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  1. 1. Dipterocarp Biology as a Window to the Understanding of Tropical Forest StructureAuthor(s): Peter S. AshtonReviewed work(s):Source: Annual Review of Ecology and Systematics, Vol. 19 (1988), pp. 347-370Published by: Annual ReviewsStable URL: http://www.jstor.org/stable/2097158 .Accessed: 16/03/2012 09:49Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .http://www.jstor.org/page/info/about/policies/terms.jspJSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range ofcontent in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new formsof scholarship. For more information about JSTOR, please contact support@jstor.org. Annual Reviews is collaborating with JSTOR to digitize, preserve and extend access to Annual Review of Ecology and Systematics.http://www.jstor.org
  2. 2. Ann. Rev. Ecol. Syst. 1988. 19:347-70Copyright ? 1987 by Annual Reviews Inc. All rights reservedDIPTEROCARPBIOLOGY AS AWINDOW TO THEUNDERSTANDING OF TROPICALFOREST STRUCTUREPeter S. AshtonProfessorof Dendrology, Departmentof Organismicand EvolutionaryBiology, Har-vard University Cambridge, Massachusetts02138INTRODUCTIONMy aim is to show, by one example, why systematics must provide afoundation equal to that of ecology if the structureof tropical forests, andparticularlytheir floristic structureand often extraordinary species richness, isto be understood.Species composition accounts for much of the geographicalvariationin structure thatoccurs among forests in differentregions sharingthesame habitat. Our knowledge of rain forest structurehas advanced from thedescriptionof whole plant communities, or often their tree component alone,to a contemporaryinterest in the demographyand genetics of species pop-ulations, and to the physiological ecology of individuals. Always, though,systematic as well as ecological relationships must be understood if thisknowledge is to contribute to understandingof the structureof the wholeforest. The biological attributes shared among the individuals of species, andwhich decide their success in interspecific competition, determine both theecological guild to which they belong and, in part, their systematic rela-tionships. Systematics aims to classify species into a hierarchyof categoriesof increasing rank. The hierarchy is aimed to reflect evolutionary rela-tionships, and it thereby provides inferential evidence for the origin of themajor species groups constituting tropical rain forest communities. I arguethat an understandingof the floristic structureof tropical forests, and more 347 00664162/88/1 120-0347$02.00
  3. 3. 348 ASHTONspecifically of the way species invade and survive in mixture in these com-munities, of the way the communities vary in species composition and ofwhy, in particular,these forests vary in species richness-all these can beachieved only by understanding how the hierarchiesof systematicand ecolog-ical relationshipsare intermeshed. My vehicle for analysis is the Dipterocarpoideae,the species-rich Asiansubfamily of a pantropical family that, because its trees dominate bothinternationalhardwoodmarketsand also the emergent canopy of most low-land rain forests in Asia, has been the subject of more-and a broaderrangeof-research than any otherrain forest taxon of comparablesize. It will soonbecome obvious though that dipterocarpsare unique in many importantecological and systematicrespects, and it is only partiallypossible to general-ize from them. This underlineshow important is to apply the same approach itto other groups. This review is structuredby systematic categories, startingwith the sub-family itself and terminatingwith a more elaboratediscussion of the species.It serves to show how fragmentary knowledge still is and where research ourmust now be directed.The DipterocarpoideaeAshton (10) has elsewhere reviewed the systematic and ecological literatureon the group. Dipterocarpsare trees; their simple penninervedleaves havearticulatedstalks. Their bisexual and star-shapednodding flowers have five-merous perianthsin which the sepals and petals, respectively, overlap. Thesepals enlarge and become winglike in fruit. Petals and fruit sepals aregenerally twisted. The single ovary has three cells, each of which generallycontains two ovules; it generallyripens a single seed in a dry indehiscentnut.The pollen grains are ellipsoid, slightly sticky, with smooth thin walls.Dipterocarpsare insect pollinated. Fruit dispersal, if it occurs at all, is bywind or more often by gyrationalone. Rats commonly scatter-hoard nuts thebut are thought not to carry them far (L. Curran,personal communication).Asian dipterocarpsare distinguishedfrom others by their resin canals, whichare abundantin many tissues, and by details of wood anatomy, pollen, andstamens. Two tribes are recognized, and these differ in details of the fruitcalyx and wood anatomy, and in basic chromosomenumber;any ecologicalimplications of these differences are unknown. Though there are only 12 dipterocarpgenera in Asia, some 470 specieswith at least 100 infraspecific entities are recognized. This makes themparticularlysuited for this review. Thoughspecies diversityis now centeredinBorneo and surroundingregions, systematic analysis suggests that the sub-family originally invaded Asia by way of the Indian fragmentof Gondwana(10). Total species diversity is markedlyinfluenced by historical biogeogra-
  4. 4. DIPTEROCARPBIOLOGY 349phy, there being only 26 species east of Wallaces line, and 287 in Borneo asagainst 7 in Sulawesi, which is only 80 km east of it at the same equatoriallatitude. The absence of a towering emergentcanopy dominatedby dipterocarpsinNew Guinea gives the structureof lowland forests there an aspect quitedifferentfrom those of Asia, and similarin many respectsto that of neotropi-cal forests. Many other families fill the gap and are more abundantin thecanopy there, though tall emergentsare either more scatteredthan in diptero-carp forests or absent. The southwest of Sri Lanka, in an area some 180 kmsquare, possesses 45-55 dipterocarpspecies, all but one endemic. The re-latively low numberin this case must have an island biogeographicexplana-tion (17). These regional differences in species diversity indicate majordifferences in forest floristic structure.It is clear from the start, then, thathistoric accident has been a major influence on the role of dipterocarpsinAsian forests. Dipterocarpsare exclusively components of the forest maturephase, onlygradually invading successional forests after a closed canopy is fully es-tablished. Most are confined to wet climates, with a dry season not exceedingfour months. All but a handful are evergreen. Dipterocarpspecies (but notindividuals) are dramaticallymore abundantin aseasonal than seasonal cli-mates. Thus, of the 155 occurringin peninsularMalaysia, only 27 occur alsoin seasonal Indo-Burma,whose total dipterocarp flora is only 58 species (53).In the Far East, the majorityare confined to the lowlands, with a few speciesendemic to higher altitudes. Curiously, this is not so in Sri Lanka, where amajority of the large endemic genus Stemonoporus occur in hill or sub-mountaneforest, and the family is best representedin moist premontane[inthe sense of Holdridge (37)] forests at 500-800 m (8). The overall speciesrichness of forest tree communitiesseems to reach a maximumat this altitudein Sri Lanka(33), althoughelsewhere in the Asian tropics the maxima are inthe lowlands. This could reflect periodsof aridityin the geological past, whenthe South Asian mixed rain forests might have been restrictedto an areaimmediatelybeneathand within the cloud belt on the mountainslopes, as theyare today in central peninsularIndia. In seasonal climates, dipterocarpsare confined to relatively infertile soils.Thus, in IndiaShorea robusta forests are concentratedon graniteand schists,and are replaced by deciduous teak forest on basalts and other calcareousrocks. In Indo-Burmathe Dry Dipterocarpforests are confined to podsolicsands and laterites, and mixed deciduous forests replace them on mesic sites(23). In the aseasonalhumidtropicsof the FarEast, abundanceof reproductively PeninsularIndia and the island of Ceylon (Sri Lanka)
