AmericanJournal of Botany 82(9): 1131-1136. 1995.

EFFECT OF SUCCESS ON FLORAL LONGEVITY IN THE ORCHID CALYPSO BULBOSA ()'

HEATHER C. PROCTOR2 AND LAWRENCE D. HARDER Departmentof Biological Sciences, University of Calgary,Calgary, Alberta, T2N 1N4

The lifespanof an individualflower is oftenaffected by pollination success. Species differ regarding whether male function (pollenremoval), female function (pollen deposition), or bothtrigger floral senescence. We studiedsenescence in thesingle- flowered,deceptive orchid Calypso bulbosa by manipulating the degree of male and femalereproductive success. We found thatdeposition of any amount of pollen resulted in dramaticchanges in shapeand colorwithin 4 d, whereasunmanipulated flowersand thosethat had had polliniaremoved remained unchanged for 8-11 d aftertreatment. Selection may favor the reproductivefunction that is less easilysatisfied as thetrigger for senescence, because a flowerthat senesces after accom- plishmentof thisfunction is likelyto have alreadysucceeded at themore easily satisfied one. Deceptive(i.e., rewardless) flowersare morelikely to satisfymale than female function since the latter requires that a pollinatorbe fooledtwice, first to pickup pollenand secondto depositit. A surveyof naturally pollinated Calypso showed that male function, pollinium removal,was morelikely to occurthan female function, deposition (95% vs. 66% ofvisited flowers); thus floral senescence in Calypsois triggeredby achievementof thefunction less likelyto succeed.Studies of senescencetriggers in speciesin whichfemale function is morelikely to be achievedthan male are necessaryto furthertest this hypothesis.

The lifespanof an individualflower, the period during spans thatare independentof whethermale or female whichit is attractiveand available to pollinators,can pollinationfunctions have been achieved.For example, measurefrom minutes to months(van derPijl and Dod- theCommelinaceae, Convolvulaceae, Pontederiaceae, and son, 1966). At the end of its lifea flowermay change Tumeraceaehave flowersthat invariably last onlyone color,halt production of scentor ,and its corolla day(Primack, 1985). On theother hand, flowers may not maychange orientation, collapse, or abscise (Gori, 1983). have a fixedlifespan but rather be subjectto pollinator- Althoughphylogeny may sometimesbe a constraint inducedsenescence, triggered by depositionor removal (Stratton,1989), in mostspecies flower lifespan is likely of pollen. In this lattergroup, species differregarding to be an adaptivecharacter; however, despite its potential whetherthe onset of senescence is determinedby female effectson pollinatorvisitation or levelof inbreeding, lon- success(pollen receipt) or male success(pollen removal) gevityof individualflowers is seldomincorporated into (e.g.,receipt in Encyclia krugii, Ackerman, 1989; removal studiesof plantreproductive strategies (Primack, 1985; in Campanula rapunculoides,Devlin and Stephenson, Stratton,1989; Ashmanand Schoen,1994). 1984). Pollinator-inducedsenescence may allow reallo- Thereare twobasic categoriesof floral longevity based cationof resources to developingseeds (e.g., Harrison and on thevalue ofa senescentflower to theinflorescence. In Arditti,1976) or decreasetranspirational water loss and thefirst, a retains flowers after they cease functioning energycosts of maintaininga flowerwhose usefulness is in male(pollen presentation) or female(pollen reception) at an end (Primack,1985). roles to maintainthe overallattractiveness of an inflo- How finelytuned is theflower's "decision" to senesce? rescence'sdisplay. In thesespecies, changes in flower form If senescenceoccurs regardless of the amountof pollen and color may directa pollinator'sattention to flowers removedor depositedit maybe at theexpense of future withinan infloresencethat have not been visited(Gori, reproductivesuccess. For example,the orchidCleistes 1989; Weiss,1991). Speciesin thesecond