Fruit

Preface byKenArnold

Foreword byStephenD.Hopper

Fruit–Edible,Inedible,Incredible

WhatisaFruit

Whatisafruitandwhatisavegetable?

Angiosperms,Gymnosperms andthosethatcopulateinsecret

Thenaked-seededones

Thenon-naked-seededones

Anabominablemystery

Angiospermextremists

NoFlower,noFruit?

Isapineconeafruit?

NoCarpel,noFruit?

Ashamelessdisplay

NotquitetheovaryofEve

Unwittingcouriers

Wind,sexandgenderseparation

What’sinaFruit?

Babylonianconfusion

Enhancedfemaleperformance

Howtobeacarpologist

Thetruemeaningoffruits

SimpleFruits

Thetruthaboutberries

Themiraculousmiracleberry

Goldenapples

Fragrantcitrons

Buddha’shand

Sizeablepepos

Softshell,hardcore or howtobeadrupe

Nutsaboutnuts

Walnutsorwaldrupes?

Glansquercus

Twofruitsinone–cashewnutandcashewapple

Wheat“grain”andsunflower“seed”–caryopsisandachene

Samaras–nutsgoneairborne

Cypselas–achenesgoneairborne

Podsandsuchlike

Capsulesorsevenwaystoopenafruit

Teeth,fissures,cracksandlids

Follicleandcoccum

Podsasin“peapods”

Sweetbeanpods

TheWorld’slargestbeanpod

Seedsinprison

Inside-outdrupes

Tobeornottobeadrupe

opposite: Phytolaccaacinosa (Phytolaccaceae)–Indian pokeweed;nativetoeastAsia–flower.Typicalof dicotyledons,theIndianpokeweedpossessespentamerous flowerswithfivewhiteorreddishtepals(acalyxisabsent) andtwowhorlsoffivestamens(intheflowerillustratedthe anthershavealreadydroppedoff);onlythenumberof carpels(eight)isdeviant.Althoughunitedintoasuperior syncarpousgynoecium,constrictionsclearlymarkthe boundariesbetweentheindividualcarpels,eachof whichhasitsownstyle;diameterofflower7.5mm

Galanthusnivalis subsp. imperati ‘Ginns’(Amaryllidaceae)–snowdrop,gardenvariety;thewildformnativetosouthern Europe–flower;typicalformonocotyledons,thesnowdrop possessestrimerousflowerswiththreelarge,whiteouter perianthsegments(‘sepals’)andthreesmaller,innerperianth segments(‘petals’).Thegreenswollenpartoftheflower belowtheperianthistheinferiorovarythatconsistsof threejoinedcarpels

thisrespectisthedefinitionadoptedbymanybotaniststhat“afruitisamatureovary includingtheseeds.”Theinspirationforthisnarrowconceptprobablygoesbacktothefirst carpologicaltreatmentinhistory,JosephGaertner’s(1732-91)well-knownbook Defructibus etseminibusplantarum (Onthefruitsandseedsofplants),published1788-92.Gaertner distinguishedbetweenfruit(“fructus”),whichheapplied(interalia)totheconeof Pinus, whereasformostangiospermfruitsheusedtheterm pericarpium,whichhedefinedasa “matureovary.”ThismayseemconfusingtodaybutGaertnerformulatedhisideaslong before1827whenRobertBrown(1773-1858)pointedoutthefundamentaldifference betweengymnospermsandangiosperms,whichuntilthenwerenottreatedseparatelyby botanists.Also,attheendoftheeighteenthcentury,thedetailedstructureofthegynoecium wasnotyetfullyunderstood.Infact,inthethinkingofGaertnerandhiscontemporary,the greatCarlvonLinné(1707-78),manyangiospermousfruits(e.g.thoseofthesunflower family,Asteraceae)weredeemedtobenakedseeds.

Inthenineteenthcentury,JohnLindley(1832)summarizedGaertner’stermsfor pericarpiaasnamesforfruittypesanddefinedfruitas“theovariumorpistillumarrivedat maturity;but,althoughthisisthesenseinwhichthetermisstrictlyapplied,yetinpracticeitis extendedtowhateveriscombinedwiththeovariumwhenripe.”

Althoughthehistoryismorecomplicatedthancanbeexplainedhere,littlehaschanged overthepast170years.Most“modern”authorsstillchoosetodefineafruitastheproduct ofamatureovary,althoughsomeallowotherpartsoftheflowertobeincluded(e.g.Raven etal.1999;Mauseth2003;Heywoodetal.2007),an“inconsistency”alreadypointedoutby Lindley.Sincegymnospermshavenocarpelsandthereforenoovaries,theyare,asalogical consequence,unabletobearfruits–atleastaccordingtothispopulardefinition.

