POLLINATORS, ROLE OF

David W. Inouye University of Maryland

I. What Is Pollination? Adaptations to subterranean life often include reduced II. The Diversity of Pollinators metabolism, longer life spans, reduced aggressive III. Coevolutionary History of Plants and Pollinators behavior, elongation of appendages, and reduction of IV. Pollinators in Natural Systems eyes and pigment. Eye and pigment loss (evolution in V. Pollinators in Agriculture and Their Economic reverse) are especially common and likely result from a Value combination of natural selection and genetic drift. VI. Conservation Biology and Pollination Colonization of subterranean environments may be active or passive (e.g., stranding). After isolation, migration is often highly restricted and levels of ende- mism are very high. Species stranded by the regression of marine seas often leave a record of ancient events, THE SUBTERRANEAN DOMAIN includes both air- for example, the pre-Triassic breakup of Pangaea. and water-filled spaces, both large (e.g., caves) and Species richness is especially high in the Dinaric karst small (e.g., gravel aquifers). They share an absence of of the western Balkans, probably because of the light, limited productivity, biological activity, and extensive karst development and because drying events reduced environmental variability. Major subterranean in the Mediterranean may have forced animals into aquatic habitats include percolating water (epikarst), subterranean habitats. For troglobionts, diversity is cave streams, permanent groundwater lakes, and highest a mid-latitudes in the Northern Hemisphere. interstitial habitats, both shallow and deep. Major This ridge of high diversity corresponds to the zone of subterranean terrestrial habitats include air-filled maximum surface terrestrial productivity, the ultimate caves, air-filled cavities in epikarst, cracks and fissures source of energy in caves. A largely unsampled habitat in rock and debris, and deep soil. Except in rare cases that is particular diverse in those few areas where it has there is little or no primary productivity in the sub- been sampled is epikarst. Protection of subterranean terranean domain, and most organic matter is brought fauna requires the protection of surface riparian habitat, in by the action of water or in the case of terrestrial protection excessive water draw-down for aquatic cave habitats, the results (especially fecal material) of habitats, and protection of the flow of energy in and the movement of animals in and out of caves. Some out of cave entrances in the case of terrestrial fauna. systems, especially deep phreatic aquifers and a few caves, have chemoautotrophic production. Some plants and animals typically live at cave entrances I. WHAT IS POLLINATION? and some species (especially bats) spend part of their life cycle in caves. Obligate subterranean dwellers Pollination is the transfer of a pollen grain (male (terrestrial troglobionts and aquatic stygobionts) gametophyte) to a flower’s stigma (receptive surface of include many Crustacea (especially Amphipoda, the female reproductive organ), where it may germin- Copepoda, and Isopoda), Arachnida, Diplopoda, and ate, grow through the style, and fertilize an ovule to Insecta (especially Coleoptera and Collembola). produce a seed. This transfer can be accomplished by

Encyclopedia of Biodiversity Copyright & 2007 Elsevier Inc. All rights of reproduction in any form reserved. 1 2 ______POLLINATORS, ROLE OF______abiotic agents such as wind and water, but the majority and at least one reptile have been recorded as polli- of pollination is effected by animal pollinators seeking nators. Table I shows a list of pollinator classes for the nutritional rewards such as pollen and nectar, or world’s wild flowering plants (the angiosperms; sometimes other resources such as floral perfumes, B240,000 species), and estimates of the number of oils, or resins. The relationship between the plants and species in each. Much work remains to be done to pollinators is commonly assumed to be mutualistic, confirm the activities of these taxa as pollinators, but with the plants benefiting from the transfer of pollen these numbers are the first estimates available. and the pollinators receiving a nutritional or other re- ward, but there are also instances in which the plants appear to provide no reward and cases in which polli- A. Invertebrate Pollinators nators may also be seed predators. This rich diversity Although flower visitation has been observed by species of relationships has been fertile ground for investigat- from at least 16 orders of insects, only four of them ion by pollination biologists for hundreds of years. include many species that regularly pollinate flowers The importance of pollination in agriculture has also and that seem to have been involved in coevolutionary been a powerful stimulus for the study of plants and interactions with plants. These are the beetles (Cole- pollinators. optera), flies (Diptera), butterflies and moths (Lepid- There is an important distinction to be made be- optera), and ants, bees, and wasps (Hymenoptera). In tween ‘‘flower visitor’’ and ‘‘pollinator.’’ Visitors to addition, the thrips (Thysanoptera) include some flowers (anthophilous animals) cannot be assumed to pollen-eating species that may be pollinators, some be pollinators, as in reality they may be nectar or pol- stoneflies (Plecoptera) and true bugs (Hemiptera) will len thieves which, owing to a mismatch in morphology visit flowers and eat pollen and nectar, and some or an unusual behavior, do not pollinate. For example, lacewing (Neuroptera), scorpionfly (Mecoptera), and ‘‘base workers,’’ or insects that remove nectar from caddisfly (Trichoptera) species eat nectar. Additional between the petals of a flower with an unfused corolla, work is needed to confirm whether most of these lesser- or insects too small to contact the reproductive parts known flower visitors are indeed pollinators. of a flower, would not be pollinators despite the fact that they may spend a lot of time harvesting nectar. However, their activities may be detrimental to the 1. Beetles flowers’ pollination, as pollinators may be deterred by Beetles have been abundant since at least the finding no nectar in flowers already visited by nectar Mesozoic, and it is likely that some of them have thieves. Similarly, a small insect that collects pollen from anthers but never contacts stigmas is an example of a pollen thief that does not pollinate. Simple ex- TABLE I periments, such as collecting stigmas of flowers to Pollinator classes for the world’s wild flowering plants (B240,000 confirm pollen deposition, or the observation of trans- angiosperm species). The numbers are ‘‘the number of species com- fer of a pollinium (a packet of pollen, characteristic of prising the invertebrate and vertebrate genera, families, and orders flowers in the Orchidaceae or Asclepiadaceae), can in which there are more known effective pollinators than there are help to distinguish between visitors and pollinators. pollen or nectar cheaters, robbers, or avoiders’’ Unfortunately, many animals observed on flowers are Pollination categories Estimated pollinator taxa probably best categorized as flower visitors because Wind (abiotic) 20,000 this kind of confirmation of pollination has not been Water 150 conducted. It is surprising that much remains to be All insects 289,166 learned about the pollinators of many important agri- Bees 40,000 cultural species, in addition to other plants. Hymenoptera (bees and wasps) 43,295 Lepidoptera (butterflies and moths) 19,310 Diptera (flies) 14,126 Coleoptera (beetles) 211,935 Thrips 500 II. THE DIVERSITY OF POLLINATORS All vertebrates 1,221 Birds 923 The list of species of animals that serve as pollinators Bats 165 Mammals other than bats 133 is long and diverse. The largest group of pollinators is insects, but both flying and nonflying mammals, birds, Reproduced from Nabhan and Buchmann (1997), with permission. ______POLLINATORS, ROLE OF______3 been flower visitors since the origin of the earliest sapromyophily. The basis for attraction of the flies is angiosperms. For example, the current association of floral fragrances that mimic rotting flesh or dung, and beetle pollination (cantharophily) with primitive typically the flies do not receive any nutritional reward woody angiosperms (Magnolia is an example) proba- for their visits. Some of the most spectacular flowers in bly dates back to the evolutionary origins of both the world are fly pollinated, such as the inflorescence groups. Beetle pollination is considered to be the most of the titan lily (Amorphophallus, not really a lily), primitive type of pollination by animals, and is not which can reach 10 ft tall and is called the corpse lily very important in cool temperate regions. It is most for its fearsome odor; it attracts and is pollinated by common in the moist tropics, and to a lesser degree in flies. Another example is the largest flower in the arid areas. Beetles constitute the largest order of in- world, Rafflesia, found in Borneo, which can reach a sects, and some of this diversity is thought to have meter in diameter and smells like rotting meat. arisen through the same evolutionary radiation of Blood-feeding Diptera such as mosquitoes and biting flowers and insects during the Tertiary that led to the flies (Tabanidae; horseflies, deerflies) are also some- origin of the other major orders of flower-visiting times pollinators, attracted to flowers by the nectar insects. they offer. A tabanid fly in South Africa that visits flowers with long corolla tubes has a proboscis length of up to 35 mm, while another species in the 2. Flies Nemestrinidae has a proboscis up to 57 mm (and flies Flies are probably the second most common order of with the proboscis folded under its body and sticking flower visitors (after Hymenoptera). Fly visitors from at out behind). least 71 families of Diptera to flowers in 137 plant families have been recorded in the literature (compila- tion by Inouye). The families Syrphidae (hoverflies), 3. Butterflies and Moths Bombyliidae (bee flies), and the Muscidae are especially The Lepidoptera (butterflies and moths), as a conse- common as flower visitors. In tropical areas, the diver- quence of their two distinct lifestyles as primarily sity of flower-visiting Diptera can rival or exceed that of herbivorous larvae and commonly flower-visiting the Hymenoptera. For example, 4856 species of Diptera adults, have dichotomous relationships with plants. are recorded from Australasia from flower-visiting In at least one case, the pollination of yucca, the act of families, compared with B2570 bees (superfamily pollination by yucca moths, is accompanied by ovi- Apoidea), while for the Neotropics the estimates are position and the larval moths are seed predators. 