category have bifariaundergoes senescence only after receiving a large flowersthat undergo complete senescence and are not load ofpollen (Gregg, 1991), and Lupinusargenteus (Fa- maintainedon an inflorescence;here changes in colorand baceae) senescesonly after its pollen has becomeinviable formcan be interpretedas epiphenomenaof thephysi- (Gori, 1989). By manipulatingthe degreeof male and ologicalprocess of senescence.Both categoriesof floral femalereproductive success in the orchid Calypso bulbosa longevitycan be furthersubdivided according to the caus- wetested the sensitivity ofthis species' decision to senesce. al agentof senescence.First, flowers may have fixedlife- MATERIALS AND METHODS

' Manuscriptreceived 20 May 1994; revisionaccepted 6 February Ecologyof Calypso bulbosa -Calypso bulbosa(Linnae- 1995. us) Oakes var. americana(R.Br.) is a single-floweredor- The authorsthank Myra Wiebe, Sarah Shima, and KristinOlson for chiddocumented to showpost-pollination changes (Gori, help in surveyingnaturally pollinated Calypso, and the staffof Kan- 1983). It occursin mossy,coniferous forests across Can- anaskisField Station for friendly assistance. Research was supported by ada and the northernUnited States (Petersonand a NaturalSciences and Engineering Research Council of Canada (NSERC) PostdoctoralFellowship to HCP, and an NSERC OperatingGrant to McKenny,1968). In theRocky Mountains of Alberta, C. LDH. bulbosablooms frommid-May to earlyJuly (Proctor, 2 Authorfor correspondence, current address: Department of Biology, personalobservation). Each rametproduces a singlelong- Queen'sUniversity, Kingston, Ontario, Canada K7L 3N6. stemmedleaf and a solitarypendant flower at thetop of 1131 1132 AMERICANJOuRNAL OF BOTANY [Vol. 82 a 5-20 cmstem. The flowerhas five pink-to-fuchsia sepals andpetals, an inflatedslipper-like lower lip bearing purple stripesand a tuftof yellowhairs, and a convexcolumn or "upperlip" withanther and stigmaon itsundersurface (Fig. 1). The antherbears a pollinariumconsisting of two pairsof flat,waxy pollinia (one smalland one largepol- liniumper pair) thatare attachedto a commonsticky base (Fig. 3). Calypsobulbosa provides neither nectar nor usablepollen; instead it relieson brightcolor, anther-like hairs,and sweetsmell to deceive naive pollinators, mainly queenBombus and (Mosquin, 1970; Boyden,1982). A visitingbee removesthe entire polli- nariumwhen the viscidium attaches to itsthorax, and if it is carryinga pollinariumfrom another flower it may depositone, two,three, or fourpollinia on theflower's stigma(Proctor and Harder,1994).

Pollination andfloral lifespan-We studied Calypsoin May 1993 near the Universityof Calgary'sKananaskis fieldstation in thefoothills of Alberta's Rocky Mountains (115003'N, 5 1001'W). Starting7 May we bagged unopened flowersto precludepollinator visits. Emasculation was unnecessarybecause Calypso does not self-pollinate (Mos- quin, 1970;Proctor, personal observation). After a flower openedand its sepalsand petalswere fully erect (Fig. 1), we subjectedit to one of fivetreatments chosen to span . . . ~ ~ ~ ~ ~ ~ ~ / the rangeof male and femalepollination success. For f I ~~~~mm control(CONT) flowers,pollen was neitherremoved nor deposited.Flowers with pollinia removed (REM) had the pollinariumand anthercap removed,but receivedno pollen.We usedtwo pollen loads for treatments involving polliniumdeposition: 1/2-DEP flowers were pollinated withone-half of a small polliniumtaken from another flowerat least 5 m away (the flower'sown pollinarium was notremoved); 2-DEP flowerswere treated similarly Figs.1-3. Calypsobulbosa flowers and pollinarium.1. Lateralview to 1/2-DEPbut wereprovided with one smalland one of Stage I flower.2. Lateral view of Stage V flower.3. Front view of largepollinium. Finally, 2-DEP, REM flowersreceived pollinarium showing the two pairs of pollinia attached to a common one largeand one small polliniumand had theirown