  5. 5. 350 ASHTONmaturedipterocarpsis greateston yellow and red lowland soils (5). Not onlyis the family as a whole generally dominantin the emergent stratum,therecomprising 80-100% of all individualson yellow-red soils (e.g. 21, 5), butsingle species dominancemay be approachedboth on highly fertile (10, 15)and highly infertilesites (1, 58). Dipterocarpspecies populationsare general-ly aggregatedinto loose clusters of reproductiveindividuals, with juvenilesconcentratedaroundthem (6). The ecological characteristics the majortree families of Far Easternrain offorests differ to a greateror lesser extent. Species richnessin Myrtaceaevariesin ways similarto Dipterocarpaceae relative to soil for instance, but there arefew emergent species and clustering is less evident. Myrtaceae seeds aremostly animal dispersed. Meliaceae and, to a lesser extent, Rubiaceae andEuphorbiaceae broadlyincreasein species richness with increasingsoil nutri-ent status (5). Dipterocarp ecology, however, remarkablyrecalls that ofFagaceae. Fagaceaereachtheirlimits of species diversityin the submontaneforests ofeastern Himalaya, Indo-Burma,southernChina and western Malesia.2 Theyare represented,thoughmore poorly in species and abundance,in the lowlandforests of the Far East. Like dipterocarps, few Fagaceae appear east ofWallaces line. Fagaceae are absent from peninsularIndia and Sri Lanka,presumablyfor historicalbiogeographicalreasons. The altitudinal distributionof the two families is suggestive of interfamilialcompetitive exclusion. Asian Dipterocarpaceae and Fagaceae are both unusual among rain foresttree families in being apparentlyobligately ectotrophicmycorrhizal(52; 54,55). Trees of both families possess abundantmats of superficial fine roots.These are best developed on less fertile soils. Smits (55) has evidence thatmany basidiomycete mycorrhizalspecies are symbiotic with dipterocarps. Dipterocarps,like many othertropicaltrees (19), experiencehigh mortalitybetween anthesis and fruit set. Mortalityis extended throughoutthis period.Many fruit with fully extended winglike sepals apparentlyripen, but thecarpels of most are empty. Dipterocarps (including saplings) flush in-termittentlyonce or twice a year. In most species inflorescences are bothterminaland axillary, andthey arise from the same positions from which leafyshoots would otherwise originate. Ashton (12) has therefore suggested thatthe retentionof sterile fruits until full sepal extension may serve to increasephotosyntheticarea at a time when energy demandis high but when the treelacks its usual leaf complement. It would be interestingto observe whetherfruit survivorshipis the same among species with winglike fruit sepals asamong those many species in which all the sepals remain short. Whetherdipterocarp sepals function in the way suggested or not, it seems that the and west of SulawesiandBali. 2Malaysia, Philippines Indonesia
  6. 6. BIOLOGY DIPTEROCARP 351reproductionimposes severe stress on the trees. Primack& Chai (47) showedthat dipterocarpsexperience dramaticarrestment growth in fruitingyears. of Dipterocarpsand tropicalFagaceae also sharereproductivecharacteristics.Both have poorly dispersed, one-seeded fruits. Both have seeds of high fatcontent, lacking dormancy but nevertheless scatter-hoarded rodents. In byboth, the seeds are chemically defended by phenolic compounds and areenclosed in a woody pericarp,though the dipterocarp pericarpis also richlyfurnishedwith resin-canals.In both, the seeds are predatedby beetles beforematurationand by vertebratesafterwards.Both are notorious for mast fruit-ing, though this does not seem to occur in the same years in the two families.This lack of fruiting synchrony between the families appears largely toexplain the celebratedmigrationsof hordes of wild boars (Sus barbatus) inBorneo, and formerlypresumablyelsewhere in WesternMalesia (22). Janzen(40) suggested that mast fruitingof the whole family is an adaptation avoid topredation, among poorly defended seeds, by means of predator satiation.Ashton et al (13) have provided furtherstrong inferentialevidence for thishypothesis. Dipterocarpsflower annuallyin the seasonal, and at intervalsofabout five years in the aseasonal, tropics. They found a correlationbetweendipterocarpflowering years and El Ninloclimatic events, during which pro-longed depression of minimum night temperature correlatedwith onset of isinflorescence development. Unusually heavy fruiting occurs at similar in-tervals in the seasonal tropicsalso, and intensityof seed predationis very highthere except in these years. Ashton et al (13), elaboratingon Janzen (40),nevertheless suggest that the seed predatorsatiationachieved by intensifica-tion of the mast fruiting event is occasioned in the aseasonal tropics by theabsence of an annual climatic cue to flowering. This may partially explainhow the Dipterocarps, as putative invaders, have become so successfulthere. The period between germinationand establishmentis critical for diptero-carps. The invasion of mycorrhiza has never been studied. Ashton (10)speculatedthatthe rarityof fruitingamong tropicalforest basidiomycetesmaybe associated with poor spore dispersal and low spore dormancy in thewindless moist and equable rain forest understory.If this is so, and fungalhost specificity is variablebut high in some cases (e.g., see 36), fungal spreadmay be principally through the soil, and this could partially explain whydipterocarpsare clustered in forests at both species, genus, and also familylevel (Figure 1; see also 6, 10). Dipterocarp seedlings once established are generally able to survive in shade, and many persist in the absence of canopy gaps between mast fruitingyears (28). This capacity appears to be limited by water stress (20). In seasonal evergreen dipterocarpforests, few seedlings of dipterocarpsor ofother mature-phasetree species survive beyond a year on this account (see
  7. 7. 352 ASHTON I.-A,A h 6 6 6 6 d . .9 .9 z .9, O o ICICx 0 0 0 0 0 x x x x ai d 13 LU Oco" 0 O O IC I.- 0 Lxu a (L iz .. 0 0 0 IC Lu J, & x I.- Z O (L >- LU L0 .. 9 - . . " : . . izo 0.13 lP: Q)LU ui ui ui ui ui ui 0-ix(.) IC IC IC IC IC ICui 0 0 0 0 0 0(L x x x x x x 0 0 :0 OL 0 00 (DO 0 0 D. ri ,C 13 Cld u Cld cld 4-4 e4) 1-4Cld O 0 C-n Cd 4-4 0 0