Admittedly,carpelsarearemarkableinventionandhavesomemerit.Infact,the possessionofclosedcarpelsinsteadofopenmegasporophyllsisoneofthemostsignificant advantagesthatangiospermshaveovergymnosperms.Advancesinotherareas,suchasa moresophisticatedwoodstructurewithimprovedwaterconductivity,arefinedsexlife,a highlyeconomicalmethodofseedproduction5 andgreaterflexibilityinseedling establishmenthavealsohelpedtomaketheangiospermscurrentlytherulingclassamong plants.However,asdiscussedinourpreviousbookonseeds,sexualreproductionandseed dispersalremainthemostcrucialeventsinthelifecycleofaseedplant.Therefore,probably morethananything,itwastheamazingabilitytoadaptandperfecttheirflowers,fruitsand seedsinsomanydifferentwaysthatbestowedonangiospermstheirevolutionarysuccess. Alas,thebotanists’difficultyindefiningafruitdoesnotendwiththeexclusionofthe gymnosperms.Asweareabouttodiscover,thecomplexityoftheproblemincreaseswithin

Actinidiadeliciosa (Actinidiaceae)–kiwiorChinese gooseberry;nativetosouthernChina– opposite: microscopic detailoffruitsurface;ontheoutside,kiwisarecoveredwith twotypesofhairs,largemulti-cellularhairsandsmall,twocelledhairs;picturedarea4mmwide– below: –crosssection offruit(berry);thekiwifruitdevelopsfromasuperiorovary formedby30ormorejoinedcarpels.Themanywalls(septae) betweentheindividualcarpelsareclearlyvisiblebetweenthe tinyblackseeds,resemblingthespokesofawheel;diameter c.4cm– bottom: kiwifruits'onthevine'

Thetruemeaningoffruits

Knowinghowfruitsareformed–andwhichorgansplantsutilizetoachievetheirbaffling variety–isafascinatingtopiceveniftheclassificationoffruitsaccordingtotheirstructure mayseemlikeanattempttoforcetheiroverwhelmingdiversityintoamorphological straitjacket.However,searchingforgeneralpatternsanddefiningprecisecategoriesisan essentialscientificpractice.Itaimstofacilitatecommunicationwithinthescientific communityandhelpstobringsomeorderintotheotherwiseunmanageablechaos,no matterwhataspectofthenaturalworldisstudied.Asforfruits,understandingtheir structureanddevelopmentisonlythestartingpointforthestudyofallotheraspectsof theirnaturalhistory.Infact,puremorphologyisanabstractionandwhyfruitslookthe waytheydocanonlybefullyunderstoodwhentakingintoaccounttheirbiological function,namelythedispersaloftheseedstheybear.

Forreasonsthatwillbediscussedlaterindetail,successfulseeddispersaliscrucialfor thesurvivalofaspecies.Thisvitalfunctionexposesfruitsandseedstohighlyadaptive pressuresduringthecourseofevolution.Effectively,theenormousdiversityoffruittypes displayedinnatureisadirectconsequenceofthesefunctionalpressures,whichoftenlead toastonishingsimilaritiesbetweenunrelatedspeciesfacingsimilarecologicalchallenges. Intriguingthoughsuchconvergencesare,theycauseyetmorecontroversyforcarpologists becauseoftheunnaturalrelationshipsamongmanyofthetaxathatarerepresentedbya particulartypeoffruit.

Armedwiththisbriefintroductiontothescienceofcarpology,andwithoutuncovering moredisconcertingtruthsabouttherealnatureoffruits,weshallnowbeginourjourney intothecarpologicaluniverse,startingwiththesimplestfruittypeofall.

SIMPLEFRUITS

Sincethemajorityofangiospermshaveflowerswithasinglepistil,whetheritconsistsof justoneindividualcarpelorseveraljoinedcarpels,wearemostfamiliarwithfruitsthat developfromsuchflowers,especiallyifweliveinthetemperatenorthernhemisphere.Fruits thatdevelopfromasingleflowerwithasinglepistilarecalled simplefruits,irrespectiveof whethertheyarefleshyordry,dehiscent(opening)orindehiscent(non-opening).Green beans(Phaseolus spp.),peapods(Pisumsativum)andcarob(Ceratoniasiliqua)areallsimple fruitsofthelegumefamilyand,assuch,developfromasinglecarpel.Tomatoes(Solanum lycopersicum,Solanaceae),oranges(Citrussinensis,Rutaceae),kiwi(Actinidiadeliciosa, Actinidiaceae),giantpumpkins(Cucurbitamaxima,Cucurbitaceae)andpapayas(Carica papaya,Caricaceae)aresimplefruitsformedfrom compoundpistils.Suchsyncarpous

Galinsogabrachystephana (Asteraceae)–nativetoCentral andSouthAmerica–fruit(cypsela);inthetinyshuttlecocklikecypselasofthisspeciestheraysofthemodifiedcalyx performastinyfeatherywings;2.5mmlong

Xanthismatexanum (Asteraceae)–Texassleepy-daisy(name alludingtothecapitula,whichcloseatnight),theonly speciesofthemonotypicgenus;nativetothesouth-eastern UnitedStates–fruit(cypsela);althoughitsspreadingpappus raysareabletoassistwinddispersal,theyareverynarrow withteethalongthemarginthatmakethemevenbetter adaptedtoanimaldispersal(epizoochory);7mmlong

examplesistheGulfStream,whichcarriestonsofexoticdriftseedsfromSouthAmerica andtheCaribbeantotheshoresofnorth-westernEuropeeveryyear.Amongthemost frequentarrivalsonEuropeanbeachesaretheseedsofthepredominantlyneotropical Entadagigas,whosesuggestiveshapeexplainstheirpopularname“seahearts.”Themore rectangularseedsofthepaleotropical Entadarheedii,knowntodriftseedcollectorsas “matchboxbeans”or“snuffboxbeans,”aremainlyfoundonbeachesinsouth-eastAsiaand thePacificregion.Bothseaheartsandmatchboxbeanshavebeenusedingames,asbaby teethersand,hollowedoutandhinged,assnuffandmatchboxes.