42940 species for Diptera and 5630 species for bees Although not all Lepidoptera feed as adults, most, if (Roubik, 1995). In some parts of the world, including not all, do depend on nectar as a source of both sugars the Faroe Islands, New Zealand, and Australia, where and amino acids. Some of the longest lived of all but- bees are nonexistent or relatively rare, flies have filled terflies, the neo-tropical Heliconius species, also feed that ecological niche of pollinators. regularly on pollen by collecting it on their proboscis Pollination by flies (myophily) is economically and regurgitating nectar on the pollen mass to leach important; in tropical areas flies are the primary polli- out amino acids. Female butterflies of some species are nators of cacao and also pollinate mango, cashew, and dependent upon the amino acids and sugars they col- tea. Roubik (1995) lists pollinators of 785 species of lect in nectar to provide nutrients needed for making cultivated plants in the tropics, and 26–31 of these eggs, so the more nectar they can collect the more eggs plants are apparently pollinated only by flies, 32–33 by they can lay (Boggs and Ross, 1993). The floral re- flies as the primary pollinators, and 87–101 more by wards sought by Lepidoptera are not always nutri- flies as secondary pollinators. In Europe, flies are used tional; some species are attracted to flowers by the commercially to pollinate protected crops of onion, pyrrolizidine alkaloids that they produce, which the chive, carrot, strawberry, and blackberry. In both male butterflies require for the production of phero- tropical and temperate areas, flies appear to be more mones, for mating success, and for the establishment important as pollinators than has been generally of multispecies leks. Lepidoptera, as agents of natural recognized, and there is need for additional research selection, may be responsible for much of the diversity on them. of defensive chemicals in plants as well as diversity in In addition to the more specialized flower- flowers and the rewards they offer. visiting flies, carrion and dung flies are pollinators of Two families of moths stand out as pollinators. some plants, in a category of pollination called One is the hawk moths (Sphingidae; also called 4 ______POLLINATORS, ROLE OF______sphinx moths), and the other is the noctuid moths been studied in part because of interest in attracting (Noctuidae; the largest family in the order Lepidop- and sustaining populations of parasitoid wasps (which tera). The hawk moths are strong and agile fliers that prey upon pest insects) in agricultural situations. But maintain very high body temperatures (e.g., as high predatory and social wasps have also been recorded as as 461C) while in flight. Some diurnal species are flower visitors and a few species of plants are special- easily mistaken for hummingbirds (e.g., the European ized for pollination by pseudocopulation by male hummingbird hawk moth, Macroglossum stellatarum). wasps (see Section IV.B.2). Some of the most special- Some hawk moths are migratory, and (in successive ized relationships between plants and pollinators are generations) may move hundreds of kilometers those between species of figs and the wasps that pol- during a summer in North America. Hawk moths in- linate them; many of those relationships are reported clude the pollinators with the longest known tongues; to involve single species of wasps pollinating each fig most of these extraordinary species are found in species. The wasp larvae develop in seeds produced by Madagascar. Darwin measured nectar spurs in some the pollinating activity of their mothers. orchids from Madagascar that were 29 cm long, and There are fewer species of bees than beetles, but a concluded that there must be moths there that have much higher proportion of bees are pollinators than proboscis lengths of the same length. Forty years after are beetles. Almost all species of bees, both adults and his prediction, a hawk moth with a proboscis that larvae, are dependent on flowers for pollen and nectar reaches over 24 cm in some individuals was found as nutritional resources, and of all the insect bees are and given the name Xanthopan morgani praedicta. the most highly adapted for flower visitation and There is actually a large guild of long-tongued hawk pollination. Their behavior, morphology, and senses of moths and flowers with matching corolla lengths in vision and smell all appear to be adapted for finding Madagascar. and collecting floral resources. For example, the tri- Some noctuid moths are long-distance migrants, chromatic color vision of bumblebees and honeybees flying distances as far as 1600 km. One species is re- includes ultraviolet, which allows them to see the ported to travel as much as 1000 km in a day when ultraviolet reflectance patterns that many flowers use migrating