Bird-pollinated flowers in an evolutionary and molecular context

Journal of Experimental Botany, Vol. 59, No. 4, pp. 715–727, 2008

doi:10.1093/jxb/ern009 Advance Access publication 7 March, 2008

FLOWERING NEWSLETTER REVIEW PAPER

Bird-pollinated flowers in an evolutionary and molecularcontext

Quentin Cronk* and Isidro Ojeda

Botanical Garden and Centre for Plant Research, University of British Columbia, 6804 SW Marine Drive, VancouverV6T 1Z4, Canada

Received 2 November 2007; Revised 21 December 2007; Accepted 7 January 2008

Abstract

Evolutionary shifts to bird pollination (ornithophily) have

occurred independently in many lineages of flowering

plants. This shift affects many floral features, particularly

those responsible for the attraction of birds, deterrence

of illegitimate flower visitors (particularly bees), pro-

tection from vigorous foraging by birds, and accurate

placement of pollen on bird’s bodies. Red coloration

appears to play a major role in both bee-deterrence and

bird-attraction. Other mechanisms of bird-attraction in-

clude the production of abundant dilute nectar and the

provision of secondary perches (for non-hovering birds).

As a result of selection for similar phenotypic traits in

unrelated bird-pollinated species, a floral syndrome of

ornithophily can be recognized, and this review surveys

the component floral traits. The strong convergent

evolution evident in bird-pollinated flowers raises a ques-

tion about the nature of the genetic mechanisms un-

derlying such transitions and whether the same gene

systems are involved in most cases. As yet there is too

little information to answer this question. However,

some promising model systems have been developed

that include closely related bee and bird-pollinated

flowers, such as Ipomoea, Mimulus, and Lotus. Recent

studies of floral developmental genetics have identified

numerous genes important in the development of the

floral phenotype, which are also potential candidates for

involvement in shifts between bee-pollination and bird

pollination. As more whole-genome information becomes

available, progress should be rapid.

Key words: Anthocyanin pigmentation, bird-pollination,

candidate gene, developmental genetics, honey-eaters,

hummingbirds, nectar, ornithophily, pollination syndrome,

sunbirds.

Introduction

The concept of pollination syndrome, whereby specificfloral traits are associated with particular pollinationmechanisms, dates back to the work of the Neapolitanbotanist Federico Delpino (1833–1905). The attractionand utilization of a specific group of animals forpollination, for instance, is associated with specificcharacteristics of flower morphology, colour, nectar,odour, and orientation (Faegri and van der Pijl, 1966;Proctor and Yeo, 1973; Fenster et al., 2004). However,pollination systems are often more complex than floralmorphology would at first sight suggest, and this has ledto criticisms of the pollination syndrome concept, mainlybased on the evidence that flowers attract a broaderspectrum of visitors than expected (Waser et al., 1996).Nevertheless, there is ample evidence supporting a strongassociation between certain floral traits and functionalgroups of pollinators that exert similar selective pressures(Fenster et al., 2004).One well-recognized syndrome of floral traits is that

associated with bird pollination (ornithophily). Ornith-ophilous flowers (Fig. 1) are very often red with copiousdilute nectar. Furthermore they lack characters associatedwith other pollination syndromes, such as scent.In this review the main phenotypic traits of bird-

pollinated flowers are summarized and discussed. Bird-pollination has evolved many times (usually from bee-pollination) and the aim is to highlight the majorphenotypic convergences in plants with this pollinationsyndrome. The convergent evolution of this floral pheno-type raises questions about the genetic mechanismsunderlying such transitions and whether the same genesystems are involved in all cases. Three promising modelsystems are considered in this review. The first isa transition in the genus Ipomoea, where changes in the

* To whom correspondence should be addressed. E-mail: [email protected]

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control of the anthocyanin biosynthetic pathway areassociated with shifts in flower colour from purple to red,and shifts from bee to hummingbird pollination. Thesecond system is the genus Mimulus, where changes offlower colour and shape underlie a transition to bird-pollination. In this case, a single quantitative trait locus(QTL) of large effect controls the pigmentation of theflower and influences relative visitation rates of bees andhummingbirds. Finally, a transition to bird pollination isdescribed in the legume genus Lotus, associated withdifferences in colour, flower orientation, flower size andpetal morphology. We conclude by highlighting candidategenes that could potentially shed light on the evolution ofthis syndrome.

The syndrome of ornithophily

The birds

Many birds will casually visit flowers in search of food,often primarily to seek insects concealed in inflorescencesalthough they will take nectar if it is available. Flowervisiting of some sort has been reported in as many as 50families of birds (Proctor and Yeo, 1973; Proctor et al.,1996). However, three families of birds have evolved asmajor groups of flower specialists. These are the hum-mingbirds (Trochilidae), the sunbirds (Nectariniidae), andthe honey-eaters (Meliphagidae) (Fig. 2).Hummingbirds are exclusive to the New World, ranging

from southern South America to Alaska with the highestdiversity in the northern Andes (Grant and Grant, 1968).As hummingbirds visit flowers by hovering there is no

need for a perch and, in consequence, some hummingbirdflowers are long and pendulous. Hummingbirds havebeaks that are highly specialized for nectar feeding, eventhough insects form a normal part of their diet, necessitat-ing a remarkable flexibility of the jaw (Yanega andRubega, 2004). They have undergone a major evolution-ary radiation in South America and a secondary radiationin North America (Mayr, 1964). Fossil evidence fromEurope, however, suggests that the early evolution of thisgroup was not exclusive to the New World (Mayr, 2004).Sunbirds and spiderhunters (Nectariniidae) are the major

group of pollinating birds in Africa and Asia. Thehoneyeaters (Meliphagidae) are very important pollinatorsof styphelioid Ericaceae (Epacridaceae), Myrtaceae andProteaceae in Australia and they extend north to Wallace’sline and east to New Zealand and Hawaii.Other important groups include the American orioles

