beyond floricentrism - the pollination function of inflorescences

8/6/2019 Beyond Floricentrism - The Pollination Function of Inflorescences

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L . D . H A R D E R E T A L .

2004 The Society for the Study of Species Biology Plant Species Biology

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and import (see Harder & Barrett 1996). If inorescencetraits affect attraction and the incidence and conse-quences of joint visitation of owers, then they will inu-ence mating outcomes and be subject to natural andsexual selection.

Strangely, although inorescence characteristics varyextensively within angiosperms (Troll 1964; Weberling

1989), their role in inuencing pollination and plant mat-ing has received little attention until recently (althoughsee Parkin 1914; Burtt 1965; Wyatt 1982). Even recent stud-ies examining the inuence of oral display size on pol-linator attraction and geitonogamy (reviewed below) donot explore inorescence function fully because they donot consider the reproductive consequences of inores-cence architecture. Such analysis is necessary for repro-ductive botany to move beyond oricentrism and todevelop an inclusive understanding of plant mating.

In this paper we review experimental studies of thepollination function of inorescences of animal-pollinatedspecies and consider the implications for inorescenceevolution. We specically focus on inorescence traitsthat can affect pollinator behavior, namely the numberand three-dimensional arrangement of owers that aredisplayed simultaneously and the segregation of oralsex roles within the inorescence. These display charac-teristics can differ from the aggregate characteristics of aninorescences total ower production. For example, Eich-hornia paniculata (Pontederiaceae) plants produce severalowers on each inorescence branch, such that typologi-cally their inorescences are panicles. However, typicallyonly one ower is open on a branch, thus, the E. paniculatainorescence functions as a raceme during pollinationand not as a panicle. In such cases, total inorescencecharacteristics must serve functions other than pollina-tion, such as economic allocation of resources amongowers and fruits (see Stebbins 1973; Wyatt 1982; Schoen& Dubuc 1990), and are largely beyond the scope of thisreview. In considering the mating consequences of ino-rescence display, we are interested both in the extent towhich outcomes differ from those expected from examin-ing owers in isolation, and in new perspectives on thefunction of individual owers that arise from recognizingthe pollination function of inorescences.

Why subdivide reproduction?

Most plants produce more than one large ower duringa reproductive season, suggesting that multiple owersenhance success as a female and/or male parent. Thissubdivision of reproduction involves two components.First, many plants display only a fraction of their owersat once. Given a limit on daily resource availability, thistemporal subdivision probably allows production of moreowers (and fruits) during the entire reproductive season

(Stebbins 1973). Sequential ower production alsoreduces the risk of insufcient pollination during unpre-dictable periods of pollinator scarcity (e.g. inclementweather). In addition, staggered ower presentation isthe most effective mechanism for restricting pollenremoval by individual pollinators. Such pollen packagingincreases total pollen export when the proportion of pol-

len removed by individual pollinators that reaches stig-mas varies negatively with the amount removed (Harder& Thomson 1989). Diminishing returns of this sort canresult from pollinator grooming and layering of pollen onthe pollinators body (reviewed by Harder et al. 2001).

The second aspect of the subdivision of reproductionoccurs when plants display multiple owers simulta-neously. At least two pollination benets could arise fromdisplaying more than one ower. Even slight separationof owers within a display increases total display area,which should improve attractiveness to pollinators because an objects area determines the maximum dis-tance from which it can be detected (reviewed by Dafniet al. 1997; Giurfa & Lehrer 2001). This enhancement of attractiveness appears to involve a trade-off between thenumber and size of owers in a display, rather than asimple alteration in the number of owers. For example,among species, nectar production per ower typicallyvaries inversely with the number of open owers (Harder& Cruzan 1990; Harder & Barrett 1992), so that a roughlyequivalent expenditure of resources is partitioned amongall open owers. In addition to increasing attractiveness,simultaneous display of multiple owers reduces pollenremoval by individual pollinators, compared to a singlelarge ower, because pollinators usually visit only a frac-tion of available owers. As mentioned for staggeredowering, restriction of pollen removal enhances totalpollen export, provided the display attracts enough pol-linators that they eventually remove all pollen (Harder &Thomson 1989). Resolution of the conicting functions of attracting many pollinators and restricting their behavioronce they arrive is a recurring theme in the evolution of oral displays (Harder & Thomson 1989; de Jong et al.1992; Iwasa et al. 1995; Harder & Barrett 1996).

