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Pollination and Floral Ecology$

Pat Willmer

Print publication date: 2011

Print ISBN-13: 9780691128610

Published to Princeton Scholarship Online: October 2017

DOI: 10.23943/princeton/9780691128610.001.0001

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Other Floral Rewards

Other Floral Rewards

(p.221) Chapter 9 Other Floral Rewards
Pollination and Floral Ecology

Pat Willmer

Princeton University Press

Abstract and Keywords

This chapter examines a variety of rewards that can be obtained by pollinators from flower visits, including oils, waxes, scents, and resins and gums. Fatty oils as an offering in flowers are now known from at least eighty genera across several families and from nearly 1 per cent of flowering plant species. Floral resins have been reported in occasional genera that are abundant in the tropics. The chapter also considers stigmatic exudates, which provide a good oily food source that sometimes can be the primary reward; examples of fragrance as a reward; floral tissues; and other possible nonfood rewards such as brood sites, microclimatic protection and warmth, and meeting places. Most of the rewards discussed in this chapter may be the key to some particularly fascinating pollination systems and open up possibilities for new dimensions in animal–flower interactions.

Keywords:   reward, pollinator, oil, wax, scent, resin, flower, stigmatic exudate, floral tissue, pollination


  1. 1. Oils

  2. 2. Resins and Gums

  3. 3. Stigmatic Exudates

  4. 4. Scents

  5. 5. Floral Tissues

  6. 6. Other Possible Nonfood Rewards

  7. 7. Overview

Occasionally flowers offer neither pollen nor nectar as a foodstuff to their visitors but instead yield other rewards; or they may offer these as “extras” in addition to some pollen. This chapter reviews these possibilities, considering a range of oils, waxes, scents, and resins (on which topics Simpson and Neff [1981, 1983] provided earlier reviews), as well as some less tangible rewards that can be obtained from flower visits.

1. Oils

First described in detail by Vogel (1969), fatty oils as an offering in flowers are now known from at least 80 genera across several families (table 9.1) and from nearly 1% of flowering plant species (Buchmann 1987; Steiner and Whitehead 1991). The oil flowers occur in four distinct domains of the world, those in the New World being unrelated to those of the Old World but convergently similar. In each case the oils are produced by secretory hairs termed elaiophores, which are usually in paired glands sited at the base of a flower (fig. 9.1); these have evolved independently several times, and once evolved, they have rarely been lost. They may be derived from either epithelia or trichomes (fig. 9.1A,B). In the orchid genus Grobya, there may be three different elaiophores, the one on the lip providing an “oil guide” that entices bees onward to the deeper-sited glands (Pansarin et al. 2009).

The oils produced in flowers are mainly diglycerides, with C14–C18 (rarely C20) backbones (fig. 9.2), often with smaller amounts of hydrocarbons, esters, and aldehydes; they differ in character from the lipids that are sometimes found as trace components of nectar. They tend to be colorless or pale yellow and are usually odorless.

All known examples of oil flowers are essentially solitary-bee pollinated, and the bees are mainly from the taxa Melittidae, Ctenoplectridae, and especially Anthophorinae. Most harvest the oil using their feet rather than their mouthparts (Roberts and Vallespir 1978; Buchmann 1987; Steiner and Whitehead 2002). There may be an association between the oil-collecting habit and pollen gathering by sonication, since most of the anthophorines that gather floral oils also use buzz-pollination at least some of the time (Simpson and Neff 1983), thereby acquiring rather dry pollen that lacks much lipid content (chapter 7). The oils the bees obtain could then act as lubricants, aiding pollen packaging and perhaps reducing pollen desiccation, although they may also be used as a cement to help line, and thereby waterproof, the nest cells. There is no doubt, however, that the collected oils also serve directly as a liquid foodstuff for the bee larvae, with or without added nectar or pollen. Oils as a food are particularly nutritious, two- to threefold more valuable weight for weight than a reasonably concentrated sugary nectar (table 8.5). When they occur in flowers, oils (p.222)

Table 9.1 Plant Families Interacting with Oil-Gathering Bees

Oil produced; oil bees visit

Deceptive, no oil production; oil bees visit without reward, or take nectar












are often the only collectable reward visible, the pollen being hidden, although a few species do offer both oils and nectar.

