numbers and their organization the honeybee seems more or less to have taken charge of its floral environment, much like man.

In conclusion, plants and pollinators have adapted and coevolved many different types of relationships over time. The diversity we see today is largely a product of the myriad morphological, chemical and behavioral adaptations that have shaped the earth’s plant-pollinator communities. These relationships and the survival of the participants are threatened by a number of converging factors. The most vulnerable mutualists, those without alternate partners, are clearly endangered in many parts of the world, but other, less specific relationships are also in jeopardy. The study of fragmented habitats and island environments point us in the direction of likely scenarios.

The loss of pollinators may lead some plants that can evolve quickly to become self-pollinating. This strategy, while ensuring the plant’s short-term survival, carries with it a reduction in genetic diversity and an increased risk of inbreeding depression. The loss of plants would likely favor the survival of generalist pollinators. This also carries risks for the productivity and survival of plant populations. Generalist pollinators may cause stigma clogging in plants or be less efficient pollinators leading to reduced seed and fruit set. As our scientific understanding of pollination ecology and our appreciation of the complexity of ecological systems increase so does our capacity to fundamentally alter the environment and cause the extinction of many species.

The Pollination Crisis in Agriculture

Pollinators of Our Food

The quality and variety of our food system depends on a multiplicity of pollinators and pollination strategies. Grains supply man with energy and globally provide over 50% of our daily calories (FAO, 1998, 14). The primary grains (rice, wheat, maize, sorghums, millets) are either wind-pollinated or self-pollinated. Appendix D describes the world’s major energy foods, their contribution to our caloric intake, and their main pollinators.

Insects pollinate the majority of our cultivated crop species. A recent survey conducted by David Roubik tallied 1330 different crops. He estimates that 73% of cultivars are pollinated at least partially by bees, 19% by flies, 6.5% by bats, 5% by wasps, 5% by beetles, 4% by birds and 4% by butterflies and moths (Buchmann, 1996, 193). Appendix E lists many common food crops and their primary pollinators.

Fifteen percent of the average American diet consists of fruits, vegetables and nuts, most of which are insect-pollinated. Another 15% consists of animal products, such as beef, poultry, pork, lamb, and dairy products that derive their calories from insect-pollinated hays (alfalfa, clovers and lespedezas). More than 50% of the oils we eat come from oilseeds (coconuts, cotton, oil palm, olives, peanuts, soybeans and sunflowers) that rely on or benefit from insect pollination. When all of these food sources are considered over 30% of our daily intake is directly or indirectly dependent on insect-pollination (McGregor, 1999, 1).

Economic Value of Pollination

Accurate estimates of the economic value of pollination services are difficult to obtain. The United States Department of Agriculture (USDA), the main governmental agency compiling agricultural statistics, only captures pollination data on European honeybees despite the fact that over 20% of all agricultural pollination is done by other pollinators (Buchmann, 1996, 194). In 1976, Samuel McGregor of the USDA estimated that at least 150 major crops relied to some extent on wild and semi-managed pollinators. Wild insects are the primary pollinators of cashews, squash, mangoes, cardomen, cacao (chocolate), cranberries, and blueberries. Wild animals are critical to the production of seeds used in planting onions, carrots, kapok, sunflowers, cinnamon, clover, figs, and coconuts (Buchmann, 1996, 192).

Many economists have tried to estimate the agricultural value of honeybee pollination. In 1983 Levin looked at the output of 49 honeybee-pollinated crops produced in the United States and attributed an annual value of $18.9 US billion to honeybee pollination services. His calculations included the value of crops and commodities derived from pollinated seeds and the values of alfalfa hay, the cattle, and the milk production that depended on honeybee pollination (Free, 1993, 9). In 1989 Robinson looked at 40 major crops grown in the United States and considered that honeybees were responsible for 80% of their insect pollination. Excluding dairy and livestock production, he calculated that honeybee pollination contributed $9.3 US billion or 31% of the total value of the crops he examined (Free, 1993, 10).

In addition to increasing the agricultural output of the crops they pollinate, insects help increase the productivity of all crops. In the United States, bees are responsible for pollinating the major legumes. These nitrogen-fixing crops restore soil productivity without the use of chemical fertilizers.

While economists attempt to calculate the economic value of pollination services, it is clear that the quality, variety and productivity of our food production system is dependent on pollinating insects, particularly bees.

Man’s Relationship with Bees

Man’s relationship with bees has centered on two activities – gathering honey from hives and selling pollination services. Honeyhunting, the practice of raiding hives for honey, is perhaps the earliest form of human use of bees. At Barranc Fondo in eastern Spain petroglyphs in a rock shelter depict five human figures ascending a ladder towards a nest while families wait below eager for a taste of honey. The petroglyph is estimated to be at least 6000 years old. Similar images of ladders leading to giant bee nests can be found throughout Asia and Africa. Dr. Eva Crane, founder of the International Bee Research Association claims that the ancient petroglyphs suggest that early human cultures "developed an affinity with the bees from which [they] took honey, in spite of the stings, and the bees were often revered as magical, or even divine" (Buchmann, 1996, 152). Honeyhunting rituals are still practiced in many parts of the world today.

