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Mean inter-flower distance during foraging (m)

Fig. 8.3. Boundary values of minimum nectar rewards per flower visit for 7.5-g Hylonycteris underwoodi (Phyllostomidae, Glossophaginae), a Central American nectar and pollen specialist. Data were calculated from Eq. 8.6 assuming a nightly flight activity of 4.5 hours for foraging. Inter-flower distances are mean distances between flowers in the habitat. As bats will not forage with 100% search efficiency, the actual flight distances between flowers will surpass the theoretical minimum. For the continuous line, it was assumed that successive flowers were visited with a search efficiency effs equal to 40% of the theoretical minimum, whereas for the broken line, an efficiency of 80% was assumed (from Y. Winter & O. von Helversen, unpublished data). The energy content of nectar with 17% sugar (wt/wt) is 2.9 J |l~i (see Table 8.1).

This equation allows an approximation of the minimum nectar energy that must be available during a flower visit for given values of daily energy expenditure (DEE), flight time budget Tf, and search efficiency effs. Values for DEEs to be used in this linear model can be computed from the equation given in Table 8.1. Daily flight-time budgets (Tf) are typically 4-5 h per night for glossophagine bats (Horner et al. 1998; Y. Winter & O. von Helversen, unpublished data).

For the minimum nectar energy densities shown in Fig. 8.3, we used Eq. 8.6 with two different values for search efficiency effs, 40% and 80%. The 7.5-g Hylonycteris rainforest bat needs 13.4 ml of 17% sugar nectar (wt/wt or 181.5 g l-1) to balance a daily energy budget of 38.7 kj d-1. Let us assume a mean distance between flowers in the habitat of 30 m and a total foraging flight time of 4.5 h. Then a bat with a search efficiency of 40% would have an effective mean flight distance between flowers of 75 m. It could make approximately 700 flower visits, each of which would need to yield a minimum average of 19 ^l of nectar (with 17% wt/wt sugar). At a higher search efficiency of 80%, 1400 flowers could potentially be visited within 4.5 h of flying time, and they need to provide only 9.5 ^l per visit.

We consider this result to be of central importance for the relationship between plant and forager: reducing the cost of foraging (by reducing the effort per individual flower) reduces the minimum amount of nectar energy required by a bat during a flower visit in order to balance its energy budget. It is this relationship that offers plants the possibility of enhancing their attractiveness without having to invest in nectar sugar. Furthermore enhanced detectability and locatability can allow a plant to reduce the amount of energy offered to a bat without falling below the profitability threshold of the forager. The offering of smaller nectar portions may increase the number of flowers that a forager will visit per unit of time (cf. Heinrich & Raven 1972). This, in turn, may increase rates of pollen transfer.

The "syndrome" of chiropterophily: adaptations of glossophagine flowers to their visitors' sensory physiology

Our discussion of the floral adaptations for glossophagine pollination will focus on two hypotheses. (1) Plants increase their ability to compete for pollinators by improving the cost-benefit ratio of pollinator foraging. As mentioned above, a reduction in costs eventually pays off for a bat in the same currency as an increase in rewards. Therefore, easy locatability is an important factor in reducing pollinator costs. Detectability involves a whole suite of sensory (olfaction, vision, echolocation) and cognitive (spatial memory) abilities. (2) The nectar and pollen rewards are often protected against unwanted visitors to preserve them for the energy-demanding glossophagine bats. Thus, detectability for unwanted visitors should be reduced.

The cutting of foraging costs: addressing the senses and cognition

Olfaction

Olfaction is probably the primary sense for the long-distance detection of many bat flowers. Nearly all bat flowers have a strong, characteristic smell, at least to the human nose (Porsch 1931; van der Pijl 1936; Vogel 1958). To date, the scent spectra of 22 different bat flowers from at least 10

plant families have been analyzed (Knudsen & Tollsten 1995; Bestmann et al. 1997). Four types of scent components predominate: aliphatic, aromatic, terpenoid, and sulfur-containing compounds. Sulfur-containing compounds are important in most of the scent-bouquets. These compounds (particularly dimethyl-disulfide, dimethyl-trisulfide and dimethyl-tetrasulfide) are rare in non-bat flowers but are produced by many bat-pollinated plants that are not related to each other (Knudsen & Tollsten 1995); they seem to be the result of true convergent evolution.