  8. 8. DIPTEROCARPBIOLOGY 353references in Ashton-12). This indicates a fundamentaldifference in thedynamics of rain forests under seasonal and aseasonal climates. In theaseasonal rain forest, gap regenerationis dominatedby establishedregenera-tion except where the soil is disturbed,whereas pioneers play a more promi-nent role in seasonal forests. There, dipterocarpsestablish through laterinvasion, following a mast year and the establishmentof a pioneer canopy. Predationon Dipterocarpseedlings is surprisinglylow in comparisonwiththat on the seeds, though fungal pathogens may be an importantsource ofmortality(20). Low seedling and saplingpredationmay be associatedwith thepresence, possibly ubiquitous, of sugar-secretingglands on the upper, andsometimes lower, leaf surface and stipules (29). These may attractants thatmay defend the seedling againstpredators,thoughthis has not been observed. With the exception of Dry Dipterocarpforest species, dipterocarp trees areremarkablefor their poor capacity for reiteration(12, 35), a charactersharedby many gymnosperms. As seedlings, they have high capacity for shootreiteration, often through formation of accessory buds (45). By maturity,however, the capacityto form new branchesby reiteration becomes limited orlost. Also, whereas seedlings and saplings respond to increased light withincreasedgrowth, this capacity apparentlydeclines as the plant matures(48).Thus, the need for self-repairapparentlydeclines as maturityis approached,and selection may thus decline and even cease once the tree reaches fullheight. Some evidence (e.g. 46) suggests that dipterocarpsare not uniqueamong trees of the maturephase in these respects, which, in view of their ofimplicationsfor understanding floristic and dynamicstructure the forest theand the relationshipbetween ontogenesis and changing selection pressures,merit more study. In summary, Dipterocarpoideaeare seen to be as ecologically distinct agroup in Asian tropicallowland evergreenforests as they are systematically.Their usually dominantpresence distinguishesthese forests from those else-where. Their success as a family there is apparentlydue to their ability tomaintainabundantseedling populationsthrough satiation of seed predators,possibly through offering rewards to predatorsof seedling herbivores, andthrough their ability to enhance nutritionon leached infertile soils by sym-biosis with ectotrophic mycorrhizae. Dipterocarpsappearto trade abundantphotosynthatefrom theiroften emergentcrowns for cheap defense and superi-or nutrient acquisition in a limiting environment. Analysis of the cladisticrelationshipsof Dipterocarpaceae with other families has not been attemptedbut would be valuable. Ashton (10) argues for including them in Malvales.Thoughmany Malvales are emergentforest trees with the same architecture asemergent dipterocarptaxa (which is unusual and perhaps unique; this isdiscussed below), none share the family dominance and gregarioushabits ofdipterocarpoids.None have seed and seed dispersal characteristicsof dip-
  9. 9. 354 ASHTONterocarpoids, though some have small winged seeds. Some, such as manyDurio (Bombacaceae), may fruit supraannually the wild, but fecundity is inlow in these large-seededtrees. Rather, it is the Fagaceae, a quite unrelatedfamily within the angiospermsand one with a quite separatebiogeographichistory (49, 43, 10), with which dipterocarpoidshave most in commonecologically and with whom, it seems, they survive at a familial level throughcompetitive exclusion. Here, then, is evidence that taxa of familial rankmaymanifest niche specificity within the teaming forests of the humid tropics.Genera and SectionsThough only 13 genera exist among Dipterocarpoideae,the large generaShorea andHopea are divisible into 14 sections and4 subsections,respective-ly, and Anisoptera is divisible into 2. These sections approachthe status ofgenera on structuralgrounds in some cases, but others distinguishedon thesame set of character-statesare less distinct. This is the reason for theirinfrageneric status (4). All these taxa represent natural groups within thefamily. Each containsan averageof 16 species, thoughthereis much variabil-ity in size, and 5 are monotypic. These entities, which for simplicity I shall term quasigenera, possessdistinct geographical distributions. In some, such as Vateria, Vateriopsis,Stemonoporusand Shorea section Doona, which are endemic to southernIndia and some Indian ocean islands, their distributionmay be explained byhistoricalbiogeographyalone. The ranges of one section (and of anotherbutfor three species) of Hopea, of Cotylelobium,and of Shorea sections Riche-tioides, Ovales, BrachypteraeandMutica co-terminateat the sharpboundarybetween aseasonal and seasonal climates at the Isthmus of Kra in southernpeninsular Thailand (See 58). All are confined everywhere to aseasonalclimates. Upuna and threefurthersections of Shorea are confined to aseason-al regions in the Far East west of Wallaces line. In all, this concentrationofquasigeneragreatly enhances dipterocarpspecies richness in this zone. Thereasons for these coincident distributionswithin a continental area must beecological but remain entirely unknown. Quasigeneradiffer consistently in one or more characters,including woodand often bark anatomy, leaf venation, and in certainaspects of morphologyfor which there are not obvious adaptiveexplanations.Each quasigenushas adistinct architecturalform, afterthe models of Halle & Oldeman(34, 35), andthese models in some measurepredicatethe size at maturityof its members.Thus Vatica, and apparently also Cotylelobium, early become sympodialthroughterminalflowering of the plagiotropicbranchesand orthotropiclead-er. Both nevertheless continue to extend through apposition. Both generaapparentlyconform to Kwan-Koribasmodel. Most Vatica are understoreytrees, whereas Cotylelobiumoccupies the main canopy at reproductivematu-
  10. 10. DIPTEROCARPBIOLOGY 355rity. In Stemonoporus,many species conform to the model of Troll, wherebythe leader is initially vertical with spirally arrangedleaves but eventuallybends over, apparently under its own weight, when the leaves becomedistichous. Height is furtherextended through axillary shoots, which arisefrom the upper side of the leaning or horizontalstem and these successivelyrepeat the process. Stemonoporusspecies rarely exceed 15 m in height. Most emergent dipterocarpoid quasigenerahave a distinctive growth pat-tern that appearsto be sharedby otheremergentMalvaliantrees including, inAsia, Sterculia, Pterygota (Sterculiaceae), Pentace (Tiliaceae), andDurioneae (Bombacaceae). Apical dominance is maintained in juveniles,when the leader bears spiral leaves while branches are plagiotropic withdistichous leaves. At this stage, the branches may be arrangedin pseudo-whorls correspondingwith each extension of the leader (Massartsmodel), orthey may be arrangedin an irregularspiral (Roux model). These formspermit leaf surfaces to be spread diffusely in a horizontalplane, which willmaximize capture of sunflecks, but in such a mannerthat height incrementand the mechanicalstrengthof the eventual tree are not compromised.Whenthe stem apex emerges above the canopy, the subsequentbranchesof all but afew species are orthotropic,with ascending trajectoryand spiral leaves, andthey are thus equivalent to the leader itself (33a). At that time, floweringcommences from terminalas well as axillary inflorescencesso that branchingbecomes partially sympodial. Surprisingly, neither Vatica, Stemonoporus,Vateria or Vateriopsis, (regardedas the most primitive genera in the sub-family) nor African and South American dipterocarpshave this malvaliancharacteristic. Quasigenera frequently possess distinct embryology. Shorea sectionDoona, for instance, differs consistentlyfrom others in possessing one fleshycotyledon that remains hidden in the pericarpand is a food store, and oneminute, bract-like photosynthesizing cotyledon that emerges with the plu-mule. But there is much variabilityin the morphologyof the matureembryowithin some quasigenera,particularly Vatica and Stemonoporus in (44), someof which may be adaptive at the species level and none of which has so farbeen shown to correlate with other, independent, characters of the tree.Similarly, the presence or absence of extended wing-like sepals has for longbeen given supraspecifictaxonomic recognition, but it is uncorrelatedwithvariation in independentcharacterstates and is therefore generally only ofvalue in species delimitation (4, 10). There is some, still far too limited, evidence that quasigeneramay con-sistently differ in some of the complex secondaryhydrocarbonswith whichdipterocarp exudatesare richly endowed [for referencessee Hegnauerin (10),pp. 273-74]. If correct, some herbivores and seed predatorsmay be host-specific at a quasigeneric level. Evidence for this latter has recently been