Early humans began modern beekeeping over 4000 years ago (Crane, 1990, 3). The earliest unambiguous depictions of beekeeping are found in temple scenes along the Nile. The temple scenes, dating from 2400 to 600 B.C., show the harvesting, processing and storing of honey in large clay vessels. The Egyptians may also have been the first migratory beekeepers. Paintings dating from 3500 B.C. depict Egyptians floating their hive-laden barges up and down the Nile and selling pollination services to floodplain farmers along the way (Buchmann, 1996, 153).

The Mayans of the Yucatan peninsula were honeyhunters. They have hunted the honey of 17 different species of native stingless bees. Four species of native bees were kept in dooryard gardens as "semi-domesticates" before Columbus reached the Americas. The keeping of stingless bees, meliponiculture, still persists among the Mayans. The native bees were "as sacred as corn" and their honey was used for treating many ailments, including chills, cataracts, fevers, laryngitis, and complications at childbirth (Buchmann, 1996, 158).

Agricultural practices have changed significantly in the past fifty years, fundamentally intensifying and reshaping man’s relationship with bees. Under natural conditions there are usually no great concentrations of one flower species in a single place and the native insect population that is visiting the flowers may be sufficient for pollination. In the conditions of industrial agriculture, where hectares of a single flowering crop of a single species is grown, the wild insect pollinators are too few to provide adequate pollination services. Organized pollination services have developed to meet this need. Large commercial enterprises exist for the most important pollinating insects - solitary bees, bumblebees and honeybees.

The native alkali bee and the European leafcutter bee are two solitary gregarious bees that pollinate lucerne. Lucerne is a native crop in Eastern Europe and a major forage crop in North America. The tripping rates of these non-social bees produced two or three times as much pollination in a given period of time as the European honeybee. The alkali bees nest in bare, damp soil. Nesting beds of 10 X 17 meters placed near the crop can supply pollinators for 12 to 16 hectares of lucerne (Procter, 1996, 354). Large-scale management of the non-native leafcutter bees involves extracting healthy cocoons and storing them at low temperatures until the lucerne begins to bloom. The cocoons are then transferred to incubation trays that are placed in shelters and spread throughout the fields. Each shelter contains 10,000 to 50,000 nesting holes for the bees. After the nesting season, the cocoons are removed for storage until the next season (Procter, 1996, 356).

Bumblebees are the natural pollinator of red clover, another major forage crop in North America. Bumblebees nest in hedges and neglected patches of land. Wild populations began to decline with intensive agriculture due to a loss of nesting sites (Procter, 1996, 357). Some farmers have tried to maintain populations by creating artificial nesting boxes near their red clover fields and by leaving patches of wild areas so there is a succession of flowers for pollinators to forage among.

By the 1980s methods were developed in Europe for commercially rearing bumblebees in captivity (Williams, 1996, 70). Since then bombiculture has developed into a million dollar business. Bumblebees provide buzz pollination services to plants that do not produce nectar, but still require some disturbance of their flowers to fully pollinate. The bumblebees perform a rotating dance on the flowers that assist pollination. Tomatoes, blueberries, cranberries, eggplant, and kiwi are all buzz-pollinated.

Wild bumblebees are annual and have a relatively short flying season. Growers have developed techniques to extend the season by creating artificial colonies. A hibernated bumblebee queen is placed in a nesting box with 3-4 honeybee workers to calm her. Sugar solution and pollen is collected by honeybees and supplied to the queen who uses this food to start her brood. When the first bumblebee workers emerge the colony is transferred to another box. The same food supply is continued. When 80 workers emerge the colony is sent to the grower. The producer will keep some colonies to raise queens and drones. Each new queen mates with a drone from another colony after which she normally hibernates. The producer injects a CO2 solution to prevent hibernation so colonies are available for pollination from January to September (Procter, 1996, 359).

Apiculture, the management of honeybee colonies, is used to ensure the availability of large populations of honeybees for pollination. Honeybees are managed for honey, beeswax and as rental units for crop pollination. Honeybees are the pollinators of many orchard crops. They tend to seek out and exploit crops with large quantities of pollen and nectar. The bees try and keep an approximate balance in their intake of the two foods. Since they are much more effective in pollen collection, steps must be taken in managed environments to supply them with additional nectar. Sugar syrup is frequently placed in their hives to expand their appetite for pollen. Honeybees are also encouraged to pollinate crops by soaking the crops in honey-water or other attractants (Procter, 1996, 352). The use of honeybees for intensive crop pollination generally weakens the colonies. The combination of high-hive densities used to saturate crops and forcing the bees to forage among flowers they don’t naturally choose leaves the colony depleted. Research by Tinker in 1971 documented declines in honeybee colony weight gain during a single season. In 1929 colonies showed an average gain of 7 pounds per season. By 1963 colonies experienced an average weight loss of 24 pounds per season. This loss has been attributed to pesticide and herbicide use, pasture management that eliminates many flowers, and monocultures of large crops unattractive to bees. At the end of the commercial season, colonies must be restored through visits to wild flowers where the bees can forage at lower densities (Buchmann, 1996, 195).