Inorescence size

Of all inorescence characteristics, display size and itsconsequences for pollination and mating have receivedthe most attention and have been the subject of recentdetailed reviews (Harder & Barrett 1996; Snow et al. 1996;Harder et al. 2001). Thus, we will primarily summarize thefeatures of general relevance to inorescence function.The number of owers displayed simultaneously affectstwo aspects of pollinator behavior, which directly inu-ence the quantity and quality of plant mating: the numberof pollinators attracted to a plant and the number of ow-


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ers visited by individual pollinators. Within a plantpopulation, large oral displays typically attract morepollinators than small displays (reviewed by Ohashi &Yahara 2001); however, attractiveness increases in a decel-erating manner with display size (e.g. Harder & Barrett1995). Individual pollinators visit more open owers onlarge inorescences than they visit on small inores-

cences, but the proportion of owers that they visit eitherdoes not differ or decreases with increasing display sizewithin species (reviewed by Snow et al. 1996; Ohashi &Yahara 2001). Often the decline in the proportion of ow-ers visited by individual pollinators counterbalances thegreater attractiveness of large inorescences, so that thenumber of visits received by individual owers varieslittle with display size (e.g. Harder et al. 2001; Karron et al.2004). Given such a relationship, the characteristic size of a species oral display cannot be understood by examin-ing the pollination success of individual owers inisolation.

The tendency of pollinators to visit multiple owerswithin an inorescence creates an opportunity for self-pollination among owers (geitonogamy) provided thepollinators visit pollen-presenting owers before thosewith receptive stigmas. Geitonogamy is probably a com-mon feature of animal pollination for species with owersthat simultaneously donate and receive pollen. For exam-ple, the few studies that have measured self-pollinationwithin and among owers found that geitonogamy con-tributed over 40% of the self-pollination within inores-cences (Schoen & Lloyd 1992; Leclerc-Potvin & Ritland1994; Eckert 2000; Karron et al. 2004). In general, theincidence of geitonogamy increases with display size(Crawford 1984; Harder & Barrett 1995; Snow et al. 1996;Brunet & Eckert 1998; Rademaker et al. 1999; Karron et al.2004), as pollinators visit more owers per inorescence.

The self-pollination resulting from pollinators movingwithin inorescences can have three detrimental conse-quences. First, because geitonogamy often involves thesame pollinator behavior as pollen export, particularlywhen pollinators y between owers, pollen depositedgeitonogamously tends to reduce the amount of pollenthat could otherwise have been exported (pollen dis-counting, e.g. Harder & Barrett 1995). Second, in self-compatible species and those with late-acting incompati-

bility, self-pollination can reduce the number of ovulesavailable for outcrossing (ovule discounting, e.g. Herlihy& Eckert 2002). Finally, given self-fertilization, inbreedingdepression in self-fertilized embryos and offspring canreduce an individuals contribution to the next genera-tion (reviewed by Charlesworth & Charlesworth 1987).Together, these consequences of geitonogamy shouldcause a plant that displays a large fraction of its owerssimultaneously to have lower reproductive output than aplant that displays fewer owers at once and instead pre-

sents its owers over a longer period. Therefore, selectionon display size probably balances the attraction benetsof large displays with the limited costs of geitonogamyassociated with small displays (de Jong et al. 1992; Harder& Barrett 1996).