  11. 11. 356 ASHTONfound in some genera, such as Dipterocarpus, but not in most sections ofShorea (R. Toy, personalcommunication,L. Curran,in preparation).Somespecificity at this level may occur between dipterocarp species and mycorrhi-za, which may invade in response to the specific cue of chemical rootexudations (36). Both interdependencies,if they do exist, could help explainhow related quasigeneracan co-occur in rain forest communities, throughdensity-dependenteffects on the one hand (40, 27) and through resourceallocation (56, 57) on the other. Much is known of pollinationbiology and the functionalmorphologyof theflower, thanksto the work of S. Appanahand H. T. Chan (2, 3, 24-26) andC. V. S. and I. A. U. N. Gunatilleke(personalcommunication,in prepara-tion). One majorgroup of dipterocarpoid quasigenerasharesfloral charactersthat include large elongate yellow antherswith short appendages,a columnarstyle that protrudes beyond them, and white petals that open widely atanthesis. These include Dryobalanops, Vateria, Neobalanocarpus, Shoreasection Doona, Stemonoporus,Parashorea, Cotylelobium,and Vateriopsis.This is not a monophyleticgroup;the membersareequally represented both intribes of the subfamily. The flowers as well as other parts differ in other,taxonomicallyimportant,characters.The flowers in this groupare diurnalandlast one day. The first four are known to be principallyvisited by honey bees.The patternof visitation each morningis ostensibly the same in all cases (S.Appanah, personalcommunication;C. V. S. and I. A. U. N. Gunatilleke,inpreparation),with the large Apis dorsata, and smallerA. indica var. cerranavisiting first and then meloponid bees and various other insects. I have seenStemonoporusbeing visited by Trigonabees (Meliponidae),while no visitorshave been observed on flowers of the others. With the exception of CeylonquasigeneraShorea section Doona and Stemonoporus,species in these taxacontain few species. With the exception of species in section Doona, two ormore congeners rarelyco-occur in the same communitytype. These taxa alsooften flower more frequently between mast fruiting seasons than do otherdipterocarps. Dipterocarpus has large flowers whose large yellow anthers with longappendages and columnarstyle are enclosed in large pink and white petals.The pollinatorsremainunknown. All other quasigenerapossess small cream-colored anthers in flowers in which the petals, which are white, pink, oryellow, remain strongly contorted at the base, thereby concealing the an-droecium and gynoecium. These flowers differ at a quasigenericlevel in theshape of the stamens and of the connectival appendage, in the length of thestyle, and in the presence or absence of a stylopodium. Appanah & Chan (24, 26, 3) made a thorough study of six species inShorea section Mutica. One tree can produce four million flowers over twoweeks. They found thatthe flowers open at night and last less thana day. The
  12. 12. BIOLOGY DIPTEROCARP 357corollas fall with stamensattached.Thripslay theireggs between the petals inthe young bud. The juveniles feed on the petals. Up to five hundredadultthrips can thereby originate from one female over three generations, or fourthousandjuveniles over four, by which time anthesis begins. The thrips gettrapped during anthesis by the phalanx of connectival appendages, whichbend back against the corolla so that the anthers open inside a chambertherebycreated. There, the adultsfeed on pollen grains. Many escape though,carryingone or a few of the sticky grains. Many others, includingjuveniles,remain with the connate corolla and stamens, which together gyrate to theforest floor at terminationof anthesis. Juveniles can survive on the fallencorollas for up to five days, and pollen can remain viable for this period.Adults, some bearing pollen, fly up to the canopy each evening. Trees in this section are outbreeders(25). Thrips can be transportedonconvectional wind eddies, but they land directionally.No other floral visitorshave been observed during exhaustive studies in this section. Shorea sectionMutica, whose abundantindividualsproduce millions of flowers briefly andat long intervals, achieve pollinationthroughattraction a fecund short-lived ofpollinatorwhich rapidlybuilds up numbersby feeding on the buds of the treesthat they will pollinate. Thrips are almost ubiquitousin dipterocarpoid flow-ers. Among other pale antheredquasigenera,Appanah(in Ashton et al, 13) found bugs (Hemiptera:Miridae:Decomia) to visit flowers of Shorea pauci-flora (section Brachypterae)and plant hoppers (Homoptera:Cicadellidae: Varicopsella)to visit S. seminis (section, subsectionShorea). Neitherof these quasigenerais abundantly represented,by individualsor species, in individual forest community types. In particular,studies of pollination are needed in Shorea section Richetioides (which, after section Mutica, can occur in the largest co-occurring species series) and in Dipterocarpus. It does seem likely that competition for the services of pollinators is avoided at a quasigeneric level. Pollinator specialization cannot, however, provide a density controlling factor for the population of these taxa, and cannot thereby explain their co-existence let alone the co-existence of the multitudeof othergenera in the mixed rain forests. In the searchfor equilibri- um explanations for these coexistences we likely need to know more about patternsof predatorand herbivorespecificity at this taxonomic level, and the role of specific secondary metabolites.The SpeciesWith 12 genera and 470 species, Asian dipterocarpsserve as an example ofthose several families with large genera, the ecological range of whosemembers is the principal determinantof variationin the species richness oftropicalevergreenforest (15). We have seen that the species of Dipterocarp-oideae are naturally grouped into some 30 generic and infrageneric
  13. 13. 358 ASHTON taxa. Many of these species, as will be explained, are subdividedinto distinct geographicalor edaphic subspecies. Within quasigenera,habit is relatively uniform, though maximum stature can vary between and within species, according to site conditions, and in particular accordingto soil depth (e.g. 5). Stemonoporusand Vatica can vary substantiallyin habit, even among taxa closely related on the evidence of othercharacters.In Hopea several species in two, and most species in a third, of the four infrageneric groups are understorey trees. They differ from canopy members in coming into flower while still in the monopodialjuvenile habit, which they maintainthroughoutlife. Flowers in these neotenous species are borne solely on the plagiotropiclateralbranches.In Stemonoporusand Vatica the differencein habitbetween understorey canopy species is less extreme and owing to the sympodial habit of the understoreyspecies, but distichous leaf arrangements not give way to whorled in the understoreyspecies. In these do two genera neoteny can even differentiateinfraspecifictaxa. Vatica oblongi-folia Hook. f., for instance, consists of four ecotypically differentiatedsub- species, two of which first flower only after reaching the canopy while two are understorey taxa. Stemonoporus canaliculatusThw. occurs as two distinct subspecies, sometimes recognized as species; one is a canopy tree of high ridges, the other an understoreyshrub of lowland yellow podsolic soils. In Shorea