(Icteridae) in North and South America, the honeycreepers(Thraupidae) in tropical America, and the Hawaiianhoneycreepers (Fringillidae, subfamily Drepanidinae) inthe Hawaiian Islands. In Africa the White-eyes (Zoster-opidae) are another important group, as are the SouthAfrican sugar-birds (Promeropidae).Bird pollination is particularly common in relatively

aseasonal tropical and subtropical regions as flowers andnectar are available year-round to support nectarivorousbirds. It tends to be absent or rare in regions in whichvegetation has a long dormant period. North America isan exception, as hummingbirds migrate north during thesummer. The migration is particularly remarkable on theNW coast where hummingbirds migrate as far as Alaska.

Fig. 1. Forms of bird-pollinated flowers. (A) Strelitzia reginae. (B) Erythrina suberosa, (C) Babiana ringens with sterile inflorescences for perchingbirds (arrow). (D) Cadia purpurea, a member of the Genistioids with radial symmetry with nectar globes (arrow). (E) Ipomopsis aggregata. (F)Phygelius capensis. (G) Psittacanthus sp. (H) Fritillaria suberosa with nectar globes (arrow).

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Bird pollination is almost entirely absent in Europe and inAsia north of the Himalayas. In Europe, although there arereports that some passeriform birds occasionally feed onnectar (Kay, 1985; Proctor et al., 1996; Schwilch et al.,2001; Merino and Nogueras, 2003), there is only onereport of a bird-pollinated native plant, Anagyris foetidaL. (Leguminosae). In Spain this is apparently pollinatedby three warblers, Phylloscopus collybita Vieillot, Sylviaatricapilla L., and S. melanocephala Gmelin (Ortega-Olivencia et al., 2005).

Ecology of bird pollination

Some attributes of birds, such as long flight distances andhigh visual acuity, make them excellent pollinators,

especially valuable during inclement weather conditionswhen other pollinators, such as bees, are inactive. Birdsmay, therefore, be important supplemental pollinators inenvironments where insects have low population densities,such as high altitude ecosystems (Van der Pijl andDodson, 1966), dry environments (Stiles, 1978), isolatedislands where insect colonization has been poor (Dupontet al., 2004; Micheneau et al., 2006), and for plantsflowering during winter months when insects are few(Kunitake et al., 2004).However, birds are large and require more energy than

insects. For this reason plants with bird-pollinated flowerstend to put more energy into nectar production and oftenproduce larger flowers to accommodate their avian

Fig. 2. Approximate world distributions of the three main families of flower visiting birds: hummingbirds (Trochilidae), sunbirds (Nectariniidae), andhoney-eaters (Meliphagidae).

Flowers and bird pollination 717


pollinators. Bird-pollinated plants may also deploy moreresources in floral structures that protect against thieves oftheir abundant nectar (Stiles, 1978). Environments withlow plant productivity may be limiting for nectar pro-duction, and for this syndrome in general. The tropicalforest understorey, with limited photosynthetic rates, hasrelatively few bird-pollinated plants (Stiles, 1978) and thesame appears to hold true for cold, hyper-arid, andnutrient-poor environments. The syndrome is particularlycommon in tropical and subtropical shrublands, openwoodland, and riverine communities.

Perching versus hovering

The behaviour of those birds associated with ornithophilycan be broadly divided into two types, hovering andperching. The hovering behaviour is found mainly inhummingbirds, but is also present in some families ofpasseriforms. In hovering, birds collect nectar withoutlanding on the plant, which may therefore have hanging orpendant flowers. On the other hand, perching birds landon stems, leaf stalks, adjacent branches, and flower buds,which must provide an adequate perch. Low herbaceousplants may be pollinated by birds that perch on theground, and they usually orient their flowers verticallyerect. Examples include Lotus berthelotii Masf. and itsrelatives in the Canary Islands (Olesen, 1985), andGastrolobium praemorsum (Meisn.) G. Chandler & Crispin southwest of Western Australia (Keighery, 1982).Among birds, flower foraging by perching is more

widespread and involves fewer specialist adaptations thanforaging while hovering. Flower visiting has evolved inseveral families of perching passeriforms both in the NewWorld and the Old World. Unlike hummingbirds, passeri-forms tend to forage and travel in groups and can beeffective in cross-pollinating even large trees (Stiles,1981). In the New World, pollination by perching passeri-forms appears to have evolved recently, usually, althoughnot always, involving plant species in genera alreadyadapted to hummingbird pollination (Toledo, 1975;Cruden and Toledo, 1977).

Hermit versus non-hermit hummingbirds

Bird behaviour is important in determining the nature ofbird–plant interaction. The vast majority of bird-pollinatedspecies in the Neotropics, are herbs, shrubs, small trees,and epiphytes, and rarely large canopy trees. Solitarybehaviour and territoriality in hummingbirds do not allowthe levels of pollinator saturation or cross-pollinationnecessary for the effective pollination of large canopytrees (Stiles, 1975), which therefore tend to be bee-pollinated. Hummingbirds may be divided into twosubgroups, hermits and non-hermits, and this division hasimportant implications for pollination.

