1990_monospecific dominance in tropical rain forests

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MonospecificominancenTREE vol. 5, no. 7, January 1990

Tropical ainForests Abiotic factors

TereseB. Hart

Old-growth rain forests that are dominatedby a single canopy speciesoccur throughoutthe tropics, though they account for a lim-ited proportion of the total ruin forest urea.These forests have been considered anom-alies in which development of a more diversecommunity is deflected by harsh conditions.Very poor soils or un otherwise extremeenvironment mug promote monodomi-nunce by excluding potentially competingspecies, 6ut it is now apparent that mono-dominant tropical forests also develop under

more benign conditions. Field studies haveshown that a single species may dominateon undisturbed sites where the soils aresimilar to those of adjacent old-growth,mixed forests. In these situations the domi-nant is a superior competitor and/or isparticularly tolerant to stresses such usshade. Assertion of dominance 6g a singlespecies n an old-growth forest appears mostlikely in ar eas where the species pool con-tains few late-succession species with simi-lar life history traits.

Tropical rain forests (Box I I aregenerally more diverse in speciesthan temperate forests2,3. Richards,in his early and extensive dis-cussion of this phenomenon4 , alsocommented on the apparentlyanomalous occurrence of old-growth tropical rain forests domi-nated by a single canopy treespecies. Such forests, he noted, oc-curred on well-drained terrain and

often abutted more diverse forests.Richards described in detail onlyrelatively small discrete stands offorest dominated by a singlespecies, but he called attention tothe existence of more extensive for-mations in various tropical regions.Examples of forested areas where asingle canopy tree species contrib-utes more than 80% to the totalbasal area (hereafter, monodomi-nant forests), and that are reputedlyold-growth stands on well-drained

soil, occur throughout the tropics(Table 1 5,6 over areas of hundredsof square kilometers. See Box 2 foran example.

In Africa, the dominant species of

Terese Hart is at Wildlife Conservation Inter-national, The New York Zoological Society, Bronx,NY 10460,USA.

6

monodominant rain forests are gen-erally, though not always, membersof the legume family Caesal-piniaceae’. Mora excelsa, also ofthe Caesalpiniaceae, forms mono-dominant forests in parts of easternSouth America and Trinidad. In Asia,members of the Dipterocarpaceae,Lauraceae and Guttiferae all occuras the dominant species of largemonodominant stands2m5. In theseforests the dominant species is

present in all size classes and theforests have been considered cli-max (i.e. capable of maintainingapproximately the same speciescomposition in the absence ofsevere disturbances).

Dominance, by definition, affectsthe evenness or relative represen-tation of species. Therefore, itaffects local species diversity,although total species number maynot be altered over large areas.Early studies from all three tropical

continents reported monodominantforests having the same overallspecies composition as adjacentold-growth mixed forests5. The can-opy species associated with thedominant were all characteristic ofthe neighboring forests and thespecies of these latter forests didnot appear to be excluded from themonodominant stands. As a singlespecies assumes an ever greaterpercentage of the basal area, how-ever, other species lose represen-

tation in the canopy and rarespecies become rarer. The result isthat any small plot in monodomi-nant forest will contain fewerspecies than a plot of the same sizein mixed forest (Fig. I I.

Monodominant forests have re-ceived renewed attention duringthe last decade, and our under-standing of the possible causes ofmonodominance has advanced con-siderably. Here, I review factors re-ported to control species diversity

in tropical rain forests on well-drained soils, and summarizeexamples fr om extra-tropical andwaterlogged forests that can con-tribute to our understanding ofmonodominance. I also discuss howdominance may be related to sec-ondary succession in tropicalforests.

It seems reasonable to expectthat environmental factors thoughtto promote high species diversity in

tropical forests might also controldominance by a single species. Insome tropical areas, patterns of for-est diversity were interpreted asshowing that increased rainfall3 orsoil moisture9 promote increasedspecies richness. In an Asian study,floristic patterns were construed asshowing a direct association be-tween levels of specific soil nutri-ents and overall floristic richnessiO.The occurrence, in some cases, ofspecies-poor tropical forests on

particularly impoverished soilssuggested that extremely low fertil-ity could lead to low diversity”.