too, subtle differences of habit can occur among subspecies. For example, S. macropteraDyer has one subspecies macropterifoliathat is an emergent tree while its other three subspecies do not emerge above the main forest canopy. In some quasigenera, notably Shorea section Richetioides and Vatica, a correlationbetween habit and fruit charactersoccurs (6, 10). In these and most other groups a significantminorityof species lack winglike fruit sepals. This wingless characterhas evolved many times, at least within the more advanced quasigenera, and pairs of taxa differing only in this respect are frequent. In Shorea section Richetioides most emergentspecies have winged fruit, while all main canopy species have wingless (6). This implies that winglike sepals actually reduce survivorshipin species that drop their fruit directly into the windless subcanopy. This is quite likely, as the wings can entangle fruits among the boughs as they fall. Often, wingless fruitedspecies possess largerthan averageseed size, and the largestdipterocarp seeds are all wingless. These characters,also sometimes correlatedwith distinctcharacters of the embryo (44), may be adaptive, enhancing successful regenerationin shady habitats. Wingless fruit also occur among riparian, water dispersedspecies. The overwhelmingsourceof differencesamong species, however, is in leafmorphology, principally in leaf shape, size, and number of veins, and inpresence or absence, length, and color of indumentum.Among canopy and
  14. 14. DIPTEROCARPBIOLOGY 359emergentspecies these differences become most manifestat maturity,thoughenough are possessed by the seedling for all ontogeneticstages to be generallyidentifiable. Seedlings of related taxa are, however, generally more similarthanare reproductively matureindividuals;this implies thatselection for thesecharactersmay continue up to maturityand that it may shift duringontogenyfrom mainly intra- to mainly interspecific (6). These leaf charactersmay beexpected to influence waterrelations,but comparativestudiesof the physiolo-gy of closely related species which differ in these respects are still awaited. Large-leafed species generally also possess large buds, flowers and fruit,and stout twigs. Frequently,taxa differ in leaf and twig size, and occasionallynumberof nerves, but sharedistinctiveleaf and twig shape, indumentum,andother characters in common; these are almost always allopatric and arerecognized as subspecies (10). Occasionally, as in Shorea macroptera (6)subspecies may co-occur. In this example, no morphologicallyintermediateindividualsoccur in the mixed stands, suggesting that even when distinctionsare reduced to this level of subtlety the taxa may function as biologicalspecies. A remarkablefeatureof most dipterocarp taxa, therefore, is their morpho-logical constancy. This enables clear and consistent differentiationbetweenentities that may differ only, for instance, in leaf size and twig diameter,butwhich are generally also geographically or ecologically allopatric. Notableexceptions are those few species confined to the savannawoodlands, calledDry Dipterocarpforests, of continentalAsia, and to a lesser extent also somespecies of Seasonal EvergreenDipterocarpforests. Here variation,particular-ly in the presence, distribution,and density of indumentum,is common bothwithin and between populations (10). Populations in the driest habitats aregenerally the most tomentose. In Shorea section Pachycarpa, with ten species all endemic to the con-tinental island of Borneo, populationsmorphologicallyintermediatebetweentwo species occur in at least one locality in every species, though all co-occurwith othersthroughout much of theirrangewithoutthis evidence of hybridiza-tion. The high uniformity within these hybrid populations is curious. Anexperiment, not completed, suggested that hybridizationis possible (24). Evidence for interspecifichybridizationis otherwise scanty among diptero-carps (see review and reference in 10). It is most abundantbetween relatedspecies occurringin different, adjacenthabitats.Most examples are betweenspecies of Seasonal Evergreenand Dry Dipterocarpforests, suggesting recentdifferentiation.However, these taxa are usually strikinglydifferent in habit:those of the latter forest type are short trees frequently with larger, more incoriaceous leaves, more diffusely arranged the crown;they also have thick,fissured bark. Occasionally, species of the Mixed Dipterocarpforests of theaseasonal Far East occupying different edaphic ranges may hybridize in
  15. 15. 360 ASHTONthe ecotone between. The best known case is thatof Shorea leprosula Miq. ofclay lowland soils and Shorea curtisii Dyer ex Brandisof xeric ridges, both insection Mutica. Groupsof individualsmorphologicallyintermediatebetweenthese species are known from several localities in peninsularMalaysia. In onestandthe inferenceof hybridorigin was supportedby isozymal evidence; onefruiting hybrid individual there failed to set viable seed (30). Jong (in 10)provided evidence for hybrid origin of the tetraploid apomict S. ovalis(Korth.) Bl., a species monotypic to its section yet occurringas three geogra-phic subspecies. All evidence presently available to us, which is morpholo-gical and isozymal, suggests that speciation among dipterocarpsis as a rulegeographically or at least ecologically allopatric (6, 7, 10, 11, 12a). Biogeographical and paleontological evidence implies that dipterocarpshave been invadingthe Far East from the west since the late Eocene. Severalspecies endemic to the aseasonal southwestof Sri Lankaappearmost closelyallied to taxa in the Far East. Curiously,the FarEasterntaxon in nearlyeverycase occurs entirelyor principallyin SeasonalEvergreenforest. It is no longerpossible, on biogeographicgroundsto determinewhetherdipterocarps origi-nally arrivedin Asia, which they almost certainlydid by way of the Deccanplate (10, 17), principallyor entirely as denizens of the mixed forests of theaseasonalzone, althoughthe threearchaicgeneraendemic to the Deccan plateand Seychelles are thus restricted.Many taxa of the aseasonal Far East alsohave seasonal evergreen forest vicariants. If dipterocarpsinvaded from thewest, the original Asian dipterocarpsmay have been aseasonal mixed rainforest species. They likely speciated into Seasonal Evergreen forests andspread eastwards. Some of these furtherspeciated into the aseasonal mixedforests of the Far East, formingthe progenitorsof the rich modem flora there(7). Independent flora of the evidence for a seasonal origin for the dipterocarpaseasonalFarEast is providedby the climatic cue for flowering which appearsto be a drop in minimum night temperature.This occurs annually in theseasonal tropics, but at several year intervals in the aseasonal tropics (13).The Dry Dipterocarpforest species all seem to be of recent origin, however,as already implied by the evidence of hybridization. Wallaces Line, and the Torres Straits, have been formidablebarrierstodipterocarp spread.Only one species is sharedbetween Borneo and Sulawesi,and that is a riparian species with water-dispersedfruit. Dipterocarpsareunknown in Australiaand the BismarkArchipelago. A strikingexception tothese restricted patterns is provided by Vatica odorata (Griff.) Sym. sspmindanensis(Foxw.) Ashton of the Philippinesand northernBorneo, whichalso occurs in Hainanand Kwangsi; and by Shoreafalciferoides Foxw. of thePhilippines which is closely allied to a species so far known only from theQuilon peninsula of coastal central Vietnam, S. falcata Vidal. The mostparsimoniousexplanationfor such distributions,in the absence of a commoncontinental shelf between the two regions is typhoon dispersal, westward.