The majority of hermits have long, curved bills anda tendency to forage on flowers with long, curvedcorollas. They inhabit the understorey of the tropicalforest and decrease in abundance and diversity at higherelevations and in dry habitats. Hermits are non-territorialwith a traplining method of foraging. Traplining involvesvisiting many plants sequentially for short visits, flyingfrom plant to plant, often over some distance, and ishighly effective in promoting cross pollination (Snow andSnow, 1972; Stiles, 1975, 1981).Non-hermits have short straight bills and a tendency to

hold territories and thus non-hermit pollination behaviourfavours self-pollination. Non-hermits are widely distrib-uted but have their greatest diversity in the tropicalhighlands (Snow and Snow, 1972; Stiles, 1975, 1981).The North American hummingbird fauna comprises a fairlyhomogeneous assemblage of non-hermit hummingbirds andprobably for this reason North American ornithophilousplants are fairly uniform in floral form compared to thoseof South America (Grant, 1966; Stiles, 1981).Interestingly, the existence of these two types of

hummingbird has had a strong influence on patterns offloral diversity in the genus Heliconia (Heliconiaceae)(Stiles, 1975, 1981). Heliconia species that are pollinatedby hermit hummingbirds usually have long, curvedcorollas, and grow in the forest understorey where light islimiting. They grow in small, scattered clumps andproduce a few flowers over a long flowering period. Dailynectar production is low with usually moderate to highnectar concentration (Stiles, 1975), and hermit humming-birds trapline between clumps.By contrast, non-hermit associated Heliconia species

grow in large clumps with highly synchronous flowering,producing many flowers during a definite floweringperiod. These Heliconia species usually have shortstraight corollas and are usually found in highly pro-ductive environments of forest gaps or along rivers withabundant light (Stiles, 1975). They produce a largequantity of relatively dilute nectar. Territorial non-hermithummingbirds will defend these clumps because of theirabundant nectar reward, which is beneficial for pollinationintensity but not for cross-pollination between clumps.

Major groups of angiosperms with bird pollination

Bird pollination is widespread in the flowering plants andappears to have evolved many times. It is present in some65 flowering plant families and in most of these itprobably represents a separate origin, usually from a bee-pollinated precursor. However, bird pollination is notablyabsent in some of the largest families of flowering plants.In Asteraceae, for example, only the South Americangenus Mutisia is bird pollinated (Buzato et al., 2000;Proctor et al., 1996). On the other hand, there are somelarge clades in which bird pollination is particularlycommon, such as in the monocot order Zingiberales.

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Families of this order are Cannaceae, Costaceae, Heli-coniaceae, Lowiaceae, Marantaceae, Musaceae, Strelitz-iaceae, Zingiberaceae, and bird pollination occurs in all.Genera such as Canna (Cannaceae), Strelitzia (Strelitz-iaceae), Heliconia (Heliconiaceae), and Costus (Costaceae)are well known for their showy bird-pollinated species. Inthe Costaceae, for instance, ornithophily associated withhummingbirds evolved several times in the neotropics frombee-pollinated ancestral species (Specht, 2006).Ornithophily has also evolved several times, mainly

from bee-pollinated ancestors, in many families of theeudicots. A common pattern within these groups is theparallel evolution of the traits associated with ornithophilyamong non-closely related groups of plants. For example,within Gesneriaceae many Columnea species have similarmorphological traits—trailing epiphytes with fairly largeand showy red flowers—with another group, Aeschynan-thus. Columnea is distributed in Central and SouthAmerica and is pollinated by hummingbirds, whereasAeschynanthus is distributed in the Palaeotropics.The multiple origin of bird pollination in the flowering

plants raises the question of what pre-adaptations promotethis evolutionary transition. Two features, commonlyassociated with bee pollination, appear to be permissiveof a transition to bird pollination. One is floral zygomor-phy (monosymmetry or asymmetry) and the other is thepossession of a floral tube. Bird-pollination is common inmany families with strongly zygomorphic flowers (e.g.Scrophulariaceae, Heliconiaceae, Gesneriaceae, Legum-inosae). This feature is generally considered to be anadaptation to bee pollination and allows precise placementof pollen on the body of the bee. It seems that theseadaptations may also be important for bird-pollination.The same applies to the character of perianth segments

being connate into a tubular corolla (or the presence ofa tubular hypanthium in Passiflora and Fuchsia). Tubularflowers originally evolved for insect pollination but areequally suitable for the probing foraging of bird’s beak.Hummingbird flowers in North America are predomi-nantly sympetalous dicots and it has been suggested thatthis corolla condition, with its tubular shape, is anotherpre-adaptation to hummingbird pollination (Grant andGrant, 1968).

The floral phenotype

Types of floral adaptation

Floral adaptations to bird pollination fall into four broadtypes: (i) attraction mechanisms; (ii) exclusion mecha-nisms; (iii) protection mechanisms; and (iv) pollinationmechanisms (Grant and Grant, 1968).Attraction mechanisms are those such as copious nectar

and vivid floral display that attract birds to flowers. Thefloral display may be just red or orange, or a combination

of contrasting colours, including orange, yellow, green, andblue (‘parrot colours’). Strelitzia reginae W. Aiton, forinstance, presents a striking display of orange and blue.Exclusion mechanisms are those features that help to

deter illegitimate flower visitors that might otherwiseinterfere with pollination and rob nectar. Red colour, longand narrow floral tubes, and the absence of insect landingplatforms are the most obvious of these and are discussedfurther below. Pendent flowers, as in Aquilegia formosaFisch. ex DC., are difficult for insects to work but easy forhummingbirds. Recurving petals, as in Ipomopsis aggre-gata (Pursh) V. Grant, or the short and recurved lower lipof Mimulus cardinalis Dougl. ex Benth., serve to denyinsects a landing platform and similarly make the flowersdifficult to work except by hummingbirds. In Trichostemalanatum Benth., the long-exserted stamens are recurved toblock entrance to the tube.Protection mechanisms are also important, as birds are