Seedsinprison

Atthecloseofourcarpologicalexplorationof“pods,”onekindremainstobediscussed, namelythosemulticarpellatepodsthatwouldbeperfectlyacceptablecapsulesifonlythey wouldopen.Theserattlingpodshaveanairspacearoundtheseedsinsidetheirhardshell (whichcanbefleshyordry)andhavelongbeenacarpologicalnuisance. Amongthevarioustroublemakersaretheferociouslyspinyfruitsof Uncarinagrandidieri andthedevil’sclaw(Harpagophytumprocumbens ),bothbelongingtothesesamefamily (Pedaliaceae),chilliandbellpeppers(Capsicumannuum ,Solanaceae),andtheroseapple (Syzygiumjambos,Myrtaceae).

ThemostremarkableofallindehiscentpodsmustbethoseoftheBrazilnuttree (Bertholletiaexcelsa,Lecythidaceae),ahugetreeupto60mtallfromtherainforestsofSouth America.Whereasitsrelativessuchasthemonkeypot(Lecythispisonis)havelargecapsules thatopenwithawidelid,thefruitoftheBrazilnuttreeappearstohavelosttheabilityto produceanescapehatchforitsseeds.Hardereventhantherock-likeseeds(Brazil“nuts”), thefruitof Bertholletiaexcelsa isalargesphericalwoodypod,15cmonaverageindiameter andweighingupto2.5kg.Inside,thefruitbears15-25seedsembeddedinayellowpulp.

Whilstprovidingthepreciousseedswithmaximumprotectionagainstpredators,thealmost impenetrablepericarp,whichneedsanaxetocrackit,constitutesamajorobstacleto germination.ThisproblemissolvedbytheBrazilnuttree’snaturalally,theagouti (Dasyproctaagouti).Onlytheteethofthismedium-sizedrodentaresharpenoughtognaw aholeinthepodthroughwhichtoextractthenutritiousseeds.Theagoutis,likesquirrels, arescatter-hoardersandtendtoeatonlypartoftheirbountywhileburyingtheleftover seedssomewhereintheforestfloor,upto400mawayfromtheparenttree.Eitherdeathor forgetfulnessonthepartoftheagoutiensuresthatnewBrazilnuttreesgrowinthewild.

HoweverintriguingthestoryoftheBrazilnuttree,multicarpellatepodsthatremain stubbornlyclosedevenatmaturityposeaconceptualchallenge.Botanistswereunabletofit

opposite: Hippocrepisunisiliquosa (Fabaceae)–horse-shoe vetch;nativetoEurasiaandAfrica–fruit(camara);adapting totheshapeofthefruit,theseedsarebentaroundthe ellipticinvaginationsofthefruitwall.Althoughtheadaptive strategybehindthecuriouslyshapedpodsisdifficultto interpret,itsflatandverylightweightconstructionmayassist winddispersal.Moreover,theoverlappingmarginsofthe invaginationsandtheperipheralbristlesmayhelphookthe fruitstothefurofanimals(epizoochory);diameter1.8cm

Harpagophytumprocumbens (Pedaliaceae)–devil’sclaw, grappleplant;nativetosouthernAfricaandMadagascar–fruit(carcerulus);thelargewoodygrapplesofthisdevil’s clawareadaptedtoclingtothefeetandfurofanimals, whomaysufferterriblewounds.TheKhoisanpeoplesofthe KalahariDeserthaveusedthetuberousrootofthedevil’s clawforthousandsofyearstotreatpainduringpregnancy andtoprepareointmentstohealsores,boilsandotherskin problems.Extractsfromdriedrootsaretodaysoldasa naturalremedyagainstpainandinflammationcausedby arthritisandotherpainfulailments;fruit9cmlong

opposite: Phytolaccaacinosa (Phytolaccaceae)–Indian pokeweed;nativetoeastAsia–inflorescence;thesuperior syncarpousovaryoftheflowerhas7-8lobes,each representingasinglecarpel;diameterofflower7.5mm

Phytolaccaacinosa (Phytolaccaceae)–Indianpokeweed; nativetoeastAsia–fruit(baccarium);whenfullymature, theindividualcarpelsseparateintosingle-seededberrylets, hencethename baccarium (Latin: bacca =berry)forthis typeofschizocarpicfruit;diameter7.8mm

Alyogynehuegelii (Malvaceae)–lilachibiscus;nativetosouth andsouth-westAustralia–seed;therathershorthairsproducedbytheseedcoatinneatlongitudinalstripesare probablyanadaptationtowinddispersal;2.5mmlong

opposite: Hibiscusmutabilis (Malvaceae)–Confederaterose; nativetoChinaandJapan,naturalizedinthesouthernUSA–seed;asanadaptationtowinddispersaltheseedbearsa dorsalpatchofspreadinghairsthatforma“parachute;” seed(excludinghairs)2.6mmlong

opposite: Cyanocittacristata (Corvidae)–bluejay;nativeto NorthAmerica.Abluejaycanscatter-hoardmorethan100 acornsaday

below: Pinussabiniana (Pinaceae)–diggerpine;nativeto California–theheavy,wingedseedsarefirstwinddispersed, thenscatterhoarded;seed3.5cmlong(includingwing)

bottom: Sciuruscarolinensis (Sciuridae)–easterngrey squirrel;nativetotheUSAandCanada–inautumnsquirrels scatter-hoardnutritiousseedsandfruitsforthelongwinter

tryingtomaketheanimals’jobofcollectingandburyingtheseedseasier.Givenenough time,thewingsdropoffbythemselves.