Geitonogamy and its inuence on optimal display sizecan be reduced or eliminated when the sex roles are seg-

regated among different owers (monoecy or dichogamy)or among different plants (dioecy). The effectiveness of sexual segregation within inorescences in reducing gei-tonogamy depends on the extent to which pollinatorsvisit functionally female owers before functionally maleowers (hereafter female and male owers). Reliableoccurrence of such a visit sequence depends on a speciccombination of pollinator and inorescence characteris-tics: pollinators must follow a consistent route withininorescences; and female owers must occupy initialpositions within this route, whereas male owers mustoccupy terminal positions. For example, bumble bees(Bombus spp.) exhibit a strong tendency to begin visits tovertical inorescences, such as racemes, on lower owersand then move upward through the inorescence, depart-ing from upper owers (Fig. 1a: also see Waddington &Heinrich 1979; Corbet et al. 1981; Rasheed & Harder 1997).This tendency to move upward appears to be a xed behavior because it cannot be modied by altering thegradient of nectar per ower within racemes (Heinrich

Fig. 1

Comparison of the positions of arrivals to and departuresfrom 12-owered racemes by (a) bumble bees (

Bombus huntii

,

Bombus impatiens

and Bombus occidentalis

) and (b) rufous hum-mingbirds (

Selasphorus rufus

). Both panels depict the racemein side-view (three owers per whorl). Based on data from(a) Jordan (2000) and (b) Gross (2003).

10-20 %

>40 %

5-10 %

20-30 %30-40 %

Whorl 4

Whorl 3

Whorl 2

Whorl 1

85 %

58 %

a) Bumble bees

Whorl 4

Whorl 3

Whorl 2

Whorl 1

b) Hummingbirds

48 %


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1979). Presumably as an adaptive response to this stereo-typic behavior, many racemose species visited by bumble bees present older, female owers low in the display, withyounger, male owers presented above (reviewed byBertin & Newman 1993). Indeed, this arrangementsignicantly reduces geitonogamous self-pollination andenhances pollen export compared to the presentation of

either hermaphroditic owers or female owers abovemale owers (Harder et al. 2000; also see Routley &Husband 2003). As a result, adaptive organization of sex-ual segregation within inorescences should ease the con-straints on the evolution of larger displays to enhancepollinator attraction.

Mass-owering species, such as many animal-pollinated shrubs and trees, appear to contradict theexpectation that the pollination and mating consequencesof geitonogamy favor restriction of oral display size. Theapparent paradox arises because a pollinator that visits aplant with hundreds or thousands of open owers has anopportunity to visit so many owers that most pollenshould be dispersed geitonogamously, with little cross-pollination. To some extent, the proportion of polleninvolved in geitonogamy can be reduced if stigmas of individual owers remove only a small fraction of thepollen on pollinators bodies (de Jong et al. 1992; Harder& Barrett 1996). However, the primary resolution of theparadox of mass owering probably lies in the attractionof many pollinators by large displays (see Heinrich 1975;Stephenson & Thomas 1977; Augspurger 1980; Frankieet al. 1983; de Jong et al. 1992). As a consequence of thisattractiveness, individual owers will be depleted of nec-tar frequently and owers with different visit historieswill have accumulated different standing nectar volumes.In general, pollinators visit fewer owers on displayswith high versus low variance in nectar availability (Bier-naskie et al. 2002). This response results because pollina-tors typically leave a plant after visiting a few emptyowers (e.g. Hodges 1985; Dreisig 1989; Cresswell 1990;Kadmon & Shmida 1992), so that visit sequences by indi-vidual pollinators can involve a very small fraction of theowers displayed by intensively visited plants. For exam-ple, Augspurger (1980) found that bees visited an averageof only 8.2 of the 226 owers on Hybanthus prunifoliusshrubs. Furthermore, the proportion of owers visited