In most tropical forest studies,however, correlations between par-ticular species associations and soilfactors have given only equivocalresults2, and the high diversity oftropical forests cannot be relateddirectly to edaphic diversity12. Incertain instances, a single speciesmay form monodominant standsover a wide variety of soil types5.

Most of the large monodominantformations listed in Table 1, as wellas some smaller stands, coexist withadjacent, more diverse mixedformations across similar soilconditions5,‘3.

Biotic factorsIn tropical forests with high

species diversity, there is some evi-dence for overall enhanced growthand recruitment of rare tree speciesrelative to common species14. The

‘compensatory mechanisms’ in-volved might include concentrationof natural enemies on commonspecies, intraspecific competitionfor resources, or interference be-tween abundant conspecifics as, forinstance, through allelopathy. Dif-ferential mortality of seeds andseedlings such that the greatest lossoccurs near the parent trees hasbeen shown to occur in at leastsome tropical forest species15,16.Such mortality, whether provoked

by predation or other causes, couldpromote a more even distribution oftree species and hence greaterspecies diversity.

Treefalls have been attributed animportant role in maintaining trop-ical forest diversity, in that the gapsthey create present a rich andvaried resource for tree germination



‘TREE vol. 5, no. I, January 7990

#and growth17. The differential adap-.:ation of tropical tree species to this-esource gradient may maintain anelevated level of diversity. This

could only be true, however, if tree-tails created a level of heterogen-eity that guaranteed not only theizermination and establishment, but,~lso the continued growth into thecanopy, of a wide variety of tree,;pecies.

In the old-growth tropical mono-dominant stands where the canopy‘dominant is abundantly represen-:ed in the understory, mono-‘dominance appears to be self-oerpetuating. It may be that oncenonodomi nance is well estab-lished, compensatory mechani sms3re no longer effective in generatinggreater evenness. For example, theequalizing effect of seed predationmay be suppressed in monodomi-nant stands through predatorsatiation during synchrono us fruitproduction’8,‘9.

Any biotic factor that promotesthe interspecific competitive ad-vantage of the dominant treespecies, or improves its ability towithstand stresses of conspecificorigin, such as shade or a build-up ofleachates, would promote mono-dominance. It has been suggest edthat tropical tree species that formspecies-specific ectomycorrhizal as-sociations may have an enhancedability to form monodominantstands that will be self-replacingand able to invade neighboringmixed forest$. Ectomycorrhizae arecommon within at least two of thefamilies containing species thatachieve monodominance in tropicalrain forest environments: the Dip-terocarpaceae6 and the Caesalpini-aceae5.

Extra-tropical and waterlogged sitesExamination of examples of

single-species dominance in sub-tropical communities or in forestson poorly drained substrates mayclarify the processes leading todominance (Table 2). In many eco-systems it appears that fire isimportant in determining speciescomposition. Fires may both pro-mote and prevent dominance by asingle species. In the pine fl atwoodsof Florida, fire-resistant speciescan maintain nearly single-speciescanopies in the presence of recur-ring fires20. In Tasmanian temperaterain forests, slow-growing shade-

tolerant species are suppressed byrecurrent fires that continue to favordominance by the shade-intolerantNothofagus cunninghamii2’ (which

in some cases comprises 95% of thebasal area). On the other hand, inCalifornia chaparral communitiesthe recurrence of fire preservesdiversity. Where fire is long absent,there is a clear succession andone species eventually assertsdominance2*.

Some of the better-known trop-ical and subtropical monodominantforests occur on waterlogged orperiodically flooded substrates. InCentral America some freshwaterswamps are nearly pure stands of asingle species, e.g. Prioria copaiferaor Campnosperma panamensis23. Inthe La Selva forest (Costa Rica)there is a dramatic reduction instem density and species richnesswith increasingly poor drainage; thisis a result of the exclusion of speciesintolerant of waterlogged soi124. Thefrequency, depth and duration offlooding seem to be determinantsof species composition and domi-nance. When waterlogged forestsare drained, dominance may besuppressed; in the cypress standsof Florida, for example, hardwoodspecies have invaded drainedswamps and cypress has lost itsdominance25. It seems, therefore,that flooding, like fire, can conferadvantage to a particular species byexcluding other species.