  16. 16. BIOLOGY DIPTEROCARP 361 Within the aseasonal Far East, west of Wallaces Line, dipterocarps mani-fest three patternsof distribution: widespread,which includes several that (a)also occur in the Seasonal EvergreenDipterocarpforests of Indo-Burma;(b)island-wide endemics; and (c) local endemics and disjuncts (7). The thirdcategory includes most taxa with wingless fruits, whereas only one wing-less fruited species, Shorea multiflora(Buck) Sym. falls into the first cate-gory. Local endemism is unusual among dipterocarpsin the forests of the FarEast. Hopea contains a number of local endemic and disjunct, apparentlyrelict distributionsin the Seasonal Evergreenforest isolates of Indo-ChinaandsouthernIndia. In Sri Lanka, Stemonoporusis unique in the subfamily in theabsence of any widespreadtaxa. All species are more or less local endemics,sometimes apparentlyvicarious on the main mountainmasses but sometimesalso geographically, though not apparentlyecologically, sympatric(17). Tothis we return, but I now wish to addressa more general fact-that the vastmajority of dipterocarpswithin the aseasonal zones are restricted in theirdistributionby their edaphic and altitudinalranges. Dipterocarpspecies, particularly the aseasonaltropics, almost invariably inoccupy narrowrangesof soil fertility. Distributionis correlatedwith a numberof soil factors, but primarilywith magnesiumand then phosphorus(18, 14).Widespreadspecies are confined to widespreadsoils, endemics and disjunctsto soils (and rock substrates)themselves of local and disjunct distribution(10). No dipterocarpsare endemic to limestone or to ultramaphicrocks,though morphologicallydistinct forms occur, particularlyon the latter (10).Within a landscape on uniform rock, soil fertility is often correlated withphysiography, and congeneric and consectional species may occupy distinctbut overlappingranges along the catena (5). Ashton et al (15) have shown thatdipterocarpspecies richness within individualhabitatsincreaseslinearly withtotal mineral soil magnesium concentrationup to a thresholdof about 1300ppm Mg, above which close correlationis lost and there is a sudden drop inspecies richness. In Borneo this represents a range of between 9 and 57dipterocarp species in samples of 1000 trees. Species richness of MixedDipterocarpforest is also, and independently,correlatedwith within-samplevariation in soil fertility up to but not above the same total magnesiumthreshold, a point to which I return.Above the fertilitythreshold,dipterocarpspecies richness continues to fall erraticallyas soil Mg and P values increase,but the abundanceof the commonest species markedly increases. The soilspecificity and center of edaphic distributionof dipterocarpsis compatiblewith their apparentlyobligate association with ectotrophic mycorrhiza, andwith the possibility that some of these symbiontsmay be host specific (54, 55,personalcommunication).This implies that some secondary, species-specific metabolites may act as cues to mycorrhizalinfestation. The patternof tree species-richness overall in Mixed Dipterocarpforests is similar to that of
  17. 17. 362 ASHTONthe dipterocarpsthemselves, even though some large individual familiesincludingMeliaceae, Rubiaceae, and Euphorbiaceae most species-richon arethe most mesic fertile sites (5). Up to 11 consectional Shorea species are known to co-occur in a singleforest (Figure 1). An understandingof how these populations of closelyrelated taxa are maintainedin mixture is central to our understanding the ofmaintenanceof species richness in rain forests, while their cladistic rela-tionships may throw light on the evolution of species richness (51 and inpress). Cladisticand genetic analyses of interspecificrelationsbetween cladesare still awaited. Ecological andbiogeographicpatternsamongsmallergroupsof species, closely related on morphological and isozymal evidence, andamong interspecific taxa suggest that speciation is generally but perhapsnotalways geographically or ecologically allopatric (6, 11, 31). Host specific mycorrhizacould allow differentialexploitationof soil nutri-ent resources among consectional species. The ecological distributionof theten species of Shorea section Doona in Sri Lankacan be distinguishedalonggradientsof altitude, soil fertility (and the catena), and light response (Figure2). Shorea trapezifolia(Thw.) Ashton and S. congestiflora (Thw.) Ashton insection Doona, Shorea leprosula (section Mutica) and Dryobalanops lan-Figure 2 Schematic ecological range, in the wet zone forests of Sri Lanka, of the species ofShorea, section Doona. Key: a. Shorea cordifolia b. S. gardneri c. S. zeylanica d. S.affinis e. S. trapezifolia f. S. megistophylla g. S. disticha h. S.worthingtonii i. S. con-gestiflora
  18. 18. DIPTEROCARPBIOLOGY 363ceolata Burck differ from other membersof their groups in their exceptionalmaximal growth rates (16; P.M.S. Ashton, in preparation).Differences inshade tolerancesamong membersof quasigeneraare well known to foresters.All dipterocarpsappear, remarkably,to have low compensationpoints, andthe differences appear to be principally attributable differences in max- toimum rates of photosynthesis(A. Moad, in preparation) to rates of dark andrespiration(R. A. Sunderland,unpublished). The species with highest maximum growth rates overall are confined tofertile soils. Dryobalanops lanceolata and also Parashorea malaanonan(Blco) Merrill are unusual in combining high maximum growth rates withhigh shade tolerance as juveniles (A. Moad, personal communication). P.Hall (personalcommunication)has found evidence from Borneo that seedlingsurvivorshipof D. lanceolata is greaterin the deep shade of Mixed Diptero-carp forest on basalt-derivedsoil than is that of D. beccarii in the relativelyopen light conditions within forests on infertile leached yellow sands. Theratios of adults to saplings to seedlings, estimated in the same year, were1:5.2:87.6 in D. lanceolata, 1:1.5:46.3 in D. beccarii. High juvenilesurvivorshipin shade has also been noticed among some Shorea species onvolcanic soils in the Philippines (21). It is possible, where available soilnitrogenis high, thatspecies can maintainhigh enough photosyntheticrates inshade to compensate for night respiration rates (F. A. Bazzaz, personalcommunication).This may explain why D. lanceolata is amongthe dominantspecies on fertile soils and, conversely, why species dominance is un-correlatedwith species richness throughoutmost of the range of less fertilesoils. In most quasigenera, floral morphology is ostensibly identical amongclosely related species. Chan & Appanah (26) have shown that six co-occurring members of Shorea section Mutica in Pasoh forest, peninsularMalaysia, flower in overlappingsequence. Casual observationssuggest thatthis happens in other dipterocarpgroups where several species co-occur (6).Chan & Appanah found that flowering is very highly synchronizedwithinpopulations, but that the individualsof each succeeding species flower oversuccessively longer periods. Interestingly,the two-andone-half monthperiodover which all six species flowered is no longer than the flowering period ofShorea robusta Roxb., a single species dominantof Dry Dipterocarpforestsin northeastIndiain which individualsare more loosely synchronized.Ashtonet al (13) demonstrated that this sequentialflowering is significantly nonran-dom. Dipterocarps,includingthe species in question, are outbreeders(25; C.V. S. and I. A. U. N. Guantillekein preparation).Sequentialflowering haspresumablyarisenas a consequence of lower fruit set duringtimes of flower-ing overlap among species sharing a common pollinator. Co-occurrenceofsuch species series is only possible where barriers hybridizationare strong. to Extrapolatingback on the basis of the length and time of the flowering
  19. 19. 364 ASHTONperiods of the six species, Ashton et al identifiedthe time when inflorescencedevelopmentprobablybegan. They discovered that over a 20-year period, a20 C depressionof minimumnight temperature occurredfor several days atthis same intervalbefore each general flowering, and at no other time. Theyfurtherfound a broad correlationbetween mass flowering seasons in east-facing lowlands and the El Nifio climatic event over the Pacific, when theaseasonal region of the Far East may experience prolonged periods of clearskies and relatively low humidity, hence lower than average night tempera-tures. This can explain why dipterocarpsflower annually in the seasonaltropics, and why mast fruiting has not been observed in the Mixed Diptero-carp forests of Sri Lanka, outside the main zone of El Nifio influence. Theevidence of Ashton et al also implies that dipterocarpswere preadaptedbytheir flowering physiology to become mast fruiters when they invaded theaseasonallowlands of the Far East. It is remarkable the fruitingof the six thatspecies thatflowered in close sequencecoincide with one anotherand with theother species in the family. This lends furtherstrong supportto Janzens (40)hypothesis and suggests that new species immigrantsto a forest communitybecome entrained through selective predation to fruit synchronously withthose already established (13). In Semengoh forest, Sarawak,East Malaysia, 11 species of Shorea sectionMutica co-occur (Table 1). Some of the most abundant species are common toboth Semengoh and Pasoh, which is 1000 km to the west across the SouthChina Sea. S. acuminata Dyer and S. quadrinervis Sloot. are vicariants.Otherssuch as S. dasyphyllaFoxw. and S. parvifolia Dyer change their rankorder. We believe this is due to edaphic differences between the two sites,because the most abundant species areremarkably constanton the same soil indifferent localities in northwest Borneo (15). The difference in number ofconsectionalspecies at the two localities is attributableentirelyto the differentnumberof species of low populationdensity in each, and this has also beenfound to explain differences in forest species richness overall (15). Un-derstandinghow species of low populationdensity (which comprise the vastmajority in species rich forests) are maintainedis crucial to understandinghow species richness is maintainedoverall. Some of the rare species in the Semengoh example, such as S. slooteniiWood ex Ashton, S. rugosa Heim andS. hemsleyanaBrandisseem always tobe rare, occurringas scatteredindividualsor clumps. Othersclearly arenot. Acomparisonof the populationsof Shorea dasyphyllain Pasoh and Semengohforests provides one example (Table 1). Some species such as Dipterocarpusgracilis Bl. and Anisoptera costata (Korth)Bl. are abundantin the seasonalpartsof theirrangebut generallyoccur as far scatteredindividualsin aseason-al Borneo. Low populationdensity may reducefecundityin outbreedingtrees,and Chan (3) found evidence of this in the low density population of S.