from the Baltic States to Britain. This as nectar guides or a petal color. Humans cannot see presents the opportunity for some very long-distance these patterns without the help of cameras. gene flow on the part of their food plants! Some spe- Although pollen (primarily for feeding larval bees) cies migrate vertically, moving up in altitude some and nectar (both a larval and adult resource) are the time during the year to avoid unfavorable seasonal most common resources collected by bees, some flow- weather. Before these migrations, the moths may store ers offer oil as a reward. The oil is collected by bees in substantial quantities of fat, and at least one such spe- the family Anthophoridae; females of these species cies was an important part of human diets; the bogong have absorbent brushes for holding the oil and sharp moth (Agrostis infusa) was collected while estivating in edges on their legs that are used to squeeze the oil out the Snowy Mountains by aboriginal Australians. so that it can be mixed with pollen as food for larvae. Some bees collect resin as a floral reward, which they then use in nest construction. 4. Ants, Sawflies, Wasps, and Bees Pollination by bees (melittophily) is very important The Hymenoptera (ants, sawflies, wasps, and bees) are for agriculture (see Section V). The social bees are the the largest and most diverse group of pollinators. Ants best-known crop pollinators, and are the species most are only rarely recorded as pollinators, although they commonly managed for pollination or honey produc- are not uncommon as flower visitors collecting nectar. tion. These include honeybees (Apis), bumblebees One suggestion for why there are not more species of (Bombus), and stingless bees (Trigona). The presence plants adapted for pollination by ants is that the anti- of large quantities of honey (concentrated nectar), biotic and other secretions that ants have on their pollen, and larvae makes social bee nests an attractive exoskeletons are detrimental to pollen survivorship target for insects and vertebrates that prey upon nests and growth. Sawflies are more common as pollinators. and adult bees. Bee-eaters and honey guides are two They have herbivorous larvae, and in some cases the examples of Old World birds that specialize on such adults restrict their flower visits to the larval host resources, and honey and wax are also attractive re- plant. The adults may also eat flower parts in addition sources collected from wild colonies by humans in to nectar and pollen. Flower visitation by wasps has some parts of the world. ______POLLINATORS, ROLE OF______5

B. Vertebrate Pollinators III. COEVOLUTIONARY HISTORY OF 1. Mammals PLANTS AND POLLINATORS Although invertebrates are the most common pollina- The ‘‘abominable mystery’’ that Darwin referred to, the tors, mammals, birds, and lizards have also been origin and relationships among flowering plants, is still documented as pollinators. Mammalian pollinators being revealed. Beetle pollination is thought to be the include both bats, some of which primarily eat nectar primitive condition in flowering plants, but by 100 Ma and pollen, and nonflying species such as some Aus- butterflies and moths had joined beetles as important tralian marsupials. Most bat pollination occurs in the pollinators. Recently discovered fossil evidence indi- tropics, but some migratory bats are important poll- cates that the origin of the angiosperms (flowering inators in temperate North America to about 301N. In plants) may date back as far as the Late Jurassic, the Old World species of the family Pteropidae, fruit suggesting that the origin of the coevolutionary rela- bats, are important pollinators, while in the New tionship between flowers and pollinators may also be World flower-visiting bats are confined to the family older than previously thought. Much of the tremendous Phyllostomidae. Although pollination by bats (chir- biodiversity found in the flowering plants is thought to opterophily) is geographically widespread, the other have arisen through evolutionary interactions with poll- mammalian pollinators are more restricted and less inators, and certainly much of it is maintained through common as pollinators, including lemurs in Madagas- their flower-visiting activities that result in the produc- car and several species of Australian marsupials such tion of seeds. The remarkable diversity of flower size, as sugar gliders, honey possums, and some marsupial shape, odor, rewards, color, and pollination mechanisms mice. There are scattered reports of other mammals, is the result of these coevolutionary relationships. including mice and giraffes, that may serve as polli- nators in unusual cases. Vertebrate taxa other than mammals or birds are only rarely reported as pollina- tors; there are a few reports of lizard pollinators on IV. POLLINATORS IN NATURAL SYSTEMS islands. A. Obligate and Facultative Mutualisms The relationships between plants and pollinators range 2. Birds from obligate to facultative in nature. While one study Bird pollination (ornithophily) is common in many in Brazil found that 43% of the plants studied were parts of the world. Several families of birds are pri- visited by only a single species of pollinator, other