The Bee Crisis

Bees have suffered dramatic declines in their wild and domesticated populations over the last sixty years. These declines are the direct result of introducing new exotic species and the widespread use of industrial agricultural methods. Native bee populations have been decreasing in the New World since the introduction of European honeybees in the 1620s. Races of the European honeybee were introduced from their homelands in Europe and Asia based on their superior honey-making abilities. The European honeybee dominated the native, often endemic, solitary bees by sheer numbers, by their ability to detect floral resources, and quickly communicate their location to other members of the colony. Native bees were forced to abandon most of the productive sites, but have held their own in less productive habitats (Buchmann, 1996, 133).

Unlike the solitary bees who show a narrow specialization for the pollen of one genus or family, the honeybees are generalists. Their introduction permanently alters the amounts and types of nectar and pollen available from wildflowers as well as the pollination services rendered to native plants (Buchmann, 1996b, 126). Honeybees are lilliputian livestock – fuzzy herbivores with wings – that are just as capable of taming and altering a landscape as any cow, sheep or goat (Buchmann, 1996, 183).

The Africanized honeybee is another exotic species that was purposefully introduced to Brazil in 1956 from its homeland in East Africa. The Africanized bees were known to be aggressive, but like the European honeybee, exceptionally good honey-producers. Approximately 25 African queen bees escaped and managed to ‘Africanize’ more than 2 million honeybee colonies in tropical and subtropical South and Central America by 1990 (Crane, 1988, 3). The Africanized honeybee is a good example of how an invasive species can dominate a habitat, displace other genotypes and disrupt local species (Sugden, 1996, 158). The Africanized bees are a disturbance-loving species well-adapted to fragmented habitats. Unlike the European honeybee that forages in groups and is adapted to rich and predictable resources, the African honeybee evolved in conditions of greater unreliability of pollen and nectar. The African honeybee is an individual forager that discovers habitat quickly, reproduces rapidly, consumes resources until the habitat disappears, and then disperses to search for new habitats (Rinderer, 1988, 23).

The European honeybee is docile and easy to manage. Human artificial selection in Europe may have favored colonies that stung less which reduced the overall defensiveness of the bees. The Africanized bee evolved in Africa where resources were limited and evolution would have favored colonies that aggressively defended their resources (Rinderer, 1998, 19). As a result, the Africanized bees readily defend their territory and have been extremely difficult for beekeepers to manage. In southern Mexico, Africanized honeybees were found to be efficient pollinators of cotton but they could not be used as rental pollination units because of their aggressiveness. Producers had difficulty transporting them and farmers were unable to work in their fields when the bees were present. The aggressiveness of the African honeybee will undoubtedly diminish with time but in the short-term beekeepers must try and prevent their bees from hybridizing with the Africanized bees.

The Africanized bees took up permanent residence in the United States in 1990 and have subsequently spread throughout the southern states. Estimates indicate that 80% of U.S. beekeepers may have to abandon their hives once the African bees arrive in their area (Buchmann, 1996, 196).

The introduction of industrial agricultural methods has also caused the decline in bee populations. In the 1950s and early 1960s, dieldrin and parathion, which are highly toxic to the native alkali bees, were used extensively on alfalfa crops to control lygus bugs. An enormous percentage of naturally occurring alkali bees were killed. In 1973 in Washington the inadvertent pesticide poisoning of alkali nesting areas resulted in $287,000 loss in alfalfa revenue (Buchmann, 1996, 190). Managed honeybee colonies have also been impacted by widespread pesticide use. The number of honeybee colonies peaked in 1947 at 5.9 million. Widespread use of organochlorine pesticides after World War II contributed to a 43% drop in colonies to 2.6 million by 1995 (Buchmann, 1996, 195).

In addition to pesticide use, large commercial beekeeping enterprises have fostered the rapid spread of disease and infection. In 1992 the Southwick brothers, an economist and a bee biologist, estimated that over 50% of managed bees populations in the Northern United States may be lost due to mites and disease (Buchmann, 1996, 191). The European honeybee, like other exotic species, left their natural enemies behind when they were transported to the New World. Nature has in fact caught up, as diseases and pests have taken hold and undermined population growth (Sugden, 1996, 157). Most entymologists agree that mites and diseases are here to stay.

