baker growth and func composition

8/14/2019 Baker Growth and Func Composition

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Variation in tropical forest growth rates:combined effects of functional group compositionand resource availability

Timothy R. Baker1,2,3,*, Michael D. Swaine1 & David F.R.P. Burslem1

1 School of Biological Sciences, University of Aberdeen,Aberdeen, UK2 Max-Planck-Institut fr Biogeochemie, Jena, Germany3 Centre for Biodiversity and Conservation, School of Geography, University of Leeds, UK

Received: 12 February 2003 Revised version accepted: 28 March 2003

Abstract

Rates of tree growth in tropical forests reflect variation in life history strategies, con-tribute to the determination of species distributional limits, set limits to timber harvestingand control the carbon balance of the stands. Here, we review the resources that limit treegrowth at different temporal and spatial scales, and the different growth rates and re-sponses of functional groups defined on the basis of regeneration strategy, maximum size,and species associations with particular edaphic and climatic conditions.

Variation in soil water availability determines intra- and inter-annual patterns of growthwithin seasonal forests, whereas irradiance may have a more important role in aseasonalforests. Nutrient supply limits growth rates in montane forests and may determine spatialvariation in growth of individual species in lowland forests. However, its role in determin-ing spatial variation in stand-level growth rates is unclear. In terms of growth rate, wepropose a functional classification of tropical tree species which contrasts inherently fast-growing, responsive species (pioneer, large-statured species), from slow-growing speciesthat are less responsive to increasing resource availability (shade-bearers, small-staturedspecies). In a semi-deciduous forest in Ghana, pioneers associated with high-rainfallforests with less fertile soils, had significantly lower growth rates than pioneers that aremore abundant in low-rainfall forests with more fertile soils. These results match patternsfound in seedling trials and suggest for pioneers that species associations with particularenvironmental conditions are useful indicators of maximum growth rate.

The effects of variation in resource availability and of inherent differences between specieson stand-level patterns of growth will not be independent if the functional group compo-sition of tropical forests varies along resource gradients. We find that there is increasingevidence of such spatial shifts at both small and large scales in tropical forests. Quantify-ing these gradients is important for understanding spatial patterns in forest growth rates.

Key words: irradiance, maximum size, nutrient supply, pioneer, regeneration groups,water availability

1433-8319/03/6/01-02-021 $ 15.00/0

*Corresponding author: Centre for Biodiversity and Conservation, School of Geography,University of Leeds LS2 9JT, UK;e-mail: [email protected]

Vol. 6/1,2,pp. 2136 Urban & Fischer Verlag, 2003http://www.urbanfischer.de/journals/ppees

Perspectivesin Plant Ecology,Evolution andSystematics


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Introduction

An understanding of the patterns of tree growth is afundamental goal of ecological research in tropical

forests. Interspecific variation in maximum potentialgrowth rate consistently emerges as one of the mostimportant factors in the definition of robust functionalgroups, as growth rate integrates numerous traits thatunderlie trade-offs among strategies for resource ac-quisition, defence against natural enemies, and alloca-tion to reproduction. Such groups provide practicaland meaningful classifications of tropical forestspecies, which are needed both by foresters, for mod-elling growth and yield, and by ecologists, to explainthe life history diversity in tropical forest trees (Van-clay 1994; Richards 1996; Whitmore 1998; Turner2001). In addition to these inherent differences be-tween species, growth also varies with resource avail-ability. At the species level, this variation may help toexplain the limits to species distributions (e.g. Gu-natilleke et al. 1996; Veenendaal et al. 1996a). At thestand level, understanding the environmental factorsthat control tropical forest productivity is critical forquantifying the carbon balance of tropical forests.

Spatial variation in stand-level growth rates will de-pend on both variation in resource availability andany differences in the functional composition of tropi-cal forests. The large variation in forest compositionand dynamics at both small and large scales (Phillips

et al. 1994, in press; Burslem & Whitmore 1999, inpress; ter Steege et al. 2000) suggests that there may be

important differences between tropical forests in therelative abundance of different functional groups.These differences may be as important as gradients inresource availability for determining current and fu-

ture patterns of forest productivity.Building on the writings of Budowski (1965), Tim

Whitmore made an important contribution both to thedescription of tropical tree functional groups and tohighlighting their significance to central questions oftropical forest ecology (Whitmore 1974, 1975, 1998).He also drew attention to the relationship betweenplant functional traits, including growth rate, andtropical forest silviculture (Whitmore 1975). Whit-mores promotion of a fundamental dichotomy be-tween fast-growing, gap-demanding tree species (la-belled pioneers) and slow-growing, non-gap-deman-ders (non-pioneers or climax species) is, perhaps,one of his best known and most frequently cited con-tributions (Whitmore 1975, 1984, 1998; Swaine &Whitmore 1988). This perspective was undoubtedlyinfluenced by Whitmores own research on the dynam-ics and growth rates of seedlings, saplings and largetrees of the twelve most common large tree speciesgrowing on his plots on Kolombangara in theSolomon Islands during the period 19641971 (Whit-more 1974). Based on an initial seven-year study ofseedling responses to canopy openings, Whitmore(1974) classified these twelve species into four groups(Table 1) and emphasized the importance of differ-

ences in growth rate between species as a determinantof group membership. A link between the four groups

22 T. R. Baker et al.

Perspectives in Plant Ecology, Evolution and Systematics (2003) 6, 2136

Table 1. Characteristics of the twelve species studied since 1964 in lowland tropical rain forest on Kolombangara, Solomon Islands. The four species groupsamong the twelve common timber tree species are classified according to the conditions required for seedling establishment and onward growth and arebased on observations over 6.6 years over the interval 19641971 (Whitmore 1974). Nomenclature follows sources described in Burslem & Whitmore (1999).