marily nectarivorous and undoubtedly include impor- studies have found tens of visitor species to a single tant pollinators. These include the hummingbirds plant species. In only a few cases have researchers (Trochilidae; New World), honeyeaters (Meliphagidae; quantified the relative importance of different species Australia, New Zealand, and parts of Asia), sunbirds in cases with multiple pollinators of a single plant (Nectariniidae; Africa and Southwest Asia to the Phil- species. A common finding of multiyear studies is ippines), sugarbirds (Promeropidae; South Africa), variation, both temporal and spatial, in abundance of flowerpeckers (Dicaeidae; Asia and Australasia), and these different groups of pollinators. The visitors to a Hawaiian honeycreepers (Drepanididae; Hawaii). single plant species can include diverse taxonomic Other families that include some nectarivores or scat- groups, for example, both vertebrate and invertebrate tered records of flower visitation include the Thrau- pollinators (e.g., hummingbirds and bumblebees). By pidae (honeycreepers and some tanagers; New World), having several groups of potential pollinators, it is Icteridae (orioles; New World), Zosteropidae (white- more likely that these plants will not suffer from pol- eyes; Africa, Asia, and Australia), and Psittacidae len limitation, or a shortage of pollination; if one (lorikeets and hanging parrots; Southeast Asia and group of pollinators is unusually low in abundance at a Australasia). A number of flower-visiting birds are re- particular site or in a particular year, it is likely that cently extinct in the South Pacific islands, but in at another group will not be. Thus it can be important to least one case an introduced species has taken over the have a diversity of pollinators available. role of a pollinator for some of the endemic plants that The obligate nature of some plant–pollinator rela- were pollinated by the extinct birds. tionships extends also to pollinators, as some insects 6 ______POLLINATORS, ROLE OF______appear to visit flowers of only a single species of plant. species of birds (Diglossa, the flower-piercers) and In such cases, there must be a good match in the pheno- bees (Xylocopa, carpenter bees; some short-tongued logy of life cycles of both plant and insect to ensure Bombus, or bumblebees, and some stingless bees) may success for both partners, and one concern about global obtain most of their nectar in this fashion. Once these climate change is the potential for such phenological primary nectar robbers have created holes, other relationships to become mismatched. There are similar species may learn to use them, as secondary robbers. cases of plant species visited by only a single species of Typically, these flower species that are robbed have pollinator. Although a plant or pollinator may thus long corollas, and the nectar robbers do not have have an obligate relationship with a single partner, the mouthparts long enough to obtain the nectar without partner may be involved in relationships with multiple robbing. Although biologists at least as far back as species. Darwin have assumed that nectar robbing would have Although we assume that most plant–pollinator re- a significant negative influence on the robbed plants, lationships are mutualistic in nature, some examples more recent evidence suggests that in fact most insect appear to involve a mixture of positive and negative nectar robbers that have been studied have either a interactions from at least the plant’s perspective. beneficial or neutral effect on the plants. In the process Several studies have demonstrated seed predation or of moving around on the flowers, or perhaps while other forms of herbivory by insects that may also serve collecting pollen from the same flowers, robbing as pollinators. These examples include beetles and insects may effect pollination. Even in the absence of palms, moths and yuccas, wasps and figs, as well as such a direct effect, robbers may indirectly increase the flies and moths and some flowers that they pollinate. fitness of plants they rob by influencing the behavior of Some of these relationships (e.g., yucca flowers and legitimate pollinators. The reduced quantity of nectar their moths) can be farther complicated by the pres- in a robbed flower may induce a legitimate pollinator ence of closely related species of insects that are to visit more flowers or to fly greater distances between herbivores but not pollinators. Much detailed study is flowers, thereby increasing gene flow. needed to dissect the complicated interactions in such relationships. 