In 1984 the honeybee tracheal mite, Acarapis woode, appeared in the United States and spread throughout the country by 1986. Some states have reported a 50% decline in European honeybee colonies since the mite arrived. The tracheal mite is an internal parasite that infects the respiratory system of bees. The mite reduces the longevity of adult bees and they eventually die of starvation or from secondary infections (Gersen, 1988, 494). Treatments have been developed to suppress the infections, but scientists have been unable to develop medications to eliminate the mites.

The varroa jacobsoni parasite arrived in the United States in 1987 and since has spread to 30 states. Varroa jacobsoni is an external parasite that infects bees during the late larval stage when they become paralyzed and die or develop into unhealthy short-lived adults (Delfinado-Baker, 420). The colony quickly collapses once the worker and drone bees become infected. The Africanized honeybee appears to be resistant to the mite because the worker bees have a shorter pupal stage reducing the time of parasitic infestation. Asian honeybees, Apis cerana, have evolved physiological and behavorial adaptations to recognize the presence of the parasite and remove it from the colony. Once the parasite is recognized, the Asian bee begins a self-cleaning behavior to eliminate the mite. If the bee is unable to remove the parasite, it begins a grooming dance that prompts nestmates to use their mandibles to remove the parasite (Delfinado-Baker, 1988, 428).

The USDA and other government agencies took note of the declining bee populations once the impact was felt by commercial pollination services. If alternative pollinators are not found for the European honeybee and honeybee colonies near farmlands were to decline as predicted, the impact on agricultural production will be significant.

Responses to the Crisis

One response to the crisis has been technological. Bonita Farms is one vision of the managed-pollination services of the future. The Farm has a single glass-enclosed greenhouse covering 10 acres in Arizona. The European multinational that owns Bonita Farms plans to build more greenhouses creating a 200 acre controlled microenvironment. The greenhouse houses thousands of tomato plants growing in white plastic bricks. The bricks contain rock wool, sensors and emitter tubes that monitor the plants and release fertilizer and water on demand. Hanging above the tomatoes are electric cables, blinking lights and display panels attached to computer workstations that control the temperature, humidity and nutrient flow to each plant. The cutting-edge "organic" greenhouse uses biological agents to control weeds. Bumblebee colonies are rented to pollinate the thousands of hybrid tomatoes. The bees have been bred by the Dutch-owned Koppert Biological Systems and are rented on the basis of their capacity to pollinate a given volume of greenhouse tomatoes. The bumblebees are fed a diet of "Bee Happy" juice through a clear plastic bag above the hive. The artificial nectar is essential if the bees are to pollinate all the greenhouse tomatoes (Buchmann, 1996, 164).

Another response to the pollination crisis is to look for alternative pollinators. Strengthening the native bee populations and increasing the role for native species in the commercial pollination of cultivated crops is another vision of the future. Ironically, mites may have a positive ecological effect by relieving native species of competitive stress from honeybees, providing more resources for domestic colonies, enabling increased genetic control of honeybee populations, and reducing the supply of commercial pollination services so prices are driven up (Sugden, 1996, 157).

For native species to rebound, appropriate habitat and adequate food sources are required. Farmers will need to change their agricultural practices to increase the efficiency of pollination. This means reducing the use of chemical fertilizers and pesticides or applying them when the impact on pollinators is minimal, creating windbreaks to shelter pollinators, and breaking up large monocultures into smaller crop acreages. To maintain viable pollinator habitats in agricultural landscapes, traditional farming methods need to be reinstituted where 25% of the land is free of cultivation and mowing (Banaszak, 1996, 57). This natural habitat needs plants whose peak flowering season coincides with the seasonal peak in wild pollinators. Adequate food sources must also be available while pollinator populations are increasing (Osborne, et. al, 1991). To maximize the use of wild pollinators, agricultural lands and orchards should remain close to wildlands. Plant breeders and geneticists need to ensure the new hybrid strains they create are attractive to bees and yield abundant quality nectar (Free, 1996, 4).

Others have discussed the possibility of introducing another exotic honeybee, the Eastern honeybee, Apis cerena, to the Americas to fill the vacuum left by the European honeybee. Many strains of the Eastern honeybee are quite docile, can live in a wide range of climatic conditions, and have a proven ability to pollinate a wide range of agricultural crops. Although this may be a viable solution, careful analysis needs to be done with vigorous testing and monitoring to ensure the bees are free of undesirable traits and will not cause harm to existing ecological relationships.

Hand pollination is another alternative pollination method. Although very labor-intensive, it is often used in orchards where pollinating insects are rare. In Japan, pollen has sometimes been mixed with lycopodium powder to make it go further during hand pollination. Effort is also being put into devising economic methods for pollinating apples mechanically (Procter, 1996, 363).

Scientific research is continuing on ways to control the mites. Researchers at the University of Minnesota are attempting to breed European honeybees that are resistant to the mites. Scientists are also trying to develop treatments to eliminate the mites or chemicals to help control the spread of disease in the commercial bee colonies. In general, however, there has been a lack of public understanding of the seriousness of the problem and a lack of investment in research.