Shade-tolerance Species Conditions Conditions Wood densityclass to establish to grow up (kg m3)1

I Dillenia salomonensis High forest High forest 550Maranthes corymbosa High forest High forest 720Parinari papuanassp. salomonensis High forest High forest 660

Schizomeria serrata High forest High forest 490

II Calophyllum neo-ebudicum High forest or small gaps High forest/gaps 500Calophyllum peekelii High forest High forest/gaps 480Pometia pinnata High forest or disturbed High forest 590

or ?small gaps

III Campnosperma brevipetiolatum High forest or gaps Gaps 330Elaeocarpus angustifolius High forest Gaps 350

IV Endospermum medullosum Mostly gaps Gaps 370Gmelina moluccana Mostly gaps Gaps 410Terminalia calamansanai High forest, soon dying Gaps 460

except in gaps

1Data from Anonymous (1976, 1979).


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defined for the twelve species growing on Kolomban-gara and the dichotomy proposed in his later writingscan be made if the three species in Group IV of Table 1are treated as pioneers, and the remaining species as

non-pioneers.Since the mid 1970s, there has been a proliferation

of research on the characteristics that define the mainfunctional groups of tropical trees and their relation-ship to forest dynamics and regeneration, expandingand extending the ideas of Whitmore and his predeces-sors and contemporaries. Some authors have ques-tioned the existence of a fundamental dichotomy oflife history types among tropical trees (e.g. Alvarez-Buylla & Martinez-Ramos 1992; Grubb 1996), andthe issue has been comprehensively reviewed severaltimes (Brokaw 1985; Denslow 1987; Brown & Jen-nings 1998; Brokaw & Busing 2000; Turner 2001;Burslem & Swaine 2002). Here, we specifically exam-ine how useful these concepts are in understandingvariation in tree growth rates over gradients in re-source availability. We consider the following specificquestions:

1. What is the evidence for resource limitation oftropical tree growth?

2. How do functional groups defined in variousways differ in their growth responses to resource avail-ability?

3. Are there gradients in the functional-group com-position of tropical forests, and are they important in

determining variation in stand-level growth?We consider each of the major resources (water and

irradiance) or group of resources (nutrients) known tolimit plant growth over spatial gradients, both sepa-rately, and, where possible, in combination. We adopta broad definition of growth rate in order not to im-pose severe limitations on the scope of the review, andemphasize evidence from field-based studies of adulttrees. Thus we include studies of litter fall, fine-rootproduction, leaf-level photosynthesis, and phenologyas well as direct measures of trunk growth based onmeasurements of diameter change or the width of an-nual rings.

Factors limiting tree growth

Water

The total amount of rainfall is one of the most impor-tant factors setting the limits to the distribution offorests as opposed to woodland or thicket in the trop-ics (Holdridge 1967; Walter 1979; White 1983; Wood-ward 1987). However, the forested regions experienceconsiderable spatial and temporal variation in theavailability of soil water that acts as a major limiting

factor on overall rates and temporal patterns ofgrowth.

The importance of soil water availability is most ap-parent within forests with strongly seasonal climates.

Over ten years in dry forest in Mexico (mean annualrainfall 707 mm) the annual increment of two decidu-ous species correlated with rainfall during the midwet-season (Bullock 1997). Within the same forest,over a five-year period when annual rainfall rangedfrom 485 to 1331 mm, Whigham et al. (1990) foundthat the annual production of leaf litter correlated pos-itively with annual rainfall and that the mean basalarea increment per tree correlated positively with totalrainfall during the previous two years. Soil wateravailability also controls the timing of growth withinseasonal forests. For the evergreen species, Exostemacaribaeum, in dry forest in Puerto Rico (mean annualrainfall 929 mm), Lugo et al. (1978) found maximumdaily rates of photosynthesis were five times higherduring the wet season compared to the dry season. Inaddition, marked fluctuations in tree girth in parallelwith monthly rainfall were described by Swaine et al.(1990) for very dry tropical forest in Ghana (c. 750 mmyr1), where seasonal variation in girth was about tentimes greater than the underlying annual increment inMillettia thonningii. Direct measurement of wood pro-duction in seasonal forest from examination of thepattern of cambial activity, by measuring either thewidth of the band of differentiating xylem which

stains for cellulose (Amobi 1973), or the width of un-lignified xylem (Lowe 1968), has also demonstratedthe importance of increased soil water availability forthe initiation of growth in seasonal forests (Borchert1999).

Soil water availability also influences the timing andamount of growth in forest with substantially highermean annual rainfall than the previous examples. Forinstance, in a semi-deciduous forest in Venezuela(mean annual rainfall 1700 mm), using tree ringchronologies of seven species, Worbes (1999) reportedpositive correlations between annual rainfall andmean annual growth rates, and at three sites in season-

al forest in Panama, Devall et al. (1995) found that an-nual rainfall correlated with variation in tree ringwidth for three species. In contrast to these correlativestudies, field experiments that directly test whetherwater supply limits growth in a particular forest arerare. However, an irrigation experiment over five dryseasons in semi-evergreen forest in Panama (mean an-nual rainfall 2600 mm) showed that ameliorating theseasonal drought could increase fine-root productionand leaf longevity, and influence phenology. Dry sea-son community-level fine-root production, measuredusing in-growth cylinders with root-free soil, was fivetimes greater in irrigated plots than in control plots

Variation in tropical forest growth rates 23



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tree Trichilia tuberculata, were half as low in slopecompared to plateau positions. In addition, in season-ally dry forest in Costa Rica, species such as Astroni-um graveolens, which occur in moist localities, are

able to maintain cambial activity into the dry seasonand are leafless only for a short period, whereas girthincrement ceases during the dry season in deciduousspecies in drier sites (Borchert 1999). In both exam-ples, greater water availability in lower topographicpositions improves conditions for tree growth.

