Rathcke & Lacey

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Phenological Patterns of Terrestrial Plants

Author(s): Beverly Rathcke and Elizabeth P. LaceyReviewed work(s):Source: Annual Review of Ecology and Systematics, Vol. 16 (1985), pp. 179-214Published by: Annual ReviewsStable URL: http://www.jstor.org/stable/2097047 .

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Ann. Rev. Ecol. Syst. 1985. 16:179-214Copyright? 1985 by Annual Reviews Inc. All rights reserved

PHENOLOGICALPATTERNSOFTERRESTRIALPLANTSBeverlyRathckeDivisionof Biological Sciences, Universityof Michigan,AnnArbor,Michigan 48109ElizabethP. LaceyDepartmentof Biology, University of North Carolina, Greensboro,North Carolina27412

INTRODUCTION"FromMarchto Novembereach monthbringsa new prospect n field and forest and eachedition [of flower life] seems thoroughly o harmonizewith its own peculiarseason."

H. L. Clark (47)The termphenologyis derived romthe Greekwordphaino meaning o show orto appear.Hence, phenology is definedas the studyof the seasonaltimingoflife cycle events. Forplantsthe seasonaltimingof such eventscanbe criticaltosurvival and reproduction.In agriculturethe most common failure of in-troducedcrops is the inability to adjustto the seasons imposed by the newenvironment68). Inthepastfew years,interest ntheecology andevolution oftiming of life cycle events has grown. Here we review the literatureonphenological patternsof germination,flowering, and fruiting (includingdis-persal).Thephenologicalpatternof anylife cycle eventcanbe quantitatively efinedas a statisticaldistribution haracterizedby suchparametersas time of occur-rence(onset, mean, mode), duration range),synchrony variance),andskew-ness. For each life cycle event we discuss each parameter or which dataareavailable. Because parametersat one level can contribute to parametersathigher levels, parametersare sometimes related. For example, the degree ofsynchronywithinandamongindividualscandeterminedurationat thepopula-

1790066-4162/85/1120-0179$02.00


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180 RATHCKE& LACEYtion level. Therefore, we discuss phenological patternsat the levels of in-dividuals, populations, species, and communities. Also, we use the wordphenology in its strict sense of seasonal timing within years; and we addressvariationamong years only when it pertainsto the discussionof within-yearpatterns.The purposeof this reviewis to presenthypothesesaboutpossible evolution-ary causes and consequencesof differentphenological patternsand to discusstheevidencefor eachhypothesis.We alsobrieflysummarizenformation boutthe environmentalandgenetic controls of timingbecause these are the prox-imate factors that can influence the evolution of phenological patterns. Wedivide our review into four sections. The first three address germination,flowering, and fruiting separately. Each section covers possible selectivefactors, proximateenvironmental ues, andgenetic determinantsof differentphenological parameters.The last section focuses on the relationshipsofgermination, lowering, andfruiting,to the whole life cycle of theplant.Herewe addresspossible ecological andevolutionaryconstraints hatmaydirecttheevolutionof all life cycle events.Space preventsan exhaustive literaturereview, particularlyof descriptivestudies, so we mention representativestudies and reviews that provide thereaderaccess to additional iterature.We do not addressphenologicalpatternsof leaf production 43, 146) or the specific methodologiesfor collecting andanalyzing phenologicaldata(151, 194, 201).GERMINATIONThe seedling stageis themost vulnerable ime in the life cycle of aplant (101).Mortality s often severe because small seedlings have minimalcapacityforhomeostaticresponsesorphysiologicalretrenchmentntheface of unfavorableabioticor bioticconditions(10). Therefore, hetimingof germination houldbeunder strongselectionto occur when conditionswill continueto be favorablefor seedling establishment.SelectiveFactorsTIME OF OCCURRENCE Several studies indicate that abiotic factors favorgerminatingas earlyas possible to gainresourcesforreproduction,but not soearlythatsurvivalto time of reproductions unlikely. Generally,in temperateherbs ndividualseeds thatgerminateunusuallyearlyin the seasonhavelowerprobabilitiesof survivalthando those germinating ater, but the few that dosurvive have muchhigher reproductive uccess because of the longer growingseason(13, 20, 95, 158, 255). These effects canbe attributedo abioticfactors.By artificially wateringareas in the desert duringthe summer, Tevis (255)produced abnormallyearly germinationof Abronia. However, only one of


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PHENOLOGICALATTERNS 181many individuals survived the subsequent dry summer, but this individualproducedcopious seeds the following winter, when most other individualsgerminated.Summer-germinatingeedlingsof Leavenworthia tylosain cedarglades suffered four times the mortality of autumn-germinating eedlingsbecauseof drought,butsummerseedlings producedeight times as many seeds(20). These studies indicatethat time of germinationreflects a trade-off be-tween selection for high seed set and selection for high survivorship.Biotic factors like interspecificcompetitionmay also influence seasonaltimingof germination.Evidence comes fromobservationsandmanipulationsof species in naturalhabitats.Winterannualscanstronglysuppress hegrowthof spring-germinatingannuals (210). An early-spring emerging annual,Ambrosiatrifida, increasedmortalityand reducedthe seed set of neighboringlate-springgerminatingannuals 4). Theannual,Impatienscapensis, preemptsspace from establishedperennials by germinatingearly in the spring beforeperennial growth has begun (289). Garwood(85) suggests that, because ofintensecompetition,rapidemergence s criticalfor successfulestablishmentnlight gapsintropicalrainforests.In these cases interspecificcompetition avorsearly germination.Intraspecificcompetitionalso favors early germination. Many greenhouseexperiments show that early-emergingindividuals within cohorts preemptbiological space and gain competitive advantage over late-emerging in-dividuals(e.g. 29, 218). Ross & Harper 218) demonstratedhatthe increasedfitness of early emergersis not solely due to increased growing time; earlyemergersgrow more quickly andcontinuallyincrease theirabilityto acquireresourcesat the expense of later emergers. Several studies of naturalpop-ulations show that late-emergingindividuals suffer higher mortalityand/orreducedseed set (53, 181, 120), but these studiesdo not distinguishbetweencompetitive effects and effects produced by seasonal changes in themicroenvironment.Weaver& Cavers(279) separatedemergenceorderfromseasonal changes by sowing Rumex seeds at differenttimes into naturalhabi-tats.Theyfound that the emergenceorderwithin cohortswas more influentialthanthe emergencedatein determining eedling success (279). Abul-Fatih&Bazzaz(4) observedsimilarresultswhenexaminingthe effects of germinationtime of A. trifidaon the success of other weeds.Seasonally restrictedpredatorsor pathogens could select for timing ofgermination.Predatorsandpathogensare majorcauses of seed and seedlingmortality 17, 101). In some cases pathogenicpotentialchangesover a season(102). Lateplantingof crops can decrease some diseases (e.g. loose smutofwheat, Ustilago tritici) and increaseothers (e.g. wheat bunt, Tilletia caries)(19).. Predationof dispersedseeds should select for rapid germinationafterrelease from the parent(124), but the only support or this hypothesiscomesfromobservationsof redandwhite oaks (77). Squirrelspreferwhite oak over


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182 RATHCKE& LACEYred oak acorns. White oak acornsgerminatesoon after dispersalin autumn,whereas the less preferredred oak acorns germinate the following spring.Germination iming may reflect a compromise between the probabilities ofpredator r pathogenattackat the seed stage and the seedling stage. However,at presentwe know too little about the seasonalactivities of such predatorsorpathogensto evaluate this idea.SYNCHRONY AND DURATION The same abiotic and biotic factors that de-termine when seeds germinatemay also control the degree of germinationsynchronywithinandamong species. Correlationsbetween seasonal changesin the physical environmentandthesimultaneousgerminationof many specieswithinplant communitiessuggest that species respondto similarabiotic en-vironmental onditions.Intemperate limatesmost herbsgerminateas temper-atures rise in the spring, although they may exhibit more than one pulse ofgermination,e.g. duringthe summer(132) or in springand autumn(22). Inclimates with hot, drysummersandcold, humidwinters,herbsusually germi-nate in the autumnandearly winter (132). In desertsmany species germinatejust afterrains (25, 281). In seasonaltropicalforests in Panama, 75% of thewoody species germinateearly in the rainyseason (85). Abiotic factorsprob-ably produce this synchronous germinationamong and within species, andhabitatsthat provide only a shorttime for seedling establishment,vegetativegrowth, and reproduction hould increasethis synchrony. Competitionmayintensify synchrony indirectly by selecting for germinationat the earliestpossible time in the growing season to gain competitive advantage.Asynchronousgermination andextendedduration)s likely to be favored nhabitats where times suitable for seedling establishmentare either long orunpredictable.Severaltemperateherbsexhibit two pulses of germination-inautumn and in spring. However, seedlings often establish duringonly onegerminationpulse for any given year (13, 139, 156). InLudwigia leptocarpa,which hasonly one germinationpulse, early-emergingndividualssurpass ateemergers n survivorship,growth,or seed set only in someyears (60). Fortreespecies germinatingn theshadedunderstory f tropical orestsin Panama, herisk of mortalitys unpredictableorthe durationof therainyseason;andmanytree species extend germinationthroughoutthis season (85). In aseasonaltropical orestsof Malaysia,treespecies germinate hroughout heyear(182).In unpredictableenvironments the productionof offspring that differ ingerminationrequirements ould spreadthe risk of mortalityand representabet-hedging strategy (101). Annual species more commonly produce seedswith variablegerminationrequirements hando perennials, perhapsbecausethey risk complete reproductivefailure during a single unfavorableperiod(101). Theoreticalstudiesexaminingthe relationshipbetween environmentalunpredictabilityand fractionalgermination (e.g. 49, 267) have consideredgerminationamong years, however, rather han within years.