In mangrove forests, additionalenvironmental stresses compoundthe effect of waterlogging. Soilsalinity, tidal flows and erosional

episodes reduce growth rates andeliminate species intolerant of,or unable to compete under, thesevere conditions. Rhizophoramang/e forms self-replacing mono-cultures where tidal energy is highor ocean water deep , and Avicenniagerminans does so where wintertemperatures are particularly low26.

Monodominance nd successionThe perturbations leading to

dominance in a community neednot be so stressful or continuous asto eliminate species permanently.Absences from the forest canopymay be temporary, as in the caseof secondary succession. The lifehistory traits favored early in suc-cession, such as tolerance to fullsunlight, rapid growth and efficientdispersion of small seeds, are oftenthe inverse of traits favored in latesuccession, such as tolerance toshade and production of few seedswith large energy reserves. The re-sult is a successional sequence ofspecies as the relative competitivevalues of these traits change27.

Table 1, Old-growth mon odominan t tropical forests of well-drained soils that occur in standsof more than 100 km*

Location

Malaya, Sumatra

Borneo, Sumatra

Dominantspecies

Dryobalanopsaromatica

Eusideroxylonzwageri

Family

Dipterocarpaceae

Lauraceae

Description ofdominance

60-90% of timbertrees

‘Pure stands’

Trinidad Mora excelsa Caesalpiniaceae 85-95% of thecanopy

East Africa Cynometra alexandri Caesalpiniaceae

Central Africa Gilbertiodendron Caesalpiniaceaedewevrei

Adapted, with permission, from Ref. 5.

>75% of the canopy

>90% of the canopy

7



TREE vol. 5, no. 1, January 1990

Box 2. Exampleof an old-growthmonodominantropical rain forest

The monodominant rain forest dominated by Gilbertiodendron dewevrei, local ly knownas mbau forest, covers hundreds of square kilo meters in northeastern Zaire. The largeheavy se eds of G. dewevrei, covered by only a thin seed coat, are not dispersed by animals.They drop beneath the parent and sprout within 3-5 days, producing first-year seedlingsthat are 0.X-0.45 m high. The first seedling leaves rapidly b ecome coriaceous and resistantto herbivory. Seedlings may persist for years in the shaded understory with little furthergrowth. The representation of G. dewevrei in the understory is evident in the profilediagram of a 100 m x 10 m plot near Yangambi, Zaire, adapted from Ref. 7; all darkenedcrowns are G. dewevrei.

r0

-30

E

-20 g2

-10

-0

The homogeneity of the canopy contributes to the shade of the understory, where theshade tolerance of the dominant species permits it to persist in all subcanopy size classes,as shown in the table below. The abundant representation of G. dewevrei in the understoryindicates that mbau forest is an old-growth forest in which canopy composition is stable.

SizeMean no. of Mean total G. dewevrei as

class?G. dewevrei no. of stems percentage of

stems per ha per ha total stems

Seedlings 8000 28 000 28.6

Saplings 307 1911 16.1

Poles 138 191 72.3

Trees 62 77 80.5

Large trees 51 55 92.7

Data collected in the lturi Forest of Zaire from 24 plots of 625 mz each for all stems > 10 cm dbh. Sapli ngdata collected from 12 plots of 225 m* and seedling data from 12 plots of 25 m2,Data from Ref. 5.“Seedlings defined as height > 0.5 m, diameter at 1.3 m (dbhl 4 2.5 cm; saplings: dbh > 2.5 cm and 5 10

Species replacement occurs rela-tively rapidly in early successionand there is a distinct advantagein being the first species to be-come established. Dominance islikely to result from the fortuitousand massive est ablishment of asingle, highly vagile, rapidly grow-ing species. Monodominance iscommon during early successionsin tropical environments28. Well-known forest communities thatfit this category include mono-dominant stands of Musangacecropioides or Trema guineensisin Africa and stands of Octomelessumatranus in Asia’,4. Similarspecies occur in tropical America,such as Cecropia obtusifolia andOchroma lagopus29. The canopydominant, in each case, does notreproduce in its own shade andmonodominance lasts only a singlegeneration.

