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,