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PHENOLOGICALATTERNS 183EnvironmentalCuesThe initiation of germination s caused by a remarkablediversity of factorsincluding temperature,moisture, light intensity, light quality, photoperiod,carbondioxide, and minerals 10, 113, 132, 136, 160, 287). Some factorsthatdirectly stimulate germinationalso directly influence seedling survival, e.g.soil moisture ndeserts(97, 255, 282). Other actors hatstimulategerminationdo not affect the seedling directlybut arecorrelatedwith factorsthat do. Forexample, some desert seeds germinatein response to reduced soil salinity,which occursonly afterheavy rainsthat ensureestablishment.Seeds will notgerminateafter light rains, which may be followed by drought (97). Manyspecies requireacombinationof specific conditions o initiategermination.Forexample, some desert perennialsrespondto moistureonly if temperatures recool or moderate(10, 255, 281).Successful seedlingestablishmentdependson the preventionof germinationduring conditions unfavorablefor growth, and this is achieved through anumberof dormancymechanisms.Harper 101) succinctly summarized hese:"Some seeds areborndormant,some achieve dormancyand some have dor-mancythrustuponthem." These threetypes of dormancyare termedinnate,induced, and enforced dormancy, respectively (101). Innate dormancy isestablishedduringseed maturation,and it prevents seeds from germinatingeven whenplacedinto favorableconditionsuntil some cue releasesdormancy.Induced dormancyis acquiredafter dispersaland also prevents seeds fromgerminating ven when conditionsarefavorable. Seeds withenforceddorman-cy will germinateas soon as they areplacedin a favorableenvironment.Bothinduced andenforceddormancypermit opportunisticgerminationduringun-predictable nvironmental onditions(10). After innatedormancy s brokenbysomefactor,a seed mayremain n enforceddormancy.Seeds of some speciesgo throughpulses of induced dormancy,which prevent germinationduringseasons hostileforseedlingestablishment 22, 216). Factors nducingdorman-cy mayhave direct effects or may act as predictorsof unfavorableconditions.For example, induced dormancyin many grassland species is caused by adecreased atioof red to far-redightthatoccursbeneath eafcanopies; hislightquality s correlatedwith establishedvegetationand acompetitiveenvironment(229).Changesn environmentalactors an alter hegerminationesponses f seedsasthey matureon the parentplant (61, 98, 132, 231). This environmental re-conditioning an cause the proportion f progenywith a specific germinationrequiremento varywithinsibship.Maternal ffects can also producevariableprogeny(see EcologicalandEvolutionaryConstraintsection, below).GeneticsBecausegermination imeis strongly nfluencedby environmental onditions,the genetic componentof germination iming has been difficult to determine


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184 RATHCKE& LACEY(215, 286). Variation n germination imes of seeds collected from differentgeographicregionsis often ascribed o geneticdifferences, but environmentalpreconditioninghas seldom been eliminatedin germination ests, and mostresults are equivocal (21, 219). Growingplants underconstantconditions andthen examining the germinationof the subsequent generationof seeds canreduce environmentaleffects, but this technique has seldom been used instudies of naturalpopulations(21, 206). Ecotypic variation in germinationresponses s bestdocumented or afew weedy species (167, 258). Forexample,seeds of Silene dioica are summer-dormantn southernEuropewhere winterrains occur,whereas seeds from northernEuropearewinter-dormant258). Incontrast, many weed species from the continental climate of central Europeshow no ecotypic variation and germinateover a wide range of conditions(258). Seeds from cool-climate populationsof Typha (165) and Trifoliumsubterraneum 172) show greaterdormancyat low temperatureshan do seedsfrom warm-climatepopulations.In cool climates, low temperatures remoreoften correlatedwith even lower temperatureshat cause seedling mortality.Time requiredfor germinationis shorter in more northernpopulations ofVacciniumand Cyanococcus (58).Most available nformation n thegeneticbasis of germinationiming comesfrom agricultural tudies. Genetic crosses show that germination iming is apolygenic trait,andthatmaternal,paternal,andadditiveeffects can be signifi-cant (103, 205, 232, 286). Artificial selection has producedchanges in seeddormancy (232) and germinationphenology (290). Although genetic differ-ences inemergence imes of cropvarietiesmaybe significant,oftentheyarenotasgreatas environmental ffects (286). Thegeneticbasisof germination imingin naturalplantpopulations s less well known.InbothPapaver dubiumandP.rhoeas, artificialselectionreduceddormancy 13). Germinationimingshowslow heritability n P. dubium(13) and Geraniumcarolinianum(214).SummaryAlthoughnumerous pecificcase studiesof dormancyandgermination equire-ments exist, few have characterized he genetic componentof these require-ments. Germinationasynchronyobserved within naturalpopulationscouldresult from microenvironmental eterogeneity, genotypic differences amongindividuals,orphenotypicplasticity.Thepossible adaptivenatureof phenotyp-ic plasticity in producingvariable progeny in either flexible or fixed pro-portions, as well as the simple genetic control of germinationrequirements,needs to be explored (34, 130). No studiesof germination ime that we foundfocusedon the duration f germination,e.g. thelengthof time frombreakingofthe seed coatto seedlingemergence.Selection forrapidgermination ateshouldbe strongbut may vary over habitatsor species.The effectsof the abioticandbiotic environmentandtheir nteractionneed to


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PHENOLOGICALATTERNS 185be examined urthernmanipulative xperiments.The extent to which inter-orintra-specificcompetitiondeterminesthe fitness of seedlings in naturalpop-ulationsis still poorly known. Even less is known about the seasonaloccur-rencesof predators rpathogensandtheireffects on seed andseedlingsurvival.FLOWERINGFlowering ncludesfloralbud initiationanddevelopment,blooming(anthesis),andfloralpersistence(32, 67, 142). Here we generallylimitourdiscussion tothe blooming period, which is the time for pollination. We use the termflowering in this context unless we indicate otherwise.SelectiveFactorsTIME OF OCCURRENCE Abiotic factors are often correlatedwith floweringtimes. Intemperate egionsfrostin springandautumnmaylimit the floweringseason, althoughsome wind-pollinatedandalpine plantsflower either duringfreezing weather or under snow. In the seasonal neotropics,most herbs andshrubsflower in the rainyseason (57, 171), but twice as many tree speciesflower in the dry season as in the rainyseason (79). In contrast,in aseasonaltropical orests, no floweringpeaksoccur andmany species flower more thanonce a year (57, 187, 203). Abiotic factorsmaylimit floweringseasons eitherdirectly by affecting the ability to produceflowers or indirectly by affectingpollen vectors. These effects are seldom separated n studies.The seasonal availabilityof conditions favorablefor pollen transfermayaccount or the seasonalfloweringof some wind-pollinated pecies. Intemper-ateareaswind-pollinatedreescommonlyflower before eafemergence nearlyspring 47, 91, 217) whenpollendispersal s leastimpeded.Inthetropicsmanywind-pollinated ree species flower in the dry season (57, 75, 79), when thetradewindsare strongestand when some trees have lost their leaves (75).The seasonal availabilityof pollinatorsmay select for flowering times ofanimal-pollinatedpecies, but thisposes the "chickenandegg" paradox: s theavailabilityof seasonal pollinatorsa cause or an effect of flowering? Manystudiesshow seasonalcorrelationsbetweenpollinatorpopulationsandflower-ing (175, 217, 253). However,only a few studies show thatpollinatorpresenceis determined ndependentlyof floweringtime. Forexample, migration imesof hummingbirds,which are correlatedwith the floweringtimesof humming-bird-pollinatedplants, may be seasonallyrestrictedby otherfactors(36, 92,274, 276). Waser(274) found that seed set perflower in ocotillo (Fouquieriasplendens),a hummingbird-pollinatedhrub,was greater orplants floweringcoincidentallywith the presenceof hummingbirds han for plants floweringafterhummingbirdshadmigrated.The seasonalappearanceof lepidopterans