Some monodominant forests do

not have a history of recent or recur-rent disturbance and yet the domi-nant species is characterized bycertain early successional traits. Forexample, Nothofagus obfiqua domi-nates a Chilean forest but does notregenerate in its own shade: it hasbeen suggested that the individualsnow forming the canopy became es-tablished subsequent to a distur-bance approximately 250 yearsago30. Likewise, in Asia, the ‘stormforest of Kelantan’ is dominatedby Shorea parvifIora, a long-livedspecies believed to have grown upafter major wind destruction in18802. These example s illustratethat, given fortuitous regenerationconditions following a major distur-bance, a single tree species can be-come established and dominate thecanopy of rain forest more than acentury later.

In mid succession, monodomi-nance is less likely because the

slower growth rates prolong theperiod of coexistence of numerousspecies27. According to the ‘inter-mediate disturbance’ hypothesis3’,

the greater diversity of this stagederives from the persistence ofmature individuals of early suc-cessional species as later succes-sional species grow into the canopy.Lang and Knight32 describe a sec-tion of the forest on Barro ColoradoIsland (Panama) that exemplifiessome of these mid-successionalcharacteristics. At 60 years of age,45% of the basal area was accountedfor by four species, three of whichwere clearly early successional. Ten

years later the same species werestill present in the canopy althoughtheir relative representation hadchanged as individuals died andwere replaced by more shade-tolerant species.

if a forest remains undisturbed,the slow-growing shade-tolerantspecies will dominate an in-creasingly large proportion of thecanopy. There is little advantage, atthis stage, in having been the firstspecies to establish. Able to persistin their own shade, these individ-uals are potentially self-replacing.The best competitor, or the speciesmost resistant to prevailingstresses, will steadily increase inabundances’. Accordingly, efficiencyof dispersal is sacrificed in favorof large, heavy and often poorlydispersed seeds that producerobust, shade-tolerant seedlings33(Table 2).

Most tropical forests charac-terized by high species diversitymay be in some middle stage ofsuccession. For this to be the case,disturbances occurring at shorterintervals than the life span of thelongest-lived trees in the systems2’would have to be typical throughoutmuch of the tropical rain forest zone.

Large-scale disturbances wouldhave to occur only once every sev-eral centuries to reinitiate or reju-venate a successional sequence ina tropical forest. Diverse obser-vations from various tropical regionssuggest that such disasters may takeplace with this frequency and acrosssignificant areas of rain forest.Large-scale storms occur regularlywithin the cyclone belt between IO”and 20” north and south of theequator34. Hurricane Joan of 1988, forinstance, may have destroyed 7%



TREE vol. 5, no. I, January 1990

of Nicaragua’s total forest cover.Extensive damage, resulting fromtornadoes, may be more frequentin continental tropical forests thanis commonly recognized. Aerialphotographs and satellite imageryrevealed numerous tornado tracksthrough sparsely populated forestsof Paraguay, southwestern Braziland northeastern Argentina35. Ex-ceptional droughts can also give riseto major disturbance, as illustratedby the 1982-1983 fire that ravaged30 000 km* of tropical lowland for-est in East Kaiimantan (Indonesia).

It also appears that large tracts offorest previously thought to havebeen untouched by human popu-lations may actually have under-gone extensive anthropogenicalteration recently enough to be rel- tree species present in the systemevant to the current successional with near-equivalent life historystatus of the forest communities. traitss7. Accordingly, monodomi-Physiognomically mature and flor- nance is favored on isolated islandsistically diverse forest in Venezuela where the species pool is poor dueoccurs over buried charcoal hor- to the difficult dispersal of propa-izons whose radiocarbon dates gules across large bodies of water.suggest that the forest has been The monodominance of old-growthsubjected to two separate fires in forests on the Hawaiian Islands may

the last 500 year+. Under prevail- be partly explained in this mannerY8.ing humid conditions large fires On islands covered with rain forestwould have been likely to occur only at the time of their formation, thereas intentional phases of agricultural is also a trend towards monodomi-cycles, although fires might have es- nance as species are lost through ancaped into uncut forest during drier increased extinction rate relative toperiods. Similar extensive charcoal the colonization rate. This appearshorizons have also been found to be occurring on the smaller

under old-growth forests in centralAfrica5. t

History: disturbance and the speciespoolf

There are two further interrelated2

factors of possible significance to .imonodominance in tropical forest. aThese are ( I ) the size of the species “J,pool, or the number of species inter-acting during succes sion, and (2)major environmental change thatoccurs so rarely or at such distantintervals as to be on a time-scaleother than that of secondarysuccession.