Examples of oil-producing flowers are particularly abundant from the Neotropics, most notably from savanna and moist-forest habitats. Three plant families—the Iridaceae, Orchidaceae, and Malpighiaceae—contribute particularly large numbers of examples, with nearly all of the species in this last family producing oil rewards. However there are also oil-producing flowers in the Cucurbitaceae, which are associated with Ctenoplectra bees. Some species of the genus Angelonia (Scrophulariaceae) also produce oils, the flowers having pockets at the back where the elaiophores are located (Machado et al. 2002); these are visited by long-legged Centris bees. In South America a range of unusual dwarf epiphytic orchids also offer oil (Dressler 1993), although these are not particularly specialist since various bees visit several of them and probably also gather a range of their pollens (Schlindwein 1998). Orchids with oil rewards also occur quite commonly in southern Africa and include species of Disperis and some related terrestrial genera, which are pollinated by Rediviva bees (Steiner 1989) in a much more specialist interaction. These bees also visit oil-bearing Diascia and Ixianthes flowers, which are related to snapdragons. Steiner and Whitehead (1996, 2002) reported asymmetries of specialization: one Ixianthes species (I. retzioides) is pollinated only by Rediviva gigas, but that bee in turn visits several other oil-secreting

Other Floral Rewards

Figure 9.1 Different types of oil glands: (A) trichome elaiophores, glandular hairs on petal bases in Lysimachia; epithelial elaiophores: (B) on anther of Mouriri; (C) at base of Malpighia flower (seen from below); (D) on Oncidium orchid, seen from underside. (Parts (A) and (B) redrawn from Buchmann 1987; parts (C) and (D) redrawn from Endress 1994.)

plants and some of its populations may not visit I. retzioides at all, and similarly, Colpias flowers are entirely dependent on R. albifasciata, but that bee also visits other Scrophulariaceae.

Specializations for gathering oils do occur in some bees (fig. 9.3). Notably, the Neotropical Centris and Epicharis species have forelegs bearing unusual hairs that are like flexible combs or scoop-like blades (elaiospathes), which can rupture oil-bearing glands and then scrape up and transfer the oils to patches of stout bristles on the bee’s hind legs for carriage to the nest. Melittid bees have “hair felt” patches on their legs that take up floral oils by capillarity, while the unusual ctenoplectrids have abdominal oil-mopping hairs. The southern African Rediviva bees have exceptionally long front legs (fig. 9.3E) that can gather oil by probing into the long spurs borne on their orchid flowers.

Symphonia species (Clusiaceae) have a more unusual use for their flower oils; they produce pollen mixed in an oily fluid (anther oil), which helps the pollen to be absorbed by capillarity into the stigmatic (p.223)

Other Floral Rewards

Figure 9.2 Floral oils are normally based on free fatty acids with chain length C14–20; (above) a typical acetoxy-substituted version; (below) a diglyceride version.

pores after deposition (usually by a hummingbird; Bittrich and Amaral 1996).

The most familiar examples of oil-producing flowers in temperate habitats all have trichome oil glands and include Calceolaria from the figwort family (Scrophulariaceae) and yellow loosestrife, Lysimachia (Myrsinaceae), a common weed in damp places in most northern continents that is almost exclusively visited (as in plate 19H) by Macropis bees (Cane et al. 1983). The flowers of Lysimachia perhaps attract bees initially by specific scents in their oil (Dotterl and Schaffler 2007), but experienced bees also learn and respond to the visual cues from the flowers. Oil alone (for cell lining) and oil and pollen together (for larval food) are apparently collected in separate foraging trips.

It is an oddity of oil flowers that they very frequently act as models for deceptive orchids that match their shapes and colors and produce shiny surfaces that appear (quite falsely) to be offering oil. This is particularly common in the Oncidium orchids, which mimic many of the Malpighiaceae and also Calceolaria and attract the same bees that normally visit their models. Oncidium cosymbephorum explicitly benefits (by higher seed set) from its resemblance to the rewarding shrub Malpighia glauca (Carmona-Diaz and Garcia-Franco 2009).

2. Resins and Gums

Floral resins have been reported in occasional genera that are abundant in the tropics. Clusia and Clusiella (Clusiaceae) (Skutch 1971) and Dalechampia (Euphorbiaceae; plate 11F) are best known, although resin is also reported from Mouriri flowers (Melastomataceae; Buchmann and Buchmann 1981). The floral resins in Clusia and Dalechampia are terpenoids (usually triterpenes in Dalechampia).