Thestrategyofsacrificingpartoftheseedcroptoscatter-hoardinganimalsreliesonthe factthatnotallcachedseedswillbeeaten.Becauseoftheforgetfulnessorprematuredeath oftheircollector,agoodnumberofseedsalwayssurviveunharmed,plantedinsuitable establishmentsiteswellawayfromtheshadowoftheparenttree.

Oaks,beeches,andotherlong-livedplantssuchasbamboosproducelargecropsoffruits onceeveryfewyearsinanunpredictablepattern.Thephenomenonofsynchronousproductionofbumpercropswithinapopulationhasbeencalled“masting.”Ecologistshave paidmuchattentiontomastfruitingduringthelasttwentyyearsandhavecomeupwith numeroushypothesestoexplainthephenomenon.Onepossiblereasonislinkedtothefact thatmanywell-knownmast-fruitingspeciesarewindpollinated.Mastseedingcould thereforebeaconsequenceofmastflowering,whichincreasesthechancesofsuccessful windpollinationinmast-floweringyears.Asecondhypothesissuggeststhatplantscan predictwhichyearswillbethemostpromisingfortheestablishmentofseedlings.Thiscan applytofire-pronehabitats,forexampleinAustraliawherethemastfloweringofgrasstrees (Xanthorrhoea spp.,Xanthorrhoeaceae)istriggeredbyfire.Theburningofthesurrounding vegetationreducescompetitionandtheashofburntplantmatterincreasestheavailability ofnutrients.However,serotinousdicotyledonsandconifersstoringseedsinarmouredfruits thatreleasetheirseedsafterafirecanexploitthisopportunitymuchmorequickly.

Anotherwell-receivedtheorysuggeststhatoccasionallargereproductiveeffortsare moreeconomicintermsofseedproductionandsurvivalthanregularsmallerones.Mast fruitingproducesmoreseedsthantheavailablepopulationsofpredators(e.g.scatterhoarders,seed-eatinginsects)areabletoconsume,ensuringthatinmastyearslarger numbersofseedsescapeunscathed.Thegreatvariationofseedproductionfromyeartoyear canhaveastrongeffectontheplantpopulationsinvolvedandonthepopulationsofthe animalsthateattheirseeds.Inbetweenmastyearspredatorsstarveandtheirnumbersfall untiltheyareoverwhelmedbyfoodduringthenextbumpercrop.Althoughthissurprise tacticsoundsplausible,itssuccessdependsontheresponseofthepredator.Specialist predatorscanbehithardbutnumbersofgeneralistswhogorgeonthenutritiousseedsonly whenavailable(e.g.acorn-eatingdeerandpigs)remainthesame.However,evenspecialists aresometimesabletooutwitthecunningruseofmastseeding.

NewZealand’skakapo(Strigopshabroptilus),theworld’sheaviest(upto3.5kg)andonly flightlessparrothaslongbeenknowntobreedonlyinyearswithanoverabundanceoffood supplies.Oneeventthatincitesthekakapotolayeggsisthemastfruitingoftherimutree

“specialized”and“generalized”dispersalsyndromes.Despiterecentcriticismofthe theoreticalfoundationunderlyingtheconceptofdispersalsyndromes,manyecological studiesconfirmthatcertainfruittraitssuchascolour,sizeandprotectionareclearly associatedwitheitherbirdormammaldispersal.Whetherquantifiableornot,colour,texture andaromausuallyprovidethebestcluesastowhetherbirdsormammalsarethepreferred dispersersofaparticularfruit.