ViSCidi.um. pollinariaremoved. We chose theselevels of pollende- positionbecause we had previouslyfound that one-half ofa smallpollinium (1/2-DEP) is insufficientto pollinate all ovules available,fertilizing on average5,000 seeds Viabilityofpollenfrom senescedflowers -To determine comparedto the 16,000fertilized by theone large,one whetherpollinia fromflowers that had undergonemor- smalltreatment (2-DEP) (Proctorand Harder, 1994). Thus phological and color changes could still (a) elicit changes the2-DEP treatmentwould satisfy female function more in other flowers,and (b) fertilizeovules, we removed completelythan 1/2-DEP. Flowers were treated between pollinaria fromfive senesced 2-DEP flowerson 18 May 10 a.m. and 3 p.m. on 10 May (N= 1), 11 May (N= 7), and placedthem on stigmasof five flowers that had been 12 May (N = 10) and 13 May (N= 4) for a total of 22 baggedprior to theiropening. On 24 May we checkedthe replicatesof the five treatments. Flowers were kept bagged recipientflowers for signsof color and morphological and color and morphologywere monitored daily after change,and on 16July we collected and dissected capsules treatmentuntil 21 May (8-11 d aftertreatment, with the to determinewhether seeds had been fertilized. dayof treatment considered Day 1). We monitoredcolor ofsepals and petalsby comparing them to an assortment RESULTS ofPrismacolor? pencils (Berol?, Toronto), and recorded floralmorphology by sketching a side view of each flower Course of morphologicaland color changes- Calypso to indicatethe attitude of thelower lip to the stemand bulbosaflowers underwent a seriesof morphological and thatof sepalsand petalsto thecolumn and lowerlip. color changesfollowing pollination (Table 1). A flower withoriginally erect sepals and petalsand an ovarythat Surveyof naturalpollination success-On 20 May we projectedout from the stalk (Stage I) graduallydeveloped surveyedunmanipulated C. bulbosain the fieldstation a droopingovary that approached the stalk,and sepals vicinityto determinenatural rates of male and female and petalsthat collapsed over the column and lip (Stage pollinationsuccess by checking whether flowers had pol- V) (Fig.-2). Eventually,as the ovaryswelled, the flower linariaremoved or polliniadeposited on theirstigmas. rose again untilit stoodat rightangles to the stalk,but September 1995] PROCTOR AND HARDER-CALYPSO FLORAL LONGEVITY 1133

1 5 TABLE 1. Morphologicalchanges in 62 pollinatedCalypso flowers. Although 4 . theorder of changewas thesame forall flowers,some 1 Cl flowersskipped one or morestages. 13 1/2 DEP Number 1 2 _IiZ2-DEP of Stage Description flowers 11 KZSI~~~~~2-DEP,REM I Ovaryat >900 in relationto stem,sepals about 900 62 10 in relationto column 9 II Ovarypartially collapsed towards stem, sepals 900; 11 or sepalspartially collapsed towards column, ova- 8 ry 900 7 III Ovarypartially collapsed, sepals partially collapsed 26 IV Ovarycompletely collapsed, sepals partially col- 22 6 lapsed 5 V Ovarycompletely collapsed, sepals completely col- 59 lapsed L. 4 VI Ovarybeginning to rise,sepals completely collapsed 24 VII Ovary >900 again,sepals collapsed 34 o 2

3 was a pinkishorange tone that manifested soon before 1 2 3 4 5 6 7 8 9 or aftercomplete collapse of the flower (Stage V). First day of color change Effectof treatmentson rapidityof changes-Pollen re- 14 b ceipt,but not pollen removalalone, almostinvariably E 13 inducedfloral senescence. All ofthe 21 survivingcontrol z 123 flowersretained their initial color and morphology(Color 0, Stage 1) throughoutthe 8-11 d observationperiod. 