2. Pollination by Deception There is no doubt that long-lived or highly mobile Cheating in pollination biology is not restricted to the pollinators must interact with a large number of plants, pollinators. Plants also provide fascinating examples of as their life spans or travels extend beyond the temporal deception, attracting some pollinators by falsely adver- or spatial availability of single plant species. Thus a tising opportunities for feeding or sex. The orchid group of plant species, even if they are not sympatric, family is perhaps the best known in this regard, as could be considered mutualists if in concert they many species of orchids have flowers with no nectar, sustain and share a particular pollinator. This kind of and pollen that is not accessible or attractive to polli- multispecies relationship has significant conservation nators. In such species, it appears that the pollinators implications, as it may be necessary to conserve plant gain nothing from visiting (and pollinating), and species flowering widely separated in time and space to quickly learn to avoid the flowers. Other orchids have conserve a (for example, migratory) pollinator. This flowers that, in both morphology and odor (produc- idea has led to the concept of a ‘‘nectar corridor’’ to tion of insect sex pheromones), resemble female in- sustain long-distance migratory pollinators. Hum- sects well enough that males attempt to copulate with mingbirds are an example of a species that requires them and in the process pollinate (pseudocopulation). nectar resources along a long migratory route; many North American species overwinter in Mexico but reproduce during the summer as far north as Alaska. V. POLLINATORS IN AGRICULTURE AND THEIR ECONOMIC VALUE B. Cheaters in Pollination Our knowledge of the pollination biology of crop spe- 1. Pollen and Nectar Robbers cies is surprisingly sparse. For example, the pollina- The nutritional rewards that pollinators find in flow- tion requirements of about one-third of the crop ers, pollen, and nectar are sometimes harvested by species grown in the European Union are still un- flower visitors that may pierce or bite holes in the known. These plants include at least 264 species that flowers to obtain the resources ‘‘illegitimately.’’ Some are cultivated as crops, or gathered from the wild, for ______POLLINATORS, ROLE OF______7 human and/or livestock food, or for the essential oils anywhere specifically for pollination was the introduc- they contain. The best-known pollinators of cultivated tion of European bumblebees to New Zealand in 1885 food plants are honeybees, which have been widely (to pollinate introduced clover for the introduced cattle), introduced around the world (see Section VI). and subsequently they were also introduced to Australia. However, honeybee populations in the United States The second successful introduction of a pollinator was a have been decimated in recent years by the introduc- fig-pollinating wasp (Blastophaga psenes) into California tion of two species of parasitic mites, and are also in 1899. being threatened by introduction of a hive beetle. Most In these cases, the incentive for introducing bees or feral colonies of honeybees in the United States have wasps was for the pollination of introduced species of disappeared since the arrival of the Varroa and tracheal plants that were not attractive to or could not be mites in the 1980s, and the number of managed col- pollinated by native pollinators (e.g., clover in New onies has declined to less than half of its peak. This Zealand and figs in California). More recently, interna- decline has resulted in a growing reliance on and ap- tional transport of bumblebees has been the result of preciation of the roles of other, native, species in the their use in pollination of greenhouse crops, especially United States and elsewhere as pollinators of crops. tomatoes. In the 1980s, techniques were developed for The rapid growth of the almond industry in the year-round commercial-scale propagation of bum- California around the beginning of the twenty-first blebee colonies (which normally have an annual life century has had a significant impact on commercial cycle of a few months). Commercially produced colo- beekeeping of honeybees. Almonds require pollination nies of bumblebees have now largely replaced the to produce fruit, and the value of the crop is so high tedious hand pollination of tomato flowers with elec- that almond growers are willing to pay significant fees tronic vibrators (tomato flowers produce no nectar, (e.g., B$136 per colony in 2006) for use of the bees but are visited by bees that ‘‘buzz’’ the flowers to release during the few weeks of flowering. Beekeepers from as pollen from poricidal anthers to collect it for feeding far away as Florida have moved bees to California to to their larvae, and in this process they pollinate the take advantage of these fees, creating shortages for flowers) and the use of chemical sprays to induce some other parts of the country. fruit set. These problems with honeybee availability have In the early 1990s, a European species of bumblebee also prompted some attempts to quantify the economic (Bombus terrestris) was introduced to Japan for use in value of pollination services provided by both greenhouse pollination; it has subsequently escaped managed and wild pollinators. A recent model esti- and is now established in the wild. Although an effort mates that US consumers realize $1.6–5.7 billion in is being made to exterminate the introduced species annual social gains that would be lost if honeybee in the wild (and to develop native species for use in services for 62 crops were reduced. The potential value greenhouse pollination), it is likely to be unsuccessful. of nonhoneybee pollinators in the US agricultural The phenomenon of ‘‘pathogen spillover’’ has been economy