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186 RATHCKE& LACEYcoincides witharelative ncrease n the numberof moth-pollinated pecies thatare flowering (79, 122). The appearance f these lepidopteransalso coincidesw th the flush of new foliage necessaryfor larvaldevelopment. Schemske et al(226) observedthatseed set was commonlylimitedin many temperatewood-land herbs. They attributed his to the variance in the seasonal availabilityofinsect pollinators.A lack of reliableenvironmental ues that accuratelypredictpollinatorpresence may make perfect timing impossible (226).Seasonalpollinatorpresence s probablymorecommonlyaneffect of flower-ing. Manypollinators e.g. tropicalbirds andbats) arehighly opportunistic nddisperse ocally to areasof abundant loral resources(72, 74, 107, 204). Otherpollinators (e.g. multivoltine or social bees) can extend their life span orreproductiveperiod if the flowering season is extended (87). A dramaticexampleof a populationresponseto floweringis seen in thrips,which are themajorpollinatorsof theMalaysiandipterocarpshat lowertogetherevery 7-10years (44). Thripspopulations ncrease morethana thousand-foldon the firstspeciesthatflowers and arethus availableforsubsequently lowering species.SYNCHRONY AMONG SPECIES Aggregated flowering of different speciescould be advantageousf facilitationoccurs, i.e. if thepresenceof one speciesincreases the visitationrates and seed set of anotherspecies (208, 260, 262,275). Although aggregated loweringis common, little evidence suggests thatfacilitationcurrentlyoccurs.Incontrolled-density xperimentswith two wood-land herbspecies the presenceof heterospecificneighbors ncreasedvisits butalso increased nterspecificpollentransfer 176, 177). In several otherspecies,positivebut weakcorrelationshave beenreportedbetween thepresenceof oneplantspecies andvisitationratesor seed setof anotherplantspecies (260, 262).Coincidentalflowering of species with visually similar flowers has beenconsideredmimicryin which one or all speciesbenefitfromincreasedpollina-tor visits (36, 197, 224). Only Bierzychudek 28) has done the criticaltests offloralmimicry (288), and she found no evidenceforthemimicryhypothesisinher examinationof three tropical herbs with visually similar flowers. Thesimilarityin flowers and timing for variouspurportedmimics could simplyreflectresponseto selectionby the samepollinators;moretests, however, areneeded.Asynchronyor divergenceof floweringtimes among species could arise intwo ways. First, interspecific competition for pollinatorvisits could favordivergencebecause reducedvisitation can decreasepollen donation and seedset. No strongevidence supports his as a primarycause of divergence (208,275). Second, interspecificpollen transfer ouldfavordivergencebecause thistransfercould reduce pollen donation, reduce seed set, and produceless fithybrids. Two studies provide strong evidence that divergence in floweringtimes hasbeen causedby interspecificpollen transfer.Waser(275) found that


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PHENOLOGICALATTERNS 187sympatricpopulationsof Delphiniumnelsonii andIpomopsisaggregataalwaysflower sequentiallyandthat they differ in the orderof flowering in differentgeographic ocalities;this suggeststhatthey have divergeddifferently n localpopulationsin response to each other. To determinethe possible cause ofdivergence, Waser (272) artificially created coincidentally flowering pop-ulations and demonstrated hat interspecificpollen transferby shared hum-mingbirdpollinators significantlyreducedseed set of D. nelsonii. The mostlikely cause of the reduced seed set appearsto be stigma clogging by in-terspecificpollen(273). McNeilly & Antonovics (166) showed that sympatric,heavy-metal-tolerantand-intolerant populationsof bothAnthoxanthum ndAgrostishaverecentlyevolved differences n flowering times. The most likelycauseappears o be selectionagainstgene flow andhybridization.Competitionforpollinators ould notbe thecause because these species arewind pollinated.Otherpossiblecases of character ivergence nfloweringtimes(161, 208, 275)need furtherexamination.Interspecificdivergence in flowering within plant communities is rarelyfound.Most statistical estsof flowering dispersionwithin seasons have shownfloweringto be aggregated 9, 189, 196, 208, 260) or indistinguishableromarandom pattern (207, 283). Random models with different assumptions,however, can give different results (208). For example, phenological dis-placementsreported or two plantassemblages 52, 88, 193, 250) have underadifferentanalysis (196, 260) beenreported o be aggregated.Thus, the resultsandinterpretations asedon randommodelsremaincontroversial,and resultsshouldbe viewed cautiously.Divergenceof floweringtimesmaybe rarebecausefloweringtimeisjust oneof several pre-mating solationmechanisms hat can reduceinterspecificgeneflow (149). Floweringtime may be the easiest mechanismto altergiven theevidence for simple genetic control (178, 190), but because flowering timeseems to be such a phenotypicallyplastic character,divergencein floweringtime may not preventhybridizationas effectively as would changes in suchother plant charactersas floral morphology. The absence of evidence forflowering divergence at the community level may reflect such alternativesolutionsforreproductivesolation.Many closely relatedspecies areseparatedby habitatrather hanby flowering time (121, 217, 249).Evidence thatcompetitionfor pollinatorscurrentlyoccurs in naturalplantpopulations s sparse.Competitiveeffects on seed set have seldom been foundeitherbecausepollinatorsareveryabundant41, 71, 176, 208, 275) or becauseplantsproducepersistent lowers (176) or areselfing or apomictic(133, 223).Current ompetitionhas been detected in artificialor disturbedsituations.Inhybridseed gardens,competitionfor honeybeevisits commonlyreduces seedset amongcrop varieties (65, 66, 81). In old fields in Michigan, introducedhoneybees visit Solidago graminifolia only after other plant species have


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188 RATHCKE& LACEYceased flowering;consequently,earlyflowering clones set fewer seeds (96). Innaturalpopulations, traits other than flowering times may lessen potentialcompetitive effects.Divergence may also be uncommonbecause competitionamong plant spe-cies is inconsistentand nondirectionalover time. Consistent flowering se-quencesbetweenyearshave beenreported n a few studies (44, 253, 266), butthe degree of flowering overlap often varies. In other studies (75, 252),flowering times vary greatly and independentlybetween years. For tropicaltrees thatflowerinresponse o rainfall,local rainscan causehighly patchyandasynchronous lowering between species and within a species (16, 32). In-terspecific nteractionsareunlikelyto causedirectional electionon floweringtimes in these cases. Interspecific nteractionsare also likely to vary over aspecies' geographic range as other potential competitors and pollinatorschange. These different nteractionswould select for unique flowering timesthat are initiatedby different environmentalconditions. Some species showecotypic variation n flowering (112, 143), but the influence of interspecificinteractions s unknown. However, the ability to predict flowering times inmany temperate woody species over wide latitudesusing cumulative day-degrees (212, 235, 266) suggests that local interspecific nteractionshave notinfluenced flowering times. Anomalous populations should be sought andexamined.DURATION, SYNCHRONY, AND SKEWNESS WITHIN SPECIES Floweringdurationwithin populationscan last from a single day to the entireyear fordifferentspecies (24, 78). Gentry(86) firstcategorized lowering patterns orspecies baseduponduration: pecies with short durationscommonly producemassesof flowers in a synchronousdisplay (mass flowering)whereasspecieswith extended durationscommonly produce a few flowers a day over longperiods(steady-state lowering).Intropical orests,massfloweringis commonamongtreesthatflowerduring hedryseason whereassteady-state loweringisfoundin most understory pecies (14, 24, 79, 86, 122, 187). Variationsexistbetween these two extremes.Within ndividuals,extendeddurationof flowering maybe advantageousorspreading herisk of uncertainpollination.Obligateoutcrossingspeciestend toflower longerthanautogamousor self-compatiblespecies (24, 195), and thismayreflect thegreateruncertainty f pollination.Extendedduration ouldalsoallowindividuals o trackand accumulate esourcesneeded forseed maturationin environmentswhere resourcesare eithertemporallyunpredictable r sparse(24). Extendedflowering is more common in aseasonal environments andoccurs in most understoryspecies in tropical forests (79); this may reflectunpredictableor sparseresources. Alternatively,this extended durationmayreflect a lack of seasonal differencesin resource or pollinatoravailability.