Thebird-dispersalsyndrome

Volantbirdsarebyfarthemostimportantdispersersofseeds.Theabilitytoflyaffordsthem excellentmobilityandenablesthemtotransportseedsintheirgutquicklyandoverlong distances.Intermsoftheireffectivenessasseeddispersers,birdsareprobablyonlyrivalled byfruitbats.Mostlydiurnalcreatureswithexcellentcolourvisionbutapoorsenseofsmell, birdsrelyontheireyesratherthanontheirnosestolocatefoodthattheyareunableto chewbecauseoftheirlackofteeth.Onlyafewgroupsofbirds,includingparrots,crowsand NewWorldblackbirds(familyIcteridae),arecapableofbreakinguptough-skinnedfruits withtheirfeetandbeakstoreachpulpandseeds.Mostotherbirdsswallowfruitswhole, whichcouldbethereasonthattheyarenotputoffbythesourorbittertastethatrenders manybird-dispersedfruitsunpalatableforhumans.Nevertheless,birdshaveaclearbias towardscertainfruitsandpreferthemwhentheyarefullyripe.Thecoloursof ornithochorousfruitsaremostlikelytheresultofaco-adaptiveresponsetobirds’sensory preferences.Theirfunctionistoprovideaconspicuous,reliablesignalthatindicatesasafe, nutritiousreward.Takingintoaccountallgeneralavianstrengthsandlimitations,except thoseofground-dwellingflightlessspecialistssuchasratites(ostriches,emus,rheasand cassowaries),apredictablepatterncanbeformulated,termedthevolantbirddispersal syndrome.Whenripe,bird-dispersedfruitsaretypicallysmallandhaveanattractive,brightly colouredbutinodorousediblepartenclosingbitterorpoisonousseedsthatareprotected byhardseedcoats(berries)orendocarps(drupes).Hardouterrindsareabsentandthefruits remainattachedtotheplantuntiltheyareharvested.Naturally,notallcharactersofthe syndromearenecessarilyexpressedatthesametime.

Meetingthesensorycapabilitiesoftheirdispersers,themostobvioussignalsentoutby bird-dispersedfruitsiscolour.Themajorityofornithochorousfruitsareredorblack,less frequentlyyellow,orange,blue,whiteorgreen;ortheydisplayamixedpatternthat combinesseveralofthesecolours.Althoughithasoftenbeenassumedthatredisthecolour thatbirdscandistinguishbestagainstabackgroundofgreenleaves,thereislittleevidence tosupportthistheory.Moreover,thevisualsensitivityofbirdsextendsintoultraviolet

Ramphastostoco (Ramphastidae)–tocotoucan;nativeto tropicalSouthAmerica–thetocotoucanisthelargest memberofthetoucanfamily. Ramphastostoco andother toucanspeciesliveprimarilyonfruitswhichiswhytheyplay suchanimportantroleasseeddispersersinthetropicalparts ofCentralandSouthAmerica

fruit.Anyharvestedfruitisusuallytakentoaroostoranothersafeplacenearbybeforebeing eaten.Mostofthetime,theysuckoutthejuicefromthepulpanddiscardtheremnants, includingtheseeds.Consequently,theaveragedispersaldistanceisonlyafewhundred metres,despitethefactthatsomespeciesofflyingfoxesareknowntovisitfeedinggrounds upto40kmawayfromtheirroostingsites.Onlyverysmallseedssuchasthoseoffigs,which areswallowedwiththepulp,haveanychanceofbeingtransportedformanykilometres beforebeingdepositedwiththefaeces.

WithinthezoologicalorderChiroptera(bats),frugivoryhasevolvedindependently amongOldandNewWorldbats.TheOldWorldfruitbatsallbelongtothePteropodidae, theonlyfamilyinthesuperorderMacrochiroptera(=largebats),sonamedbecauseitboasts thelargestbatsintheworld.Althoughthesmallestmembersofthefamilymeasureonly67cmfromheadtotail,flyingfoxes(Pteropus spp.)canbeaslongas40cmwithawingspanof 1.7m.ThePteropodidaearewidelydistributedthroughoutthetropicalandsubtropical regionsofAfrica,AsiaandAustralia,andincludemorethan160species.Theirfrugivorous counterpartsintheNewWorldaregenerallysmallerandbelongtothefamily Phyllostomatidae(Americanleaf-nosedbats)intheorderMicrochiroptera(=smallbats). ContrarytoOldWorldfruitbats,whichhaverelativelysimpleears,NewWorldfruitbatsuse sophisticatedecholocationfortheirnavigation.Withjustoneexception,thePteropodidae lacktheabilityforecholocationandrelyonvisiontoavoidobstacles,andtheirsenseofsmell tolocatefruit.Thetwogroupsalsodifferslightlyintheirdietarypreferences.WhereasOld Worldfruitbatsliveentirelyonnectarandfruits,theirNewWorldcousinsarelessstrongly co-adaptedtofruitsandgetalargeamountoftheirproteinfrominsects.Despitethese differences,thepostulatedbatdispersalsyndromeappliestobothgroupsoffrugivorousbats. Fruitsadaptedtobatdispersal(chiropterochory)havemanytraitsofthegeneralmammaldispersalsyndrome.Astale,sour,evenrancidodourreminiscentoffermentingfruitis specificallybat-related;thehintofbutyricacidinthefruitsoftheMediterraneancarobtree (Ceratoniasiliqua,Fabaceae)isagoodexample.Thefondnessofbatsforthiskindofodour isprobablyinspiredbytheanimals’ownsmell.Thisisnotmeanttoimplythatallbatdispersedfruitsstink.Thereareplentyoffragrantexamples,includingtheMalabarplumor roseapple(Syzygiumjambos,Myrtaceae).Thispopularfruittreefromsouth-eastAsiais plantedasanornamentalthroughoutthetropics,whereitsometimesbecomesinvasive.Its small,paleyellow,pear-shapedfruitshaveapleasanttastereminiscentofwatermelon,and afinearomaofrosewater,henceitsSanskritname“jambu”(rose-appletree).Otherfruits popularwithbatswithapleasantthoughfaintperfumearefigs(Ficuscarica,Moraceae),dates (Phoenixdactylifera,Arecaceae)andcashewapples(Anacardiumoccidentale,Anacardiaceae). Pteropusualanus (Pteropodidae)–flyingfox,feedingon thefruitofascrewpine(Pandanus sp.,Pandanaceae);photographedonKosraeIsland,Micronesia–membersofthe genus Pteropus,commonlyknownasflyingfoxesorfruit bats,arethelargestbatsintheworld.Afterbirds,fruitbats arethemostimportantconsumersanddispersersoffruitsin thetropics