There is evidence that Clusia resin rewards are specifically antibacterial within the nest (Lovkam and Braddock 1999), and the same may be true for the resins of other genera. Quite a range of bees, especially megachilids, will collect resinous plant secretions oozing from vegetative structures (stems and leaves) where the resins have a protective antiherbivore effect (p.224)

Other Floral Rewards

Figure 9.3 Oil-collecting apparatus in bees: (A) anthophorid bee collecting oil with its front-leg mops (the oil then transferred to the hind legs); (B) the collecting mop on the foreleg, and (C) in transverse section; (D) the mop being drawn as a scraper across the oily hairs of the oil gland; (E) a Rediviva bee extracting oil from a Diascia flower with its elongated spurred front legs. (Parts (A–D) modified from Barth 1985, based on earlier sources; part (E) redrawn from Whitehead et al. 1984.)

for the plant; the bees take them back to their nests again to serve as a cell-lining and so help prevent fungal growth (e.g., dipterocarp resins, Messer 1985). This may give a clue as to how the habit of offering resins arose in flowers; floral resins may be more attractive to bees than stem-oozes, being more easily gathered or worked with, and they would also be more predictably located once a floral search image had been acquired.

The flowers of Dalechampia normally have a pair of conspicuous and highly colored bracts around otherwise very reduced corollas (fig. 9.4), and it is the lip of the bract that forms a resin gland (Armbruster and Webster 1979; Armbruster 1984, 1997). Female bees (euglossines, meliponines, and megachilids, plus occasionally Apis) have been recorded as visitors, gathering the resin as a nestlining material. Armbruster et al. (2005) showed that visiting Heriades bees selected flowers by the size of their bracts, rather than by gland area, even when the latter was easily visible; the bracts appear to serve as an “honest signal” for the size of the reward.

Some aroids are also known to have floral resins.

Other Floral Rewards

Figure 9.4 A Dalechampia inflorescence with oil gland sited above a small group of flowers.

(Redrawn from Armbruster 1996.)

(p.225) The functioning of these deceit-pollinated trap flowers is covered in chapter 23, but it may be noted here that the upper part of the spathe has male flowers with pollen, whereas the lower part (which forms the trap for visiting flies) has female flowers that in at least some species produce resinous secretions.

Once again, orchids are mimics and have the occasional habit of mimicking resin plants, a notable example being some Maxillaria species that have a patch of shiny apparent resin on their lower lip, which in reality is nothing more than callus tissue.

3. Stigmatic Exudates

Stigmatic exudates are common in angiosperms, where their main functions relate to pollen capture, adhesion, and germination (chapter 2), together with protection of the stigma against damage or desiccation. However, in many cases these exudates also provide a good oily food source, and sometimes this can be the primary reward, attracting beetles, flies, and some other insects. Generally the material exuded is composed of lipids and amino acids, with some phenolics, alkaloids, or antioxidants also present (F. Martin 1969; H. Baker et al. 1973; Lord and Webster 1979). In a few cases the reward is targeted rather specifically, as for example in certain Aristolochia that are primarily pollinated by flies which become trapped in a floral chamber where they feed on these amino-acid-rich exudates (Baker et al. 1973). Exudates are also abundant in some palms, where again it is mainly flies that feed on them (Simpson and Neff 1981).

Nearly all orchids also have stigmatic exudates, which are primarily used to stick the pollinia to visitors; in these cases the exudate is rarely fed on and is sometimes secreted almost explosively. But some Dactylorhiza orchids provide an exudate that is a food source (whereas most of the genus is food-deceptive, having no nectar and no other reward); the common spotted orchid D. fuchsii has an oily exudate that is also rich in glucose and amino acids and is fed on by both honeybees and bumblebees (Dafni and Woodell 1986).

Whereas the above examples have oily stigmatic secretions, there are a few cases—for example, species of Anthurium—where the stigmatic fluid may be up to 8% sugar (Croat 1980). In some Asclepias species this same kind of sugary exudate flows away from the stigma and collects in a nectar reservoir where it is visited by pollinating insects, so producing a reward in a group that is normally rewardless.

In plants where exudates are used as food, the styles tend to be short or rudimentary and have a broad stigma, so that the pollen-receptive function and the growth of pollen tubes are both relatively resistant to damage.

4. Scents

Fragrances as rewards to flower visitors are found in at least seven different plant families, all from the Neotropics. Orchids are by far the most common examples, up to seven hundred species having been recorded as dispensing scent.