The size of the species pool isPlot size

likely to contribute to dominance in Fig. I. Species-a rea curves illustrate that small plots in

old-growth forests. In late succes- diverse forest support more species than plots of equal

sion the prolonged coexistence ofsize in adjacent monodominan t forest. This is the result

species is related to the number ofof increased rarity of nondominant species, not necess-ariiv the exclusion of particular mixed forest speciesfrom monodominant &nds.

islands isolated by the formationof the Panama canal (F. Putz, pers.commun.).

Major environmental changes af-fect the species pool by causinglocal extinctions of rainforest trees.

Replenishment of the species poolafter suitable growing conditionsare re-established depends uponspecies mobility. The movement oftree species northward after the lastglaciation has been documentedby pollen cores. Range expansionvaried between 100 and 400 m per

Table 2. Characteristics f monodominantorests n extra-tropicaland wet tropical sites

Forest type

Extra-tropicalorests

Location Environmental factor pertinentto dominance

Traits of dominant species Refs

Nothofagusforest

Tasmania, Chile Past major disturbance Shade-intolerant 21,30

Cypress swamps Southeast USA Flooding and fire Shade-intolerant, tolerant to fire and 25flooding

Pine fiatwoods Florida, USA Fire and flooding Shade-intolerant, variable tolerance 20to fire and flooding

Tropical orests without pronounceddry season

Swamp forests Central and South

America

Flooding, waterlogging Tolerant to stress 23

Storm forests ‘Hurricane belt’ Past disturbance Shade-intolerant 2

Mangrove Coasts Disturbance, stress of tides Tolerant to stress, rapid colonization 26and salinity and growth

Evergreen rain Throughout tropics Variable, well-drained soils Slow growth, shade-tolerant, poor 4-6forest dispersal

9



-.

Table 3. Community haracteristics f tropical rain forestsat different stagesof succession

Early succession: Mid succession: Late succession:monodominance even coexistence monodominance

Life history traits of Rapid growth rate; Wide spectrum Slow growth rate;canopy species tolerates direct represented tolerates shade; few,

sunlight; numerous, large, poorlysmall, well- dispersed seeds;dispersed seeds; long life spanshort life span

Disturbance regime Frequent, large intermediate Infrequent, small

Species pool Variable, advantage Many species with Single competitivelyto first species to similar life history superior speciesestablish traits

~_-_.-

year for common wind- or animal-dispersed forest species of eastern

North America39. The tree speciesthat form monodominant stands inmature tropical rain forest haveheavier seeds and many are withoutanimal dispersal agents. Their rangeexpansion woul d accordingly beslower.

Subsequent to a regional extinc-tion, the local forest canopies wouldcontinue to be composed of lessshade-tolerant, more vagile speciesuntil they were invaded by slow-dispersing, more shade-tolerant

species. Accordingly, Whitmoresuggested that Central Americamight be in a stage of arrestedsuccession. The extensive pre-Columbian agriculture on forestlands may have drastically reducedthe propagule sources of mature-phase trees. Presumably, well-dispersed mid-successional speciesof similar life history traits remainedin the region.

Human dis turbance is not theonly imaginable cause of local ex-

tinctions in the tropics. In Africa, ason other tropical continents, therehave been marked changes in thetotal extent of rain forest area overthe last 15 000 years. These vari-ations have been associated withwet and dry climatic cycles40,4’. Thelocal composition of the mature-phase forest that re-establishedduring wet periods would havebeen dependent on which treespecies survived intervening dryperiods in small pockets main-

taining suitable climatic conditions.The more shade-tolerant, slow-growing rainforest species oftenhave relatively restricted distri-butions4*. The size of the area overwhich a species occurs and the ex-tent of the stands that it forms mayreflect its dispersal potential rela-tive to the time elapsed since re-

lease from conditions unfavorablefor dense forest growth. If such a

species is a self-replacing competi-tive dominant, then the compo-sition of old-growth forest in thearea where it occurs is determinedby its unique presence in thespecies pool. The extent of mono-dominance is, thus, the expressionof the slow expansion of such aspecies from remnant populations.