large and potentially destructive pollinators. A commonform of protection is provided by mechanical strengthen-ing of the flower by the formation of sclerenchyma orcollenchyma tissue in various floral parts. The ovary andovules, often situated near to the nectaries, are particularlyvulnerable to the probing of bird’s beaks. Protection ofovules takes many forms. There may be separation ofovary and nectary, either by the sheathing of the ovary bya staminal tube, or by a stalked or inferior ovary.Alternatively, there may be a groove formed by thecorolla to guide birds’ beaks to the nectary withoutcausing damage, or ridges of the corolla to provide directprotection to the ovary. In addition, the style may beprotected in a groove formed from ridges of the upperpetals, as in Justicia californica (Benth.) D. Gibson. InPenstemon it is the nectaries rather than the ovary thatshift. In bird-pollinated species, the nectaries are displacedupwards from the base of the ovary to the outer bases ofthe upper pair of stamens.Pollination mechanisms are those that enhance the

precise deposition of pollen on bird and stigma. Theseinclude both spatial and temporal relations of the re-productive organs to the position of pollinating birds. Thelong exserted stamens of bird-pollinated species ofAquilegia (e.g. A. formosa), Fuchsia, and Ribes (e.g.R. speciosum Pursh) dust birds’ heads or even backs, withpollen. In the radially symmetrical Ipomopsis aggregatathe ring of five stamens place pollen all around the base ofthe birds’ beaks. Zygomorphic flowers, on the other hand,tend to place pollen on the top of the beak or on the top ofthe bird’s head.

Why red?

Explanations for the remarkably consistent association ofbird-pollination with red or reddish flowers take twoforms, either avoidance of bees (and other insect polli-nators), or attraction of birds.



It seems that red colour is not necessary to attract birds.There are examples known where birds are effectivepollinators of species with orange, yellow, and whiteflowers (and less frequently reddish violet and blueflowers) (Proctor and Yeo, 1973; Ortega-Olivencia et al.,2005; Micheneau et al., 2006). This has led to thesuggestion that avoidance of bees (which cannot see red)is more important than attraction of birds (Proctor andYeo, 1973; Proctor et al., 1996). Birds perceive colourover wavelengths ranging between 300 nm and 660 nm,whereas bee vision is in the range 300–550 nm. In theneotropical forests bird-pollinated flowers have beenshown to have typical median reflectance greater that 585nm, outside the visual range of bees (Altshuler, 2003).However it should be noted that bees can perceive (and dovisit) some flowers seen as red by humans, if they have atleast some reflectance in the shorter wavelengths as well(Chittka and Waser, 1997).However, as well as its invisibility to bees, the fact that

red is very readily detectable by birds is also likely to besignificant. For instance, the visual prominence of red maybe important for migratory hummingbirds, which caneasily detect red flowers when entering a new habitat andassociate it with reward (Grant, 1966). Indeed, theassociation of red flowers and bird pollination may beexplained via optimal foraging theory and the relativeefficiency of bees and birds in detecting red (Rodriguez-Girones and Santamarıa, 2004), with red flowers acting asa signal of high caloric reward (Raven, 1972). With theassociation between high energetic rewards and the colourred already well established, there may be strong selectivepressure for other bird-pollinated flowers to adopt this‘common advertising strategy’. However, there is a curioustwist in Fuchsia excorticata L.f. of New Zealand, inwhich a developmental change, from green to red flowercolour, signals lack of nectar reward in post-reproductiveflowers (Delph and Lively, 1989). Birds, therefore, avoidthe red flowers in favour of green.

Flower colour and its perception

Flowers that appear red to humans are of three types(Chittka and Waser, 1997). Some species have anadditional peak that stimulates the blue receptor of bees;for example, the red flowers of Dianthus carthusianorumL. are perceived as blue by bees, as this species hasa reflectance peak that stimulates the blue receptor ofbees. The red flowers of field poppies (Papaver rhoeas L.)have a reflectance peak below 400 nm and are perceivedby bees as ultraviolet. However, typical red hummingbirdflowers, such as Ipomopsis aggregata and Justicia rizziniiWassh., will be perceived as green by bees (Chittka et al.,1994; Chittka and Waser, 1997). These flowers onlystimulate the green receptor of bees, and there is noadditional peak of reflectance in other wavelengths. This

type of flower, with a peak only in the red, and with noblue or UV reflection, is more difficult for bees to detectthan flowers of other colours (Chittka et al., 1994; Chittkaand Waser, 1997).On the other hand, birds are tetrachromatic and they

have an additional UV receptor compared to humans,making colour perception in birds more complex than inmammals (Bowmaker, 1977). Further, they have oildroplets that can act as filters that increase the complexityof colour perception. Birds can see, in theory, twice thenumber of colours compared with trichromats (Odeen andHastad, 2003). It seems that birds do not have an innatepreference for the red colour, although most of them havetheir greatest spectral sensitivity and hue discriminationtowards the long wavelength end of the spectrum (Stiles,1981). Experiments with hummingbirds have shown thatthey learn to associate a range of colours with rewards andthat this behaviour can be modified (Proctor et al., 1996).Floral pigments (anthocyanidins and flavonols) have the

major impact on the wavelength of light reflected fromflowers. There are three major types of anthocyanidinpigments: pelargonidin (generally red), cyanidin (typicallymagenta or blue depending on pH) and delphinidin(generally blue). Bird-pollinated flowers are much morelikely to contain pelargonidin and much less likely tocontain delphinidin than flowers generally (Scogin, 1988).A general predominance of pelargonidin in tropical floras(Beale et al., 1941) has been attributed to the tropicaldistribution of hummingbird pollination (Harborne, 1976).A difference in pigment composition has been reported incomparisons between perching-bird and hummingbird-visited flowers (Scogin, 1988), with a greater prevalenceof cyanidin, as opposed to pelargonidin, in perching-birdflowers.