Irradiance

Irradiance declines exponentially with decreasingheight in tropical forests (Yoda 1978) and increasedcanopy illumination has a clear, positive effect on treegrowth. For example, in moist evergreen forest inPanama, saplings of ten species showed greater heightgrowth in high-light environments (King 1994) and atLa Selva, Costa Rica, positive correlations were foundbetween growth rate and crown illumination categoryfor eight species in size classes up to 30 cm diameter(Clark & Clark 1992). For large trees, many studieshave used Dawkins (1958) classification of tree crownposition in the canopy to show effects on tree growth(e.g. Korsgaard 1986; Silva et al. 1995; Alder & Silva2000). For example, in individuals of Carapanicaraguensis, 3040 cm in diameter in swamp forestin Costa Rica, Webb (1999) showed that median di-

ameter increments were significantly higher in highercrown-score classes. Also, in a study of 15 species intropical forest in Puerto Rico (mean annual rainfallrange 25004500 mm), Parresol (1995) demonstratedthat maximum growth rates were five times higher indominant trees than in trees in the suppressed crown-class categories.

Variation in irradiance also influences temporal pat-terns of growth, and may be particularly important inaseasonal forests, where water availability is not limit-ing. For instance, in the absence of any correlation ofgrowth with rainfall at La Selva, Costa Rica (mean an-nual rainfall 3659 mm), Clark & Clark (1994) sug-

gested that inter-annual variation in irradiance deter-mined the consistent long-term growth patterns ofadult and juvenile trees. In addition, studies of pheno-logy have indicated that trees may time the productionof new leaves during the months of the highest irradi-ance, if water supply is not limiting. Wright & vanSchaik (1994) found that in two weakly seasonalforests, at La Selva, in Costa Rica and at the DuckeReserve in central Brazil, the number of species thatcentred leaf production in the three-month period ofhighest irradiance was significantly greater than ex-pected by chance. Also, they found that in four season-al forests, two thirds of deep-rooted species flushed

(Cavelier et al. 1999), and dry season leaf fall was de-layed for two out of nine tree species (Wright &Cornejo 1990). In addition, for three shrub species,the proportion of leaves retained, of those that were

newly flushed at the start of the experiment, was ap-proximately 20% higher over the first two years in theirrigated plots (Mulkey et al. 1993). However, this ex-periment also demonstrated that not all aspects ofgrowth, and not all species, are limited by seasonalwater shortage in this forest. Irrigation did not affectcommunity level leaf-litter production (Cavelier et al.1999), stem diameter growth of five shrub species(Wright 1991), or the timing of leaf fall for seven outof nine study species (Wright & Cornejo 1990).

There is mixed evidence on whether water supplysubstantially limits growth in forests growing in asea-sonal climates, where annual variation in soil wateravailability is minimal. At La Selva in Costa Rica (meanannual rainfall 3859 mm), Hazlett (1987) found thatthe lowest rates of girth change for two tree species,Carapa guianensis and Goelthalsia meiantha, occurredduring the driest period of the year, and at a well-drained site; Breitsprecher & Bethel (1990) found thatcessation of growth for five out of eight species was alsoassociated with the drier part of the year. However, inthe same forest, Clark & Clark (1994) found that varia-tion in growth rate failed to correlate with variation inrainfall over eight years, for both adult trees and juve-niles. In another forest in Costa Rica (mean annual

rainfall 3970 mm), a negative correlation was found be-tween rainfall and shoot growth rate of a liana species,Passiflora pittieri (Longino 1986).

All the studies described above concentrate on sin-gle sites; forest growth in the tropics has rarely beencompared along rainfall gradients. However, Harring-ton et al. (1995) examined the growth ofAcacia koaalong an altitudinal gradient in Hawaii, where annualrainfall ranged from 8501800 mm. These authorsfound that increment in aboveground woody biomassincreased as phyllode 13C values became more nega-tive, but was not correlated with phyllode nutrientconcentrations, suggesting that water rather than nu-

trient availability limited growth. Soil water availabili-ty also varies at small spatial scales, differing betweentopographic positions in both evergreen and semi-de-ciduous tropical forests (Becker et al. 1988; Dawset al. 2002; Green & Newbery 2002; Baker et al.2002, 2003) but the influence of these differences ontree growth has rarely been studied. However, topo-graphic variation in soil water availability does influ-ence plant water relations and patterns of cambial ac-tivity in seasonal forests. Becker et al. (1988) demon-strated that during the dry season in a semi-evergreenforest in Panama, pre-dawn water potentials of theshrub Psychotria horizontalis and of saplings of the




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during the dry season, when irradiance was highest.Finally, results from a biogeochemical model of forestproductivity also suggested that light may limit growthin aseasonal forests, as a decline in modelled estimates

of net primary productivity at the wettest sites along atransect in Brazilian Amazonia was attributed to re-duced irradiance (Potter et al. 1998).