ConclusionDominance in early rainforest

succession may be established

rapidly by a single species sub-sequent to its fortuitous massiveestablishment. At a late stageof succession, monodominance isagain possible if the life historytraits of a single species render itthe competitive dominant (seeTable 31. Monodominance is leastlikely during the mid-successionperiod, as has been previously pro-posed by the ‘intermediate distur-bance’ hypothesis12,31.

The presence of numerous

species with similar life history traitsmitigates against dominance by anysingle tree species. The number ofco-occurring species may be re-duced by environmental stressesthat preclude survival of somespecies in a given system, or bylocal extinctions that reduce thespecies pool. The impoverishedassemblage of poorly dispersed,late-succession species continuesto reflect the impact of local ex-tinctions after populations of more

vagile species have converged. Theabsence of such species delaysprogress towards monodominance.Because late-succession speciesoften have localized distributionsand slow invasion rates, it is likelythat the monodominant stands theyform will expand only in regions un-disturbed over long periods.


In order to construct a completecontext in which to examine the dy-namics of a community of long-livedorganisms, such as rainforest trees,sufficient historical informationmust be available to allow a per-spective that encompasses eventspertinent to succession within thecommunity and movement of slowlydispersing organisms in and outof the community. In temperateregions, where the impact ofPleistocene climate change on thecomposition of vegetation has beenthe subject of much recent research,the importance of propagule avail-

ability subsequent to climate shiftshas been well documented39,43. Themethods for such studies are onlynow being worked out for moisttropical areas, but the results mayhelp to clarify the processes thathave led to the variable diversityand dominance of tropical rainforests.

ReferencesI White, F. I 1983)Vegetation Map of AfricaSouth of the Sahara (2nd edn), UnescolAETFAT/UNSO2 Whitmore, T.C. I I9841 Tropical RainForests of the Far East (2nd edn 1,Clarendon Press3 Gentry, A.H. (1982)Evol. Biof. 15, I-844 Richards, P.W. II9521 The Tropical RainForest, Cambridge University Press5 Hart, T.B., Hart, I.A. and Murphy, PG.(1989) Am. Nat. 133,613-6336 Connell, J.H. and Lowman, M.D.Am. NatIin press)7 Louis, j. (1947) in Comptes Rendus de laSemaine Agricole de Yangambi Idu 26fevrier au 5 mars 19471, pp. 902-915, Publ.Inst. Nat1 Etude Agron. Congo (Hors S&iel8 Lorimer,C.(l9801 Ecofogybl, 1169-11849 Hall, I.B. and Swaine, M.D. I1981 1Distribution and Ecology of Vascular Plantsin a Tropical Rain Forest: Forest Vegetationin Ghana, JunkIO Ashton, P.S. (19771 Ann. MO. Bot. Card.64,694-705II Ianzen, D.H. (19741Biotropica 6, 69-10312 Huston, M. 119791Am. Nat. I I?, 81-101I3 Swaine, M.D. and Hall, J .B. (I981 1 nTheBiological Aspects of Rare PlantConservation (Synge, H., ed.1, pp. 355-363,Wiley & SonsI4 Connell. I.H., Tracey, I.C. and Webb, L.I(1984) &co/. Monogr. 54, 141-164

I5 Augspurger. C.K. ( 19841Ecology 65,1705-1712I6 Clark, D.A. and Clark, D.B. II9841Am. Nat.124, 769-788I7 Denslow, J.S. (19871 Annu. Rev. &of. Syst.18. 431-451I8 Boucher. D.H. ( I98 I tOecologia 49,409-4 I 4I9 Augspurger, C.K. II981 1Ecology 62.775-78820 Abrahamson, W.C and Hartnett. D C. in

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Ecosystems of Florida (Myers, R.L. andEwe\, J.I., edsl, Academic Press (in press)21 Read, 1. and Hill, R.S. (1988) 1.Ecol. 76,558-584

22 Walker, D. (19821 in The PlantCommunity as a Working Mechanism(Newman, E.I.. ed.), pp. 27-43, Blackwel lScientific Publications23 Hartshorn, G.S. (19881 in North AmericanTerrestrial Vegetation (Barbour, M.G. andBillings, W.D., edsl, pp. 365-390. Cambr idgeUniversity Press24 Lieberman. M., Lieberman, D.. Hartshorn,G.S. and Peralta, R. ( 1985) /. Ecol. 73,505-51625 Marois, K.C. and Ewel, K.C. (1983)ForestSci. 29v627-64026 Lugo, A.E.( I9801 Biotropica I2 (Suppl.l,65-7227 Huston. M. and Smith , T. 119871Am. Nat.