declines strongly with mean display size for 17 plant spe-cies (Fig. 2). Such limited visitation of the available ow-ers in large displays by individual pollinators should limitgeitonogamy and promote outcrossing provided the pol-linators move between conspecic plants. However, theeffectiveness of high variance in nectar availability as amechanism for increasing pollinator movement between,rather than within, plants may vary during a plants ow-ering period, as more pollinators include individualplants in their foraging routes. Stephenson (1982) attrib-

uted the peak in fruit set during the nal phase of ow-ering in Catalpa speciosatrees to such a change in visitationintensity per ower. Unfortunately the hypothesis thatattraction of many pollinators by mass displays reducesthe number of owers visited by individual pollinatorsremains largely untested because few studies of mass-owering species have reported relevant aspects of polli-

nator behavior (note the paucity of examples with > 50owers in Fig. 2).

Inorescence architecture

The extensive diversity of inorescence architecture (e.g.Troll 1964; Weberling 1989) demands explanation; how-ever, the function of display architecture has receivedalmost no experimental analysis. If display architectureaffects mating outcomes, then it must do so by inuencingpollinator behavior. The preceding review of the conse-quences of display size and sexual segregation forpollination leads to parallel expectations that displayarchitecture affects three aspects of pollinator behaviorthat could affect pollination and mating: pollinator attrac-tion, the number of owers visited and the consistency of movement patterns within inorescences.

Fig. 2

Relationship between mean oral display size and theaverage proportion of owers visited by pollinators of 17 plantspecies, with multiple observations for some species. Data

were collected from the literature (Pyke 1978; Augspurger 1980;Geber 1985; Andersson 1988; Schmid-Hempel & Speiser 1988;Klinkhamer et al.

1989; Pleasants & Zimmerman 1990; Barrett

et al.

1994; Robertson & Macnair 1995; Brody & Mitchell 1997;Goulson et al.

1998; Ohashi & Yahara 1998; Johnson & Nilsson1999; Vrieling et al.

1999; Galloway et al.

2002; Ohashi 2002; Mitch-ell et al.

2004). The regression line is based on an analysis thatconsidered the dependence of ln(number of owers visited) onln(oral display size) and accounted for the repeated measure-ment of individual species by single studies (

F

1,24.5

=

76.26,

P

40 %

5-10 %

20-40 %

Percentage of

movements froma location

Whorl 4

Whorl 3

Whorl 2

Whorl 1

d) Raceme

a) c) b)

5 cm


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(2000) simulated pollen dispersal with six of the 12owers in inorescences only receiving pollen (femaleowers) and the remainder only donating pollen (maleowers). Female owers were assigned to the six posi-tions on a specic architecture at which bees began ino-rescence visits most often, whereas male owers occupiedthe remaining six positions. Sexual segregation reduced

self-pollination by 3080%, with the strongest effect forracemes and the weakest for umbels. This reduction inself-pollination was accompanied by enhanced pollenexport (after accounting for differences in the numberof pollen-presenting owers). These differences resulted because bees were much more likely to move from maleto female owers on umbels than on racemes, with pani-cles being intermediate. This difference in the consistencyof bee movement patterns would allow sexual segrega-tion to limit geitonogamy on racemes more effectivelythan the less consistent routes followed by bees on pani-cles and, in particular, umbels.

Jordans (2000) simulations suggest that particularcombinations of inorescence architecture and sexual seg-regation should be expected for specic pollinator types.The particular advantages of racemes in this context mayexplain the prevalence of this architecture among plantspollinated by large-bodied bees and the relative rarity of umbels. Some species pollinated by large-bodied bees doproduce umbels; however, many of these species exhibitsynchronous protandry, whereby all owers in theinorescence open simultaneously and proceed togetherthrough male and then female phases (e.g. Aizen 2001;Bhardwaj & Eckert 2001). Such a owering pattern neces-sarily eliminates self-pollination and its mating costs(Harder & Aizen 2004) and may be implemented rela-tively easily in umbels, given the common origin of owerpedicels.