In conclusion, we as humans, depend on insect pollinators for variety and quality in our diet. Our industrial mode of agricultural production, however, is destroying many of the wild pollinators that have provided pollination services for free in the past. The managed pollinators are also facing significant declines in their populations. Through the introduction of exotic species to increase production and our over-dependence on one pollinator, the European honeybee, we have created the beginning of a disaster. The homogenous, controlled environments we try to create go against the diversity in nature and become a breeding ground for diseases. As scientists work to develop methods to combat mites, we need to step back and take a multifaceted approach that is based on maintaining biodiversity if we hope to continue having quality food at reasonable prices. Many questions still remain: What are the potential impacts of genetically-modified organisms on pollinators? How much genetic diversity remains in the native pollinator populations? Can we rebuild the native bee populations?

Conclusion

Much of the diversity we see in the world today is the result of pollination of flowering plants by a variety of biotic pollinators. This diversity has exploded in the last 144 million years, giving us beauty in nature and bounty in our diet. Throughout history man has interacted with nature and reshaped it to meet his needs. Through technology and migration, the reshaping of nature has accelerated in the last 100 years to the point that one of the pillars of our wealth, diversity in nature, is threatened. Population growth and the drive to maximize profit have contributed to loss of habitat, the introduction of exotic species (including the European honeybee and the African honeybee) and an industrial agriculture that seeks increased productivity by creating a homogenous environment.

Overall land use patterns have created fragmented habitats, disrupting and sometimes eliminating plant-pollinator relationships. Agricultural methods have led to a decrease in wild bee populations and threatened managed bee colonies. While technology can be applied in advanced industrialized countries, at a cost, to mitigate some of the effects on our world food supply, it cannot reverse the trend. Only people, acting consciously, can hope to do that. We need scientists to continue researching the causes of rarity in plants to help us understand fragmented habitats. How much habitat is required to preserve a diversity of pollinators? What type of habitat? What is a viable population size? What if only generalist pollinators survive? We need educators raising people’s awareness of the problem. What is pollination? Why is biodiversity important? What services does biodiversity provide us? How do we need to change our thinking about the natural world? We need activists organizing people to make a difference. Why do we need to act now? What can each of us do? What can environmentalists do? What can the small struggling farmer do? What can the organic grower do? What can the city dweller do? What can children do?

Glossary of Terms

abiotic pollination. The movement of pollen grains from plant to plant by abiotic vectors. Wind pollination is the most common form of abiotic pollination.

adaptive radiation. The spread of species of common ancestry into different niches.

Africanized bee. A subspecies or race of highly defensive honeybees which originated in Africa. They were purposefully brought to South America and have spread throughout the southwestern United States.

alfalfa leafcutter bee. An introduced Eurasian species, Megachile rotundata, belonging to the leafcutter family Megachilidae, that forms the basis for a multimillion dollar agribusiness for pollinating alfalfa.

alkali bee. Native North American bee belonging to the genus Nomia. One species has been managed as a pollinator of alfalfa.

Allee effect. The pioneering ecologist W.C. Allee described what occurs when the population of a species drops below a certain threshold.

angiosperm. Angiosperms are flowering plants, the dominant plant lifeform today with approximately 246,000 species. Their "double fertilization" and uniquely resistant (to desiccation, fire and abrasion) seeds may explain their extraordinary evolutionary success since the Cretaceous period.

anther. The pollen-containing part of the floral stamens.

apiculture. The scientific study of honeybees and their management for increased honey production, beeswax, queen bees, or commercial rental for pollination services.

aphid bee. The common name for any bee in the honeybee family, Apidae, which now includes orchid bees, bumblebees, stingless bees, true honeybees and digger bees.

bee bread. The vernacular name for pollen combined with nectar or honey and stored in hexagonal comb cells by honeybees.

beekeeping. The intentional stewardship of honeybees and stingless in hives made of various materials for the harvest of honey, beeswax and brood by various human cultures. Beekeeping is at least 5000 years old.

biota. The collection of animals, plants and other organisms occurring together in a certain geographic region.

bombiculture. The culture and management of bumblebee colonies (Bombus species) to provide pollination services – as in the recent development of buzz pollination of tomatoes in Europe.

buzz pollination. A specialized form of pollen harvesting and pollination used by many bees (but not honeybees) to extract pollen from the anthers of many flowering plants, including blueberries, tomatoes, cranberries, eggplant and nightshade. About 8 percent of the world’s flowering plants exhibit this form of pollination sometimes called sonication.

cascading extinctions. The premise that one or several extinctions, especially of key organisms in tropic areas, can lead to a rapid sequence of extinctions of other ecologically linked organisms.