Dimethylsulfides are strong attractants for glossophagines. In field experiments, free-ranging Glossophaga commissarisi were attracted to mock flowers when these contained either dimethyl-disulfide or 2,4-dithiapentane. Several other scent components were considerably less effective (von Helversen et al. 2000). This scent preference seems to be innate; laboratory-reared animals without any experience with flowers also significantly preferred dimethyl-disulfide (Fig. 8.4).

Vision

Bats are generally believed to be color-blind (Jacobs 1993), and Glossophaga bats are unable to discriminate between wavelengths in color discrimination tests (J. Lopez, Y. Winter, & O. von Helversen, unpublished data). The color spectrum of bat flowers extends from greenish through whitish to brownish and brown-red; the colors are never glowing, but rather are unsaturated and usually dusky (Vogel 1969). Some glossophagine flowers are white, presumably because they have evolved from hawkmoth flowers (e.g., Bombacaceae such as Pseudobombax septenatum and Bombacopsis quina-tum, Bauhinia spp., Capparis spp., Cactaceae, etc.). Reddish or red-brown colors may indicate evolution from bird flowers (e.g., Erythrina glauca, Calliandra, also Old World Musa). Green and brown colors probably help to make the flowers inconspicuous for other visually oriented foragers such as sphingid moths and probably also birds.

In contrast to color vision, the visual pattern-recognition ability of flower bats is well developed (Suthers et al. 1969). Black-and-white contrasts may help in finding flowers that are white if they contrast against dark foliage, and the exposed position of many flowers probably helps approaching bats when they fly up from below the horizon and view the flower against the light sky. Most bat flowers project into the open air, so that the bats encounter no obstacles when flying up to them. This exposure is achieved by a great variety of morphological arrangements; individual flowers may be raised above the foliage on long stems, the flowers

Fig. 8.4. Relative olfactory attractiveness of 20 flower scent compounds in spontaneous choice experiments conducted in the laboratory with a group of Glossophaga soricina. Values are means (± 1SE) of the preference factors for the respective compounds. The preference factor describes the relative preference of the respective scent in comparison to the scentless control (without any volatile substance). A preference factor larger than 1.0 indicates that the scent compound was preferred compared to the scentless reference; a factor value of less than 1.0 would indicate a repellent effect of the scent compound. Tests were carried out on a total of 52 nights; the number of visits counted was 7551 (von Helversen ei al. 2000).

Fig. 8.4. Relative olfactory attractiveness of 20 flower scent compounds in spontaneous choice experiments conducted in the laboratory with a group of Glossophaga soricina. Values are means (± 1SE) of the preference factors for the respective compounds. The preference factor describes the relative preference of the respective scent in comparison to the scentless control (without any volatile substance). A preference factor larger than 1.0 indicates that the scent compound was preferred compared to the scentless reference; a factor value of less than 1.0 would indicate a repellent effect of the scent compound. Tests were carried out on a total of 52 nights; the number of visits counted was 7551 (von Helversen ei al. 2000).

may be situated at the ends of twigs, or flagelliflorous inflorescences may hang down for meters from the canopy (Porsch 1931; van der Pijl 1936; Vogel 1968, 1969; Tschapka et al. 1999). Furthermore, many chiropteroph-ilous trees bloom when leafless (Vogel 1968, 1969). This open exposure allows unencumbered access (Fig. 8.2) and probably also increases the detectability of flowers by vision or echolocation. Glossophaga bats are unexpectedly sensitive to ultraviolet radiation, differing from nearly all other mammals tested except for a few rodents (Jacobs 1993; Lopez, Winter, von Helversen, unpubl. data). This sensitivity might enable the bats to detect some white flowers against a dark background, because some bat-pollinated flowers reflect UV (Burr et al. 1995).

Echolocation and flower shape Glossophagine bats orient mainly by their highly developed system of echolocation. Therefore, flowers that send back conspicuous echoes should be especially well detectable for a bat. A bat-pollinated flower that attracts its pollinators with its echoes is Mucuna holtonii (Fabaceae). This liana grows high in the canopy, from where its many-flowered inflorescences hang down on peduncles up to several meters long. The flower's erect upper petal (vexillum), which measures about 19 by 19 mm, is formed like a small concave mirror. In field experiments, we showed (von Helversen & von Helversen 1999) that the bats detect the flowers by echo-location. Filling the concave cavity of the vexillum with a pad of cotton wool, which changes only echo reflectance, not shape or odor, drastically reduced the numbers of visits.