Orchids and Euglossine Bees

Many genera of orchids use scent as their main lure to flower visitors and offer no other rewards; perhaps 10% of all species of Orchidaceae fall into this category (van der Pijl and Dodson 1966). For most of these, their main visitors are bees from the Euglossinae subfamily, an exclusively Neotropical taxon common in the canopy of rain forests (Dressler 1982). These bees (about two hundred species) live in small primitively social groups or in solitary nests (chapter 18). Females gather nest materials and collect pollen and nectar in the normal bee fashion. However, the males, which are not associated with the nests and must forage for nectar for themselves through their unusually long lifespan of three to six months, will also gather flower scents, and in a fashion unique to this group.

Since their scent gathering is almost always from orchids (Lunau 1992b; Eltz et al. 1999; N. Williams and Whitten 1999), these animals are sometimes termed orchid bees. The orchids they visit are strongly fragrant but have no nectar and no accessible edible pollen. Instead, the male bees scrape up oily and waxy compounds from the scent organs on flower (usually on the orchid labellum). For this they use brush-like structures on their front tarsi that act like mops (fig. 9.5), taking up by capillarity the fragrances that seep out of the flower. The droplets of scent are transferred to a rake of hairs on the middle legs and then passed to a small opening on either of the very swollen hind tibiae. These openings bear fine feathery hairs that (p.226)

Other Floral Rewards

Figure 9.5 Brushes on feet of euglossine bees: (A) setae from front tarsal brush; (B) hind tibia, with slit surrounded by setae; (C) detail of hind tibial setae.

(Redrawn from photographs in Williams 1983.)

receive the scented material and pass it through a channel to a large hollow chamber within the leg. Here the perfumes are finally stored; the chamber has many internal ridges, each bearing masses of feathered hairs that take up the scented liquid (fig. 9.6). This tibial chamber functions as a perfume bottle, and each male euglossine is effectively carrying around its own built-in lure. A single male bee may carry up to 60 μ‎l of scent material (Vogel 1966).

The scents gathered contain some benzenoids but are predominantly monoterpenes, including classic floral fragrances such as cineole, myrcene, ocimene, pinene, eugenol, limonene, and linalool; any one flower may offer a mixture of 6–10 compounds (Dodson et al. 1969) from this range. In quite a few of the euglossine-visited flowers, the relatively unusual monoterpene trans-carvone oxide is present, and it may be a key attractant for these bees (Whitten et al. 1986; Teichert et al. 2008). There are indications that the bees also add compounds of their own making to the mix from glands within the tibia (fig. 9.6), perhaps making lipid materials that reduce the volatility of the scent mix and so prolong its useful life. From their labial glands, which act as extractors and carriers for the fragrances, they also add straight-chain lipid materials, which are then recycled back from the hind-tibial pockets for reuse, forming a “lipid conveyor belt” (Eltz et al. 2007).

The floral fragrances are so attractive to the males that with a few drops of eugenol or cineole on a filter paper, it is easy to attract large numbers of euglossines down from the canopy in most central and southern American rainforests.

It was initially assumed that the scents are subsequently released by the males for reproductive functions, perhaps specifically as pheromonal cues for reproduction (N. Williams 1982; Dressler 1982). However, females are not attracted directly to the scents in the flowers, and a simple sex-pheromone function therefore seems unlikely. Male behavior involves trap-lining between flowers, and the same route may be used by more than one male at different time intervals. At particular sites on their own route, males will rest on the vegetation and flutter their wings before flying up and circling the site for a while. Eltz, Sager, and Lunau (2005) showed that the males perform specific and intricate leg movements during this circling flight, transferring perfume from the tibial pouches to a tuft of hairs on the mid-tibia, where they are ventilated and wafted into the air by the wing movements, confirming that the scents are in use at this stage and that the males are emitting a puff of perfume into the air. But it is still unclear whether they are a signal to females, to other males, or to both. Often a few more males will arrive, presumably attracted by the scent. Females are attracted to the patrol routes, and particularly to these sites, but whether the attraction is the scent itself or the presence of a small lek of fluttering, circling, and conspicuous males, is debatable.

Issues of specificity are interesting in these particular associations. The bees depend heavily on the orchid fragrances they collect for their reproductive success, and the orchids likewise depend on the euglossine bees for pollination. However, each bee species needs to assemble its own unique and species-specific fragrance (p.227)

Other Floral Rewards

Figure 9.6 The tibial sponge-like glands in a male euglossine bee: (A) in situ, with slitlike entrance; (B) a cutaway view, including the gland tissue and the spongy tissues that store the scent; (C) a close up of the hairs making up the spongy storage tissue.