Strelitziaceae

Fabaceae

Meliaceae

Myrtaceae

Arecaceae

Fabaceae

Taxaceae

Combretaceae

Malvaceae

Fabaceae

Apiaceae

Araliaceae

Zygophyllaceae

Malpighiaceae

Ericaceae

Valerianaceae Violaceae Santalaceae Vitaceae

Welwitschiaceae Araceae Asteraceae Poaceae Zosteraceae

Strelitziareginae Aiton

Sutherlandiafrutescens (L.)R.Br.

Swieteniamahagoni (L.)Jacq.

Syzygiumjambos (L.)Alston

Tahinaspectabilis J.Dransf.&Rakotoarinivo

Tamarindusindica L. Taxusbaccata L. Terminaliacatappa L. Theobromacacao L. Tipuanatipu (Benth.)Kuntze

L. Valerianellacoronata (L.)DC.

Violasororia Willd.

Viscumalbum L. Vitislabrusca L.‘Isabella”

Welwitschiamirabilis Hook.f.

Wolffiacolumbiana H.Karst.

Xanthismatexanum DC.

FOOTNOTES

bird-of-paradiseflower balloonpea

Cubanmahogany,WestIndianmahogany roseapple nocommonname tamarind,Indiandate Englishyew

Indianalmond,Malabaralmond,tropicalalmond,seaalmond cacao tiputree

Mediterraneanhartwort,Romanpimpernel creepingcarrot puncturevine,caltrop,devil’sthorn helicopterfruit blueberry,Americanblueberry,highbushblueberry nocommonname commonblueviolet commonmistletoe,Europeanmistletoe Isabellagrape treetumbo,tumboa Columbianwatermeal Texassleepy-daisy maize eelgrass,grasswrack,ulvamarina

1 Inascientificcontext,theusageoftheterms“primitive”and“advanced”requiressomeexplanationinordertoavoid confusion.Referringtocertainplantsas“advanced”suggeststhattheypossesssome“improvements”incomparisonto “primitive”plants.However,bydefinition,extantplantsareequallyevolvedbecausetheyhaveallbeenaroundforthesame lengthoftimesincelifebeganandtheyareallwelladaptedtotheirspecificenvironments.Amoderngymnospermisnot lessevolvedthananangiosperm.Gymnospermsaremore“primitive”thanangiospermsonlyinthesensethattheyaremore similartotheextinctancestralformsfromwhichtheyevolved.

2 Analternativetheorypostulatesthattheprimitivecarpelwasnotconduplicative(i.e.formedthroughthefoldingofa megasporophyll)butascidiate(i.e.formedfrominceptionasacylindricaloutgrowth).Althoughformerly,theconduplicative carpelwasconsideredthemostbasictypeofcarpel,thebasal-mostangiosperms(Amborellaceae,Nymphaealesand Austrobaileyales)havebeenfoundtopredominantlypossessascidiatecarpelswhichiswhythistypeofcarpelformationis currentlywidelyconsideredthemostprimitivestateofcarpelevolutionintheangiosperms.Nevertheless,conduplicative carpelsarefoundinmanyangiosperms(e.g.Magnoliales)andprovideavalidmodeltoillustrateoneofthepossiblepathways ofcarpelevolution.Theconduplicativeandascidiatetypeofcarpeldevelopmentaresodifferentfromeachotherthatthe questionastohowtheyarelinkedevolutionarilyisstillunanswered.

3 Anevenmoresignificantadvantageangiospermshaveovergymnospermshastodowiththewayinwhichtheyproduce theirseeds.Whereasangiospermsputtheirenergyintotheformationoftheexpensive,energy-richseedstoragetissue (endosperm)onlyaftersuccessfulfertilizationoftheovule,gymnospermssuchasginkgos,cycadsandconifersproducetheir storagetissue(themassivemegagametophyte)inadvance,beforetheeggcellisevenfertilized.Intheraceofevolution conservationofresourcesisalwaysagreatadvantage.

4 Inmanybasalangiospermsthecarpelisclosedonlybymucilage,notbyfusionofthecarpeledges.

5 Readerswhowouldliketoknowmoreintimatedetailsabouttheintriguingsexlifeoftheangiospermsarereferredto Seeds–TimeCapsulesofLife.