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PHENOLOGICALATTERNS 189Synchronyatboththepopulationand individual evels affectsfloraldensity.Increased ynchronycanbe eitheradvantageous rdisadvantageousdepending

upon density-dependent nteractionswith other organisms. Increasing syn-chrony may increasethe attractivenessof a floral display, or it could satiatepollinatorsor predators 208). To test the effects of synchronyon pollinatorsand seed predators,Augspurger (15) experimentallycreated asynchronousfloweringwithin populationsof a tropical shrub,Hybanthusprunifolius; shefound thatindividualsflowering synchronouslywith the population attractedmore pollinators, set more seed, and suffered less seed predationthan didindividuals flowering asynchronously with the population. These effectsappeared to be caused by the different densities of synchronous andasynchronous ndividuals. In contrast, Zimmerman(293, 294) found thatindividualsof Polemoniumfoliosissimumhat loweredwhenfloraldensitywashigh, attracted ewer bees, produced ess seed andsuffered more seed preda-tion. The conflicting results from these two species suggest that trade-offsbetweenpollinationandpredationdependuponthe relativedensitiesof pollina-tors, seed predators,and flowers.Asynchronymay be favored in a numberof situations. Although somedegree of flowering synchronywithinpopulationsobviously is necessaryforoutcrossingamong individuals, slight asynchronywouldpromoteoutcrossingif it forced pollinators o move between individuals(80). Asynchronywithinpopulationscould also reduceintraspecificcompetition orpollinators,reduceeffective population size (23, 200), and increase the numberof mates astemporalneighborschange (24). Theseeffects have not been examined.Addi-tionally, in monoecious species with temporallyseparatemale and femaleflowers, asynchronyof the male and female phases within the populationisnecessary;synchronyof each phasewould precludeany chance for reproduc-tion. In Cupania guatemalensis, a monoecious tropical shrub, asynchronybetweenthe sexual phases is assuredbecause individuals start with differentphases andeach sexual phase has a variableduration 23).Asynchronous lowering within individualsof hermaphroditicpecies canreducegeitonogamyandpromoteoutcrossing by forcing pollinatorsto movebetweenplants(24, 152, 227, 246). In monoeciousspecies the sexes are oftenasynchronouswithinan individualplantandso reducegeitonogamy (23, 37).The mostextremeexampleof asynchronous loweringboth within andamongindividuals s seen in Ficus (125, 170). Within an individualplantthe femalephase may be separatedfrom the male phase by a month or longer. Thepollinatingwaspsenterareceptivesyconium,depositpollen, oviposit, anddie.Individuals f thenextgenerationdevelopover severalweeks andcollectpollenwhile exitingfrom the syconiumwhichis now in the malephase. Waspsmustfly to anothertree with receptive syconia to deposit pollen and oviposit.Individualfig trees flower at irregular ntervals, and this may maximize the


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190 RATHCKE& LACEYprobability hat one will be female while anotherindividualis male in thepopulation 125). Such asynchronywithin fig populationshas the additionalbenefitof maintaininga populationof pollinatingwasps, dependentuponfigsand apparently hort-lived.Sudden, synchronousonset or cessation of flowering by many individualsproducesa skewed flowering distributionwithin a population.Many specieshave rightor positively skewed floweringdistributions, .e. flowering beginsabruptlyand thentails off (207, 227, 261). Thomson(261) hypothesizedthatright skewing could increase detectabilityand attractiveness o pollinators,which would then continue to visit these known plants even as floweringdeclined. However, the same patternis observed in wind-pollinatedplants(207) and in an autogamousspecies (227). Synchronousonset of floweringprobably eflectssimilarresponsesto a uniformandunambiguous nvironmen-tal cue (124, 227).EnvironmentalCuesOnly three majorphysicalenvironmental actors have been identifiedas cuesthat initiateonset of flowering: photoperiod,temperature,and moisture (67,142, 228). Photoperiodiccontrol has been reportedprimarily or short-livedherbs (67, 142). Most temperatewoody species (151, 212, 235) and someperennialherbs (266) flower in responseto temperature,which usually actsthroughcumulativeheatsumsabove some threshold evel. In seasonaltropicalforests, floweringis often inducedby rainfall(8, 16, 73, 115, 186). Heavierrains ncreasesynchronyof floweringwithinpopulationsof sometropical rees(16, 17). Bochert 32) has shownthatfloweringin sometropical reesoccurs inresponseto decreasedwaterstress which maybe stimulatedby either leaf lossor rainfall.In desertsthe dryingsoil, which indicates the end of the growingperiod,causesannuals o flower(282, 255). A numberof environmentalactorsmay interactto determineflowering onset. In some plants floral buds areproducedonly aftera sequenceof environmental ues thatmay occur severalmonthsapart 67, 142). Forexample, low temperaturemayinducebiochemicalchanges n theseed that aterpermit hevegetativeplant o flower inresponsetoa second cue such as short nights (105). The timing of bud initiation anddevelopmentand the cues involved are little known (211).GeneticsEcotypic differentiation n seasonal flowering times between naturalpop-ulationshasbeenfound in uniformgardenexperiments 112, 143). Ingeneral,populationsromhigher atitudes lower earlier handopopulations rom owerlatitudeswhenplantedat low latitudes.Stagesof floweringthatoccur ate in thegrowing season, such as flower bud formation, tend to show greater in-terlatitudinalariation hanstagesoccurringearlyin thegrowingseason(211).Evidencefor the genetic basis of floweringtiming is stronger han thatfor


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PHENOLOGICALPATTERNS 191germination iming. Geneticvariationwithinnaturalplantpopulations s highin a few species (3, 6, 127, 128). Distinctearlyandlate floweringgenotypeshavebeen foundwithinpopulationsof Melandrium,Arabidopsis, andseveralcerealcrops(5, 145, 163, 282a). Artificiallyproducedpolyploidsflower laterthen their diploid progenitors(84). Agriculturalstudies, involving selectionandcrossing of different ines, havedemonstrated ormanyherbaceous peciesthatonly one or a few genes determine loweringonset (178, 272). Genotype-environment nteractionsare strongin some species (e.g. 173). Selection forfloweringtimeinseveralspecieshasproduced ignificantchanges withinafewgenerations(40, 190).SummaryPhenotypicvariation npatternsof floweringinnaturalpopulationsmayreflectheterogeneous environmental factors, differences among genotypes, orphenotypicplasticity. The causes of thisvariationneedfurther tudy. Correla-tions betweenfloweringtime andseed set (14, 96, 226, 227, 272, 273, 293,295, 296) areconsistentwith theassumption hatfloweringtimeaffectsfitness.However, the causalrelationshipremainsto be demonstrated.Both maternalandpaternalcontributions o fitness must be measured.Ingeneral, therearemanymorehypotheses aboutultimate actorsthatmaymoldfloweringtimes thanthere arethoroughstudiesthatpermittestingthem.Thus,atthistime it is difficult to evaluate hehypotheses.Experimental tudiesareneededtoclarifytherole of pollinatorsasselectiveforces intheevolutionofflowering times. Plantsandpollinatorsmay coevolve andincrease heirpheno-logicalmatching,butevidencethatvariance nseasonalflowering timesaffectspollinator itness is lacking. Otherbiotic factors,such as parasitism 106), caninfluenceflowering time, but these effects have received little attention.Wealso have little informationaboutthe directeffects of seasonaltiming on theability to produce or maintainflowers or to mature seeds. Schmitt (227)suggests thatearlydryingof serpentine oilshasselectedforearlier lowering ntwoLinanthusspecies. Schemske(225) has strongevidence thatherbivory nmid- and late-summerhas selected for early-summer lowering in some Im-patienspopulations.Theseexamplesindicate hatit maybe necessaryto studythe entirelife historyin orderto understandhe selective forces thatinfluencefloweringtimes. We hope thatwe will not need to extendstudiesover twelvecenturiesas theJapanesehavedone in theirobservationsof theblooming datesof Kyoto cherrytrees (12).

FRUITINGFruitingncludes nitiation,growth,andripeningof fruitandthepresentation ffruitto dispersers,as well as the eventualdispersalof fruitsfrom the parentplant. Herewe discussonly thetimingof fruit(orseed)ripeninganddispersal.