(Redrawn from photographs in Williams 1983.)

mixture; for example, three species of Euglossa have quite distinctive mixtures (table 9.2). To acquire their mixes they must normally visit more than one orchid species; so there is a constraint acting against full specialization. Eltz, Roubik, and Lunau (2005) showed that individual bees are less attracted to the orchid species they have previously visited, so they must learn and remember the fragrances they have already collected, and so are showing a limited kind of negative floral constancy. However, Dressler (1968) showed that 11 different species of orchid deposited and picked up their pollinia from 11 distinct sites on a euglossine’s body (fig. 18.14), so that effective specificity for the orchid can still be considerable.

How exactly do male bees foraging for fragrances benefit the plant? Scent gathering takes a significant time, and on at least some of their preferred orchid species, the male bees appear to suffer an intoxicating effect from the odors, becoming clumsy and rather sluggish, with a loss of full motor control (Evoy and Jones 1971). This may help the flowers to “manage” their visiting bees quite precisely and direct them into places they could otherwise avoid. For example, Stanhopea and Gongora orchids proffer their scents in tissues sited where the male bee must hang upside down, and when intoxication sets in and his control lessens, he loses his grip on the slippery surface and falls off onto the cushioning anthers below. Some Stanhopea species additionally have a chute-like arrangement to ensure that the bee lands correctly with his dorsal thorax aligned on the sticky pollinia. Even more specialist examples occur in the orchid genera Catasetum and Cycnoches, both with unisexual flowers. Catasetum orchids are pendant, the male flowers showy and the females drab, but both have the same scent (H. Hill et al. 1972); the males have a large viscid disk below the pollinia, and the rostellum projects forward into two antenna-like structures, such that a touch on these by a scent-gathering bee (working at the waxy scent-bearing tissues in the hooded labellum) causes the disk and the pollinia to be shot forward onto the bee’s back. The same bee visiting a female flower (which is inverted) has to hang upside down to gather scent, and the pollinia then swing off his back under their own weight, on an elastic thread, and are picked up on the grooved stigma below. The swan orchid Cycnoches operates similarly, requiring a visitor to hang upside down to gather scent and to let go with his hind legs, so that his body swings down and touches a cover that conceals the anthers, again causing an explosive reaction that shoots the pollinia onto the underside of his abdomen. (p.228)

Table 9.2 Fragrance Mixtures in Three Species of Euglossa Bee


E. cognata

E. imperialis

E. tridentata





Unknown sesquiterpene ketone




Methoxy cinnamic alcohol




Unknown A




Unknown B




Unknown C








Methoxy cinnamaldehyde








Benzyl benzoate




Methoxy cinnamyl acetate




Dimethoxy benzene




Benzyl cinnamate




Geranyl acetate
















Source: From Eltz, Roubik, and Lunau 2005.

Note: Values are percentages for any component making up at least 5% in any one species.

Perhaps even more extraordinary are the large and elaborate bucket orchids in the genus Coryanthes (Dodson 1965), which combine scent offerings with trapping (fig. 9.7). Male bees (usually Eulaema or Euglossa) are attracted by scent to the pendant flowers, where they find a textured zone at the base of the lip at which they scrape vigorously to gather scent in the normal way. In the process, some fall off and land in the “bucket,” a large cup formed by the labellum, into which drops of fluid drip and collect. The bees cannot climb out of this bucket except via a narrow hole near the base of the column; this first leads them beneath the grooved stigma (which extracts any pollinia the bee was carrying) and then, as they approach daylight and “freedom,” past the anthers and pollinia. It may take up to thirty minutes for a trapped bee to get free of the flower, because the last part of the route out is very narrow and the rostellum restrains the bee while pollinia are glued to his back. Each flower needs only one bee to pass through its exit route to fulfill both its male and female functions, and once this has occurred the flower ceases scent production and wilts within a few hours.

Other Examples of Fragrance as a Reward

Scents are also gathered from a solanaceous genus Cyphomandra (M. Sazima et al. 1993) by euglossine bees; three different species in this plant genus have very different scents and attract three different euglossines. As the male bees gather scent droplets from the flower, they push against the anthers and trigger a pneumatic bellows-arrangement such that the poricidal anthers eject jets of pollen and cover the bees’ sternum with pollen grains. Curiously, postpollination events here include a substantial enlargement of the corolla with an accompanying color change.

Some Neotropical species of Dalechampia vines have volatile scented oils instead of resins, which again are collected by male euglossines. In chapter 6 we also met examples of aroids, such as Sauromatum, that release pleasant scents within their trap chambers, along with the rather putrid odors from the spathe. Another example is Anthurium, where in some species the lower part of the spathe has perfume sacs, from which scents are gathered by euglossines (Croat 1980).