Nutrients

Most tropical forests grow on relatively nutrient-poorsoils. The effect of soil fertility on growth has thereforebeen a focus of much experimental work, and fertilisa-tion experiments on adult trees in natural forests pro-vide some evidence that nutrient supply does limitgrowth rates. In montane forest in Venezuela, Tanneret al. (1992) demonstrated that trunk growth of allspecies approximately doubled in plots fertilized withN and P, and in montane forest in Colombia, N and Pfertilization also significantly increased growth for twoout of three species (Cavelier et al. 2000). On soils ofvolcanic origin in montane forest in Hawaii, Vitouseket al. (1993) demonstrated that N limited growth onthe two youngest sites (30 cm), and soil nu-trient status across 13 plots in high-rainfall forests in

Borneo. However, neither of these studies comparedgrowth rates across the large differences in soil fertilitythat are found along regional gradients of rainfall, anddifferences in site fertility on this scale do influenceplantation performance. In stands of teak (Tectonagrandis) more than 10 years old in West Africa, for ex-ample, total N in the topsoil (010 cm) and rootingdepth were the most important factors determiningvariation in growth (Drechsel & Zech 1994). Also, forplantations ofTerminalia ivorensis across seven forestreserves in Ghana (mean annual rainfall 12801650mm), soil total N and C concentrations, cation ex-change capacity and exchangeable Ca and Mg concen-

trations were significantly negatively correlated withthe degree of die-back, a condition that leads to wilt-ing, chlorotic leaves, poor growth and high mortality(Agyeman & Safo 1997). Plantation studies have also

indicated that variation in nutrient supply may be im-portant over topographic gradients. Variation ingrowth of teak over a catena in the rain forest zone ofLiberia (mean annual rainfall 2553 mm) was relatedmost strongly to variation in soil pH and percentagebase saturation (Zech & Drechsel 1991).

Experimental studies of seedling growth alsodemonstrate that regional and topographic gradientsof soil fertility can cause differences in growth of indi-vidual species. Veenendaal et al. (1996a) studiedseedling growth in a range of irradiances in well-wa-tered pots of soils from semi-deciduous (pH >6.1) andevergreen forest (pH


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tion experiments in the field appears to depend on theinherent fertility of the soil and the magnitude of dif-ference in irradiance between gap and understoreytreatments. For example, Dalling & Tanner (1995)

found a response to fertilisation of seedlings of threespecies transplanted onto nutrient-poor landslides inJamaica under high irradiance, but no effect of fertili-sation in the understorey. However, Fetcher et al.(1996) found no difference in the effect of fertilisationin a comparison of gap centre and gap edge sites on alandslide in Puerto Rico. In contrast, Denslow et al.(1990) found no effect of fertilisation in either gap orunderstorey conditions for seven species of shrubs onmore fertile soils at La Selva, Costa Rica.

Other interactions, between light and water supply,or water and nutrient supply have received even lessattention, even for pot-grown seedlings, and therehave been very few field-based studies. However, Fish-er et al. (1991) showed a positive interaction betweenwater supply and irradiance on height growth and leafarea production ofVirola surinamensis seedlings in anirrigation experiment in semi-evergreen forest in Pana-ma. An interaction between nutrient supply and wateravailability may be important in determining differ-ences in the spatial pattern of tree growth observed indifferent years. Baker et al. (2003) studied diametergrowth of trees >20 cm diameter of two species overtwo years in semi-deciduous and evergreen forest inGhana. During the first year, when there was similar,

low rainfall in both sites, growth did not differ be-tween forests. However, during the second year, whensoil water availability was generally higher at bothsites, growth was greater in the semi-deciduous than inthe evergreen forest. This difference between the twosites, apparent only when there was sufficient rainfall,was attributed to the higher soil nutrient availability insemi-deciduous forest.

In summary, within tropical rain forests, it is evi-dent that water availability is an important influenceon tree growth rates, particularly in seasonal forests,where it determines both the inter- and intra-annualpatterns of growth. However, it is less clear whether

the substantial spatial variation in soil water availabil-ity between different tropical forests, or the smallerfluctuations in soil water availability within aseasonalforests, determine important differences in treegrowth. Variation in irradiance is the primary factorthat limits plant growth within forest stands, and pos-sibly over long timescales for aseasonal forest as awhole. Variation in soil fertility appears to be impor-tant for determining variation in the growth rates ofsome species, but may have a smaller role in control-ling overall stand-level patterns of growth. However,truly broad-scale comparisons from a large number ofsites are currently lacking.

Tree growth and functional groups

We now consider variation in tree growth from the per-spective of differences between functional groups. Afunctional group can be defined as a suite of speciesthat share similar species-specific patterns (i.e. evolvedtraits, not phenotypic) of resource use, a similar re-sponse to disturbance, or a similar range of growth,mortality and recruitment rates (Gitay & Noble 1997).By recognising groups of species that share suites of co-varying characteristics we may be able to scale-up fromthe well-studied responses of few species, to modelcommunity- or stand-level responses to perturbationssuch as climate change or tree harvesting (Vanclay1994; Condit et al. 1996). The main purpose of recog-nising aggregations of traits in life histories is thus to

provide a semi-quantitative foundation for these prac-tical objectives, while in practice most ecologists em-phasise continua rather than discontinuities in thespectrum of life histories of coexisting species.

Turner (2001) identified regeneration class andmaximum height as the primary factors that differenti-ate tropical tree species, and below we review brieflythe evidence for trends in growth rate and response toresource availability among functional groups definedin these ways. Finally, we propose a new way of defin-ing a functional group, based on differences amongspecies in their distribution at large spatial scales in re-spect of soils and climate, and illustrate differences

among groups defined in this way for trees growing atone site in semi-deciduous forest in Ghana.

Groups defined by regeneration strategy

The major axis of differentiation in ecological charac-teristics used to separate species in tropical forests hasbeen related to light requirements for regeneration, be-cause light is the primary limiting factor for growthrate within a forest stand, and because it is possible toallocate species on the basis of field observation alone.Species that require the high light environment of agap for seed germination and/or establishment (pio-

neers), are separated from species that are able to es-tablish under canopy shade (non-pioneers) (Swaine& Whitmore 1988; Whitmore 1989). These two cate-gories mark sections on what is now agreed to be acontinuum of responses to the range of light environ-ments found on the forest floor (Swaine & Whitmore1988; Alvarez-Buylla & Martinez-Ramos 1992).