112 Similarly,all buttwo of the REM flowersremained Color 0, Stage 1 (N = 22); the two exceptionsdeveloped Color 1 0 3 and collapsedsepals and petalson Days 5 and 9, re- 9 spectively.In contrastto pollinatedflowers, however, the 8 ovariesof these two REM flowersdid notdecline towards 7 thestems. Fifty-nine of 62 flowersin thethree treatments involvingpollen deposition attained complete morpho- 6 logicalcollapse (Stage V) and colorchange (Color 3) by 5 the end of the observationperiod (Fig. 2). Two of the 4 exceptionsalso exhibitedcomplete morphological change, buttheir color changed less dramatically (to Color2). The 3 remainingexception, a 1/2-DEPflower, remained in ini- 2 tialcondition; it seemslikely that the small piece of pol- liniumfailed to adhereto the stigma.For plantsthat 0 receivedpollen, the amountof pollen applied did not 2 3 4 5 6 7 8 9 significantlyaffect either the rapidityof onsetof color 1 change(Fig. 4a: Kruskal-WallisH = 3.39, P > 0.1), or First daiy ait Staige V therapidity of morphological change (Fig. 4b: H = 0.118, P> Fig. 4. Firstday at whichpollinated Calypso flowers reached (a) 0.5). Color 3 and (b) StageV for1/2-DEP (solid bars), 2-DEP (openbars), and 2-DEP, REM (hatchedbars) treatments. Naturalpollinationsuccess-Of 520 C. bulbosa flowers examined,212 (41%) showedevidence of havingbeen visitedby a pollinator:11 (2%) had onlypollinia depos- itspetals and sepalsremained collapsed over the lip (Stage ited,72 (14%) had onlypollinia removed, and 129 (25%) VII). Mostpollinated flowers passed from Stage I to Stage had polliniaboth deposited and removed.Thus of visited III or IV beforereaching Stage V, withsome passing flowers,201 (95%) had polliniaremoved and 140 (66%) throughII and othersgoing directly to V. By theend of had polliniadeposited. the observationperiod, approximately half of thepolli- natedflowers had reachedStage VII. Color changealso wentthrough several temporal stages. Initially sepals and Viabilityof pollen from senescentflowers-All five C. petalsvaried in colorfrom pink to fuchsia(Color 0). Post- bulbosapollinated with pollinia from senescent flowers pollinationcolor change typically involved a gradualfad- had reachedColor 3, StageV whenreexamined 7 d later. ingto a palemauve (Color 2), occasionally passing through We stainedand examineda subsampleof seeds (312 to a stagein whichthe tips of sepalsand petalswere Color 429) fromeach capsuleand foundthat more than 98% 0 buttheir bases were2 (termedColor 1). Finally,Color containedembryos. 1134 AMERICAN JOURNAL OF BoTANY [Vol. 82

I I I I I I T DISCUSSION 80 Morphologicaland color changesin Calypsobulbosa t' 70 occurredin responseto depositionof pollen on thestigma ratherthan to removalfrom the anther, as has also been 60 foundfor the orchids Cypripedium acaule (Primackand 4-, CD) R7 Hall, 1990) and Encycliakrugii (Ackerman, 1989). In 50 R/D1 R6 Cymbidiumspecies, on theother hand, color changes can -4- . be inducedby removalof pollinia and anthercap (Wol- R/D2 tering,1990). The speed of onsetof changesin Calypso -C 40 did not dependon the amountof pollendeposited; in U) contrast,the orchidsCleistes bifaria and Leporellafim- L* 30 R3 .- 00 briatafade morerapidly after receiving larger doses of pollen(Gregg, 1991; Peakall, 1989). Why does senescence o O 220 0 _ ~~DD22 bDl0 in thesespecies appear to be moresensitive to pollenload . R5 thanC. bulbosa?Differences in pollenpackaging may be 10 . o D3 Dl theexplanation. Leporella has mealypollinia and Cleistes s o si ~~Rl D4 producesgranular pollen that is dumpedon pollinators. In both speciesit is possiblefor a pollinatorto deposit loads of pollenmonads or tetradsfar too smallto suc- 0 10 20 30 40 50 60 70 80 cessfullyfertilize all availableovules. However, the waxy % polliniaof Calypsocannot be depositedin a load any of flowers with pollinaria removed smallerthan one pollinium,which carries enough pollen I I I I I . to fertilize 11,000ovules (Proctor and Harder,1994). n 60 R4 For Calypso,unlike for Cleistes and Leporella,one de- 4J~~~~~~~~~~~~~~~~ positioncan be guaranteedto produce a respectablenum- b berof seeds. Thus there may have been no selectivepres- o 50 sureto responddifferentially to insufficient pollen loads becausesuch loads cannotnaturally occur. R/D2 In Calypso,floral senescence was unaffectedby male 40 success.By senescingimmediately after receiving pollen irrespectiveof pollinarium removal, Calypso flowers ap- O 30 _ pear to forgopotential reproductive success. Pollination doesn'timpair the vigor of a flower'sown pollen, as pol- R/D1 liniafrom Stage V, Color3 flowerssuccessfully pollinated ovulesin otherplants. This contrastswith Gori's (1989) 20 D2bR2 D2c findingthat color changes in Lupinus argenteus (Fabaceae) occuronly after pollen has becomeinviable. Casper and L 10~~~~~~~~~~~~~~~~~~ . 