6 GwilymLewis,personalobservation.

PICTURECREDITS

Page23:©MikeBailey&SteveWilliams;page28&29:AndrewMcRobb©RBGKew;page36:©Vidar.a;page38:©JamesWood,Hobart, Tasmania;page52:HanneloreMorales©RBGKew;page53:©MikeBailey&SteveWilliams;page74:©SuzanaProfeta;page78(bottom): ©GwilymLewis;page94(top):©MikeBailey&SteveWilliams;page95:LegumesectionatHerbarium©RBGKew;page108:©Mike Bailey&SteveWilliams;page116(bottom)&117:EllyVaes-shotonlocationatFairchildTropicalBotanicGarden,courtesyFairchildTropical BotanicGarden;page122:©TimWaters,www.flickr.com/photos/tim-waters;page123(top):©AlexV.Popovkin;page123(bottom):© DineshValke;page142:NHPA/RichKirchner;page146(top):©StephenLyle,BBCBristol;page176(top):NHPA/A.N.T.PhotoLibrary; page176(bottom):CrownCopyright:DepartmentofConservation/TePapaAtawhaipage;page192:RachaelDavies©RBGKew;page195: ©MikeBailey&SteveWilliams;page196&197:PaulLittle©RBGKew;page198(bottom):©KoladeNurse;page203:NHPA/Haroldo PaloJr.;page214:©VeronicaOlivotto;page215:©TrevorJames;page216:©GwilymLewis;page219:Getty/TimLaman;page220:NHPA /KevinSchafer;page229:©KimWolhuter,www.wildcast.net;page231:©NigelDennis/AfricaImagery;page233:©LucyCommander; page233:©FilipedeOliveira;page235:©TheNaturalHistoryMuseum,London;page239(top):©PhillipMerritt;(bottom):Andrew McRobb©RBGKew;page246: Dromornisstirtoni,firstpublishedinPeterF.Murrey&PatriciaVickers-Rich(2004), MagnificentMihirungs IndianaUniversityPress;page248:©JamiliNais

Wegratefullyacknowledgethegrantingofpermissiontousetheseimages.Everypossibleattempthasbeenmadetoidentifyandcontact copyrightholders.Anyerrorsoromissionsareinadvertentandwillbecorrectedinsubsequenteditions.

SouthAfrica SouthAfrica tropicalAmerica south-eastAsia endemictoMadagascar cultigen,probableorigintropicalAfrica Europe,Mediterranean widelygrownthroughoutthetropicsasanornamentaltree;probableoriginIndomalesia domesticatedalreadyinpre-Columbiantimes,originallyfromtheAmazonrainforest SouthAmerica(Brazil,Bolivia,Argentina)

EuropetowesternAsia Australia nativetotheOldWorld nativetoKenya,Tanzania easternNorthAmerica centralandsouthernEurope,NorthAfrica,south-westandcentralAsia easternNorthAmerica Eurasia cultivar,locallynaturalizedinEurope desertofSouth-WestAfrica(Angola,Namibia) NorthandSouthAmerica south-easternUSA(Texas,Oklahoma,NewMexico) originCentralAmerica,widelycultivated Europe

ACKNOWLEDGMENTS

Manypeoplehaveinmanyways,eitherdirectlyorindirectly,contributedtotheamazingwealthofmaterial,knowledgeandideasthat providedthematerialforthisbook.Althoughitisimpossibletomentionallthescientistswhosepainstakingobservationsandpublications overdecadeshaverevealedsomanyfascinatingfactsaboutfruits,andthepeoplewhodiscovered,collectedorgrewthefruitsshownhere,we wouldliketogiveaspecialmentiontothefollowing.

Wethankourpublisher,AndreasPapadakis,forthesupportandfreedomhehasgivenusthroughoutthepreparationofthisbookandhis daughterAlexandraforusingheroutstandingtasteandartisticskillstocreatethebeautifuldesignthatprovidessuchaspectacularbackground forbothtextandimages.WearedeeplyindebtedtoRichardBateman,PaulaRudallandRichardSpjutfortheirverythoroughreviewsof themanuscriptandtoSheiladeValléeforeditingthetext.

WewishtothankKenArnold,HeadofPublicProgrammes,WellcomeTrust,forhisperceptiveprefaceandProfessorStephenD.Hopper, DirectoroftheRoyalBotanicGardens,Kew,forhisencouragementandhelpfulcommentsonthemanuscript,andforacceptingour invitationtowritetheforeword.

WearegratefultoPaulSmith,HeadoftheSeedConservationDepartment(SCD),andJohnDickie,HeadofInformationSection(SCD), forallocatingresourcesoftheMillenniumSeedBankProjecttowardsthepreparationofthisbook.TheMillenniumSeedBankProjectis fundedbytheU.K.MillenniumCommissionandtheWellcomeTrust.TheRoyalBotanicGardens,Kewreceivesanannualgrantinaidfrom theU.K.DepartmentofEnvironment,FoodandRuralAffairs.

WethankthestaffoftheRoyalBotanicGardens,Kew&WakehurstPlace,particularlytheMicromorphologySection,allmembersofthe SeedConservationDepartmentandthemanypartnersoftheMillenniumSeedBankProjectallovertheworldwhohavecontributedtothe outstandingcollectionthatprovideduswithmanyextraordinaryandunusualexamplesoffruits.Weespeciallyacknowledgetheuseof materialcollectedinthefollowingpartnercountriesoftheMillenniumSeedBankProject(MSBP):Australia,BurkinaFaso,Kenya,Lebanon, Mali,Mexico,Madagascar,SouthAfrica,UkraineandtheUnitedStates.AttheKewHerbariumwewouldliketothankthemembersofthe LegumeSection,PalmSection,MalpighialesSectionandtheSouth-EastAsianRegionalTeamforgrantingusaccesstotheircollectionsand theMicromorphologySectionoftheJodrellLaboratory,especiallyPaulaRudallandChrissiePrychid,forgrantingusaccesstotheirScanning ElectronMicroscopeandfortechnicalsupport.AttheSCD,wearegratefulforthekindsupportofthemembersoftheCurationSection, andespeciallyJanetTerry,whowasinstrumentalinsourcingmaterial.