Something rather similar to the euglossine behavior (p.229)

Other Floral Rewards

Figure 9.7 Coryanthes (bucket orchid) structures: whole flower and cut-away view showing labellum and a bee emerging past the column.

(Modified from Barth 1985.)

is now known to occur in at least two groups of flies. Tephritid fruit flies pollinate Bulbophyllum orchids (Tan and Nishida 2005; Tan et al. 2006), and here the male flies land on the petals and climb to the orchid lip, forcing it open and lapping at the oily scented compounds secreted there. Then the fly is catapulted into the orchid’s column as the lip springs back, so picking up the pollinia. These flies subsequently use the phenylpropanoids from the flower, probably to make their own pheromone. Fruit flies in the subfamily Dacinae, particularly the genus Bactrocera, also collect floral scents, mainly from orchids, that they store in their rectal glands and use as a pheromone (Nishida et al. 2009).

Although not strictly volatile scents, pyrrolizidine alkaloids are acquired from various parts of their host plants (including flowers) by some danaid butterflies, and these can become part of their pheromones as well as of their defenses (Boppré 1978; Reddy and Guerrero 2004).

5. Floral Tissues

In a few instances, particularly in the more basal plant families, special areas of a flower are modified as food bodies, which have high contents of carbohydrates, lipids, or proteins, and flower visitors will nibble or scrape away some of this tissue to eat. The modified areas are often at the base of petals or the tips of stamens and are derived from epidermal or parenchymal cells.

Consumption of such tissues requires mouthparts that can chew, so this phenomenon is most commonly found in beetles, but also in some birds and a few bats. Floral food bodies are primarily provided with translocated carbohydrate reserves (sugars and starch) from the phloem; much more rarely they are enriched with protein, as reported in Calycanthus, which is fed on by beetles (Rickson 1979). Some bat-visited flowers, rather surprisingly, offer sugary bracts that are eaten (e.g., Freycinetia, Cox 1982; and chapter 16). However, cytoplasm is also a possible reward, and one Epidendrum orchid has modified liquid-filled cells lining the corolla base that yield a cytoplasmic reward to visiting moths, whose proboscis tip is covered in tiny spines (chapter 14) that can scrape at the tissues.

Whenever a significant part of a flower is eaten by chewing or scraping, it is essential that the flower as a whole is relatively sturdy and relatively long-lived. It is also necessary that visitors are attracted away from the ovules and anthers and toward the expendable parts, and this is probably achieved by localized odor cues.

6. Other Possible Nonfood Rewards

Brood Sites

Flowers functioning as a brood place could be considered as a further possible reward offered by particular plants. This scenario occurs where a flower-eating or seed-eating animal lays its eggs in flowers (which would normally make it a floral parasite), but then gets exploited in turn by the flower as a pollen vector. Simple examples of this occur in large-headed flowers, such as thistles, a favorite brood site for many flies.

As an alternative to (or an extension of) this, the (p.230) progeny of the flower visitor, once hatched from the eggs, may consume the seeds of their host plant. Probably the plant then gets a net loss overall, and the mutualism breaks down, although some examples of this nursery pollination do provide a net benefit to the plant (chapter 26). In a very few spectacular examples these brood-site mutualisms have been elaborated into active pollination, as in Yucca and in Ficus, where the seed parasites of a plant have become the key pollinator. These cases are again dealt with fully in their own right in chapter 26.

Microclimatic Protection and Warmth

Flowers can offer suitable shelter from rain and wind for many small insects, and a number of bees are particularly noted for taking shelter in flowers or using them as sleeping places, at which time a certain amount of pollen is then exported on the body, a concept called shelter pollination. This practice occurs especially in the males of solitary bee species, which lack their own nest; a well-known temperate example is Chelostoma florisomne, which can often be found sleeping in the pendant flowers of harebells. Serapias orchids are also quite common sleeping sites for bees. In the eastern Mediterranean, clusters of scarab beetles commonly occur overnight in bowl-shaped flowers (chapter 12). Certain beetles in the genus Pria may have more specific relations with female Leucadendron flowers, which are more cup-shaped and enclosed than the male flowers and are used apparently specifically and solely as shelter from frequent rain (Hemborg and Bond 2005), being visited 90% more often on wet than on sunny days.