An obvious corollary to the predicted association between pollinator types and inorescence architecturesis that differences between pollinators in movement pat-terns should favor contrasting inorescence characteris-tics. This expectation is clearly illustrated by a comparisonof Jordans (2000) observations of bumble bees andGrosss (2003) observations of hummingbirds feeding onarticial racemes (Fig. 1). In contrast to the bottom-upforaging pattern of bumble bees (Fig. 1a), hummingbirds

begin visits to racemes indiscriminately with respect toposition and move up or down with roughly equal fre-quency, departing from either top or bottom owers(Fig. 1b; also see Wolf & Hainsworth 1986). Clearly, pre-sentation of female owers below male owers on araceme would be less effective in reducing geitonogamyduring hummingbird visits than during bee visits. Giventhat hummingbird pollination in North American oratypically evolved within bee-pollinated lineages (Grant &Grant 1968), it appears likely that such transitions involv-

ing ancestral, racemose species induced changes in eitherinorescence architecture or the organization of sexualsegregation within the inorescence.

For example, most Delphinium species are pollinated bylarge-bodied bees and have vertical racemes. In these bee-pollinated species, oral development proceeds acro-petally and owers are protandrous, so that inorescences

typically present older, female-phase owers belowyounger, male-phase owers (e.g. Fig. 4a). In contrast, ahummingbird-pollinated species, Delphinium cardinale,has similar inorescence architecture, but owers on themain raceme open simultaneously. Given protandrousoral development, this synchrony results in an inores-cence with either female- or male-phase owers (Grant &Grant 1968). Although the separation of sex roles resultingfrom this pattern of oral development breaks downsomewhat when small, lower inorescence branches begin owering (Fig. 4b), it should greatly reduce geito-nogamy during visits by hummingbirds with inconsistentmovement patterns. This example illustrates that differ-ences among pollinators in their movement patterns mayselect for contrasting inorescence characteristics, therebycontributing to some of the diversity in oral displaysobserved within angiosperms.

Fig. 4

Comparison of the frequencies of female- and male-phaseowers in inorescences of (a) bee-pollinated Delphinium stachy-deum

and (b) hummingbird-pollinated Delphinium cardinale

. Datacollected in the Santa Rosa Mountains, Nevada (

D

. stachydeum

)and at Santa Barbara, California (

D. cardinale

) by W. E. Gross(unpubl. data, 2000).

Proportion of female-phase flowers

0 - 0.25 0.25 - 0.5 0.5 - 0.75 0.75 - 1

P r o p o r t

i o n o

f p

l a n

t s

0.0

0.1

0.2

0.3

0.4

0.5

0.6

0 - 0.25 0.25 - 0.5 0.5 - 0.75 0.75 - 1

P r o p o r t

i o n o

f p

l a n

t s

0.0

0.1

0.2

0.3

0.4

0.5n = 20

n = 21

a)

b)


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Relationship between inorescence andoral characteristics

The preceding review clearly illustrates that owers donot act independently to determine plant mating when-ever plants display multiple owers simultaneously. As aresult, oral evolution must occur within the mating con-sequences for the entire display. Similarly, inorescenceevolution must depend on the characteristics of the com-ponent owers. We now briey consider three examplesof the consequences of this reciprocal dependence for theevolution of reproductive traits.

Selection of display size

We have proposed that a species oral display size is anadaptation that balances the benets of attraction againstthe costs arising from geitonogamy. However, display sizeis not an intrinsic, unitary trait that can be selected inde-pendently. Instead, display size arises from the aggregatephenology of individual owers (Ishii & Sakai 2001;Meagher & Delph 2001) and is determined by the relativerates at which owers open and wilt. As a result, selectioncan alter display size only by affecting anthesis rate and/or oral longevity. Correspondingly, the scope for selec-tion to alter these oral traits depends on the matingconsequences associated with changes in display size (e.g.Schoen & Ashman 1995). Clearly, complete understandingof oral and display dynamics requires recognition thatowers do not function in isolation and that display sizeis an aggregate trait.