can be estimated at $4.1–6.7 billion each documented recently for bumblebees, with wild bees year. An estimate of the global value of pollination found close to greenhouses having a higher incidence services has been placed a $117 billion/yr. of disease than those further away; presumably, this results from contact with infected commercial bees that are foraging outside the greenhouse. There is some A. Introduced Species of Pollinators suspicion that the loss of a native North Ameri- can bumblebee species (Bombus occidentalis) in much Undoubtedly, the largest-scale introduction of pollinators of its former range along the west coast may be a con- has been the global traffic in the European honeybee sequence of disease or parasites introduced by the (Apis mellifera). Such continental-scale introductions cultivation of colonies in Europe from wild-caught have a long history. For example, European colonists queens that were then reintroduced to the United in North America imported honeybees as early as 1641. States (having acquired the parasites or diseases during This species went on to establish feral colonies over rearing in Europe). much of North America and, probably through subse- Other species of pollinators have also been intro- quent introduction, to much of the neotropics. They duced. The wasp pollinators of figs have been intro- were also introduced to Australia. Probably, the second duced to New Zealand and the United States, largest introduction of pollinators has been the spread where they pollinate naturalized figs. The Japanese of bumblebees (Bombus). The first introduction of bees white-eye, an introduced passerine in Hawaii, has 8 ______POLLINATORS, ROLE OF______taken over the role of a pollinator of two native plants difficult for them to locate and visit patches of flowers that lost their original pollinator to extinction. An that are isolated by areas of different, perhaps non- Asian bee is now the primary pollinator of alfalfa plants preferred, habitat. But even winged pollinators may be grown for seed production in the United States, and a reluctant to leave a preferred habitat, such as undis- Japanese bee is used in the United States and Canada turbed forest, to fly across a newly created pasture to for pollination of apples. The alfalfa leaf-cutting bee another patch of forest. If the fragments are small (Megachile rotundata) was introduced to North Amer- enough to affect the size of pollinator populations, ica to pollinate introduced alfalfa, and has also been there may be negative genetic consequences for the introduced recently to Australia. Every year, millions of smaller populations. these bees are imported to the United States from Modern agriculture can have a variety of negative Canada, where they are raised and then shipped as impacts on pollinators. The creation of large fields that pupae. are disturbed regularly by plowing can prevent ground-nesting bees from establishing populations, and if only a single plant species is available there may B. Pollinators as Vectors and Victims of not be enough pollen and nectar resources to support Engineered Genes the life cycle of a pollinator species. The use of pes- ticides to control agricultural pests can have a negative As genetic engineering of crop plants has become more impact on pollinators, and herbicides may remove common, and as these crops are approved for cultivat- species that could provide resources for the pollina- ion in the field, concerns have arisen about the po- tors. Pesticide use in nonagricultural areas, such as tential for gene flow through pollen transport between spraying of large tracts of forest to control lepidopte- the engineered genomes and wild plants. One ran herbivores, has also been shown to have strong management tool to prevent, or at least minimize, negative impacts on nontarget pollinator populations. this potential is to plant a buffer zone of unengineered The introduction of exotic plants, such as weedy plants around a field of engineered plants in hopes of plants, could have potential implications for the pol- intercepting pollinators carrying pollen before they lination of native plants. If the exotics are close re- can visit related native plants. latives to native species, there is the potential for There is also the potential for pollinators to be hybridization. And if the exotics are prolific producers victims of engineered genes. For example, laboratory of nectar or pollen, they may draw pollinators away studies of monarch butterfly caterpillars showed that if from native species that may then suffer a deficit in they eat significant quantities of corn pollen from seed production. The potential for these kinds of con- plants engineered to have the Bacillus thuringiensis sequences is not yet well understood, but this area is (BT) toxin in their leaves, it can kill them. Corn is beginning to attract attention from researchers. wind pollinated, and a likely scenario is that large The ecological consequences of widespread intro- quantities of corn pollen could be distributed onto ductions of A. mellifera and Bombus for native plants leaves of milkweed plants at the margins of cornfields. and pollinators are not well known because of a lack of The potential for