More than simple shelter may be on offer however. Flowers quite often exhibit their own internal microclimate (fig. 9.8, and other examples in fig. 8.10) by virtue of relatively elongate, enclosed corollas, and thus they offer significant amelioration of climatic conditions to their visitors. Within a moderately large and sturdy corolla tube there may be substantial temperature increments, giving a microclimate that allows a visiting insect to warm up, although the primary benefit to the plant may be that of potentially speeding up ovule maturation, pollen tube growth, fertilization processes, and seed development (Kjellberg et al. 1982). Bumblebees will choose to forage at warmer flowers, given a choice (Rands and Whitney 2008).

There are more specific cases where flowers offer warmth to insects. This reward to a visitor may be a side effect, in that the main benefit accruing to the plant may again be accelerated reproductive development, or a faster volatilization of plant scents, or even a better resemblance to a warm piece of dung or carrion. But in cooler habitats it may play a significant secondary role as a means of attracting flying insects to a flower (Hocking and Sharplin 1965; Cooley 1995), thus improving their energy budgets by reducing thermoregulatory costs (which will be discussed in the next chapter). Heat from cones is known to attract pollinators to cycads (Terry et al. 2007) and seed-feeding insects to conifers (Takács et al. 2008). Whitney et al. (2008) showed that warmth and sugar concentrations in angiosperm flowers were assessed independently by bumblebees, but sucrose levels usually took precedence over warmth (or at least over nectar temperature).

Additional warming in flowers can be achieved in at least four different ways:

  1. 1. THERMOGENESIS: Thermogenic tissues occur in at least ten plant families, mainly among the basal angiosperms (Thien et al. 2000), and are especially well studied in aroids and palms. Floral tissues in various aroids can generate heat from the spadix, often at specific times of day (e.g., Bay 1995; Seymour and Schultze-Motel 1998). In Syngonium the warming may occur each night during a three-day lifespan, and in some species there are two periods of warming on particular nights (Chouteau et al. 2007). In Homalomena, thermogenesis increased the floral odor emissions from the spadix which specifically attracted Parastasia scarab beetles that served as effective pollinators, whereas other beetles were unaffected by the heat or scent and visited the flowers indiscriminately at all stages (Kumano-Nomura and Yamaoka 2009).

    Some thermogenesis also occurs in members of the Annonaceae, where the closed floral chamber of Xylopia has been recorded as 8°C above the ambient temperature (Ratnayake et al. 2007). Night-flowering water lilies in both South America and West Africa are moderately thermogenic too and have specific associations with scarab beetles, suggesting a coevolved specialized relationship going back at least to the early Cretaceous (Ervik and Knudsen 2003). Seymour and Matthews (2006) observed beetles spending long periods in these flowers, in the absence of any nutritional reward, and suggested that the temperatures maintained (p.231)

    Other Floral Rewards

    Figure 9.8 Microclimate within a flower patch, here for Justicia aurea in Costa Rica, showing the higher relative humidity and lower temperatures within the patch, especially in insolated areas (A). The solid bars show flower height.

    (Modified from Willmer and Corbet 1981.)

    in water lilies are precisely adjusted to reward the captive beetles by allowing their active mating behaviors to continue.

  2. 2. HIGHLY ABSORPTIVE SURFACES: Flowers that are dark in color are likely to be particularly absorptive of solar radiation and may therefore warm up well above ambient temperatures; this warmth would be especially useful at dawn when other possible sites are still cold. The Mediterranean iris Oncocyclus has large, dark-colored flowers, with hidden pollen and no nectar, and in Israel it is not visited in the daytime but does provide a night shelter to solitary male bees. These bees emerge from the iris flowers earlier than from any other site at dawn, when the irises are around 2.5°C above air temperature (Sapir et al. 2006); it appears that floral heat is the only reward on offer here.

    High absorptivity may also be achieved by specific cell structures, for example, the poppy Papaver radicatum from arctic regions, in which the inner layer of the petal epidermis is papillate and traps light reflected from the underlying mesophyll cells (Q. Kay et al. 1981).

  3. 3. PARABOLIC REFLECTION: Some bowl-shaped flowers have unexpectedly raised internal temperatures (p.232) at their centers. This phenomenon is generally associated with highly reflective white or yellow internal surfaces and an effectively parabolic shape (fig. 9.9), giving maximum reflection of the incoming radiation onto the center of the flower (Kevan 1975c; Heinrich 1993). Insects basking in this central zone can have a body temperature 5–15°C above the ambient air temperature. Cup-shaped flowers of this kind may therefore be especially useful at high altitude or latitude (chapter 27) or in the early spring in temperate habitats. There are also instances of nodding flower heads in some high-altitude plants whose intrafloral temperature is kept above ambient by reflection from the substratum.