cereal crop. True cereals come from the grass family. The grain constitutes a fruit in which the dry ovary wall closely invests and fuses with a single seed and its coats. Cereals possess a concentrated store of food material, largely carbohydrates.

coevolved. The idea in evolutionary ecology that certain mutualistic organisms have directed or redirected each other’s evolutionary trajectory.

cross-pollination. The transfer of pollen from the anthers of one plant to a recipient stigma on another plant that may result in fertilization and fruit set. Also known as out-crossing.

diffuse coevolution. The process by which one or more species with an ecological association evolve more or less together to their mutual benefit.

dioecious. The separation of male and female flower on different plants, e.g. jojoba.

endemism. The process whereby a species is restricted to a small geographic area. "Endemic" species originated or evolved in that area.

extirpation. The elimination of a population from a locality either by human or other activity.

facultative mutualism. A mutualistic (beneficial to both partners) relationship that is not obligate, that is, the partners need not enter into an ecological "pact" for them to prosper and survive to reproduce.

fertilization. The penetration of the egg cell membrane by an individual sperm cell at time of conception.

floral reward. The diverse array of attractants, and often nutritious food present in flowers to invite and lengthen visits by floral visitors. The major substances used are pollen, nectar, floral oils and food bodies.

floral visitor. Any animal that visits a flower to find food, shelter, a mate, or a place to rest. Such visitors need not be pollinators.

fruit. A term used to describe a matured ovary, especially of seed-bearing plants. Fruits are more or less fleshy and a concentrated source of energy.

fruit set. Fruit is set by blossoms when the ovules are fertilized and the plant has enough energy and water reserves to develop and ripen the fruit. Fruit set is enhanced by pollinators.

gene pool. The alleles for all genes within a fairly interbreeding population of organisms drawn upon by plant breeders.

generalist. A pollinator that visits a wide variety of flowers for nectar and pollen during its lifetime. A generalist blossom is one that is quite open and can be visited and pollinated by unrelated groups of animals.

genetic variation. The various genes and their relative frequencies within a population of organisms.

hand pollination. The human pollination of flowers, usually crop plants or those growing in research plots, with fresh or stored pollen. Some endangered native plants now have to be pollinated by hand to set fruits and seeds.

honeyhunting. The ancient practice of raiding the colonies of social honeybees, or stingless bees, for honey, beeswax and larvae for human food and other purposes. Honeyhunting has been depicted in caves throughout the world and predates beekeeping.

hybridization. Reproduction between two related species that results in the formation of viable progeny usually intermediate in character between the parental types.

hymenoptera. The second largest order of insects which includes sawflies, bees, ants and solitary and social wasps. The name "membrane wing" refers to their two pairs of diaphanous wings.

inbreeding. Sexual reproduction that involves the interbreeding of closely related individual plants through self-pollination and backcrosses.

keystone mutualist. A plant or animal whose importance in a community is inordinately tied to other plants and animals. When removed from a system, keystone mutualists can cause a cascade of linked extinctions. Fig trees in the neotropics are an example.

lepidoptera. The insect order that contains butterflies and moths, insects with two pairs of wings covered by scales. Moths vastly outnumber and are more important pollinators than butterflies.

linked extinctions. Extinctions of plants or animals that may be "linked" in the sense that when one organism goes extinct, it may be living in a mutualistic relationship with others in the food web and the original extinction may cause other lifeforms to go extinct.

meliponiculture. The ritualized keeping of stingless bees (meliponines) by Mayan Indians in Mexico and Central America. The bees are usually kept in hollow logs and periodically raided to obtain honey and wax.

mess-and-soil pollination. A type of pollination usually occurring in primitive flowering plants and effected by beetles. The beetles blunder around the flowers chewing on floral parts, eating pollen and defecating.

migratory beekeeping. A form of beekeeping practiced in the United States and other countries with large beekeeping industries. Beekeepers use trucks to transport their colonies to "follow the bloom" and custom-pollinate agricultural crops.

monoecious. Literally "one house." A reproductive system in which both male and female blossoms are carried on the same plant – as in squashes, gourds and pumpkins.

mutualism. A type of symbiosis in which all partners derive benefits from the association.

nectar. A watery, floral secretion containing sugars, amino acids, lipids and antioxidants. Nectar varies greatly in its sugar concentration.

nectar corridor. A series of different plants offering abundant nectar seasonally along an annual migratory pathway –as in the case of the century plant and cactuses and bats.

nectar robber. A floral visitor that "burglarizes" blossoms by taking nectar through forceful entry and without pollinating.

nectary. A specialized region of floral tissue, usually at the base of the inner-most floral tube, where nectar is secreted. The nectar forms pools in this region and pollinators drink from it.

nut. A nut is a seed or fruit that is a concentrated source of oil.

obligatory outcrossing. A flowering plant species that, for reasons of physiological incompatibility, must receive and donate pollen in the form of cross-pollination. It cannot pollinate between flowers on the same plant. Greater levels of seed set are achieved with outcrossing, as well as increased genetic recombination.