1 0 . 3DD6D4-7... La Pine (1984) also foundthat changed flowers of Cryp- ..07 00 tanthahumilis (Boraginaceae) contained inviable pollen. o D5 D8 In a studyby Richardsonand Stephenson(1989) Cam- ~~- 0 ~~ D2a 0 9 panula rapunculoides(Campanulaceae) flowers that ex- IIII I periencedrapid rates of pollen removal had a significantly 0 0 10 20 30 40 50 60 shorterlifespan than those experiencing slower rates. Sim- ilarly,Devlin and Stephenson(1984) foundthat the du- % of flowers with pollinaria removed rationof the staminate phase of Lobelia cardinalis (Cam- Fig. 5. Comparisonof male and femalereproductive success in re- panulaceae)was correlatedwith the amountof pollen warding(R), deceptive(D) and mixed-strategy(R/D) orchids where the remainingin theflower. dottedline indicatesequal success:(a) % of flowerswith pollinaria Whyis floralsenescence in Calypsotriggered only by removedvs. % thatset fruit; (b) % of flowerswith pollinaria removed femalesuccess? In general,rapid senescence after success vs. % withpollen deposited. of one functionseems risky, as it maypreclude success FigureAbbreviations: R I = Anacamptispyramidalis, Waite, Hopkins, of the otherfunction. We proposethat the triggerused and Hitchings,1991; R2 = Comparettiafalcata (meansover 2 yr), may indicatewhich of the two functionsis less easily Rodriguez-Robles,Melendez, and Ackerman,1992; R3 = Dactylorhiza satisfied,e.g., if pollenremoval is likelybut deposition fuchsii,Waite et al., 1991; R4 = Goodyeraoblongifolia, Ackerman, 1975; rare,then a flowerthat senesces after deposition will most R5 = Habenariaobtusata, Thien and Utech,1970; R6 = Platanthera stricta,Patt et al., 1987;R7 = Prasophyllumodoratum, Bernhardt and likelyalready have had somepollen removed and would Burns-Balogh,1986; DI = Aspasiaprincipissa, Zimmerman and Aide, 1989; D2a = Calypsobulbosa, Boyden, 1982; D2b = Calypsobulbosa, Mosquin,1970; D2c = Calypsobulbosa, this study; D3 = Epidendrum ciliare,Ackerman and Montalvo,1990; D4 = Stelisargentata, Chris- tensen,1992; D5 = Thelymitraantennifera, Dafni and Calder,1987; and Profita,1975; DI0 = Polystachyarosea (means over three sites), D6 = Cymbidiellaflabellata, Nilsson et al. 1986; D7 = Cypripedium Petterssonand Nilsson,1993; R/D1 = Cleistesbifaria (means over 2 acaule (meansover 2 yr),Davis, 1986; D8 = Diurismaculata (means yr),unpublished data, K. Gregg,Wesleyan College; R/D2 = Cleistes oversix transects), Beardsell et al., 1986;D9 = Eulophiacristata, Lock divaricata(means over 2 or 3 yr),K. Gregg,personal communication. September 1995] PROCTOR AND HARDER- CALYPSO FLORAL LONGEVITY 1135

not totallyforgo male success.Calypso bulbosa is a de- lymitranuda (Orchidaceae). Plant Systematics and Evolution151: ceptivespecies that advertizes rewards to pollinatorsbut 187-202. does notprovide them, a phenomenoncommon among BOYDEN, T. C. 1982. The pollinationecology ofCalypso bulbosa var. americana (Orchidaceae): initial deception of visitors. orchids(Ackerman, 1986). In itsinitial visit to a deceptive Oecologia55: 178-184. flower,a naive insectmay remove pollen but it willnot CASPAR, B. B., AND T. R. LA PINE. 1984. Changesin corollacolor and have any to deposit.Insects quickly learn to avoid re- other floralcharacteristics in Cryptanthahumilis (Boraginaceae): wardlessflowers (Dukas, 1987; Peakall,1990; Wadding- cues to discourage pollinators?Evolution 38: 128-141. ton and Gottleib,1990; Weiss,1991); an insectthat has