Our review of display size implied that this size is axed adaptation. However, optimal display size dependson pollinator abundance (Harder & Barrett 1996), whichcan vary considerably within and between owering sea-sons and among populations. In such cases, adjustmentof display size in response to the prevailing pollinatorabundance would be advantageous. The aggregate natureof oral displays allows for such exibility when orallongevity varies negatively with the rate of pollen receipt,which is the case for many angiosperm species (vanDoorn 1997). In such species, infrequent pollinationextends oral longevity, so that the anthesis of new ow-ers combined with the persistence of older owers results

in a larger oral display. In contrast, when pollinatorsvisit frequently, pollinated owers senesce quickly, result-ing in a smaller display comprised mainly of youngowers (Karrenberg & Jensen 2000; L. D. Harder & S. D. Johnson, unpubl. data, 2001). This facultative response of display size to pollinator abundance allows for greaterattractiveness when pollinators visit rarely, and reducedgeitonogamy when pollinators visit frequently (L. D.Harder & S. D. Johnson, unpubl. data, 2001). Because of these contrasting benets, selection on display size should

often result in the evolution of oral mechanisms thatallow adjustment of display size in response to a plantsrecent pollination history.

Dichogamy as a oral and inorescence mechanism

Our discussion of sexual segregation focused on its role

in reducing geitonogamy and associated pollen discount-ing. One form of segregation, dichogamy, also reducesintraoral self-pollination and could enhance pollenexport of individual perfect owers through temporalseparation of pollen presentation and stigma receptivity(reviewed by Lloyd & Webb 1986; Bertin & Newman 1993;although see Galloway et al. 2002). This ability of dichog-amy to serve both oral and inorescence functions raisesquestions concerning the relative importance of theseroles (Routley & Husband 2003).

The importance of dichogamy as a mechanism reduc-ing intraoral versus geitonogamous self-pollinationprobably varies with oral display size (Routley & Hus- band 2003). In small displays, pollinators necessarily visitfew owers. In this situation dichogamy must primarilyreduce interference between sex organs within owers,including intraoral self-pollination. Larger displaysallow pollinators to visit more owers per inorescence,thereby enhancing the opportunity for geitonogamy andassociated pollen discounting. By counteracting thisopportunity, dichogamy becomes more important as ameans of reducing negative interaction between owers.Therefore, the primary function of dichogamy probablydepends on the pollination context established by ino-rescence display size. This functional diversity can beappreciated only when the roles of dichogamy are viewedwithin the context of the entire inorescence.

Sex allocation within inorescences

Flowers within inorescences can experience differentpollination environments depending on when they openduring their inorescences blooming period and wherethey are located within the display. As a result, owerswithin an inorescence can differ in their ability to func-tion as female and male organs. If this heterogeneity inperformance occurs predictably within inorescences,

then selection should modify allocation to female versusmale function among owers to enhance a plants matingperformance (see Brunet & Charlesworth 1995).

For species with staggered anthesis of owers that liveseveral days, display size changes from small initially, tomaximal during peak owering, and then to small againas only the nal owers remain (e.g. Ishii & Sakai 2002).Given the positive relationship between pollinator attrac-tion and display size, the rate of pollinator visitation toinitial owers probably increases during their lives as


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they participate in a growing display, whereas nal ow-ers probably experience declining visitation as displaysize declines. Given such a temporal pattern in visitationrate, initial owers of a protandrous species will havelimited opportunity for pollen export during their initialmale phase, but better prospects for pollen import duringtheir later female phase (e.g. Ishii & Sakai 2002). In con-

trast, nal owers will receive more pollinator visits dur-ing the male phase than during the female phase. Thisshift in performance should favor ovule-biased invest-ment in initial owers and pollen-biased investment innal owers of protandrous species.