  4. 4. SOLAR TRACKING (HELIOTROPISM): Solar tracking occurs in at least 18 plant families, most familiarly in the sunflower (Helianthus) where it can be easily observed occurring en masse in a field crop. In effect the stalk rotates so that the corolla is always pointing directly at the sun through the course of the day (fig. 9.10), thus achieving maximum warming (Kevan 1975c, 1989; Ehleringer and Forseth 1980; Kjellberg et al. 1982; Luzar and Gottsberger 2001). Heliotropism tends to occur in flowers from warmer climates that flower early in the season when pollinators are scarce. For example, the Mediterranean marigold (Calendula arvensis) traverses an angle of about 20° east to west each day and can thus maintain a 20°C temperature excess, enough to attract bombyliid flies, which warm up sufficiently to fly on to another flower (Orueta 2002). At least some of the reflective bowlshaped

    Other Floral Rewards

    Figure 9.9 Parabolic reflection, with Arctic flowers shaped to act as internal reflectors, warming the ovules.

    (Modified from Kevan 1975a.)

    flowers from northern tundra or polar habitats (e.g., some Papaver, Dryas, Pulsatilla, and Ranunculus species) also use this strategy.

    In heliotropic flowers the stalk undergoes continual slow movements, which in Ranunculus adoneus involve an eastward-bending of the peduncle (by differential growth on the shaded side) in the morning, with gradual unbending through the day (Sherry and Galen 1998). This is controlled by light at the blue end of the spectrum (Stanton and Galen 1993). It has clear benefits to the plants, so that Ranunculus flowers that were artificially restrained (Galen and Stanton 2003) had about 40% fewer pollen grains germinating than those undergoing their natural solar tracking.

Some flowers are known to combine several of the above effects and act as “micro-greenhouses,” their enclosed structure and reflectance properties allowing noticeable internal warming. Crocus flowers, for example, can be 2–3°C above ambient air in cold weather, which will stimulate opening of the corolla, access by pollinators, and pollen tube growth (McKee and Richards 1998); white and purple varieties warm up more than yellow ones. Narcissus flowers can have an internal temperature excess of 8°C in early spring, especially around the stigma and anthers (fig. 9.11); Andrena bees caught inside the flowers had markedly raised temperatures, and their visitation rate was positively related to the floral temperature (C. Herrera 1995b). Even more precisely, Jewell et al. (1994) noted that keel temperatures in Lotus corniculatus were higher in morphs with dark keels than in those with light keels and that the darker morphs tended to occur in the cooler microsites within a population. Given that bees can choose flowers on the basis of their warmth and can learn to associate flower color with flower temperature (Dyer et al. 2006; chapter 18), further observations of floral temperature increments in natural situations are much needed.

On the other hand, some flowers in hot climates may have a problem keeping the gynoecium cool and thus avoiding damage to the carpels. Some tropical Convolvulaceae flowers were shown to exhibit strong evaporative cooling effects, and if greased to prevent such evaporation, their internal organs could overheat (Patino and Grace 2002). The flowers also showed nonrandom orientation, pointing toward, but not directly at, the sun, which may have facilitated transpiration (Patino et al. 2002). Whether floral cooling could also (p.233)

Other Floral Rewards

Figure 9.10 Solar tracking, or heliotropism (A), and the resultant temperatures inside (open circles) and outside (closed circles) in (B) Papaver and (C) Dryas flowers. (Parts (B) and (C) drawn from data in Hocking 1968.)

Other Floral Rewards

Figure 9.11 Variation in temperature within Narcissus longispathus at four points along the corolla, showing the higher temperature close to the anthers and style.

(Modified from data in C. Herrera 1995b.)

be of benefit to pollinators remains unclear, but it would not be unexpected in very hot climates, where flying insects can easily overheat (chapter 10).

Meeting Places

Flowers can also offer a kind of reward to visitors in that they provide a reliable place to encounter other flower visitors. This may be particularly useful for mating opportunities, or for predatory opportunities. This theme will be discussed in more detail in chapter 24.

7. Overview

Most of the rewards discussed here are very minor in a numerical sense, although they may be the key to some particularly fascinating pollination systems. They do open up possibilities for new dimensions in animal-flower interactions, many of them currently underexplored. In fact these rather unusual kinds of rewards are always worth bearing in mind when investigating new interactions, and may prove to be rather more commonplace than is presently appreciated.