Nectar

Bird-pollinated flowers generally produce a large quantityof dilute nectar as the main pollinator reward. Nectarcharacteristics, such as (i) volume, (ii) sugar concentrationand viscosity, (iii) sugar composition, and (iv) amino acidcomposition, are extremely important in determining thesuccess of plant–pollinator interactions (Baker and Baker,1983a; Proctor et al., 1996) and nectars of bird-pollinatedplants tend to be recognizable as such.The volume of nectar in flowers is generally correlated

with the size of the flower (Baker, 1978). However, sizefor size, bird-pollinated plants tend to secrete largerquantities of nectar relative to bee-pollinated species. Thesame is true in bat-pollinated species. Some bat-pollinatedBombax species, for example, can produce between200–300 ll of nectar daily (Baker, 1978).Nectar concentration is a characteristic often inversely

linked to nectar volume. This holds true in bird-pollinatedflowers, which produce relatively dilute nectars but in

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large quantities. Mean sugar concentrations in nectars ofbird-pollinated flowers range between 20% and 26% (Pikeand Waser, 1981; Stiles and Freeman, 1993; Proctor et al.,1996) with extremes between 10% and 34% (Baker,1975). The sugar concentration of nectar determines itsviscosity, which is an important physical property that isthought to affect the ease of uptake of nectar by birds.Large quantities of nectar at low concentrations havetherefore been explained on the basis of constraints of itsuptake associated with viscosity (Baker, 1975), and nectarviscosity tends to remain constant even under differentenvironmental conditions (Proctor et al., 1996). However,dilute nectar with low sugar concentration is less optimalfor bees, and so this trait may be more anti-bee than pro-bird (Bolten and Feinsinger, 1978). Nectar with sugarconcentration below 18% is not beneficial to honeybeesbecause of the high energetic cost of evaporating water inorder to produce honey (Percival, 1965).Nectar sugar composition is also important. Nectar is

mainly composed of fruit sugars such as glucose andfructose (hexoses), and/or the disaccharide sucrose. Basedon composition, the following types of nectar have beendistinguished: (i) sucrose-dominant nectar, (ii) sucrose-rich, (iii) hexose-rich, and (iv) hexose-dominant (Bakerand Baker, 1983a). Hummingbird-pollinated flowers gen-erally have sucrose-dominant nectar, whereas flowerspollinated by passerine perching birds tend to havehexose-dominant nectar (Baker and Baker, 1983b, 1990;Freeman et al., 1984; Lammers and Freeman, 1986; Elisensand Freeman, 1988; Stiles and Freeman, 1993; Bakeret al., 1998; Perret et al., 2001). Bee-pollinated flowerscharacteristically have sucrose-rich or sucrose-dominantnectar (Baker and Baker, 1983a), so such nectar compo-sition in hummingbird-pollinated flowers that haveevolved from bee-pollinated flowers is not surprising.More difficult to explain are the hexose-rich nectars.Passerine birds often feed on fruits as well, and it has beensuggested that the ‘taste’ for hexose fruit sugars derivedfrom this (Baker and Baker, 1983b). Also, there isevidence that some Old World birds (such as Sturnidae,which includes some facultative nectarivores) have diffi-culty digesting sucrose (Schuler, 1977).Amino acids are another important constituent of nectar.

They provide a source of protein-producing substances,perhaps affect the ‘taste’ of the nectar (Baker and Baker,1983a) or stabilize the sugars in the nectar, i.e. avoidcrystallization (Baker and Baker, 1983a). Surveys havereported between 2–24 amino acids on nectar from differentspecies (Baker, 1978). Bird-pollinated flowers contain lowconcentrations of amino acids, which is because birds haveadditional sources of protein-building amino acids (Bakerand Baker, 1986). One exception to this trend has beenstudied in Erythrina (Leguminosae) pollinated by territorialorioles and tanagers, whose uptake of amino acids mainlydepend on this plant (Baker and Baker, 1982).

Corolla morphology in bird-pollinated flowers

Flower morphology associated with ornithophily candivide bird-pollinated flowers into five major groups(Proctor et al., 1996). In the brush-flower the flowers arearranged in clusters, usually in spheres or cylinders, withprotruding stamens, and pollen placement is generalized.The Australian flora is particularly notable for its brushflowers, for instance in Proteaceae and in Acacia species(Lara and Ornelas, 2001). Another common flower trait isthe hanging bell, producing copious nectar. Examples ofthis are found in Canarina (Campanulaceae) (Dupontet al., 2004; Valido et al., 2004), Fritillaria (Liliaceae)(Burquez, 1989; Peters et al., 1995), and Cadia (Faba-ceae) (Citerne et al., 2006).However many ornithophilous flowers have long sym-

petalous corolla tubes. Such corolla tubes differ fromthose of bee-pollination by being long and narrow (theshape of a birds beak rather than a bees body) and theinconspicuous size and position of the corolla lobes.Rather than forming a landing platform, as in bee-pollinated flowers, the lower corolla lobes are oftenreflexed under the flower so preventing the alighting ofinsects. This has been termed the ‘dogfish’ flower-type(Proctor and Yeo, 1973) from a fancied resemblance tothe backwards-sloping snout of elasmobranch fish. Thelong, narrow tubular corolla is important in deterring beesfrom accessing nectar. However, this trait may be circum-vented by nectar robbing (Lara and Ornelas, 2001) if thebase of the corolla tube is not protected by a robust calyx.The corolla tube may also be downcurved (arcuate) ina similar way to many bird beaks. There is also a benefitto being downwardly directed in that insect access is moredifficult. However, most North American hummingbirdshave relatively short straight beaks and, probably inconsequence, most North American ornithophilous flow-ers have rather similar short straight and narrow corollatubes (Fig. 3).Differences between corolla tubes of bee and bird-