Furthermore,webothwishtothankcolleaguesandfriendsatKewwhokindlysupportedusinmanydifferentwaysbyofferingtheir expertise,technicalsupportandtimetohelpusanswerdifficultquestions,byprovidinguswithhelpfulcommentsandideasconcerningthe manuscript,bygivingusaccesstoimportantmaterialandsupportinguswithphotographs,inparticular,atthe SCD:JohnAdams,Matthew Daws,IlseKranner,HanneloreMorales,EmmaYork.Atthe Herbarium,WSwouldliketoextendspecialthankstoGwilymLewisfromthe LegumeSection,whonevertiredofansweringquestionsandkindlyallowedustodrawonhisslidecollectionofFabaceae.Alsoatthe Herbarium ourthanksto:BillBaker,GillChallen,MartinCheek,TomCope,AaronDavis,JohnDransfield,DavidGoyder,YvetteHarvey, PetraHoffmann,TerryPennington,BrianSchrire,DavidSimpson,TimUtteridge,SueZmarzty.AnneGriffinfromtheKew Library deserves averyspecialthankyouforthespeedwithwhichshetrackeddownthemanybooksandscientificpapersneededforourresearch.Alsoat theLibrary,ourthankstoJuliaBuckleyandAnneMarshall.At HPE:DavidCooke,LauraGiuffrida,MikeMarsh,WesleyShaw.AlsoatKew: AndrewMcRobbandPaulLittle(MediaResources),MarkNesbitt(CentreforEconomicBotany),IanParkinson(WakehurstPlace). AttheNaturalHistoryMuseum,London,wethankChristopherLyalforhelpwiththeidentificationoftheMalagasysnoutbeetle. OutsidetheUnitedKingdomwethankRetoNyffeler,InstitutfürSystematischeBotanikundBotanischerGartenderUniversitätZürich, Switzerland,forprovidinguswithmaterialof Wolffiacolumbiana andJean-YvesRasplus,INRA–CentredeBiologieetdeGestiondes Populations,Montferrier-sur-Lez,France,forprovidinguswithspecimensof Blastophagapsenes.ForassistanceinthefieldWSwouldliketo thankSarahAshmore,PhillipBoyle,RichardJohnstone,AndrewCrawford,AndrewOrme,AndrewPritchardandTonyTyson-Donnellyin Australia;andIsmaelCalzadaandUlisesGuzmánin Mexico

In SouthAfrica,WSwouldliketothankErnstvanJaarsveldandAnthonyHitchcock(KirstenboschBotanicalGarden,CapeTown),and JohanHurter(LowveldNationalBotanicalGarden,Nelspruit)fortheirtime,hospitality,andpermissiontophotographplantsintheir collections;in Australia,thestaffofKingsParkandBotanicGarden,Perth;GeelongBotanicGardens;BrisbaneBotanicGardensatMtCoottha;theRoyalBotanicGardens,Melbourne;theRoyalBotanicGardens,Sydney;andMountAnnanBotanicGarden,NewSouthWalesfor theirhospitalityandpermissiontophotographplantsintheircollections.In NewZealand WSwouldliketothankhisfriendandcolleague TrevorJamesforhishospitalityandcompanyinthefieldwhilevisitinghiscountryandforphotographingthefruitsofthetitokitree (Alectryonexcelsus,Sapindaceae)specificallyforthisbook.AlsoinNewZealand,thankstoJaneMarshallandPhilKnightbridge(Department ofConservation,Hokitika)forsharingtheirideasondispersalecology.

OthercolleaguesandfriendswhokindlysupporteduswithimagesincludeLucyCommander(Perth,Australia),PhilKnightbridge,Stephen Lyle(BBCNaturalHistoryUnit,Bristol),AndrewMcRobb(Kew),FilipedeOliveira(UK),EllyVaes(Hawai'i)andJamesWood(Hobart, Tasmania).WeareparticularlygratefultoPeterTrusler(Australia)forpermissiontoreproducehiswonderfulpaintingof Dromornis AtCentralSaintMartinsCollegeofArt&DesignwethankJaneRapleyOBE(HeadofCollege),JonathanBarratt(DeanofGraphicand IndustrialDesign),KathrynHearn(CourseDirector,CeramicDesign).

AtPapadakis,ourthankstoHayleyWilliamsforherpainstakingworkontheproductionofthisbook,andtoMikeBaileyandSteveWilliams fortheirphotographsthatwerespeciallyforthisbook.

Asalwayslookingaftertherestofmylife,AgalisManessi.RK

Finally,mywarmestthankstomywife,EmmaLochner-Stuppy,forherloveandsupport,alwayspatient,alwaysencouraging,never complaining,despiteherhusband'syear-longmentalandphysicalabsencewhileworkingonthisbook.WS