CHRISTENSEN, D. E. 1992. Noteson thereproductive biology of Stelis beenfooled once and is carryingthe pollen of a deceptive argentata Lindl. (Orchidaceae: Pleurothallidinae) in eastern Ec- flowermay be disinclinedto revisitthat species. Thus in uador.Lindleyana 7: 28-33. DAM, A., AND D. M. CALDER, 1987. Pollination by deceit and floral deceptiveplants, pollen removalseems moreprobable mimesis in Thelymitraantennifera (Orchidaceae). PlantSystem- thandeposition, and a senescencetrigger based on female aticsand Evolution158: 11-22. successmay be favored.Pollinia deposition was rarer than DAVIS, R. W. 1986. The pollination biology of Cypripediumacaule pollinariumremoval in our studypopulation (66% vs. (Orchidaceae). Rhodora 88: 445-450. 95% of visitedflowers), even thougheach quadripartite DEVLIN, B., AND A. G. STEPHENSON. 1984. Factorsthat influence the staminate and pistillatephases of Lobelia cardinalis flowers.Bo- pollinariumhas the potentialto pollinatefour stigmas. tanicalGazette 145: 323-328. Thissuggests that bees quickly learn that Calypso provides DUKAS,R. 1987. Foragingbehavior of threebee species in a natural no rewardsand rarelyrevisit; pollinia would be removed mimicrysystem: female flowerswhich mimic male flowersin Ec- on the firstvisit but wouldnot have theopportunity of balliumelaterium (Cucurbitaceae). Oecologia 74: 256-263. beingdeposited. But is thedifference in polliniaremoval GORI, D. F. 1983. Post-pollinationphenomena and adaptive floral vs. depositiontruly a resultof pollinatoravoidance of changes. In C. E. Jones and R. Little [eds.], Handbook of experi- mental pollination biology, 31-49. Van Nostrand Reinhold, To- deceptiveflowers, or is ita generalfeature of orchids? Fig. ronto. 5 illustratesrelative success of male and femalefunctions 1989. Floral color change in Lupinus argenteus(Fabaceae): in rewarding(R) and deceptive(D) orchidspecies, com- why should plantsadvertise the location of unrewardingflowers to paringpollinium removal with two aspects offemale func- pollinators?Evolution 43: 870-881. tion: fruitset (Fig. 5a) and pollendeposition (Fig. 5b). GREGiG,K. B. 1991. Reproductivestrategy of Cleistesdivaricata (Or- Withregard to fruitset, rewarding species are more likely chidaceae).American Journal of Botany 78: 350-360. to have equal male and femalesuccess. HARRISON,C. R., AND J. ARDiTTi. 1976. Post-pollinationphenomena Studiesof pollen in orchidflowers. VII. Phosphatemovement among floralsegments. depositionin rewardingspecies are relativelyscarce, and AmericanJournal of Botany 63: 911-918. morework is neededbefore a valid comparisoncan be LOCK,J. M., AND J. C. PROFITA. 1975. Pollinationof Eulophia cristala made usingthis measure of female success. Two species, (SW) Steud. (Orchidaceae) in southernGhana. Acta Botanica Neer- Cleistesbifaria and C. divaricata,are identified with R/D; landica24: 135-138. theyare a mixtureof the two strategies in that they provide MosQuIN, T. 1970. The reproductivebiology of Calypsobulbosa (Or- no nectarand henceare deceptive, but bees in somepop- chidaceae).Canadian Field-Naturalist 84: 291-296. NILSSON,L. A., L. JONSSON,L. RASON, AND E. RANDRIANJOHANY. 1986. ulationshave learnedto exploitthem as pollensources. The pollination of Cymbidiellaflabellata (Orchidaceae) in Mada- Interestingly,they fall closer to theR thanthe D taxaon gascar: a systemoperated by sphecid wasps. NordicJournal of Bot- Fig. 5. any6: 411-422. Accordingto ourhypothesis and thepattern in Fig. 5, PATT, J.M., M. W. MERCHANT, D. R. E. WILLiAMS AND B. J.D. MEEUSE. deceptiveorchids should be morelikely than rewarding 1989. Pollination biology of Platanthera stricta(Orchidaceae) in ones to relysolely on femalesuccess as a triggerfor se- Olympic National Park, Washington.American Journal of Botany nescence.Unfortunately, there have been no investiga- 76: 1097-1106. PEAKALL, R. 1989. The uniquepollination of Leporellafimbriata (Or- tionsof rewardingorchids to