We examined the echoes reflected from a Mucuna flower exposed to artificial sound sweeps that imitated natural echolocation calls. By comparing echoes sent back by virgin flowers, by buds, and by flowers in which the vexillum had been filled with pads of cotton wool, we discovered that the echo of the entire flower was strongly dominated by the echo of the vexillum (Fig. 8.5). The echo had an astonishingly high amplitude; the spectral composition was dependent on the angle of sound incidence, but the amplitude was high within a large cone of incidence angles (about -40° to -50°, to +40 to +50°; Fig. 8.5). Thus, the vexillum ofMucuna hol-tonii acts similarly to a cat's eye or a triple mirror in the optical domain, reflecting most of the energy back into the direction of incidence. The echoes of such a concave vexillum should be acoustically conspicuous because they persist during a series of calls emitted by a passing bat. This is different from many other loud echoes, i.e., from leaves, which reflect

Fig. 8.5. Ultrasound echoes reflected from Mucuna holtonii flowers. Echoes from (left) a virgin, intact flower; (middle) a bud; (right) a flower in which the vexillum was filled with a pad of cotton wool. Degrees show the angle of sound incidence. The signal was a 1-ms sound sweep, the frequency of which was linearly modulated from 110 to 60 kHz (von Helversen & von Helversen 1999).

Fig. 8.5. Ultrasound echoes reflected from Mucuna holtonii flowers. Echoes from (left) a virgin, intact flower; (middle) a bud; (right) a flower in which the vexillum was filled with a pad of cotton wool. Degrees show the angle of sound incidence. The signal was a 1-ms sound sweep, the frequency of which was linearly modulated from 110 to 60 kHz (von Helversen & von Helversen 1999).

echoes in only one direction - and therefore for only a single call from a passing bat.

The peculiar concave geometry of the Mucuna holtonii vexillum may be a direct adaptation to the echolocation system of glossophagine pollinators: neither Palaeotropical bat-pollinated species of Mucuna, which are visited by small megachiropterans that do not echolocate, nor bird-pollinated species of the genus possess vexilla with the specialized shape and stiffness.

We expect similar adaptations to be found in other glossophagine-pollinated flowers. One promising case involves several columnar cacti that display their flowers within a hairy zone, the "cephalium" of the cactus. This cephalium probably absorbs sound energy, enhancing the contrast to the more reflective flowers. The surface of many bat flowers is especially smooth and waxy, and glossophagine bats examine objects with smooth surfaces when they are searching for flowers (personal observation).

Spatial memory

In marked contrast to the single-night blooming of the individual flowers, the flowering period of chiropterophilous plants is often much longer than that of related, non-bat-pollinated species (Vogel 1958, 1968, 1969). For instance, chiropterophilous Vriesea species remain in bloom for up to 2 months, chiropterophilous Cleome moritziana for about 5 months, a single inflorescence of Mucuna holtonii for as long as 6 weeks - extreme cases of what has been called "steady-state flowering" (Gentry 1974). This flowering behavior may be an adaptation to the spatial memory of bats. Evidence for spatial memory in bats is fragmentary. During obstacle-avoidance experiments, bats build up a memory of exact obstacle positions that they retain for over a month (Neuweiler & Mohres 1967). We observed that after removal of an accustomed feeder in the laboratory, individuals of Glossophaga soricina inspected the former feeder location by hovering in mid-air at the former feeder position for several nights.

We tested for the ability to memorize feeder locations in a laboratory experiment with three Glossophaga soricina bats. When feeders had contained a nectar reward for a 1 hour-period during the night preceding the test, then these feeders - which remained unrewarded during the test night - were visited three times more often (38 visits per feeder, n = 5 feeders) than identical control feeders (11 visits per feeder, n = 4 feeders) that had never been rewarded (D. von Helversen, personal communication).

Spatial memory for food location is likely to be the most important mechanism enabling glossophagines to relocate flowers and minimize search costs. The experimental investigation of spatial memory and orientation will therefore be especially important.

Securing the goods: repulsion of unwanted visitors

Secretion of nectar is much greater in bat flowers than in all other pollination syndromes (although glossophagine flowers may still have less nectar than "big bat" flowers). Typical glossophagine flowers secrete 1 to 2 ml of nectar per night, with a lower limit of about ioo ^l/night; "big bat" flowers may secrete more than 20 ml/night (Dobat 1985). The sugar concentration of the nectar is only 5%-29% sugar wt/wt (often 15%-17%, thus containing about 180 mg sugar per ml of nectar; von Helversen 1993), which is much less than the concentration preferred by the bats in laboratory experiments (55% sugar; Roces et al. 1993). The nectar sugars are dominated by hexoses (Baker et al. 1998).

