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the birds learned the positions of the rewards in the array, irrespective of distance. Following the shift, all birds were worse at visiting the previously rewarded flowers, but this effect was much greater following the shift of 160 cm. Flower color pattern had no effect on post-shift performance. It appears, then, that the birds use different types of spatial information depending on the spatial scale - when the flowers are close together (<40 cm), the birds use within-array cues to relocate rewarded flowers, and when farther apart they use cues which are outside the array. When foraging on real flowers, then, it may be that birds are remembering locations of single flowers or flower clumps but that within a clump or an inflorescence the birds are more likely to remember which flowers to avoid by remembering the positions of flowers relative to each other. It is not yet clear how the performance observed in these experimental manipulations is related to that which would be demonstrated in real foraging. For example, we do not know whether there is any ecological validity to the spatial scale we used in this experiment. Different populations or species ofhummingbirds might use spatial cues differently, but to understand such differences, one would need to know on what plants the birds forage (and how they and their flowers are spatially and temporally distributed). If, as is likely, all species forage on both single and clumped flowers, they may then all show a similar switch in scale of spatial cue use.

Summary

Recent evidence supports the notion that hummingbirds, at least territorial hummingbirds, use memory for avoiding flowers on which they have recently fed. They use location cues to do this, seemingly paying little attention to the color/pattern cues of the flowers themselves. And yet, the role for flower color in the relationship between plants and their hummingbird pollinators seems to be a major one, made more explicable when an understanding of the birds' perceptual and memory capabilities is taken into account. To persuade a hummingbird to make a first visit to a flower, visual conspicuousness seems to outweigh spatial proximity. With little evidence that birds use movement rules between making flower choices, the spatial distribution pattern of flowers also seems of little consequence.

On the other hand, for plant pollination, the role of a hummingbird's spatial memory - either in accuracy, capacity, or duration - is much less clear in spite of its psychological dominance. Rufous hummingbirds, certainly, can remember after a single, very short visit the locations of small numbers (at least) of flowers, and they avoid these for short periods of time. On the other hand, locations of food sources that do not deplete require multiple visits before the birds reliably return to them. They can also discriminate between flowers that are close together (a few cm) using either other nearby flowers or more distant, larger landmarks as cues. The capacity and duration of hummingbirds' spatial memory have received little attention, not least because assessing these capabilities is logistically difficult. Whether or not plants have managed to respond to or manipulate these cognitive capacities is unclear.

In order to understand just how well plants have managed both to exploit and to be manipulated themselves by the perceptual and cognitive abilities of their hummingbird pollinators will require an interdisciplinary, integrative approach. Avenues for investigation include: field tests of learning and memory in hummingbirds using real plants, growing naturally, to assess the accuracy, capacity, and duration of spatial memory; collection of comparative data (there are almost no data of this kind to date) to determine whether hummingbird species show differences in cognitive abilities that correlate with differences amongst plants in visual, spatial, and reward features; and collection of quantitative data on the numbers of flowers, nectar refilling rates, and variation in quantity and concentration of nectar within and between plants.

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Bats as pollinators: foraging energetics and floral

Bat pollination is a pan-tropical phenomenon, performed in the Old World by small megachiropterans (Pteropodidae) and in the New World by microchiropterans of the leaf-nosed bat family Phyllostomidae (Dobat 1985). Flower-visiting bat species total about 50 worldwide, while Dobat (1985) listed about 750 bat-pollinated plant species in 270 genera (590 for the Neo- and 160 for the Palaeotropics). Since then, many more cases have been found.

Although plants independently enlisted "megabats" and "microbats" as pollinators, it is likely that both systems have links to one common root: pollination by ancient, nocturnal, non-flying mammals dating to the late Cretaceous (Sussman & Raven 1978). The extinction of most of these early mammalian flower visitors coincided with the radiation of bats from the Eocene onward in the Old World, and during the Miocene in South America (Sussman & Raven 1978). Genera like Parkia may have developed mammal pollination before the separation of African and South American plates; they still retain this trait (Vogel 1969, 1980). Of the plant species found to attract bats today, however, the vast majority evolved their adaptative traits more recently (Vogel 1990).

In the Neotropics, it is useful to consider a continuum ranging from less specialized "fruit-bat" flowers to true "glossophagine" flowers (von Helversen 1993; cf. Johnson & Steiner 2000). For Costa Rica, we estimate that two-thirds of the bat-pollinated plant species are glossophagine specialists. Among the leaf-nosed bats, the subfamily Glossophaginae, with about 35 species and body masses ranging from 6 to 35 g, has evolved the highest degree of specialization for feeding from flowers. This includes the ability to feed during hovering flight, using a protrusile, brush-

tipped tongue nearly as long as the body (von Helversen & von Helversen 1975). This group of bats probably accounts for the greater expansion of chiropterophily in the Neotropics than in the Old World (see above). In the Neotropics about 0.7% to 1% of the angiosperm flora is bat-pollinated, including rather delicate or herbaceous plants that can only be exploited by highly maneuverable, hover-feeding visitors.

Bats are "expensive" pollinators in that they need large amounts of nectar (even glossophagine flowers produce at least 100 ^l of nectar per night, and flowers visited by large bats produce at least a few milliliters). These requirements should severely restrict the circumstances under which bats become the preferred pollinator for a plant species. On the other hand, bats offer pollen transfer over potentially large distances, which can be important for self-incompatible plants that grow sparsely. A bat may fly 60 km (von Helversen & Reyer 1984) to 100 km (Horner et al. 1998) in a single night's foraging and commuting, and may fly from several hundred meters up to several kilometers between successive plants.