pollinated species are well illustrated in the genusStreptocarpus (Gesneriaceae) (Harrison et al., 1999;Hughes et al., 2007). Between the bee-pollinated S. rexiiLindl. and the bird-pollinated S. dunnii Mast. there arefive major floral differences associated with pollinationsyndrome. S. dunnii has small flowers that are massed intolarge inflorescences, while in S. rexii the floral display isprovided mainly by the large individual flowers. S. dunniihas a cylindrical corolla tube suitable for probing bya bird’s beak, whereas S. rexii has an open funnel-shapedflower allowing for ingress by relatively large bees. Theorientation of the flowers is varied in S. rexii, while inS. dunnii all the flowers on the inflorescence face the single,large leaf that probably serves as a perching surface forbirds. S. dunnii has red flowers without nectar-guides,whereas S. rexii has pale violet flowers marked with the



dark nectar-guides that are often found in bee pollination.Finally, S. dunnii has a slightly longer adaxial than abaxialcorolla tube length, producing a straight or slightly down-curved flower. This morphology is suitable for anascending approach by a bird perching on the foliagebelow. S. rexii, on the other hand, has a shorter adaxialthan abaxial corolla length, giving a swept-back flower, soproviding an insect landing platform.

Other characters associated with bird pollination

Whereas red flower colour and characteristic nectar arenearly universal in ornithophily, a number of othercharacters are more minor or associated only with specificexamples of ornithophily. These include: (i) floral posture,(ii) secondary perches, (iii) protection, (iv) floral cluster-ing, (v) prominent nectar, and (vi) absent characters.Floral posture is closely correlated to pollinator

behaviour. Nodding flowers without perches such asFuchsia and bird-pollinated Aquilegia species are in-variably hummingbird pollinated, as hummingbirds havethe ability to hover under a downward facing flower anddirect their beaks upward into what is generally a longnectar path. This posture effectively excludes otherpollinators by making the flower difficult to access.Bee flowers, by contrast, are often horizontally oriented,

in accordance with the generally horizontal approachflight of bees and have horizontal or near-horizontal lowerlips for alighting. Flowers pollinated by perching birdsthat probe from above for nectar are often upwardlyoriented. The genus Tillandsia provides examples of both

types: short inflorescences with upwardly directed flowersfor foraging by birds perching on the stiff leaves, or longarching inflorescences bearing pendulous flowers forhummingbird pollination. The bird-pollinated Strepto-carpus dunnii has a single leaf, which probably functionsas a perch for foraging birds and the flowers areunidirectionally oriented and down-curved towards thesingle leaf. Related bee-pollinated Streptocarpus specieshave flowers oriented in all directions. The South AfricanPhygelius capensis E. Mey. ex Benth. has flowers that aresomewhat resupinate, turning back towards the stemsfrom where they may be easily probed by perching birds.By contrast, insect pollinated and hummingbird pollinatedflowers tend to face outwards towards the incoming flightpath of the pollinators.Secondary perches are important for facilitating polli-

nation by birds requiring a perch for floral foraging. Themost striking example is provided by the ‘rat’s tail’babiana (Babiana ringens Ker Gawl.) (Anderson et al.,2005). This produces completely sterile robust inflores-cence stalks functioning exclusively to provide a perch forforaging by the malachite sunbird [Nectarinia famosa(L.)]. The stiff inflorescence bract of Strelitzia providesa strong perch for birds working the Strelitzia flowers withtheir feet.Protection. Large vertebrate pollinators can be damag-

ing to all but the most robust of flowers. Perching birdsare frequently highly destructive of flowers and maydestroy them in the search for insects and nectar. For thisreason many flowers have protection in the form of toughconstruction of parts. Strelitzia reginae is an example ofa flower in which the floral parts are rather cartilaginous intexture and robust enough to survive rough foraging bypollinating birds.Floral clustering. Dense inflorescences are frequently

associated with pollination by perching birds in the OldWorld. Rather than flying from single flower to singleflower as bees and hummingbirds do, perching foragerswill exploit flower clusters by probing several flowersfrom the same perch. A good example is provided by therobust, multi-flowered inflorescences of Banksia, whichare pollinated by honey-eaters and other animals.Prominent nectar is frequently associated with bird

pollination in those flowers wide enough for the nectar tobe seen. Birds have great visual acuity and often nectar ispresented to birds with striking visual cues. The ‘nectarglobes’ often found at the base of hanging bell shapedflowers are an example of this. In Fritillaria imperialis L.,a plant known since the 18th century to attract birds tofeed on the nectar (White, 1789), these take the form ofprominent white depressions in the bases of the perianthsegments that fill with large drops of nectar. Nesocodonmauritianus (I.B.K. Richardson) Thulin has nectar that isprominent for a different reason, it is coloured red with anaurone pigment, a phenomenon which is surprisingly

Fig. 3. Length and width of corolla tubes of a sample of bird-pollinatedplants from western North America. Typical dimensions of the floraltube are from 15–27 mm long and from 2–5 mm wide, corresponding tobeak dimensions of North American hummingbirds. The speciesgraphed are: (1) Fouquieria splendens, (2) Ipomoea coccinea, (3)Ipomopsis aggregata (Sierra Nevada), (4) Salvia spathacea, (5) Trichos-tema lanatum, (6) Castilleja stenantha, (7) Diplacus puniceus, (8)Mimulus cardinalis, (9) Galvezia speciosa, (10) Penstemon barbatus,(11) Penstemon centranthifolius, (12) Penstemon newberryi, (13) Keckiaternata, (14) Justicia californica, (15) Bouvardia glaberrima, (16)Lonicera involucrata ssp ledebourii, (17) Epilobium canum ssp latifo-lium, (18) Aquilegia formosa ssp truncata, (19) Delphinium cardinale,(20) Delphinium nudicaule. Data from Grant and Grant (1966).