Many studies have examined growth responses oftropical tree seedlings with differing regeneration strate-gies to variation in irradiance (e.g. Thompson et al.1992; Lehto & Grace 1994; Veenendaal et al. 1996a).This work has shown that under high-light conditions,pioneers have higher growth rates than non-pioneers.




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For example, in a comparison of Ghanaian treeseedlings, three pioneer species (Terminalia ivorensis,Milicia excelsa and Albizia zygia), all had higher relativegrowth rates than a group of five non-pioneer shade

bearers (Strombosia glaucescens, Cynometra ananta,Guarea cedrata, Celtis mildbraedii and Chrysophyllum

pruniforme) at 16% of ambient irradiance (Veenendaalet al. 1996a). At lower light levels, whether pioneershave higher growth rates than non-pioneers appears todepend on exactly how the comparison is performed. Acompilation of the results of seedling growth studies of194 species grown under contrasting light regimesfound that pioneers and light demanding non-pioneerspecies had higher relative growth rates than moreshade-tolerant species, at up to 5% irradiance(Veneklaas & Poorter 1998). However, 5% irradiance isgreater than the compensation point of all tropical treesso far tested, and when lower irradiances are included inexperiments (e.g. Agyeman et al. 1999) pioneers arefound to grow more slowly than shade-bearers, and typ-ically show negative growth at 2% irradiance. Thetimescale of the experiment also influences the interspe-cific differences that are observed (Sack & Grubb 2001).When measured over short periods in low irradiance,seedlings of light demanding species may have highergrowth rates than more shade-tolerant species, due tothe higher growth relative growth rates associated withsmaller seed sizes. However, over longer timescales,shade-tolerant species are expected to out-perform light

demanders (Sack & Grubb 2001).Amongst adult trees in the field, pioneer species are

usually found to grow faster than more shade-tolerantspecies, presumably because they both have higher in-trinsic growth rates at a given irradiance, and becausethey are found in high-light sites. Swaine (1994) re-ported growth rates of pioneer trees in semi-deciduousforest in Ghana more than double those of any moreshade-tolerant group, and in semi-evergreen forest inPanama, Condit et al. (1996) found that species colo-nizing index, defined as the proportion of recruitsfound in light gaps, was positively correlated withspecies growth rates in the 1020 cm diameter class.

However, adult tree growth rate is not always simplyrelated to regeneration strategy. For example, Miltonet al. (1994), working in semi-evergreen forest inPanama, compared the growth rate of two groups ofspecies, defined on the basis of whether recruitmentwas significantly higher, or did not differ, between lowand high canopy sites, based on previous work byWelden et al. (1991). Over 13.6 years, for trees >19.1cm diameter, growth rates were significantly higher inspecies whose regeneration was not related to lowcanopy sites. This complexity is at least partly causedby the considerable variation in growth rate that isfound in non-pioneer species beyond the seedling stage

due to changes in species light requirements during on-togeny (Clark & Clark 1992, 1999). For example,many species that are shade-tolerant as seedlings re-quire a large increase in canopy illumination as

saplings to reach the canopy (Jones 1956; Clark &Clark 1992; Hawthorne 1995). In addition, othershave noted small-stature species whose seedling estab-lishment requirements match those of pioneers, butwhich later in life tolerate deep shade, and behave asshade-tolerant understorey trees, such as the crypticpioneers of Hawthorne (1995, p. 16). An analogousontogenetic shift in light requirement is displayed bythe small-seeded canopy tree Alseis blackiana on BarroColorado Island, Panama, which establishes only incanopy gaps but persists for several years in the shadeafter canopy closure (Dalling et al. 2001).

In addition to higher growth rates at high irradi-ance, pioneer species also have greater photosyntheticplasticity and show greater growth responses to in-creased irradiance than shade-tolerant species. A com-parison of the range of maximum photosyntheticrates, under high and low light, for species subjectivelydescribed as early- and late-successional (16 and 24species, respectively), showed that early-successionalspecies have a greater range in Amax values than late-successional species, because of significantly highervalues under high light (Strauss-Debenedetti & Bazzaz1996; Thomas & Bazzaz 1999). For adult trees in thefield, Welden et al. (1991) working in a semi-evergreen

forest in Panama, noted that increased growth in lowcompared to high canopy sites was a particular featureof six pioneer species.

Nutrient addition experiments with seedlings showsimilar patterns to those with irradiance, with agreater response in pioneer and early-successionalspecies. Huante et al. (1995) demonstrated that threeearly-successional species from a deciduous forest inMexico showed a greater proportional increase inbiomass (3.7124 fold increase) between low and high(0 and 41 ppm) P treatments, than four late-succes-sional species (1.22.4 fold increase). In addition,Raaimakers & Lambers (1996) showed that the

biomass of a pioneer species from Guyana, Tapiriraobtusa doubled over six months at high (>250 mg Pper plant) compared to low (


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Groups based on maximum height

A second axis of differentiation amongst tree species intropical rain forest, related to the vertical gradient in

irradiance, is caused by differences in maximumheight. Species with low maximum heights typicallyhave low growth rates. For example, in semi-decidu-ous forest in Ghana, Swaine (1994) found that meanannual diameter-increment of large shade-tolerantspecies was double that of small-stature species, and inSungei Menyala Forest Reserve in Malaysia,Manokaran & Kochummen (1987) found that meanannual diameter increments of understorey specieswere less than 2 mm yr1, compared to incrementsgreater than 3 mm yr1 for emergent species. Growthrates are also less variable in species with low maxi-mum heights. At La Selva, Costa Rica, Lieberman &

Lieberman (1987) demonstrated that total variation ingrowth rate is approximately five times greater inshade-tolerant canopy species than in understoreyspecies.