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192 RATHCKE& LACEYA ripeseed has severed its attachmento theparent.A ripe fruithasdevelopedcharacteristic roperties, ike color and flavorsthat attractdispersersor effectdispersal.Usuallyfruitsripenbeforethey are successfullydispersed;however,the fruits of some species, e.g. avocado and durian,develop their attractivepropertiesonly afterthey have fallen from the parentplant (184).Selective FactorsTIME OF OCCURRENCE Abiotic factors may limit ripeningtimes, but fewstudies address his relationship.In temperate egions, latefrostsin springandhigh temperatures n summer occasionally cause significant fruit mortality(245). Pecan clones that develop late in the seasonproducesmallerfruits thando early-ripeningclones because the nut is filling while conditions are poor(259). Daucus carota seeds dispersed ate usually have low viability(139). Inthe tropics, fruits of Hybanthusshrubs atypically producedduring the dryseason are often abnormallysmall and contain nonviable seeds (14).The time of fruitripeningshould reflecttimingof conditionsthatinfluencedispersal success. Offspring movement away from the parent is usuallyassumedto be advantageous 119). Evidence for this comes fromcorrelationsbetween times of fruit ripeningand abiotic conditions favoring dispersal inwind-dispersed pecies. In seasonaltropicalforests most wind-dispersed pe-cies ripenandreleasefruitsnear heendof thedryseasonwhen the tradewindsarestrongandwhenmanyleaves have fallen(56, 75, 119, 122, 150, 182, 203,236). This dispersaltiming also minimizes the time that seeds will lie on thegroundbefore germinatingat the beginningof the rainyseason (85).Availability of animal dispersersshould also select for ripeningtimes inanimal-dispersed pecies. In temperateareas most species with fleshy fruitsripentheirfruitsduringautumnbirdmigrations 109, 111, 174, 238, 243, 248,257). In aseasonal ropical orestsinMalaysia,where animaldispersersmaybeavailablethroughoutheyear, fruitingoccurs all yearand no fruitingpeaksareevident (203). In Panamanianorests, a slightly greaterproportionof speciesripenfruits n autumnwhenbirdsarrive rom northern reasthanat othertimesof the year (75, 122, 131). In more seasonal, tropicalforests, the numberofspecies with animal-dispersed ruit show a peak of fruitripeningduringtherainyseason(75, 76, 122, 131, 150, 254). Manycorrelationsbetweenripeningtimes andpresenceof dispersersexist, but the conclusions thatmaybe drawnfrom thesecorrelationsarelimited.Dispersalsuccess is logisticallydifficult tomeasureand is seldom known. Ultimately, one must follow individualoff-springand quantifytheir fitness.Althoughdisperseravailabilityshould select forripening imes, theproblemof circularityarises again as with flowering andpollinators:Is seasonalityofdisperseravailabilitya causeor an effect of fruiting ime?Migratingbirdshave


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PHENOLOGICALATTERNS 193been hypothesizedto select for autumn ruit ripening n temperateplants, butthis hypothesis rests on at least two assumptions. One is that birds would notmigrateearlier f fruits were availableearlier. No studies address his assump-tion. The second is that dispersalis more successful during migrationsthanearlieror laterin the season. Thompson& Willson (257) found that removalrates were fasterfor species with autumn-ripeningruitsthan for species withsummer-ripeningruits. Duringthe springand summer, the local, territorialbirds are sparse and feed primarilyon insects-high-protein food that birdsrequirefor reproduction.Birds may switch to fruits in autumnbecause theyneed high energy for migration(248). Temperatewoodland herbs that ripenfruits in spring are often ant-dispersed,whereas bird-dispersedherbs ripenfruits n latesummer 256). The fateof dispersedseeds, however,has notbeenfollowed.Seed mortalitycaused by seasonal predatorsor pathogens could also in-fluence timesof ripeninganddispersal.Most evidence comes frominterspecif-ic comparisonsrather than from studies of individuals within populations.Several studies of temperateherbsshow how species thatripen seeds duringsummersufferhigher predation hancongenersthatripenseeds earlier in thespring(35, 93, 99). Inseveraltemperate hrubs,fruitdamageby pests is moresevere for species with summer-ripeningruit than for species with fall- orwinter-ripening ruit (109, 257). Pre-dispersalpredatorsor pathogens candestroy seeds, makingfruit less attractive o dispersers (124, 248).SYNCHRONY AMONG SPECIES Facilitationcould select foraggregated ruit-ing times amongspecies by increasing he numberof dispersersorby increasingthe movement of frugivores between species (284). Dispersal away fromconspecifics, it is hypothesized,increasesseedlingsurvival(119, 284). Seed-lingsof Caseareanitidasurvivedbetterunderunrelatedperch reesusedbybirddispersers hanunderconspecifics(118). Synchronous ruitingwould be neces-saryfor a mimicand tsmodel(164), butthemimicryhypothesishas neverbeentested for fruits.Interspecificcompetitionfor animaldispersersshould select for phenologi-cal asynchronyor divergence among species (164, 236, 237). Snow proposedthat competitioncaused staggered fruitingtimes of bird-dispersedMiconiaspeciesin Trinidad237). However,thisstaggeredpatternhas beenshown to bestatistically ndistinguishable rom a randompattern 88). In general, fruitingtimes of animal-dispersed pecies tendto be aggregatedorrandomrather handisplaced 75, 79, 88, 109, 110, 111, 257, 283). Currentnterspecificcompeti-tion among plants for dispersershas not been studied. Occasionalanecdotalreportsof undispersed ruitssuggestthatcompetitionmayoccurattimes (108,119, 164), but otherenvironmental actors could producesimilarresults.If interspecificinteractionsare to select for divergenceor convergence in


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194 RATHCKE& LACEYfruiting times, fruiting sequences should be fairly consistent between years.Few long-termdescriptionsof fruitingpatterns xist. For tropical rees fruitingtimes can be inconsistentwithin andbetweenyears (75). In aseasonal orests inMalaysia, intervals between fruiting were often irregularboth within andbetween species (203). Individualsof manytropicaltrees may skip fruiting nsome years (121, 124, 169); this would eliminate or change any interactiveeffects amongor within plant species for dispersers.DURATION AND SYNCHRONY WITHIN SPECIES Durationof individual ruitsmust be separatedntopotentialduration orpersistenceability) and observeddurationdeterminedby removalrates. Mortalityof ripe fruits and seeds on theparent ould select forrapidreleaseor removalafterripening 124) andfor shortpotentialand observed durationtimes. In temperateregions, bird-dispersedfruits nsummerhave been foundto rot ordryrapidlywhereasautumn ruitscanremainattractiveorweeks ormonths(248). Stiles (248) hypothesized hattheshort potential duration times of summerfruits reflect rapid removal ratescaused by territorialbirds that learn the locations of fruits (257). Autumn-ripening ruits ast longerbecausethey must be discoveredby migratingbirdsthatare unfamiliarwithplant ocations. Since conditions are less favorable ormicrobialandpest attackon fruitsduringthe autumn, ripe fruits can persistlonger. Morphologicalor chemical mechanismsmay also deterpests (234).Withinan individualplant, extended durationof dispersalmay representabet-hedging strategy against uncertainty n colonization opportunities (24,139). Intheneotropicsearlysuccessional treeshavelonger fruiting imesthando foresttrees, which may increasethe probability hat theirseeds will reachgaps, which are formedthroughout he year (186). Extendedripeningcouldalso reflectthe seasonalunpredictabilityrscarcityof resourcesneededfor fruitdevelopment 24). Extended ruiting s more commonamong understory lantsthan among canopy trees (79), and resourcesmay be more limited for un-derstoryplants. Colonizing weedy herbscommonlyhave long periodsof seedrelease (102). In D. carota, extended durationof seed release, partiallycon-trolledby the parent (138), probablyincreasesdispersaldistance (139). Ex-tendedduration or a species couldbe causedby asynchronous ruitingwithinindividualsand/oramong individuals,and these have not often been separatedin species surveys.Increased ruitingsynchronybothwithin andamongindividualsmayfacili-tatedispersal f increases n fruitdensitycause the attraction f relativelymoredispersers.Intemperateareas, synchrony s greater orshrubspecies thatripenfruits in autumnthan for species that ripen fruits in summer (257). Theconsequently larger displays may attractmigrantbirds unfamiliar with thelocationsof specific plants (174, 257). These largerdisplayscould also satiatedispersers;however, this is less likely duringautumnmigrations (257). Re-


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PHENOLOGICALATTERNS 195searchers have hypothesized that the degree of fruit specialization by thedispersers elects forsynchrony nfruitingwithin individualplants(117, 164).Because specialized frugivoresare locally sparse, they are likely to be satiatedby large, synchronousfruit crops; hence, asynchronous, small fruit cropsshould be favored.Incontrast,because nonspecialized, opportunisticdispers-ers areabundant,dispersalsuccess should increasewithlarger ruitingdisplaysand greater synchrony (117). Most studies do not support this hypothesis.Removal ratesof fruits areusually highly variableand unrelated o either fruitcrop size or disperserspecialization (119).Within an individual, synchronous fruiting could be disadvantageous ifdispersers pend long times at one tree andthereforedropmost seeds under heparenttree. This effect could be eliminatedif predationon dispersersforcesdispersers to move frequently (116). Pratt & Stiles (198) show that crypticbirds,which shouldbe less susceptible opredation,havelonger linger timesinfruiting rees thando noncrypticbirds. Effects on fruit dispersalsuccess werenot measured.Synchronous ruitingboth within and among individualsmay satiate seedpredators.Augspurger 15) artificiallycreatedasynchronyamong individualsofHybanthusprunifolius,atropical hrub,and showedthat ndividuals ruitingasynchronouslywiththepopulationexperiencedhigherseedpredationhandidindividualsfruiting.synchronously.Janzen(123, 124) proposedthatpredatorsatiation has selected for mast fruitingin trees whose nutrient-rich eeds aredispersedby themajorseedpredator. nseveralmast-fruiting pecies, seedlingestablishmentoccursonly during he mastyear. Individuals ruitingasynchro-nouslywith thepopulation, .e. in a nonmastyear, leave no offspring(33, 234,240, 241). No studies have examined similar effects withinyears. Synchronybothwithin andamongindividualsmaybe limited to species whereseeds arewind-dispersedand satiation s unimportant 27) orwhere thepredatorand thedisperserare the same species and satiationis advantageous.