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Hypothesesor the Evolution fOver the last decade, new hypotheses havebeen proposed for the evolution of dioecy iMplants. Most of the selective mechanismsinvoked have been suggested and supportedby phylogetietic correlations. Here we re-view ( I) the validity of the correlations(especially in light of recent critiques of thecomparative method], and (2) the conform-

ity of the proposed mechanisms to empiri-cal data. None of the hypotheses can beflatly rejected on existing evidence, but thestrength of their support varies. Futurecorrelational studies nzust explicitly con-sider phylogeny; more importantly, suchbroad studies should also 6e supplementedby detailed studies of particular lransitionsto dioecy (e.g. within genera) - studies ofthe sort that have clar$ed analogous issuessuch as heterostyly.

Any evolutionary change that hasoccurred independently in nu-merous lineages is likely to offerinsight into fundamental mechan-isms of evolution. When that changeis one that Darwin confessed tofinding ‘much difficulty in under-standing”, it gains the statureof a central problem in biology.The evolution of dioecy from her-maphrodite ancestors is such aproblem. An obvious conseque nceof separate sexes is the impossi-bility of selfing. Thus, the avoid-ance of inbreeding has traditionallybeen invoked as an importantselective force in the evolution ofdioecy2-4 (despite an early caution

lames Thomsonand lohanne Br unet are at the Deptof Ecol ogy and Evo lution, State University of NewYork. Stony Brook, NY 11794,USA

Dioecyn SeedPlantJames D. Thomsonand JohanneBrunet

by Darwin’). Starting about t en

years ago, however, a number ofalternative hypotheses have beenpresented5-‘I. These hypothesesusually have two parts, a correlationand a mechanism. The correlationsare phylogenetic: dioecious taxa aremore likely t o exhibit fleshy ‘fruits’(sensu late), the woody habit, smalland inconspicuous flowers, islandhabitats, or heterostyly. Some ofthese correlations date to Darwin,but most have been described onlyrecently. The mechanisms typicallyinvoke ecological circumstancesthat favor dioecy in ways specifiedby theoretical models of sexualselection and sex allocation theory.

Here, we discuss the currentstatus of these proposal s and theprogress made over the last decade.We consider several pairs of corre-lations and mechanisms, assessingboth the validity of the correlationand the adequacy of the mechanism.We do not dwell on ‘pathways todioecy’ or on population geneticmodels12-16, although a full in-terpretation of the correlationsmust include genetic constraints.

General difficulties with correlationsRecent critiques of the compara-

tive method have established stan-dards of rigor matched by few of theearly papers concerning dioecy17,18.

First, because most authors were

typically concerned with only asingle relationship, covariationamong the ‘driving’ characters wasusually ignored, with the risk thatspurious or indirect correlationsmight have suggested incorrectcausal relations. Muenchow” andCharlesworth’ discuss this generalstatistical problem with particularrespect to dioecy arguments.

Second, the statistical signifi-cance of phylogenetic correlationsis hard to assess because of non-independence of taxa within lin-eages; Pagel and HarveyI reviewseveral recent proposals for solvingthis difficulty. Importantly, the‘sample size’ should reflect thenumber of evolutionary eventsrather than taxa. Thus a genus con-taining five species, all dioeciousand all woody, is properly countedas only one datum for a correlationanalysis, not five. For testing aparticular mechanism, the relativeorder in which the correlated traitsoriginated in a lineage is also im-portant: Donogh ueZO discusses thisand other issues with particular ref-erence to the correlation betweendioecy and fleshy fruits. None of theother correlations discussed belowhave received this level of scrutiny.Ideally, testing for correlation oftraits requires mapping those traits

(C 1990 Elsev~er Scercp Publishers L k? IlJKi 0169~5347,90:$02 00 11

1990_monospecific dominance in tropical rain forests

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