Pollinator economics

Most pollinators visit flowers to gather food. In general, foraging involves economic principles whereby a resource's utility depends ultimately on its relative contribution to the forager's fitness. However, animals probably cannot evaluate the fitness consequences of different foraging options; rather, they must assess opportunities based on the proximate benefits and costs associated with current physiological and ecological conditions. Often, the behavior of experienced feeding animals maximizes a single variable, or foraging currency, that integrates foraging benefits and costs (Stephens & Krebs 1986). Such behavior bears diverse consequences for pollination, because it affects a pollinator's choice of plant species (e.g., Rasheed & Harder 1997a), choice of individual plants (e.g., Heinrich 1979; Waser & Price 1983; Thomson 1988), and behavior on those plants (e.g., Galen & Plowright 1985; Hodges 1985; Rasheed & Harder 1997b).

Foraging pollinators typically visit flowers for nectar and/or pollen; these resources differ distinctly with respect to both foraging benefits and costs. Most pollinators visit flowers for the concentrated, easily digested energy in nectar. Because animals ingest nectar, they can readily determine their intake rate and whether a flower is empty (e.g., Dreisig 1989). The main handling cost of nectar collection involves the time and energy required to drink nectar from flowers. This cost depends primarily on the volume of nectar ingested, its depth within a flower, the animal's body size, and the length of its proboscis (see Montgomerie 1984; Harder 1986). Consequently, the choice of plants within and between plant species varies with pollinator size and morphology (e.g., Harder 1985, 1988). Furthermore, because the rate of flower manipulation increases with experience, foraging decisions can depend on an individual pollinator's learning ability (Gegear & Laverty, this volume).

Unlike nectar, pollen offers a rich source of protein, amino acids, lipids, and sterols, compared to most other plant tissues (Stanley & Linskens 1974). However, pollen use requires specific collecting and digestive abilities, given the small quantities of pollen available in individual flowers and the indigestibility of pollen exine. Consequently, only some pollinators (primarily non-parasitic bees, syrphid flies, and masarine wasps) satisfy their protein needs by feeding from flowers. Instead of ingesting pollen directly from anthers, most of these animals harvest it in three steps: (1) external removal on the animal's body; (2) grooming; and (3) either consumption or transfer to specialized, external carrying structures (scopae, including corbiculae) for transport to a nest (Holloway 1976; Michener etal. 1978; Thorp 1979). The removal step can be cost-free if it occurs passively during nectar collection, or it can require considerable effort, as when bees contract their flight muscles rapidly to buzz pollen from poricidal anthers (reviewed by Buchmann 1983; also see Harder & Barclay 1994; King & Buchmann 1996). Grooming also elevates the cost of pollen collection relative to nectar collection, especially because it typically occurs during flight (Holloway 1976; Harder 1990a; Michener et al. 1978), which increases metabolic effort 1o-fold (Ellington etal. 1990). Even though most bees carry pollen externally, they detect variation in the amount and quality of pollen removed from individual flowers (Cane & Payne 1988; Buchmann & Cane 1989; Harder 1990a; Robertson etal. 1999), perhaps by setae on the scopae that are coupled to displacement sensors (Ford etal. 1981) or by assessment of grooming effort. In response to such variation, bees alter their behavior to promote pollen-collection profits (Rasheed & Harder 1997a, b). This behavior often results in individual bees not depleting flowers of pollen, even when they visit for no other resource (Harder 1990b; Harder & Barclay 1994).

In addition to handling costs, the relevant foraging currency must incorporate the time and energy expended on other activities. These additional costs always include travel within and between plants. For animals that visit flowers to provision offspring, transit costs between nests and foraging sites are also relevant, so that foraging costs equal the total expense of foraging. In contrast, pollinators that visit flowers to sustain other activities, such as defending a territory, finding mates, or searching out oviposition sites, must accommodate the additional costs associated with these activities (Montgomerie et al. 1984; Houston & Krakauer 1993).

Given the benefits (B), time costs (T), and energy costs (E) of nectar and pollen collection, what currencies do pollinators typically maximize.? The behavior of nectar feeders usually maximizes either net intake rate ([B-E]/T: Hodges 1981; Gass & Roberts 1992; Hainsworth & Hamill 1993) or net foraging efficiency ([B-E]/E: Schmid-Hempel & Schmid-Hempel 1987; Tamm 1989), whereas that of pollen feeders maximizes gross efficiency (B/E: Rasheed & Harder 1997a, b). Maximization of foraging rate maximizes daily gains for animals that forage to satisfy their own needs, whereas animals that maximize efficiency while provisioning other individuals maximize the overall daily delivery of resources to their nests (Ydenberg etal. 1994). In addition, a provisioning forager that maximizes its foraging efficiency promotes its reproductive output when the chance of mortality increases with foraging effort (Houston et al. 1988). In general, energy costs influence efficiency more than rate, so that when pollinators maximize efficiency they limit expensive behaviors, especially flight. As a result, maximizing efficiency rather than rate requires pollinators to visit more flowers per inflorescence (Rasheed & Harder 1997b) and to work each flower longer. As we discuss below, both of these behavioral responses affect pollination, so that foraging currency will affect plant mating.