Distinguishing whether these patterns are caused bya correlation between tree diameter and absolute mea-sures of diameter growth, lower levels of crown illumi-nation for smaller trees, or because small trees havelower inherent growth rates under similar levels of ir-radiance, requires comparisons that control for tree di-ameter and the light environment. In Pasoh Forest Re-serve, Malaysia, using asymptotic height derived from

height/diameter relationships as an estimator of maxi-mum species height, Thomas (1996) found a linearcorrelation (r2 = 0.56, P < 0.001) between maximumheight and mean annual growth rate of adult trees for38 species. In addition, the same positive correlation(r2 = 0.20, P < 0.01) was found using the growth ratesof saplings (12 cm diameter) rather than adult trees,suggesting that the relationship is not confounded byvariation in tree diameter. Also, in a comparison ofphotosynthetic characteristics of similar-sized saplings,under similar light conditions, of species with differentasymptotic heights, smaller-statured species werefound to have an inherently lower leaf level photosyn-

thetic capacity (Amax), compared to species withgreater maximum height, within the same genus(Thomas & Bazzaz 1999).

Both inherently lower diameter growth rates andlower levels of crown illumination therefore charac-terise species with low maximum heights. However, itis important to note that all of the above studies referpredominately to shade-tolerant tree species. Thesespecies establish in the understorey and therefore ex-perience increasing light levels as they increase in size.This pattern will inevitably lead to increased growthrates in larger individuals, and, on an evolutionarytimescale, favour increased capacity for growth in tall-

statured species (Thomas & Bazzaz 1999). In contrast,pioneer species establish under high light conditions,so there will not be a positive correlation between lightavailability and plant size. Therefore, similar ecologi-

cal or evolutionary arguments for faster growth inspecies with greater maximum height are unlikely toapply to pioneers (Thomas & Bazzaz 1999).

Groups defined by species associationswith specific environmental conditions:a test from the forest zone of Ghana

A third axis of differentiation of tropical forest speciesmay relate to the associations between species distri-butions and climatic and edaphic factors. Species dis-tribution in respect of edaphic factors has beendemonstrated to be a useful predictor of growth ratesin studies of temperate plants, where species from dif-ferent habitats have been grown under the same envi-ronmental conditions. The generalisation to emergehas been that species from nutrient-poor habitats typi-cally have lower maximum growth rates than speciesfrom nutrient-rich sites when they are grown under thesame experimental conditions (Grime & Hunt 1975;Grime 1979; Chapin 1980; Chapin et al. 1986), al-though this is not universally applicable (Grubb1998). Tropical forest tree species have often beenshown to have distinctive distributions across large-scale edaphic and climatic gradients (e.g. Gartlan et al.

1986; Newbery et al. 1986; Baillie et al. 1987;Tuomisto et al. 1995; Swaine 1996). However, the rel-evance of these associations to variation in growthrate within one site has not previously been examined.Here, we test this idea using the extensive ecologicalknowledge of Ghanaian forest species, and inventorydata from a semi-deciduous forest.

Firstly, we developed a classification of tree speciesincorporating both their regeneration requirementsand their association with different parts of a majorresource gradient. Within Ghanaian tropical forests,regional scale patterns of species distribution havebeen comprehensively described across a gradient of

increasing rainfall and decreasing soil fertility towardsthe south-west of the forest zone (12002300 mm yr1,soil pH 7.03.8; Hall & Swaine 1976, 1981). The firstaxis of a multivariate ordination of compositionaldata from 155 closed-canopy forest plots was shownto quantify species position along this gradient, withdecreasing axis one scores in the wettest, least fertileforest sites (Hall & Swaine 1981). To categorisespecies environmental preferences, the median score(25) of all species from 23, 1-ha plots in a range ofGhanaian forest types was used as an arbitrary thresh-old value (Baker 2000). Species with axis one scoresabove this value were classified as dry forest special-




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ists, and species with scores below this value were clas-sified as wet forest specialists. This categorization rep-resents a coarse division of species responses to a re-gional scale environmental gradient, and does not con-

sider local (e.g. topographic) influences of water andnutrient availability. However, the environmental fac-tors that determine species distributions at differentscales are likely to be similar. For example, in Ghana,the abundance of Celtis mildbraedii declines as thelandscape becomes wetter, both at local and regionalscales (Swaine & Hall 1986; Hawthorne 1995).Therefore, we are confident that our classification ade-quately, if crudely, represents species environmentalpreferences.

Species were also grouped according to their regen-eration requirements (pioneer, non-pioneer light-de-mander and non-pioneer shade-bearer), followingHawthorne (1995). Therefore, overall, species weregrouped into six categories, each including specieswith a range of maximum heights.

Inventory data were obtained from permanent sam-ple plots located in Bobiri Forest Reserve, in Ghana(11523W, 64042N), which is classified as MoistSemi-deciduous Forest (Hall & Swaine 1981). Meanannual rainfall (19611993) for Kumasi, 15 km westof the forest is 1183 mm. The main dry season occursfrom December to March (Swaine et al. 1997), with aless severe drier period from July to September (Vee-nendaal et al. 1996b). Most of the reserve contains

soils developed over upper and lower Birrimian phyl-lite (Adu 1974), with gently undulating topography.The soils consist of red, silty clay loams in summitareas and become paler in colour lower downslope.Valley soils are grey, sandy loams and clays (Adu1974).