  20. 20. DIPTEROCARPBIOLOGY 365 Table 1 Relative densities of reproductiveindividualsShorea, sec- tion Mutica, species in two lowland mixed Dipterocarpforests Pasoh Research Forest Semengoh Forest PeninsularMalaysia Sarawak Shorea acuminata 3.0/ha Shorea quadrinervis 4.7/ha Shorea parvifolia 2.8/ha Shorea scabrida 4.7/ha Shorea leprosula 2.7/ha Shorea macroptera 4.6/ha Shorea macroptera 2.4/ha Shorea dasyphylla 3.5/ha Shorea lepidota 1.6/ha Shorea slootenii 1.1/ha Shorea ovata 1.0/ha Shorea parvifolia 0.9/ha Shorea dasyphylla 0.3/ha Shorea leprosula 0.2/ha Shorea rubra 0.1/ha Shorea rugosa 0.1/ha Shorea hemsleyana 0.07/hadasyphylla and in isolated individuals of S. leprosula. Chan (24, 11) found S.dasyphylla to be the only species, among the 6 members of Shorea sectionMutica whose flowering phenology he studied, whose flowering period en-tirely overlapped with those of other species. It strains the imagination tobelieve that all 11 species at Semengoh possess distinct flowering times. Thephenology and reproductive biology of the rarer species there would repaystudy. It is curious that dipterocarps of the seasonal tropics tend to have higherpollen/ovule ratios than do those of the aseasonal tropics (9). In those fewquasigenera where staminal number varies, such as Shorea sections Shoreaand Anthoshorea, and most particularly in some understory Hopea and Stemo-noporus, a broad albeit inconsistent tendency exists for local endemics tohave reduced number of stamens. In Stemonoporus this is accompanied alsoby a reduction of the number of ovules to four. It is unknown whether thistrend is accompanied by increases in self-compatibility. These patterns would appear to be consistent with the presence-to a stilllargely unknown extent but on inferential evidence probable in manygenera-of apomixis through pseudogamous agamospermy (41, 42). Aga-mospermy has been confirmed in one species of Hopea and two of Shorea andinferred, on the presence of polyembryony or triploidy, in some 10 of 70species examined cytologically to date. Apomixis has been found or inferredin abundant and widespread species such as S. ovalis and S. macroptera, butalso in one local endemic of specialized habitat (Hopea subalata Sym.), inone gregarious species of river banks (H. odorata Roxb.), and another of Dry
  21. 21. 366 ASHTONDipterocarpforest (DipterocarpustuberculatusRoxb.). S. macropterais thefirst of its section to come into flower. Pollinatornumbersmay not yet be atfull strengththen, and it may be supposedthatS. macropteraexperiencesthegreatest vicissitudes in securing successful cross-pollination. Certainly,adventive embryony provides a means of maintaining fecundity withoutreductionof heterozygosity,but a cost is paid in reducedgenetic variabilityatpopulation level. The proportion of seeds with multiple and perhaps apomictic embryosvaries between species, and in some cases between individuals within pop-ulations (24, 13). Isozymal analysis of population samples of reproductiveindividualsof Shorea species indicatesthat genetic variabilitycan be remark-ably high (31, 32, D. Buckley in preparation).In a population sample ofalmost matureindividualsof S. trapeziflora,variationconformedwith Hardy-Weinberg expectations. Whether this is due to outcrossing patterns or todifferential mortality between the progeny of selfed and cross-pollinatedflowers is so far unknown (D. Buckley in preparation).Gan (30) and Chan(25) had evidence that isozymal and leaf morphological variation withinpopulationsamples of S. leprosula increases with distancesbetween trees upto 200 m, and wi-thin-population genetic variability can exceed variabilitybetween populations 100 km distant. On the other hand Gan (30) foundsibling seedlings to be isozymally uniformin the apomicticS. ovalis, thoughthisresult could have been an artifactof tetraploidy.CONCLUSIONI arguethattoo much emphasishas been put on the species as an independentunit to test for niche specificity in species-rich terrestrialplant communitiessuch as tropicalrain forests. I have endeavoredto show that dipterocarp taxain all levels in the systematic hierarchypossess charactertraits upon whichselection may be expected to act uniformlyin nature.Families, I suggest, arein competition with one another. The Dipterocarpoideaeseem to com-petitively exclude otherfamilies undercertainconditions, and not necessarilythose in which dipterocarp species richness is maximalmore thanunderotherconditions. Selection acts on different charactertraits at different taxonomiclevels. Hubbell & Fosters (39) search for significant positive or negativeassociation between the spatial and temporal patterns of different speciespopulations, and between them and habitatvariation,as a test of the equilibri-um-hypothesis of communityspecies composition, shouldbe extendedto taxaof higher rank (1 1). Association can be expected to be manifest also betweentaxa of differingrank. So far though, the relationshipbetween phylogeny andecology is largely unknown above the species level of the taxonomichierarchy.