If predatorsdiffer fromdispersers,thenthe degreeof synchronywithin andamong individualswill likely reflect a balancebetween attractingdispersersandsatiatingeitherdispersersorpredators 27). Inlimberpine, the cones ripensynchronouslywithina tree butasynchronouslywithin apopulation 27). Thisappearsto allow nutcrackers,the major disperser, to harvest seeds moreeffectively than can squirrels, the major predator.Because ripeningis syn-chronouswithin individual rees, manynutcrackers anfindaripening ree andremove seeds more quickly than can squirrels. Because ripening isasynchronouswithin the population,satiationof nutcrackerss prevented.Asynchronousripening may reducecompetitionfor dispersers,but spatialaggregation may alter this effect (157). In nutmegs (Virola surinamensis)individual rees withinclumps appear o attract elativelymoredispersers hando isolated trees, but they compete among themselves for these collectively


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196 RATHCKE& LACEYgaineddispersers 157). Isolated reesattract ewerdispersersbut do not satiatedispersers.Theadvantagesof aggregation n attractingdispersersmay needtobe balancedwith the disadvantagesof competingfor dispersers.In nutmegs,intraspecific ompetitionmaybe the stronger orce and may have selected forasynchronous ruiting (157).EnvironmentalCuesEnvironmental ues seldomstimulate he onsetof fruitripening. Rather,onsetis determinedprimarilyby internal actorsthatcontrolthe rateof fruitdevelop-ment (e.g. 55, 144). Environmentalactorsmay secondarily nfluence ripeningratesby influencingmetabolism.Forexample,lower lightintensityreduces hepercentof berriesripeat harvestdatein Vacciniumangustifolium 2). Highertemperaturesdecreasefruitdevelopmenttime in sour cherry (264). Externalenvironmental onditionscan directlyinfluence fruit dehiscence, abscission,and dispersal(138, 265). )Extremedroughtor fire initiatescone dehiscenceinmanypines. Relativehumiditycontrols he rateof seed dispersal na numberofspecies (138, 265).GeneticsEvidence for geneticcontrolof the timeof fruitripeningcomes fromstudiesofdomesticated species. Genetic variabilityin development time is commonamongclones and sibs in pecans (259). Artificial selection has significantlychangedripening times in several species, usually by changing developmenttime (flower-to-fruitnterval) (18, 82, 268). In several species fruitdevelop-ment time is a polygenic trait (18, 82, 268), and in peaches heritabilityofdevelopment ime is quitehigh(.73-.98) (268). Crosseswithinsome cultivatedfruit species have demonstrated trongpaternalcontrolof the time of ripening(55, 185, 191). Thepollensource can determine he numberof seeds, fruitsizeand hence ripeningtime (59, 62, 63). Paternalcontrol of ripeningtime wasdiscoveredeven beforescientists understood he mechanismof fertilization nplants (180).Althoughmechanisms hat controlthe time of seed dispersalhave been lostwith plant domestication n a numberof species (244, 285), little is knownabout hegeneticcontrolof dispersal iming. InLactucaseriola theopeningofinvolucal bracts, permittingdispersal,occursonly in wild populationsand iscontrolled by a single gene (285).SummaryOf the three life history events consideredin this review, temporalfruitingpatternshave received the least attention. The effects of both external andinternalenvironmentson fruitingpatternsandthe natureof genetic control offruitingarepoorlyknown. Few experimentalstudies have addressedthe hy-


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PHENOLOGICALATTERNS 197potheses about the selective forces acting upon fruiting, probably in partbecause of the difficulty in measuringoffspring dispersal success.ECOLOGICAL AND EVOLUTIONARY CONSTRAINTSStudies addressingthe ecology and evolution of phenological patternshaveusuallyconsidered he timingof each life cycle event in isolation fromthe restof the life cycle. Focusingon one eventpermitsanexaminationof the selectivepressuresactingdirectlyuponthatevent. Natural election, however, acts uponan entireorganism,andso consideringeach event alone canbemisleading(30).Phenological patterns are likely to be constrainedby plant morphology,physiology, and moregenerallythe genetic andepigenetic background f eachindividual.In this section we explorethepossible constraints hattherest of thelife cycle may place upon temporalgermination,flowering, andfruitingpat-terns. We defineaconstraintnthe broadsenseas anytrait hat ndirectly imitsthepowerof a selective force tochangeaphenologicalpattern.Constraintsmayaffect one or all phenologicaltraits.Phenologicaltraitsthemselves may con-straineach other. Few studies have specificallyaddressed hese constraintsortheirgenetic basis, and so we hopethatdrawingattention o these studieswillstimulatefurtherresearch n this area.Effectsof Resource LimitationFlowering, fruiting, and even germinationrequire an input of energy andnutrients.Therefore,resourceabundanceand aplant'sabilityto assimilateandallocatethese resourcesmayinfluencephenologicalpatterns.Floralbud initia-tion is often associated with some "ripeness-to-flower"actor(e.g. 114, 142,144). Plants of some species flower only after they have accumulated athreshold evel of resources, often measuredby plant size. In annuals, largeplants that have accumulatedresources quickly often flower earlier in thegrowing season than do smallplants (26, 127, 128). In some indeterminatelygrowing crop plants, the productionof many fruits stops furtherflowering(148). Resource levels can also influence duration of flowering. In someannuals,large plants producemore flowers over a longer time thando smallplants (39, 227). In some perennials, arge plantsflowerlonger (e.g. 14, 200,223, 292).Plants hatrequiremoreresources orreproductionhouldflower laterand/orfor a shorter ime. Indioeciousspecies, females oftenbegin flowering ater hando males.Thisdelay mayallow females time to accumulatemoreresources hatare neededfor fruitandseed development(154), althoughearlyflowering bymales may have resulted fromcompetition among males for pollinators (24).Malesoftenproducemore flowers andflower for a longertime as inJacaratiadolichaula (37), presumablybecause of the lower cost of producingpollen.


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198 RATHCKE& LACEYAlso, females flower less often than do males within (38) and among years(168). Janzen (124) argued that for many hermaphroditic ree species, in-dividualsmay flower more often than they set fruit, thus, acting as males moreoften than as females, because pollen production is less costly than fruitproduction.This hypothesis has yet to be tested.The impact of resource imitationon flowering time may depend upon theabsolute time intervalbetween floral bud initiation and anthesis. In annuals,flowering immediately ollows budinitiation, and therefore he time of attain-ment of threshold ize influencesthe time both of bud initiationand of anthesis.Perennial herbs may resemble annuals when they flower after vegetativegrowth has occurredearly in the growing season. However, if several monthsseparatebud initiation and anthesis as in many trees and shrubs, resourceaccumulationikely influencesonlytimeof budformation.Reader 211) foundthat seasonalresourceaccumulationdeterminedwhenfloral buds were formedin three ericaceousshrubspecies but that flowering was initiated by a morepredictable xternalenvironmental ue. Presumably, ubsequent ruitdevelop-mentuses resourcesaccumulatednthepreviousyearrather han n the currentyear. However, the relativeuse of storedversus currentassimilates for fruitmaturation s poorly known (245, 278).Resource limitation and the limited time for growth and reproduction nannuals 104, 122)have motivated he developmentof theoreticalmodels thatpredict when and how an annual plant should switch from vegetative toreproductivegrowth. Cohen (50, 51) proposedthatfor annualsgrowing in ahabitatwhere lengthof the growingseasonis predictable, loweringshouldbedelayed to maximize resource accumulationbut not so delayed thatthere isinsufficient ime to mature eeds. Plants should switchsharply romvegetativeto reproductivegrowth. For annualsgrowing in habitatswhere length of thegrowing season is unpredictable, lowering should begin earlier and span alonger time to insure some seed productioneven in years when the growingseasonis cut short.Resourceallocation o reproductive rowthshouldgradual-ly increase with time. Other studies extend Cohen's model to predict theoptimaltime of onset of floweringwhen plantsare subjectto vegetative andreproductive osses, e.g. via herbivory e.g. 45, 134, 188), competition(221),or seasonalvariation n photosynthesisandstoragepotential(45, 222). Of thetwo models (45, 134) testedwith datafrom naturalpopulations,the King andRoughgarden 134) model accuratelypredicted ime of onset of flowering. Ingeneral, most models have predicteda sharptransitionfrom vegetative toreproductivegrowth. Sharp transitionshave been found in Lupinus nanus(192), some annualgrasses growingin the Mediterraneanegion, andin crops(101) thatgrowin highly predictable nvironments.However, otherempiricaldata indicate that biomass allocated to reproduction ncreases graduallyinannuals(26, 45, 46, 135, 251) and thatvegetative growthand fruitdevelop-


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PHENOLOGICALATTERNS 199ment compete for resourcesonce flowering has begun (144, 184). Thus, mostempirical evidence shows a gradualtransition o reproduction.