Seven 1-ha plots that had not been damaged by fireor degraded by logging were selected in a range of to-pographic positions. They were established by theGhana Forestry Department in July/August 1990 andre-enumerated in July/August 1996. The girth of eachtree >20 cm dbh was measured to the nearest mm andeach measured tree was scored for the degree of crown

illumination (crown score) on a five point scale(Dawkins 1958). The painted point of measurementwas at a height of 1.3 m, or 50 cm above the top ofany buttress. Annual diameter growth of survivingtrees was compared between wet- and dry- forestspecies for each of the three regeneration categoriesusing Kruskal-Wallis tests.

For the three comparisons, the only significant dif-ference in growth rate was found between wet- anddry-forest pioneer species (Fig. 1). Dry-forest pioneerspecies had significantly higher median growth ratesthan wet-forest pioneers (H = 6.25, P < 0.012, n = 92,dry-forest pioneers, and 27, wet-forest pioneers). The



Fig. 1. Distribution of diameter increments within Ghanaian semi-decidu-ous forest, for six functional groups, defined by regeneration strategy anddistribution pattern with respect to climatic and edaphic conditions.(a) Shade-bearers, (b) non-pioneer light-demanders, and (c) pioneers. Thereis a significant difference in median growth rate between dry- and wet-forestpioneer species. Box size represents the range between the first and thirdquartiles, and whiskers extend 1.5 times this range. Outliers are shown asasterisks; mean (open circle) and median (shaded circle) are also indicated.


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difference in growth rate between these groups doesnot appear to be caused by differences in tree size orcrown illumination. Wet- and dry-forest pioneers com-prise trees of a similar diameter range, and there is nosignificant difference in the median diameter betweenthe two groups (Fig. 2; H = 0.52, P > 0.05). In addi-tion, the proportion of trees with high levels of crownillumination are similar: 30% of dry forest pioneers

and 29% of wet forest pioneers were classified asDawkins crown score 4 or 5.

The lower growth rates of wet-forest compared todry-forest pioneers may reflect an inability of the wetforest species, that typically occur on less fertile soils,to respond to the higher nutrient status of the soils ofthe semi-deciduous forest site. This contrast is sup-ported by seedling experiments on two pioneer speciesthat have different distribution patterns, Triplochitonscleroxylon and Lophira alata (Table 2). Both speciesare strongly light demanding, and attain large sizes,greater than 90 cm dbh (Hawthorne 1995). However,they show strongly contrasting patterns of seedling

growth on low and high fertility soils. Under well-wa-tered conditions, T. scleroxylon showed significantlyhigher growth on soil from semi-deciduous comparedto evergreen forest sites, whereas L. alata grew fasteston the less fertile, evergreen forest soil (Swaine et al.1997; Veenendaal et al. 1996a). With the results here,these patterns suggest that there may be variation inthe maximum growth rate of pioneer species inGhanaian forest, related to their association with par-ticular edaphic and climatic conditions.

In summary, in terms of growth rate, the classifica-tions of functional groups proposed by Turner (2001)differentiates groups of similar species. Classifications

based both on regeneration strategy and maximumsize, generally divide species that have low growthrates and show little response to increasing resources,from more responsive, faster-growing species. Howev-er, in both cases, exceptions occur. The growth rate ofadult trees of non-pioneer species may be modified byvariation in light demand during ontogeny, and maxi-mum size may not be associated with any systematic

variation in growth rate for pioneer species. Classifica-tions of species based on their association with partic-ular edaphic and climatic conditions may be useful forcategorizing important variation in the ecology of pio-neer species in tropical forests.

Functional gradients in forest composition

So far, we have focussed on two rather different per-spectives on tropical tree growth, and separately con-sidered variation in growth rates with resource avail-ability, and between functional groups. However, both

factors will be important for understanding spatialvariation in stand-level growth rates, if there are dif-ferences in the relative abundance of functional groupsbetween forests. There is increasing evidence of suchfunctional gradients at a range of scales within tropi-cal forests.

Studies of gradients in the functional compositionof tropical forests have concentrated on variation inthe relative abundance of pioneer and non-pioneers, orvariation in stand-level mean values for traits such aswood density, that are strongly correlated withspecies light demand (Whitmore 1998). For example,in Ghana, pioneer species are both most abundant and



Fig. 2. Annual diameter increment as a function of tree diameter for wet and dry forest pioneers, within semi-deciduous forest in Ghana.


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diverse in semi-deciduous forests, where rainfall islower and soils are more fertile than in evergreen for-

est (Hawthorne 1996). In addition, mean stand levelwood density and seed size are lowest in southerncompared to central Guyana, indicating that southernforests have a greater relative abundance and diversityof more light-demanding species (ter Steege & Ham-mond 2001). Also, in a comparison of 59 plots acrossAmazonia, mean stand level wood density was 12%higher in eastern, compared to north-western Amazonforests (Baker et al., in press).

Variation in past and current rates of disturbanceare probably the most important factor determiningthe variation in the composition of tropical forestswith respect to light demand. For both Ghana and

Guyana, higher proportions of light-demanding taxaare associated with areas that have a history of higherrates of anthropogenic disturbance (Fairhead & Leach1998; ter Steege & Hammond 2001). Past human ac-tivity has also been suggested as an important factordetermining the pioneer-rich flora of Barro ColoradoIsland in Panama (Sheil & Burslem 2003). AcrossAmazonia, it seems unlikely that there are importantsystematic differences in past human activity that havegenerated the observed variation in stand-level wooddensity (Baker et al., in press). Here, higher abiotic dis-turbance rates in western compared to eastern Ama-zon forests may explain the pattern. However, it is also

likely that soil nutrient availability influences the func-tional composition of tropical forest, as the growth

rates of pioneer species are particularly responsive tohigher soil nutrient concentrations. The forests of bothGhana and Guyana that have a higher abundance oflight demanding taxa, occur on more fertile soils(Hawthorne 1996; ter Steege & Hammond 2001). Asthis pattern coincides with variation in the intensity ofpast human disturbance, it is difficult to distinguishthe relative importance of the two factors.