obligate mutualism. A mutualistic relationship between partners who cannot survive outside the relationship.

oligolecty. The pollen-collecting behavior of certain solitary bees that specialize on a few related flowers for their pollen needs. Their floral constancy extends throughout the distributional range of their host plants, the same species which are used each year.

outcrossing. The chief means of reproduction of flowering plants. Such plants can only be fertilized by pollen from other plants.

ovary. The lower portion of the floral pistil containing the ovules that when fertilized will become the seeds in the fruits of flowering plants. Typically the surrounding tissue becomes the fruit or vegetable that people eat.

ovule. The structure in the female portion of the flower that becomes the seed.

petals. The showy, often colorful array of plant organs within flowers that have evolved as "billboards" and perfume dispensers to advertise their presence to pollinators and guide them to the hidden nectar deposits.

pistil. The female reproductive organ of a flower that is further subdivided into ovary, style and stigma.

plant/pollinator landscape. Describes a situation in which pollinators and their floral plant hosts have evolved in a mutualistic way over periods of time.

pollen. Microscopic particles in anther locules that contain the male sperm nuclei.

pollination. The process of moving pollen from the anthers of one flower to the stigma of another. Equally vital processes of fertilization and seed set follow from pollination. Pollination can be effected by abiotic means (wind and water) or biotic means (animals).

pollination ecology. The study of the ecological and evolutionary relationships involved in the pollination process.

pollination services. Pollination acts performed by all the various animals that dependably visit certain species of flowering plants.

pollination syndrome. An old concept dating back to the early works of Europeans suggesting that the floral visitors a flower receives (hummingbirds, bats, flies, butterflies, moths, bees, beetles) can be predicted from the flower’s suite of morphological characteristics and rewards.

pollinator. Any animal that not only visits a flowering plant but effects pollination, leading to fertilization and later fruit and seed set. Not all floral visitors are legitimate pollinators.

pollinator efficiency. A pollinator’s rate of foraging from flower to flower.

pollinator effectiveness. A pollinator’s rate of pollination or seed set.

pollinator-limited. A system in which pollinations are in short supply and thus limit the amount of fruits and seeds that can be produced in a local plant population.

polylecty. The pollen-collecting and feeding habits of social bees and certain solitary bees that routinely gather pollen from unrelated plant families and genera in one area over a long period of time. The European honeybee is one of the most polylectic species for its broad pollen diet.

reciprocal coevolution. The most extreme type of mutualism – each of the partners evolves with its evolutionary "dance partner." Neither species can live without the other and both have directed each other’s evolutionary trajectory.

scramble competition. A free-for-all competition in which competitors scramble for limited available food or resources.

seed set. Seed set occurs when fertilization is successful.

self-pollinated. Flowering plants that can set fully viable seeds when pollinated with their own pollen.

self-incompatible. Flowering plants that are incapable of pollinating themselves and rely on genetically distinct pollen from distant plants to form fruit and seed.

sequential mutualism. When plants growing in the same area overlap in blooming period and are pollinated by a group of coadapted mutualists.

social bee. Social bees are those that live together in a communal nest and often share foraging or nest duties. The highest form of sociality involves an overlap of generations such that the mother bee will share her nest with her offspring. Honeybees, bumblebees and certain sweat bees have overlapping generations with distinct worker, male and queen castes with a division of labor.

solitary bee. Most of the world’s 40,000 or so species of bees are solitary. Each female mates and then begins construction of underground nests that branch and end in smooth-walled cells. These cells are filled with a mixture of nectar and pollen that provide all the food for the young larvae to complete its development into an adult bee.

stamen. The male structure bearing the pollen grains in a flower.

stigma. The female part of the flower where pollen grains land and germinate, sending down pollen tubes and sex cells.

stingless bee. Group of social bees from the New World and Old World tropics that form large perennial nests and have well-established castes. Stingless bees defend their colonies with aggressive attacks including biting the intruding animal.

traplining. A feeding strategy in which certain birds and insects follow a "trapline" of blooming plants in a set order on a daily basis. These animals are familiar with the distribution and flowering status of plants on their trapline.

tripped flower. In certain legumes, such as alfalfa, floral parts are held shut until visited by a bee that forces the blossom open. This process often results in a sudden upswing of the anthers, dusting the underside of the bee. By observing the number of tripped and untripped blossoms in the field, farmers can tell if their crop is being adequately pollinated.

vector. Any biological or abiotic agent that carries something around in a directed fashion. In our case, pollinators "vector" or move pollen grains around the environment and from flower to flower.

vegetable. A term popularly used to include root crops (sweet potato), underground stems (potato), stems (asparagus), leaves (cabbage) or inflorescences (cauliflower).