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common and generally associated with bird or reptilepollination (Olesen et al., 1998; Hansen et al., 2006).Characters conspicuous by their absence. These

include scent, night blooming, and nectar guides. Incontrast to bats, which visit flowers that often havea rancid or mousey smell, many birds appear to havea poor sense of smell and bird-pollinated flowers areusually odourless. Not all birds have poor olfaction andexceptions include vultures, tube-nosed Procellaridae(storm petrels and albatrosses) and the nocturnal kiwis(Apteryx spp), all of which rely heavily on olfaction forforaging. However, nectar-feeding birds do not belong tothis type and appear to forage by sight, and strictlydiurnally. Nectar guides (markings under visible orultraviolet light that guide insects to floral rewards) aregenerally absent in bird-pollinated flowers. This is un-surprising as, while the insect compound eye is opticallycrude, bird vision is excellent (with good depth percep-tion) rendering foraging within flowers easy.

The molecular basis for the evolution ofornithophily

The bird-pollination syndrome appears to have evolvedindependently very many times in a wide variety of plantfamilies and genera (Stiles, 1981; Thomson et al., 2000).The syndrome may be initiated with birds experimentallyforaging for insects or other sources of food into theflowers (Proctor and Yeo, 1973; Proctor et al., 1996),followed by selection of mutations that increase flowervisitation and effectiveness of pollen transfer by birds.The molecular basis for these mutations has beenaddressed using model systems, in which a shift from onesyndrome to another is examined in closely related specieswith contrasting flower morphology.

Some model systems

Ipomoea: The genus Ipomoea (morning glories) hastubular flowers in a wide variety of colours associatedwith different pollinators. The ancestral colour in thisgroup is blue/purple and together with other traits (broadfloral tube, moderate nectar production, inserted stigma,and non-versatile anthers) this indicates an adaptation tobee pollination (McDonald, 1991). In one clade, however,there has been a shift to red flowers and hummingbirdpollination, encompassing some six species (including I.quamoclit L.). Generally, the anthocyanin cyanidin, andits derivatives, produces purple flowers whereas pelargo-nidin and its derivatives result in red flowers. The geneflavonoid-3#-hydroxylase (F3#H) is important in control-ling pigment production, and the flower colour shift in theI. quamoclit lineage has been shown to be due to a down-regulation of the F3#H enzyme (Zufall and Rausher, 2003,2004). F3#H is directly responsible for the hydroxylationof anthocyanidin precursors at the 3’ position that is

required for the production of cyanidin rather thanpelargonidin. Furthermore the enzyme dihydroflavonol4-reductase (DFR), with a role downstream of F3#H,seems to have lost its substrate affinity in this species.Although the major change in this case is a shift in

flower colour, other flower traits, such as stigma position,flower tube width, and the amount of nectar produced,also distinguish the two pollination syndromes.

Mimulus: In this genus two closely related species, M.lewisii Pursh and M. cardinalis Douglas ex Benth.,display a great differences in floral characteristics. Theformer is pollinated mainly by bumblebees and has pinkflowers with a wide corolla, nectar guides, and a modestamount of nectar; the latter is associated with humming-bird pollination and has red flowers with reflexed corollalobes, a narrow corolla tube, and copious production ofnectar (Ramsey et al., 2003). A major QTL for flowercolour is associated with the allele YELLOW UPPER(YUP) that controls yellow pigment concentration (Bradshawet al., 1995, 1998). In M. lewisii the dominant allele YUPprevents carotenoid deposition, thus petals have only theirpink anthocyanin pigments; whereas in M. cardinalis, therecessive allele yup allows carotenoid deposition andflowers with red coloration. Flower colour is known tohave a very marked effect on pollinator visitation(Schemske and Bradshaw, 1999), and when the allele ofM. cardinalis yup allele is introgressed into the M. lewisiibackground, hummingbird visitation increases dramati-cally, whereas bee visitation is considerably lowered(Bradshaw and Schemske, 2003). This suggests that anadaptive divergence in pollination syndrome can beinitiated by a major change in flower colour alone. Nogene has yet been cloned as responsible for YUP and itsmolecular identity still remains unknown.

Lotus: Lotus is a large genus in the Fabaceae, containingabout 130 species divided into 14 sections. Lotus flowersare zygomorphic and typical of the papilionoid legumes.There are five petals: one dorsal (the standard) usuallylarge and conspicuous, two lateral petals (wings) and twoventral petals (keel petals) that enclose the stamens and theovary. Pollination takes place when a bee lands anddepresses the wings and the keel, forcing out a string ofpollen from the stamens located beneath the keel andplacing it in the underside of the visitor. Other floralfeatures of Lotus that are associated with bee pollinationare the horizontal position, yellow colour, sucrose-dominant nectar composition, and scent production.Bird pollination occurs in four species of Lotus from the

Canary Islands (Olesen, 1985; Valido et al., 2004). In thisgroup (also known as Rhyncholotus) the flowers are red-orange in a vertical position, with hexose-dominant nectar,and no scent production (Dupont et al., 2004). However,the most striking differences are the size and shape of thepetals (Fig. 4). In the bird-pollinated species the flowers



are about twice the size of those of typical bee-pollinatedspecies and the dorsal petal is bent backwards while theventral petals point up. The floral mechanism is effectivein depositing pollen either on the top of the head or on thethroat of a foraging bird (Fig. 4), but the original birdpollinator appears to be extinct.This system is a promising one in which to study the

role of petal identity in transitions between pollinationsystems. The genes responsible for dorsal petal identityhave been identified in Lotus japonicus (Regel) K. Larsen.These are the legume CYCLOIDEA-like genes (Citerneet al., 2003; Cronk, 2006; Feng et al., 2006), which havealready been shown to be involved in the shift to bird-pollination in the papilionoid legume Cadia (Citerneet al., 2006).