this to have detrimental effects on the data from before the introductions. We can speculate monarch butterfly and other herbivores remains to be that the introduction of honeybees to North America studied but may not be as serious as was first feared. may have had significant consequences for species of bumblebees that have the same proboscis length, be- cause the perennial honeybee colonies have many VI. CONSERVATION BIOLOGY AND more workers than the annual bumblebee colonies. POLLINATION The spread of A. mellifera scutellata, the African sub- species (‘‘Africanized honeybees’’), from its point of A. Threats to Plant–Pollinator Mutualisms release in Brazil to as far north as the United States was much more recent and has provided opportunity for Pollinators now face a large variety of threats of an- some studies of their impact on native neotropical thropogenic origin. These include habitat fragmentat- pollinators (relatively minor, it appears). ion, a variety of effects of agriculture, pesticides, and Species from every major group of pollinators, herbicides, and the introduction of both pollinators invertebrate and vertebrate, have been classified as and plants. Fragmentation of habitats is likely to affect endangered, and recent extinctions have been docu- nonflying pollinators most strongly, as it may be mented for others. Thus, pollinators are just as ______POLLINATORS, ROLE OF______9 susceptible to the current human-induced mass extinc- pollination and pollinators remains to be learned and tion as any other group of organisms. it remains to be seen how many of these species can be conserved. B. Potential Management Solutions See Also the Following Articles A first step in solving problems in the conservation of plant–pollinator relationships is gathering information, EXTINCTION, CAUSES OF  EXTINCTION, RATES OF  FOREST both about the nature of the relationships and the CANOPIES, PLANT DIVERSITY  MASS EXTINCTIONS, NOTABLE EXAMPLES OF problems they face. Probably, the best way to conserve pollinators is to preserve habitat that includes their food plants and nest sites. Given that the growing human population is resulting in rapid habitat destruction, the Bibliography establishment of protected areas is an important con- Boggs, C. L., and Ross, C. L. (1993). The effect of adult food limi- servation tool. In agricultural situations, management tation on life history traits in Speyeria mormonia (Lepidoptera: techniques as simple as changing the timing of pesticide Nymphalidae). Ecology 74, 433–441. Buchmann, S. L., and Nabhan, G. P.(1996). The Forgotten Pollinators. application, leaving buffer zones around fields where Island Press, Washington, DC. bees can nest and food plants can grow, or providing Dafni, A. (1992). Pollination Ecology: A Practical Approach. IRL/OUP, suitable artificial nesting sites can make a significant Oxford. difference. Domestication of wild bees by providing and Faegri, K., and van der Pijl, L. (1979). The Principles of Pollination managing nest sites may also play a role in their main- Ecology, 3rd ed. Pergamon Press, Oxford. Grant, V., and Grant, K. A. (1965). Flower Pollination in the Phlox tenance in agricultural situations. Family. Columbia University Press, New York. If pollinators are locally extinct, it may be possible Jones, C. E., and Little, R. J. (Eds.) (1983). Handbook of Experimental to reintroduce them once the factors that caused the Pollination Biology. Scientific and Academic Editions, New York. original extinction are addressed. If the species is Kearns, C. A., and Inouye, D. W. (1993). Techniques for Pollination globally extinct, plants that were dependent on that Biologists. University Press of Colorado, Niwot, CO. Kearns, C. A., Inouye, D. W., and Waser, N. M. (1998). Endangered pollinator could be maintained by hand pollination, or mutualisms: The conservation biology of plant–pollinator inter- by the introduction of a suitable replacement. Al- actions. Annu. Rev. Ecol. Syst. 29, 83–112. though the bird was not introduced for that purpose, Matheson, A., Buchmann, S. L., O’Toole, C., Westrich, P., and Will- the presence of the Japanese white-eye in Hawaii has iams, I. H. (Eds.) (1996). The Conservation of Bees. Academic had the effect of replacing an extinct endemic avian Press, New York. Nabhan, G. P., and Buchmann, S. L. (1997). Services provided by pollinator. Another species of plant in Hawaii that lost pollinators. In Nature’s Services. Societal Dependence on Natural its native pollinator is being maintained by hand pol- Ecosystems (G. C. Daily, Ed.), chapter 8, pp. 133–150. Island lination. Removal of introduced pollinators, such as Press, Washington, DC. the honeybee, may also help to preserve populations of Proctor, M., Yeo, P., and Lack, A. (1996). The Natural History of native pollinators. Pollination. Timber Press, Portland. Real, L. (1983). Pollination Biology. Academic Press, Orlando. We have taken some important steps toward con- Roubik, D. W. (Ed.) (1995). Pollination of cultivated plants in the servation of pollinators and thus the relationships they tropics. Agricultural Services Bulletin #118. Food and Agricul- have with plants. But much basic knowledge about ture Organization of the United Nations, Rome.