For bats such as Choeronycteris and Leptonycteris, ingestion of pollen seems to be an important "reward" from the flower, as these bats depend on pollen as their nitrogen source; however, less specialized glossopha-gines such as Anoura and Glossophaga also feed voraciously on pollen when kept on an otherwise protein-deficient diet (personal observation). It has been suggested that the pollen of bat flowers is specially adapted to the needs of the bats in its amino acid composition (Howell 1973). The pollen supply of glossophagine flowers is usually larger than that of related flowers of the same size that are not pollinated by bats (Vogel 1968, 1969). Either the number of stamens is increased or the thecae themselves are especially rich in pollen. In some species, the normal hermaphroditic flowers are accompanied by a certain number of purely male flowers (e.g., Bauhinia spp., Heithaus et al. 1974; Ramirez et al. 1984; Cleome moritziana, personal observation; and others). Flowers lose many pollen grains to glossophagines because the bats interrupt their foraging flights every 10 to 20 min, hang from a twig, and clean their fur thoroughly with their tongues, thereby ingesting the pollen (personal observation; cf. Harder et al., this volume).

Because bat flowers offer unusually large amounts of nectar and pollen, they are vulnerable to parasites (Heinrich & Raven 1972). "Unwanted" visitors may deplete costly nectar or pollen (which may lead to a loss of mating opportunities), and they may damage flowers. Therefore, under certain conditions, plants should limit the spectrum of visitors. To understand how a plant may be able to "hide" its flowers from unwanted visitors or even to "repel" them, we have to know the behavior and the sensory system of the visitor to understand the plant's potential devices.

The following considerations are largely speculative, but might offer a platform for experimental investigations. All bat-pollinated plants open their flowers at night because bats are nocturnal, but, in addition, many glossophagine flowers open only after dusk and close or fade before sunrise. This is probably primarily a mechanism for excluding day-active pollinators, especially birds and bees. Only a few glossophagine flowers remain open for two or three days, and most of these are protandrous, i.e., male during the first night and female during the second (e.g., Cobaea, Paliavana, Macrocarpaea, Agave, etc.). In these cases, nectar secretion is often restricted to night. Exceptions include some generalist flowers that also attract birds; in those, some nectar is secreted diurnally (e.g., different species of Macrocarpaea and Puya in the paramo of Ecuador; F. Matt & H. Schmid, personal communication).

Bolten & Feinsinger (1978) suggested that the low nectar concentration of hummingbird flowers may be a characteristic to deter bees. This idea could possibly also hold for bat flowers, with their even lower nectar concentrations, but only a few species of wasps and bees are night-active. Nocturnal wasps can sometimes be observed on bat flowers (personal observation). Bees can commonly be observed gathering nectar and pollen left in bat flowers in the morning, or robbing nectar and/or pollen in the evening by forcing their way into buds.

The dark colors of many bat flowers should make them difficult to find and approach for sphingid moths, which orient visually. In Markea neuran-tha, for instance, the opening of the corolla tube - which is just the place where a hawkmoth would have to introduce its proboscis - is dark purple-brown, whereas the outer surface is greenish and hardly stands out against the foliage even in daylight.

Bat-flower nectar in some cases seems to have a higher viscosity than expected on the basis of its sugar concentration, due to the additional secretion of mucous substances (van der Pijl 1936; personal observation). As sphingids have to suck nectar through a very long capillary tube in their mouthparts, whereas bats lick nectar, a high viscosity may well present much more difficulty to the moths (see Heyneman 1983). Ants can steal bat-flower nectar (Haber et al. 1981; personal observation). Therefore, many mechanisms, mostly mechanical, have been developed to repel ants (Kerner von Marilaun 1876; Guerrant & Fiedler 1981; von Helversen 1993).

Conclusion

Many neotropical glossophagine pollinated flowers, which most likely evolved from flowers visited by non-flying mammals, presently show characteristics (i.e. pendant peduncles, delicate supports) that might be adaptations both to deter visits from non-flying mammals and, in combination with other cues (scent, echo reflectance), to increase detectability and accessibility to a hovering visitor. This selects in the bat population for greater agility (smaller bodies, better hovering skills). Selection pressure for small pollinator size may also be caused by interspecific exploitation competition because energy requirements decrease with body size. Because flower 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. These characteristics should interact and could reinforce each other until the system runs into some constraints which can adequately be described only with quantitative physiology.

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