This chapter concerns the energetic aspects of the consumer-resource relationship; we consider these to have played a pivotal role in the evolutionary interaction between glossophagines and their flowers (cf. Heinrich & Raven 1972). We first present a quantitative model of the foraging energetics by a glossophagine bat. This model calculates the minimal caloric reward required by a bat, from average flower visits, in order to balance its energy budget. One result is that selection for increased search efficiency is likely to be intense under conditions of food limitation. Second, we discuss how plant traits that enhance flower detectability may increase the energetic efficiency of pollinator foraging. Pollinators may compete for flower nectar, but flowers may also compete for pollinators, and pollinators will typically prefer the most profitable nectar sources. Profitability involves more than nectar sugar, however; if adaptations enhance a flower's detectability, a pollinator may be able to save energy in several aspects of foraging, including search, approach after detection (i.e., "pursuit" in standard foraging models), and locating and extracting nectar ("handling"; Chittka et al., this volume; Gegear & Laverty, this volume; Menzel, this volume). Our energy-balance model of bat foraging demonstrates how increased detectability and any other facilitation of nectar exploitation can be converted into calories of saved foraging cost by the pollinator. Detectability can thus, in principle, affect profitability, and be expressed in the same "currency" as nectar sugar, even if we do not yet know the "conversion factor" quantitatively. All else being equal, plant species with higher profitabilities will be more likely to be chosen for visitation. Within species populations, more detectable individuals will be more likely to receive visits. Therefore, we expect that natural selection will tend to increase detectability, especially if adaptations for detectability are cheap compared to nectar secretion. Because detectability and nectar sugar are linked through their effects on profitability, plants that are highly detectable may be able to attract visits even if they skimp on nectar. We expect natural selection to arrive at a balance based on the functional forms of costs, benefits, and tradeoffs involving detection versus reward.

Glossophagine bat energetics

Here we derive a quantitative estimate of the threshold requirements for nectar energy during a single flower visit by a small glossophagine bat. A pollinator can only survive in a habitat in which the available food resources allow it to balance its daily energy budget. Especially for a small homeotherm vertebrate with limited capabilities to store fat, this is a stringent requirement. This raises the question: how much energy does an individual bat need to have available in its habitat.? As the energy of an average food portion must exceed the cost of acquiring it, the spatial distribution of nectar must allow for economic harvesting. The minimum energy reward that a bat needs to obtain from the average flower visit will therefore depend on the spatial distribution of flowers within the habitat. To predict resource availability for glossophagine bats, the energetic expenditures must be known.

Daily energy requirements

We determined daily energy expenditures (DEE) of glossophagine bats both from field and laboratory measurements by using methods that included doubly-labeled water, feeding trials, and energy budget estimates derived from time budgets obtained by radio telemetry of freeranging bats (von Helversen & Reyer 1984; Winter 1998a; unpublished data). Larger glossophagine species have higher DEEs than smaller species (Fig. 8.1, Table 8.1), and the slope of this log-linear relationship coincides with values derived for other vertebrate endotherms (Nagy

Sphingid Flower

A Sphingidae □ Trochilidae • Glossophaginae

Fig. 8.1 (a) Daily energy expenditure (DEE) of nectar-feeding glossophagine bats (Phyllostomidae) as a function of body mass (data based on over 450 24-h measurements in 58 individuals from 11 species). Least-squares regression of DEE on body mass M yields DEE [kJ d"i] = 1555 M [kg] °-755 (y. Winter & O. von Helversen, unpublished data). Dashed lines are regressions of DEE based on doubly-labeled water estimates for birds (Nagy 1987) and eutherian mammals (Nagy 1994). (b) The energy cost of hovering flight as a function of body mass in sphingid moths, hummingbirds (Trochilidae), and glossophagine bats (Phyllostomidae). Solid lines are regressions relating hovering power input Ph to body mass M (see Table 8.1). At a power input of 1.1 W, the three groups of flower specialists overlap in energy expenditure for hovering but support very different body weights (from Voigt & Winter 1999). Axes are plotted on a logarithmic scale.

Fig. 8.1 (a) Daily energy expenditure (DEE) of nectar-feeding glossophagine bats (Phyllostomidae) as a function of body mass (data based on over 450 24-h measurements in 58 individuals from 11 species). Least-squares regression of DEE on body mass M yields DEE [kJ d"i] = 1555 M [kg] °-755 (y. Winter & O. von Helversen, unpublished data). Dashed lines are regressions of DEE based on doubly-labeled water estimates for birds (Nagy 1987) and eutherian mammals (Nagy 1994). (b) The energy cost of hovering flight as a function of body mass in sphingid moths, hummingbirds (Trochilidae), and glossophagine bats (Phyllostomidae). Solid lines are regressions relating hovering power input Ph to body mass M (see Table 8.1). At a power input of 1.1 W, the three groups of flower specialists overlap in energy expenditure for hovering but support very different body weights (from Voigt & Winter 1999). Axes are plotted on a logarithmic scale.

Table 8.1. Energy relations and foraging parameters inglossophagine bats and their mass dependence

Parameter

Units

Equation"

Source

Basal metabolic rateb

Wc

1.15 (2.59 M°-71)

McNab 1988; Arends et al. 1995

Daily energy expenditure

kJ d-1

1555 M0-76

Y. Winter & O. von Helversen

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