Position within a oral display can also affect a owersrelative female versus male success. For example, Barrettet al. (1994) found threefold more self-pollination in upperowers of vertical Eichhornia paniculata inorescencesthan in lower owers, as a result of the upward move-ment of bee pollinators (also see Rademaker et al. 1999).Self-pollination in this experiment signicantly reducedthe pollen available for export (Harder & Barrett 1995), sothat lower owers probably imported more outcross pol-len, but exported less pollen, than upper owers. Such apattern would favor greater ovule production in lowerowers and greater pollen production in upper owers,particularly in species with a high genetic load (Brunet &Charlesworth 1995).

In general, the scope for selection of position-dependent sex allocation will depend on the variances inself-pollination, pollen import and pollen export amongowers within inorescences. These pollination variancesshould be accentuated when pollinators follow consistentpaths among owers within inorescences. As we havealready demonstrated, such consistency differs amongpollinators and inorescence architectures. For pollina-tors that follow consistent paths (e.g. upward movementon vertical inorescences), Barrett et al. (1994) demon-strated that among-ower variance in self-pollinationdepends on the specic combination of the number of owers that each pollinator visits (a function of displaysize) and the proportion of the pollen on a pollinators body removed by each stigma (a oral trait). Pollinationvariances will also uctuate with overlap in the oweringperiods of individual owers. In species with distinctcohorts of owers (e.g. displays of 1-day owers), indi-

vidual owers have a xed relative position within thedisplay (e.g. bottom vs top), which fosters variance infemale and male performance among owers. In contrast,in species with staggered anthesis of long-lived owers,a owers relative position in the display can change asthe wave of owering progresses through the inores-cence. Such a pattern will tend to equalize female andmale performance among owers within an inorescenceand reduce the opportunity for selection on heteroge-neous sex allocation among owers.

The preceding hypotheses predict higher pollen : ovuleratios in owers produced later in an inorescences blooming period and higher on vertical inorescences.Similar patterns could result from declining resourceavailability during a plants owering period and/orreduced vasculature to distal owers (reviewed by Diggle1995). However, the predicted variation in pollen : ovule

ratios has been observed in eight liliaceous species(Thomson 1989; Nishikawa 1998) and a spring-ephermeral Corydalis (Kudo et al. 2001) in which owersare preformed during the preceding growing period. Inaddition, in several of the species studied by Thomson(1989) the owers that opened rst exhibited lowerpollen : ovule ratios, despite occupying more distal posi-tions in the inorescence. These results are more consis-tent with selection of sex-allocation patterns that enhancemating success, than with either resource competitionamong owers or positional constraints on resource dis-tribution. Thus, it appears likely that variation in thepollination environment among owers within inores-cences shapes the evolution of sex allocation.

Concluding comment

This review illustrates that pollination biology is under-going a shift in perspective from the historical oricentricemphasis to an expanded view that considers the functionof a plants entire display. This evolving perspectiveenhances understanding of many recognized oral traits(e.g. dichogamy, oral longevity) and identies inores-cence traits as subjects of interest in their own right (e.g.architecture, variation in sex allocation). This broadening

of perspective has been accompanied by increased inte-gration of ecological studies of pollination with moregenetic studies of plant mating (see Harder & Barrett 1996;Holsinger 1996; Morgan & Schoen 1997). These develop-ments hold considerable promise for progress in under-standing the diversity of oral design and display amongangiosperms.

Acknowledgments

We thank the organizers of the Society for the Study of Species Biology symposium on Diversity of ReproductiveSystems in Plants: Ecology, Evolution and Conservationfor the opportunity to compile this review of oral displayand J. C. Vamosi for comments on the manuscript. TheNatural Sciences and Engineering Research Council of Canada funded this research.

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beyond floricentrism - the pollination function of inflorescences

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