determinewhether pollin- chidaceae): pollinationby pseudocopulatingmale ants (Myrmecia ium removalaffects floral lifespan. Comparative studies urens,Formicidae). Plant Systematics andEvolution 167: 137-148. oflife history and pollination biology are necessary to test 1990. Responses of male Zaspilothynnustrilobatus Turner whetherthe relative probability of male vs. femalesuccess wasps to females and the sexually deceptive orchid it pollinates. is responsiblefor observed patterns of pollinator-induced FunctionalEcology 4: 159-167. floralsenescence in orchidsand otherflowering . PETERSON,R. T., ANDM. McKENNY. 1968. A fieldguide to wildflowers: northeasternand northcentralNorth America. Houghton Mifflin, Boston, MA. LITERATURE CITED PETTERSSON, B., AND L. A. NIISSON. 1993. Floral variationand deceit pollination in Polystachyarosea (Orchidaceae) on an inselbergin AcYERMAN,J. D. 1975. Reproductivebiology of Goodyeraoblongifolia Madagascar.Opera Botanica 121: 237-245. (Orchidaceae). Madrono 23: 191-198. PRIMACK,R.B. 1985. Longevityofindividualflowers.AnnualReview * 1986. Mechanisms and evolution of food-deceptivepollina- ofEcology and Systematics16: 15-37. tion systemsin orchids. Lindleyana 1: 108-113. ,AND P. HALL. 1990. Costs of reproductionin the pink lady's * 1989. Limitations to sexual reproductionin Encyclia krugii slipper orchid: a four-yearexperimental study. American Journal (Orchidaceae). SystematicBotany 14: 10 1-109. ofBotany 136: 638-656. , AND A. M. MoNTALvo. 1990. Short-andlong-term limitations PROCTOR,H. C., ANDL. D. HARDER. 1994. Pollen load, capsule weight, to fruitproduction in a tropical orchid. Ecology 71: 263-272. and seed productionin threeorchid species. Canadian Journalof ASHMAN,T.-L., AND D. J. SCHOEN. 1994. How long should flowers Botany72: 249-255. live? Nature 371--788-79 1. RICHARDSON,T. E., ANDA. G. STEPHENSON.1989. Pollen removaland BEARDSELL,D. V., M. A. CLEMENTS,J. F. HUTCHINSON,AND E. G. pollen deposition affectthe durationof the staminateand pistillate WILLIAMS. 1986. Pollination of Diuris maculataR.Br. (Orchi- phasesin Campanularapunculoides. American Journal of Botany daceae) by floralmimicry of the native legumes Davesia spp. and 76: 532-538. Pultenaeascabra R.Br. Australian Journal of Botany 34: 165-173. RODRIGuEz-ROBLES,J. A., E. J.MELtNDEZ, AND J. D. AcKERMAN.1992. BERNHARDT, P., AND P. BuRNs-BALOGH. 1986. Floralmimesis in The- Effects of display size, flowering phenology, and nectar availability 1136 AMERICAN JOURNALOF BOTANY [Vol. 82

on effectivevisitation frequency in Comparettiafalcata (Orchida- WAITE,S., N. HopuINs,AND S. HITCHINGS. 1991. Levelsof pollinia ceae). AmericanJournal of Botany 79: 1009-1017. export,import and fruitset among plants of Anacamptis pyrami- STRATTON,D. A. 1989. Longevityof individual flowersin a Costa dalis,Dactylorhiza fuchsii, and Epipactishelleborine. In T. C. E. Rican cloud forest: ecological correlates and phylogeneticcon- Wellsand J. H. Willems[eds.], Population ecology of terrestrial straints.Biotropica 21: 308-318. orchids, 103-110. SPB Academic Publishingby, The Hague. THIEN, L. B., AND F. UTECH. 1970. The modeof pollinationin Ha- WEIss,M. R. 1991. Floral colourchanges as cues forpollinators. Nature benariaobtusata (Orchidaceae). American Journal of Botany 57: 354: 227-229. 1031-1035. WOLTERING,E. J. 1990. Interorgantranslocation of 1-aminocy- VAN DER PUJL, L., AND C. H. DODSON. 1966. Orchidflowers: their clopropane-1 -carboxylic acid and ethylenecoordinates senescence pollinationand evolution.University of Miami Press,Coral Gables, in emasculatedCymbidium flowers. Plant Physiology 92: 837-845. FL. ZIMMERMAN, J.K., AND T. M. AIDE. 1989. Patternsof fruit production WADDINGTON, K. D., AND N. GOTTLIEB. 1990. Actualvs perceived ina neotropicalorchid: pollinator vs. resource limitation. American profitability:a studyof floralchoice ofhoney bees. Journalof Insect Journalof Botany 76: 67-73. Behavior 3: 429-441.