Most studies of the currencies that motivate pollinator behavior have considered animals feeding exclusively on either nectar or pollen. However, animals that rely on flowers for both energy and protein require a balanced diet of nectar and pollen for adequate nutrition (e.g., Haslett 1989; Camazine 1993; Plowright et al. 1993). To maintain this balance, flower-dependent animals may need to compromise the economic collection of either resource to optimize overall diet composition. Such compromises may be common, because flower-dependent animals often collect nectar and pollen from different plant species (Brian 1957; Liu et al. 1975; Teras 1985) that differ in their relative availability of these resources. N.M. Williams and V.J. Tepedino (unpublished manuscript) proposed that, in such circumstances, solitary bees minimize the total time spent collecting all the pollen and nectar required to provision a single offspring. Given relatively constant mass and quality of offspring provisions, such behavior would maximize the gross rate of resource collection per provision. Williams and Tepedino observed that female Osmia lignaria (Megachilidae) divided their foraging effort between a rich nectar source (Hydrophyllum capitatum) and a rich pollen source (Salix spp.) in proportions expected from time minimization, even though these species were separated by 300 m. In contrast to solitary bees, social bees need not always compromise economic collection of nectar and pollen, because they can achieve a balanced input by varying the proportions of dedicated pollen- and nectar-foragers (Brian 1952; Cartar 1992; Camazine 1993; Plowright et al. 1993).

If a pollinator is to maximize some benefit-cost ratio between the beginnings of consecutive foraging bouts, how should it decide whether to continue its current behavior, such as a flower visit, or switch to a different behavior.? Quite simply, an individual act serves the longer-term goal of currency maximization as long as its instantaneous benefit-cost ratio (i.e., marginal value) exceeds the average ratio expected by ending the current behavior and beginning anew (marginal value theorem: Charnov 1976). This principle underlies many aspects of pollinator behavior, including: whether to deplete individual flowers of nectar and/or pollen (Hodges & Wolf 1981); whether to move to another flower on the same plant, or to another plant (Pyke 1979; Hodges 1985; Kadmon & Shmida

1992; Rasheed & Harder 1997&); whether to move to a neighboring, or more distant plant (Cibula & Zimmerman 1984); whether to start feeding on a different plant species (Zimmerman 1981); and when to end a foraging bout and either return to the nest or transfer to another behavior (Schmid-Hempel et al. 1985). Three features of the involvement of a benefit-cost ratio in these decisions warrant notice. First, as will become apparent below, all of these behaviors influence the pattern of pollen dispersal, so that foraging currency defines the linkage between many floral characteristics and pollination success. Second, the consequences of a floral characteristic, such as nectar volume or concentration, for pollinator behavior depends on its influence on the relevant foraging currency, rather than its effects on benefits or costs alone (e.g., Harder & Real 1987). Finally, because the value of a particular behavior to a pollinator depends on the average currency in the environment, the details of pollinator behavior (and the associated pollination) are often context dependent (e.g., Harder & Barrett 1996; Kunin 1997; Smithson & Macnair 1997).

Notwithstanding the widespread occurrence of currency maximization by pollinators, some solitary bees restrict their pollen collection (but not necessarily nectar collection) to a few related plant species even when other species seemingly offer greater rewards (reviewed by Wcislo & Cane 1986). Based on the limited available data, such specialization seems to be genetically determined (Thorp 1969; Williams 1999). This innate specialization is sometimes associated with behavioral and morphological adaptations for harvesting resources from particular plant taxa, which may increase pollination effectiveness. Innate specialization can benefit pollination by promoting pollen transfer between conspecific plants, although in this respect it does not differ fundamentally from short-term specialization by a generalist pollinator that maximizes its current foraging returns (see Waser 1986). On the other hand, adaptations for collecting pollen from specific plant species can impair pollination if they enable pollen specialists to function more as pollen thieves than as pollinators (e.g., Eickwort 1967; Cane & Buchmann 1989; Williams & Thomson 2001).

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