Few studies have characterized he seasonal switch in resource allocationfrom vegetative to reproductive growth in perennials. Many studies showproportional hangesin biomass allocationthrough he growing seasonbut donot indicate whether vegetative growth continues or ceases with onset offlowering or fruiting. Carbohydrate ccumulation n the meristemmay induceflower bud formation and inhibit vegetative growth (32), producinga sharpswitchfrom shootexpansionto flowering. However, some tropicaltrees suchas coconut palms, mangoes, and bananas simultaneouslygrow vegetatively,flower, and fruit (144). Root expansion continues after flowering begins inLupinus variicolor, an herbaceous perennial (192), and vegetative growthoccurs before, during, and afterreproductionn wild strawberry 129).The life history of a species may influence seasonal resource allocationpatterns.Lupinusnanus, anannual,switchesto reproductivegrowthearlier nthe summer than does L. variicolor, a perennial (192). Likewise, annualspeciesof Lolium(48) andPlantago (199) flower beforeperennials.InLolium,annualsare inducedto flower by longernights (48). Selection may favor thisfloweringdelayin perennialsbecause thedelay providesmore time forvegeta-tive growth, which could enhancesubsequentsurvival (199). Also, becausethereis less pressure or a perennial o produceseeds withinany one growingseason, perennialscan risk flowering at a later date.Conditionsthat affect resource allocationto offspringcan affect fruit size(81, 201, 292) andripeningtimes within an individual.Competition amongfruits or resourcesmay delay ripening.Larger ruitcrops ripen aterthansmallcrops in Vaccinium(155). Fruits with more seeds may producemore auxin,accumulate resources faster, and grow larger (184). In Vaccinium an-gustifolium, many-seededfruitsripenearlierthan fruitswith fewer seeds (1).However, species thatproduce arge fruitstend to develop fruit more slowlythando species thatproducesmall fruits (201).Resourceallocationmayinfluencetemporalgerminationpatternsas well asfruitingpatterns.When plantsaregrown underthe same environmentalcon-ditions,maternal ffects often associatedwithseed positionon the mothercanproduceprogenythatvaryin theirgermination equirements 42, 97, 282). Inmany Compositae,ray and disc flowers produceseeds that differ in time ofgermination 267). InXanthium, eeds areborne npairs,with one seedusuallygerminating12 months after the other (101).Maternal ffects may influencesubsequentgermination imes by regulatingseedsize (e.g. 95, 220, 231). IntwospeciesofRumex, arge seeds, borneon theproximalportionof inflorescences, germinatemoreslowly thando small seedsborneon the distal end (42). Otherstudies show similargerminationpatterns(286). Incontrast, argeseedsgerminate arlier hando smallseeds inMirabilis


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200 RATHCKE& LACEYhirsuta (280) and at the same time in Lolium perenne (179) and Raphanusraphanistrum242).

Rates of resourceaccumulation re ikely to be controlledgenetically as wellas environmentally.Size components ike height and weight, which estimateresourceaccumulation,show stronggenetic control in severalspecies (3, 83,270, 271). Otherdata indicate that height itself has been subject to naturalselection (3, 270, 271). Gottlieb's (89) studyof StephenomeriaandSolbrig's(239) studyof violets (Violaspp.) pointout, however, thatin some cases sizemay be completelyenvironmentallydetermined.Selective pressuresandmutations hat alterresourceassimilationor alloca-tion patternscould affect the evolution of phenologicalpatterns.A mutationthatincreases assimilationandgrowthratemay causeplantsto flower earlier,and this exposes them to an effective pollinator whose presence did notpreviouslyoverlapwith floweringtime. Environmentallynducedreductions nresourceaccumulation ouldeliminate ate-floweringgenotypesfrom a popula-tion because these genotypes can no longer set seed before the end of thegrowing season. Mutationsthat acceleratefruit maturationand/ordispersalcould allow seeds lacking dormancyto germinate n autumnand grow largeenough in autumnto producematureseeds. The above are hypotheticalex-amples, but they illustratehow selection might altera phenological traitnotonly directly but also indirectly throughchanges in assimilation rates andallocationpatterns.These changesoccurindependentlyof any selective pres-sure actingdirectlyon timing.MorphologicalConstraintsDevelopmentalpatterns hatdetermineplantshape may also influencepheno-logicalpatterns.Forexample,selectionforreducedheightcouldproduceeithera reductionin number of leaves and internodeson the flowering stalk or areduction n internode ength. A reduction n leaf numbercould reducephoto-synthesisandconsequentlydelay floweringif theplantnowrequiresmore timeto reach a thresholdresource level for flowering. In contrast, shorteninginternodeswouldreducephotosynthesisonly if leaves shade eachother, e.g. ifleaves areoppositely arranged.A little leaf overlapshould not reducephoto-synthesisand thereforeshould not change flowering time.The few studiesthathaveactuallyexamined herelationshipbetweenpheno-logical andmorphologicalpatternshave focusedprimarilyon temporaldiffer-ences in floweringassociatedwith determinate ersus ndeterminate rowth.Inplantswithdeterminate rowth,the terminalmeristemof a shoot differentiatesinto an inflorescence after producingnew vegetative tissue. The separationbetween vegetativeandreproductive rowth s sharp,and ateralbuds subtend-ing the inflorescence resume vegetative growth the following season. Inplants with indeterminate growth, the terminal meristem grows only


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PHENOLOGICALATTERNS 201vegetativelyand nflorescencesareproduced rom ateralmeristem, .e. on sideshoots. Thisgrowthpatternpermitssimultaneousvegetativeandreproductivegrowth. In the seasonal tropics, determinategrowth patternsof trees mayrestrict loweringto the dry season,whereas ndeterminate rowthpatternsmaypermit lowering throughout he year(32). In temperatehabitatswhere lengthof the growing season is predictable, e.g. agricultural ields, determinategrowthhabitsare common.The determinate rowthhabit n some annualsmayallowthemtodelay floweringandyetstill set seed beforethe end of thegrowingseason(101). In habitatswherethe lengthof the growingseasonis unpredict-able, indeterminategrowth patternsare more common; this growth patternpermits"opportunists"o grow vegetativelyfrom the terminalmeristemwhileproducing flowers from lateral meristems (101). Evolutionary change ingrowth patternshas occurredrapidlyin crop plants. For example, one locusdeterminesthe growth habit in lima beans, the determinate habit havingrecently evolved from the indeterminatehabit, which predominates n wildpopulations(7).Most informationaboutmorphologicalconstraintscomes from descriptivecommunitystudies. Withinplant communities different life forms flower atdifferenttimes. In Great Britain, peak time for tree flowering is May; forshrubs-June; for herbaceousperennials,annuals,andbiennials-July; andforbulbs and corms-April-May and September (91). Herbscommonly flowerduringor attheendof the activegrowth,most often in summer 32,47,91,94).In the seasonaltropicsherbsand shrubstend to flower in the wet season (57,171), buttreesflower in both wet anddryseason (57, 79, 171). Differentlifeforms may also germinateat different times. For example, in Californiandesertsmanyannual pecies germinateonlyafter ightbutextendedwinterrainsthat occur duringmost years, whereasmost perennialshrubsgerminateonlyafter shortbut heavy summerstorms that occur only once every 5-20 years(281). Went (281) argues that annuals can maturesuccessfully on a singlewinterrainperiodbutperennialshrubsrequireboth summerrainsandsubse-quent predictablewinter rains for seedling establishment.These documentedpatternsof temporalgerminationandflowering may or may not reflect large-scale differences in developmentthat make each life form unique. In eithercase, the observationsillustrate that we still have much to learn about theecology and evolution of developmentalpatterns n plants (cf 31).Gould (90) among others has proposedthat changes in the timing of de-velopmentalprocessesstronglydirectthe evolutionof size andshape.It seemspossiblethat size andshapealso directthe evolutionof the timingof develop-ment. Themodularnatureof plantgrowth(101) may permitdifferentpartsof aplant to behave as independentphysiological units (278). Each unit, e.g. arametof a clonalplant, may control its own resourceassimilationandalloca-tion. Thedegreeof controlmay varyamong species. We thereforepredictthat