References

Barth, Friedrich G. 1985. Insects and Flowers: The Biology of a Partnership. Princeton, New Jersey: Princeton University Press.

Buchmann, Stephen and Gary Paul Nabhan. 1996. The Forgotten Pollinators. Washington, D.C.: Island Press.

Crane, Eva. 1990. Bees and Beekeeping: Science, Practice and World Resources. Ithaca, NY: Cornell University Press.

Free, John B. 1993. Insect Pollination of Crops. London, England: Academic Press.

Kephart, Susan. 1999. Expedition Briefing: Oregon Wildflowers. Watertown, MA: Earthwatch Institute.

Kephart, Susan. Douglas’ Catchfly: Causes of Rarity in Plants. (Willamette University, 1998), slides.

Losey, John, et al. 1999. "Transgenic Pollen Harms Monarch Larvae." Nature 399:214.

Matheson, Andrew et al. 1996. The Conservation of Bees. London, England: Academic Press.

___. Chapter 5. "Ecological Bases of Conservation of Wild Bees." Josef Banaszak.

___. Chapter 6. "Aspects of Bee Diversity and Crop Pollination in the European Union." Ingrid H. Williams.

___. Chapter 10. "Competition Between Honey Bees and Native Bees in The Sonoran Desert and Other Global Bee Conservation Issues." Stephen L. Buchmann.

___. Chapter 12. "Toward an Ecological Perspective of Beekeeping." Evan A. Sugden.

___. Chapter 14. "African Honey Bees as Exotic Pollinators in French Guiana." David W. Roubik.

McGregor, S.E. 1999. "Insect Pollination of Cultivated Crops." Internet. http://gears.tuscon.ars.ag.gov.

Needham, Glen R. et al. 1988. Africanized Honey Bees and Bee Mites. West Sussex, England: Ellis Horwood Limited.

___. Chapter 1. "Africanized Bees, and Mites Parasitic on Bees, in Relation to World Beekeeping. Eva Crane.

___. Chapter 2. "Evolutionary Aspects of the Africanization of Honey-Bee Populations in the Americas." Thomas E. Rinderer.

___. Chapter 54. "Varroa Jacobsoni in Israel, 1984-1986." U. Gerson et al.

___. Chapter 67. "The Tracheal Mite of Honey Bees: A Crisis in Beekeeping." Mercedes Delfinado-Baker.

Proctor, Michael, Peter Yeo and Andrew Lack. 1996. The Natural History of Pollination. Portland, Oregon: Timber Press.

Real, Leslie (ed.). 1993. Pollination Biology. Orlando, Florida: Academic Press Inc.

___. Chapter 2. "An Outline of the History of Anthecology or Pollination Biology." Herbert Baker.

___. Chapter 3. "The Role of Insect Pollination in the Evolution of the Angiosperms." William L. Crepet.

___. Chapter 4. "Pollinator-Plant Interactions and the Evolution of Breeding Systems." Robert Wyatt.

___. Chapter 5. "Wind Pollination: Some Ecological and Evolutionary Perspectives." Donald R. Whitehead.

___. Chapter 9. "Foraging Behavior of Pollinators." Keith D. Waddington.

___. Chapter 10. "The Adaptive Nature of Floral Traits: Ideas and Evidence." Nickolas M. Waser.

___. Chapter 12. "Competition and Facilitation among Plants for Pollination." Beverly Rathcke.

Spivak, Marla. 1999. Interview by author, University of Minnesota, Minneapolis, Minnesota, August 24, 1999.

Tilman, David, et al. 1994. "Habitat Destruction and the Extinction Debt." Nature 371:65-66.

United Nations Food and Agriculture Organization of the United Nations (FAO). 1998. The State of the World’s Plant Genetic Resources for Food and Agriculture. Rome, Italy: FAO.

Other References

Casper, Brenda and Richard Niesenbaum. 1993. "Pollen versus Resource Limination in Seed Production: A Reconsideration." Current Science 65(3):210-214.

Dafni, A. 1992. Pollination Ecology: A Practical Approach. New York: Oxford University Press.

Gaines, M.S. et al. 1997. "The Effect of Habitat Fragmentation on the Genetic Structure of Small Mammal Populations." Journal of Hereditary AGA Symposium Issue: Genetics of Fragmented Populations July-August 1997.

Nason, J.D. and J.L. Hanrick. 1997. "Reproductive and Genetic Consequences of Forest Fragmentation: Two Case Studies of Neotropical Trees." Journal of Hereditary AGA Symposium Issue: Genetics of Fragmented Populations July-August 1997.

Rost, Thomas L. et al. 1998. Plant Biology. Belmont, California: Wadswoth Publishing Company.

Snow, Allison. 1982. "Pollination Intensity and Potential Seed Set in Passiflora vitifolia." Oecologia 55:231-237.

Appendices

Major Crop Pollinators

Plant Pollinator Landscapes

Pollinator Classes

Worlds Staple Foods