Candidate genes and future prospects

As noted above, the major trait associated with ornithoph-ily is red colour, implicating genes of the anthocyaninbiosynthetic pathway. So far, only one gene, flavonoid-3#-hydroxylase (F3#H) in Ipomoea, has been linked withshifts to bird pollination (Zufall and Rausher, 2004).Another gene, ANTHOCYANIN-2 (AN2) of Petunia, hasbeen linked with shifts in pollinators, although from beeto hawk-moth pollination (Quattrochio et al., 1998, 1999).However, the anthocyanin biosynthetic pathway is wellcharacterized and further genes involved in this pathway

will doubtless be linked to the evolution of birdpollination in the future.MIXTA, a transcription factor of the MYB family, has

also been related to changes in flower colour perception.However, the effect is not on the pigments itself; this genecontrols the production of conical cells of the epidermis(Noda et al., 1994; Glover and Martin, 1998). Althoughthis gene has not been examined between a pair of specieswith contrasting flower morphology and different pollina-tion syndromes, the bird-pollinated Lotus species hassubstantial differences in papillose conical cells andtrichomes on the dorsal and lateral petal compared withthe bee-pollinated Lotus species (I Ojeda and Q Cronk,unpublished data), and MIXTA is under investigation fora role in the evolution of this pollination syndrome inLotus.No gene linked to scent control has yet been studied in

the context of loss of scent in bird-pollinated species.However, one gene, S-LINALOOL SYNTHASE (LIS), hasbeen identified in shifts to moth pollination in someClarkia species. Different expression patterns are ob-served between C. breweri Greene, a moth-pollinatedspecies, and other bee-pollinated Clarkia species (Ragusoand Pichersky, 1995; Dudareva et al., 1996). Anotherscent gene, ODORANT 1, has been cloned and analysed inthe control of the synthesis of benzoid compounds in themoth pollinated Petunia axillaris (Lam.) Britton (Verdonk

Fig. 4. Flowers of Lotus species. Bird-pollinated species of (A) Lotus berthelotii Masf. and (B) L. maculatus Breitfeld, two members of the subgenusPedrosia s.l. (D) The model legume L. japonicus GIFU B129 and (E) L. arenarius Brot. a closely related species of the bird-pollinated species withinthe subgenus Pedrosia s.l. (C, F) Diagrammatic representation of the hypothetical mechanism by which a bird seeks nectar in flowers ofL. berthelotii. Arrows indicate the direction in which the dorsal petal is pushed. a, Dorsal petal; b, lateral petal; and c, ventral petal. (C, F) Modifiedfrom Olesen (1985).

724 Cronk and Ojeda


et al., 2005). However, as scent is absent in ornithophi-lous species, the transition to bird pollination willprobably involve the loss or down-regulation of genes.So far, no gene has been identified in the control of

nectar production and composition. Two QTLs have beenidentified as involved in controlling these traits in Mimulusand Petunia (Bradshaw et al., 1995; Stuurman et al., 2004).Recent studies in the control of petal identity and shape

in Lotus japonicus have identified two genes (CYC-LOIDEA-like genes) in the control of dorsal and lateralpetal (Cronk, 2006; Feng et al., 2006). Papilionoidlegumes are generally bee-pollinated but the genus Cadia,with pinkish-red, hanging, open bell-shaped flowers withno scent and copious nectar, displays the bird-pollinationsyndrome. The evolution of the hanging bell froma papilionoid ancestor is due to the over-expression ofCYCLOIDEA genes, reconfiguring petal identity andrestructuring the flower (Citerne et al., 2006).Tubular bird-pollinated flowers are often narrower than

their bee-pollinated relatives. While the molecular controlof this difference in corolla form has not been investigatedwith respect to a transition in pollination syndrome,mutants in the gene CINCINNATA show how suchmorphological differences could be controlled by a singlegene. In Antirrhinum flowers, expression of CINCINNATApromotes corolla growth, apparently through a positiveeffect on cell proliferation. Some cincinnata loss offunction mutants have rather narrow corolla tubes andsmall corolla lobes somewhat reminiscent of the ornith-ophilous phenotype (Crawford et al., 2004).The previous examples use a candidate gene-based

approach, comparing closely related species with contrast-ing flower morphology and different pollination syn-dromes. A genomics-based approach will soon bepossible as two complete genome sequences are due to bereleased shortly in genera with both bee and birdpollination (Lotus and Mimulus), which should allowrapid progress in these two systems.

Acknowledgements

We thank Dr Darren Irwin (UBC) for information about humming-birds and Daniel Mosquin (UBC) for kindly making availablephotographs of bird-pollinated flowers. We thank Lindsay McGheefor drawing Fig. 2, and the following for making available imagesunder the Creative Commons license for Fig. 1; van Swearingen@-Flickr (Strelitzia), Dinesh Valke (Erythrina), and Stan Stebs(Phygelius). QC gratefully acknowledges funding from the Discov-ery grants programme of NSERC (Canada). IO thanks a scholarshipfrom CONACyT, Mexico.

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Bird-pollinated flowers in an evolutionary and molecular context

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Transcript of Bird-pollinated flowers in an evolutionary and molecular context