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202 RATHCKE& LACEYincreasedautonomyof modules and increasedenvironmental ampling by themoduleswill produce ncreasedvariation nonset andduration f flowering andfruiting within an individual plant and may produce increased variation intemporalgerminationpatternsof offspring.Phenological CorrelationsThe sequence of germination, lowering, and fruitingseems developmentallyfixed within the life cycle of an individual; at least no one has yet found aspecies inwhich individuals lowerbeforethey germinate cf 64)! However, anunansweredquestion s: "Do phenological events follow each other afterfixedtimeintervals,or arethey independently ontrolledby differentenvironmentalcues?" (233). Time of flowering and fruiting may be completely canalized(sensu 269) once germination ccurs,so thatminorenvironmental hanges willnot altertheirtime of occurrence.Alternatively, imeof flowering and fruitingmay be completely controlledby externalenvironmental ues. Flowering andfruiting times of seven chaparralannualsappeared o be partially canalizedalthoughthe effects of plant size were not considered (233). During thissix-year study (233) germinationime variedgreatly nresponse o rainfall,andflowering andfruiti~ngimes were more strongly correlatedwith elapsed timefrom germination han with any of the measured environmentalvariables.

Otherstudies have shown correlationsamong germination, lowering, and/orfruiting imes. Earlyspring-germinatingThlaspiarvense individuals lowerbeforelate spring-germinatingndividuals 163). Males of Silene species bothgerminate and flower earlier than do females, and Asparagus officinalisfemales germinateearlierbut flower later than do males (154). Onset of seeddispersalfollows onset of flowering after a predictably ixed time in Daucuscarota (139). Suchcorrelationsmayreflect the canalizationof eventsfollowinggermination.Bamboos exhibit the most striking example of canalization offlowering time, even thoughthe time scale spans years, rather han months ordayswithinyears. Individualclones flower only once every 5-120 yearsaftergermination,andcuttingsof individualclones flowersynchronously egardlessof where in the world the cuttings are grown (124). Not all studies showcorrelations,however. Early- and late-germinating ndividuals of Veronicaperegrina (153) and Teesdalia nudicaulis (181) flower at the same time.Phenologicalcorrelationshave been detected n a few species;additionalworkis needed to determinethe extent and cause of such correlations.If phenological events are canalized, then to consider the evolutionaryconsequencesof aphenologicaleventin isolationfromothereventsmaylead toerroneous onclusions.Forexample,early-floweringplantsproducemorethanthreetimesthenumberof fruitsas do late-floweringplantsof Papaverdubium(13). However, plantsflower earlybecausethey germinateearly. Thus, selec-tion may be favoring early germinationrather hanearly flowering (13, 69).


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PHENOLOGICALATTERNS 203Alternatively, each may independentlyaffect an individual's fitness and besubject to direct selective pressure (cf 140).

Evenif phenologicalevents arenotcanalized,thetimingof one eventmay bealtered by selection because that event interactswith a second phenologicalevent. For example, temporal dispersal patterns may determine temporalgerminationpatterns.In Daucus carota, the seeddispersalseasonoverlapsandextends beyond the autumngerminationseason. Dispersal time influencesoffspring fate because only seed dispersed before or during the autumngerminationseason can germinatethat autumn(139, 140). In contrast, inGeraniumcarolinianum,dispersalfinishes before the germination eason anddoes not affect germination ime (214). Ritland(213) has postulatedthat inannuals loweringtimeand seed dormancymaybejointlyalteredby selection.His optimalitymodels suggest, for example, that variation n floweringtimedependsmoreon mean value of germination ime thanon the mean value offlowering time. Though Ritland's argument focuses on the variation ingerminationover years, one could probably apply the models to within-yearvariation n germinationas well.Genetic CorrelationsMather 159) andWright 291) amongothershaveargued hatnatural electionactsuponthephenotypeof integratedgene systemsrather hanuponindividualcomponentscomprisingthe systems. Forexample, in manyweed species, oneplant may produce several types of seeds; a unique shape, size, and set ofgerminationrequirementscharacterizeseach type (101). Selection may actupon this whole suite of seed traits,rather hanupon each traitindividually,because the whole suite permitseach parent o exploit more than one habitatthrough ts offspring (100). Genetic correlationsamong traitsconstitutinganintegratedphenotypeprevent heindependent volutionof thecomponent raits(141).A few studieshave shown thattraits associatedwith time of flowering aregeneticallycorrelated o componentsof plantsize (1 1, 83), reproductive ffort(202), and frost tolerance (48). Crop studies show genetic linkage of genescontrollinggerminationandfloweringtimesincucumbers 286). Thus, flower-ing andgermination imes mayrepresentone componentof an integratedgenecomplex in some species. Flowering time is not genetically correlatedwithcomponentsof reproductive utput nLolium(54) germinationnrice (286), orself fertilityorzinc tolerance nAnthoxanthum1 ). Therefore, notherspeciesselection may act upon each trait individually as it has in Anthoxanthumpopulations growing along metal mine tailings (11). In peaches, the timebetweenfloweringand fruitripening s geneticallyfixed in one varietybutnotin another(18).


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204 RATHCKE& LACEYGeneticcorrelationsbetweennonphenological raitsmay also influence theevolutionof phenologicaltraits. In Vulpiafasciculata, early emergingplants

producemany spikeletsbut few seeds per spikelet;late emergersproducefewspikeletsbut manyseeds per spikelet(277). If the correlationbetweenspikeletnumberand seed numberperspikeletis genetically based, as are reproductivetraits n otherplantspecies, (e.g. 202) then alteringgermination ime will alterreproductivecomponentsof fitness but will not change net fitness becausereproductive omponents arenegativelycorrelated.Negative genetic correla-tions canweakendirectionalorstabilizingselectionacting uponaphenologicalpattern.In general, the degreeto which a phenological patternmay evolve inresponse to a selective pressurewill depend on the number, strength, anddirectionof genetic correlationsandon thegeneticcontrol of correlated raits.Correlations hat areeasily broken,that manifest themselves only in extremeenvironmentsseldom encounteredby a species, or that involve traits undersimple Mendeliancontrol should not constrain the timing of developmentalevents for long. Alternatively, correlationsthat are difficult to break, thatcontributestronglyto individualfitness or that involve polygenic traits maystronglydetermine he degreeanddirectionof evolutionarychange in pheno-logical patterns.

CONCLUSIONSAn environmental ressuremay precipitate neof severalalternative volution-ary responses within populations, and these responses may or may not bephenological. For example, spatiallyandtemporallyheterogeneous environ-ments may select either for increasedseed dormancyor for increaseddis-persibility (10, 101). In some cases plants have evolved dimorphicseeds,which increasebothoffspringdormancyanddispersibility,albeit in differentseeds (267). Seed predationmay select for an increase in toxic compounds nseeds, achangein seasonalfruitingorgerminationpattern,and/or hedevelop-mentof mastfruiting.Seedling competitioncould select foreitheracceleratedgermination rlarger eedsize (230). Itis timetoacknowledge hese alternativepathwaysin evolutionarystudies of phenologicalresponses.Futurestudies need to address all levels of complexity of phenologicalpatterns.We need to examine the trade-offs engenderedby countervailingselectivepressuresactingdirectlyuponeachphenologicalevent. We also needto examinethe constraints hatotheraspectsof an organisms'slife cycle mayplace upon potentialphenologicalchanges.Futurephenologicalstudiesneed toconsiderbothwhy anorganismresponds o a particular nvironmentby chang-ing its phenological patternrather hanby changingsome other attributeandhow the genetic and the epigenetic backgroundconstrain the direction anddegree of adaptation.


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PHENOLOGICALATTERNS 205ACKNOWLEDGMENTSBoth authorscontributedequally to this review and hope that there are nomisinterpretationsf cited research.Space did not permit the inclusion of allpertinent iterature.The authorsgratefully acknowledge the following col-leagues for their helpful comments on previous drafts of this review: C.Augspurger,P. Bierzychudek,J. Bronstein,J. Fry,D. Goldberg,D. Gorchov,J. Harper,D. Inouye,D. Karowe,T. Meagher,D. Rabinowitz,D. Roach, D.Simberloff, andM. Willson.LiteratureCited

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