  22. 22. BIOLOGY DIPTEROCARP 367 Patterns of species richness of Dipterocarpaceaeamong different foresttypes sharing a common climate conform extraordinarily closely with Til-mans (56, 57) equilibriummodel for the relationshipbetween species rich-ness and resource availability. The data currently available, though in-ferential, do suggest thatthe ecological range and performanceof dipterocarptaxa are influencedby a wide arrayof climatic and edaphicvariables(see e.g.18). In combination,it could easily be arguedthat every species in the mixedrain forest may possess unique ecological requirements.But to furthersug-gest, in the case of sessile organisms of large size like trees, that theirecological differences have evolved as a consequence of direct interspecificcompetitionis patentlyabsurd.The high local genetic variability,yet regionaluniformity, of morphologicaland genetic variationthat seems to characterizesome of the more abundantdipterocarps,such as Shorea leprosula and S.trapezifolia, suggests that they are panmictic species in which (curiously, inview of the biological heterogeneityof theirhabitats)selection acts unifornlythroughouttheir geographical ranges. W. Smits (personal communication)has suggested that poor seed dispersal in combinationwith stringentrequire-ments for maintainingspecies-specific mycorrhizalsymbionts could result inthe pattern of variation observed, and these might also explain the sharpthough subtle discontinuities in variation that differentiate taxa, and theapparentrarity of hybridization. Some of the scant population genetic dataavailable and the existence of adventive embryony do cast doubt on naturalselection, that is, equilibriumphenomena, as the sole mediator of floristiccomposition and species richness (15). Apomixis may serve to sustainfecund-ity in populationsof low density and may also allow survivalof taxa occupy-ing habitatfragmentsof limited area, where space precludesthe full speciescomplement of a community type and thereforewhere species compositionand abundances will be unpredictable and substantially determined bystochastic processes of immigration and extinction. Selective processesappear to determine maximum population density, but extinction in thesespecies-rich communities, stable over time, may essentially be a stochasticprocess if fecunditycan be maintained(13). The key to understanding role theof selection in determining species composition will be the knowledge ofpatterns of change in gene frequency which take place as sibling cohortsdevelop to reproductivemat, rity. I believe that the principles that govern the role of dipterocarpsin thestructureof tropical rain forests are general to all terrestrial rainforestplantsand perhapsalso to epiphytes. Obviously, differences of detail exist betweentaxa and guilds. Tree families known to be mycorrhizal,such as Myrtaceae,show patternssimilar to those of dipterocarps(5). Agamospermyis knownamong many of these also (12). Others such as Meliaceae and Sapindaceaediffer in both species distributionand breeding systems (11, 13). The role of
  23. 23. 368 ASHTONnon-equilibrium,island biogeographicprocesses may be expected to be largeramong epiphytes than terrestrial organisms. In every case, a fuller un-derstandingcan only be reached by combining systematic with ecologicalapproaches.Literature Cited 1. Anderson, J. A. R. 1963. The flora of 12. Ashton, P. S., 1988. Dipterocarprepro- the peat swamp forests of Sarawak and ductive biology. In Tropical Forest Brunei including a catalogue of all re- Ecosystems. B. Biogeographical and corded species of flowering plants, ferns Ecological Studies. (Ecosystems of the and fern allies. GardensBull. Singapore World14b). ed. H. Lieth, M. J. A. Wer- 20:131-228 ger, Amsterdam:Elsevier. In press 2. Appanah, S. 1986. Insect pollination 12a. Ashton, P. S., Gan, Y. Y., Robertson, and the diversity of dipterocarps. In F. W. 1984. Electrophoreticand mor- Proc. Third Int. Round Table Con- phological comparisonsin ten rainforest ference on Dipterocarps, ed. A. G. H. species of Shorea (Dipterocarpaceae). Kostermans, pp. 277-291. Unesco, Bot. J. Linn. Soc. 89:293- Jakarta 304 3. Appanah, S., Chan, H. T. 1981. Thrips: 13. Ashton, P. S., Givnish, T., Appanah,S. the pollinators of some dipterocarps. 1988. Staggered flowering in the Dip- Malay. For. 44:234-252 terocarpaceae:New insights into floral 4. Ashton, P. S. 1963. Taxonomicnotes on inductionandthe evolution of mast fruit- Bornean Dipterocarpaceae.II. Gardens ing in the aseasonaltropics. Am. Nat. In Bull. Singapore 20:229-84 press 5. Ashton, P. S. 1964. Ecological Studies 14. Ashton, P. S. et al. 1988. Comparative in the Mixed Dipterocarp Forests of studies in the Mixed Dipterocarpforests Brunei State. Oxford Forestry Memoir of northwesternBorneo I: Patterns of 25. Oxford: Floristic variation. In preparation 6. Ashton, P. S. 1969. Speciation among 15. Ashton, P. S. et al. 1988. Ibid. III: Pat- tropical forest trees: Some deductionsin terns of species richness. In preparation the light of recent evidence. Biol. J. 16. Ashton, P. S., Hall, P., et al. c. Ibid. II. Linn. Soc. 1:155-96 Variation in structureand dynamics. In 7. Ashton, P. S. 1972. The quaternary preparation geomorphological history of western 17. Ashton, P. S., Gunatilleke, C. V. S. Malesia and lowland forest phytogeogra- 1987. New light on the plant geography phy. In Trans. Second Aberdeen-Hull of Ceylon. I. Historicalplantgeography. Symp. Malesian Ecol: The Quarternary J. Biogeogr. 14:249-95 Era in Malesia. ed. P. and M. Ashton. 18. Baillie, I. H., Ashton, P. S., Court, M. Hull, England:Univ. Hull Geog. Dept. N., Anderson, J. A. R., Fitzpatrick,E. Misc. Series 13: 35-49 A., Tinsley, J. 1987. Site characteristics 8. Ashton, P. S. 1980. Dipterocarpaceae. and the distribution of tree species in In A Revised Handbook to the Flora of Mixed Dipterocarp forest on tertiary Ceylon, I. ed. M. D. Dassanayake, F. sediments in centralSarawak,Malaysia. R. Fosberg, pp. 364-423. Washington, J. Trop. Ecol. 3:201-20 DC: Smithsonian Institution 19. Bawa, K. S., Webb, C. J. 1984. Flow- 9. Ashton, P. S. 1980. Some geographic er, fruit and seed abortion in tropical trends in morphologicalvariationin the forest trees: duplications for the evolu- Asian Tropics, and theirpossible signifi- tion of paternaland maternalreproduc- cance. In Tropical Botany, ed. K. tion patterns.Am. J. Bot. 71:736-51 Larsen, L. B. Holm-Nielson, pp. 35-68. 20. Becker, P. 1983. Effects of insect her- New York: Academic Press bivory and artificial defoliation on sur- 10. Ashton, P. S. 1982. Dipterocarpaceae. vival of seedlings of Shorea. In Tropical In Flora Malesiana I, ed. C. G. G. J. Rain Forest: Ecology and Management. van Steenis, 9:237-552 ed. S. L. Sutton, T. C. Whitmore,A. C. 11. Ashton, P. S. 1984. Biosystematics of Chadwick, pp. 241-52. Oxford: Black- tropical forest plants: A problem of rare well species. In Plant Biosystematics, ed. W. 21. Brown, W. H., Mathews, D. M. 1914. F. Grant pp. 497-518. Toronto: Aca- Philippinedipterocarp forests. Philip. J. demic Sci. A, 9:413-561
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