These functional gradients in tropical forest compo-sition have important implications for spatial varia-tion in forest growth and dynamics, as light demand isgenerally positively correlated with species growthand mortality rates (Whitmore 1998). For example, at

a small scale, Tim Whitmores long-term study of for-est dynamics on Kolombangara in the Solomon Is-lands has yielded evidence of spatial variation instand-level turnover rates that correlates with varia-tion in functional group composition (Burslem &Whitmore 1999, in press). In addition, within a net-work of plots in aseasonal climates across Sarawak, aguild of pioneer species increased in abundance at ahigh-nutrient site, but were rare elsewhere, resulting inpositive correlations between soil nutrient concentra-tions and diameter growth of recruits (Ashton & Hall1992). At a larger scale, the lower wood density ofwestern compared to eastern Amazon forest is associ-



Table 2. Dry- and wet-forest pioneers in Ghanaian tropical forest. Nomenclature and classification of pioneers followsHawthorne (1996); association with dry or wet forest based on a multivariate ordination of species presence or absence in155 plots across the forest zone of Ghana (Hall & Swaine 1981).

Dry forest pioneers Wet forest pioneers

Species Family Species Family

Baphia pubescens Fabaceae Cola caricifolia SterculiaceaeCanarium schweinfurthii Burseraceae Daniellia ogea FabaceaeCeiba pentandra Bombacaceae Daniellia thurifera FabaceaeCeltis adolfi-friderici Ulmaceae Hannoa klaineana SimaroubaceaeCleistopholis patens Annonaceae Lophira alata OchnaceaeDraceana arborea Agavaceae Petersianthus macrocarpus LecythidaceaeFicus exasperata Moraceae Bombax brevicuspe BombacaceaeHoloptelea grandis Ulmaceae Zanthoxylum gillettii RutaceaeLannea welwitschii AnacardiaceaeMilicia excelsa MoraceaeMorus mesozygia MoraceaeNewbouldia laevis Bignoniaceae

Rauvolfia vomitoria ApocynaceaeBombax buonopozense BombacaceaeRicinodendron heudelotii EuphorbiaceaeStereospermum acuminatissimum BignoniaceaeTerminalia superba CombretaceaeTetrapleura tetraptera FabaceaeTetrorchidium didymostemon EuphorbiaceaeTriplochiton scleroxylon SterculiaceaeZanthoxylum leprieurii Rutaceae


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ated with higher tree turnover rates (Phillips et al.1994, in press) and higher stand-level wood produc-tion, calculated on both a volume and mass basis (Y.Malhi et al., unpubl. results). Finally, in a transconti-

nental comparison of the dynamics of an evergreenand a semi-deciduous forest, a guild of pioneer speciespresent only in the semi-deciduous forest was suggest-ed to determine overall plot differences in growth andmortality (Condit et al. 1999). The more seasonal for-est had higher overall growth and mortality rates thana plot lacking the guild of fast-growing pioneerspecies.

In summary, these studies demonstrate that spatialvariation in the proportion of light-demanding taxa,occurs at range of scales in tropical forests. Variationin disturbance rates appears to be the main factor thatdetermines these patterns, although soil nutrient avail-ability may also be important. The combined effects offunctional group composition and resource availabili-ty will therefore determine spatial variation in stand-level growth.

Future directions

In this review, we have used a broad definition ofgrowth rate incorporating both changes in size andcarbon content of plants, plant parts and populations.Size is important, both ecologically as an important

determinant of competitive success, and for silvicul-ture as timber yields are typically determined on thebasis of volume. In contrast, growth rates calculated interms of changes in carbon content are more closelyrelated to variation in rates of photosynthesis and res-piration and hence resource availability, and are im-portant for calculating stand-level carbon balance.The two quantities are related through variation in al-location strategies, which vary both along resourcegradients and between functional groups. In terms ofaboveground growth, inclusion of wood density in cal-culations of the growth rate of adult trees is essentialfor understanding how different life history strategies

compare in terms of carbon uptake (e.g. Enquist et al.1999). In addition, more work is required on howtrends in belowground allocation correspond to varia-tion in aboveground productivity. For example, fine-root densities in the topsoil are higher in tropicalforests on highly infertile soils (Coomes & Grubb2000), but across Amazonia it is not known to whatextent these kind of belowground patterns may offsetspatial variation in aboveground productivity (Y.Malhi et al., unpubl. results).

Comparative studies of the ecology and dynamicsof a large number of forests are required to understandthe combined effects of functional groups and resource

availability on spatial variation in forest growth rates.These studies will need to account for variation inwater and nutrient availability as well as variation inlight. In addition, quantifying the variation in life-his-

tory strategies using appropriate traits, such as wooddensity and maximum size, will allow tests of whethereffects of resource availability are independent of vari-ation in species composition. The ideas of Tim Whit-more in defining and exploring functional differencesbetween tropical forest trees will therefore remain cen-tral to future research into this fundamental aspect oftropical rain forest ecology.

Acknowledgements. For advice and assistance during field-work in Ghana we thank Dr. V.K. Agyeman (FORIG, Ku-masi) and Dr. T.K. Orgle (Forest Management Support Cen-tre, Kumasi). We also thank Kofi Affum-Baffoe, Yaw Atua-hene and Raymond Votere (Inventory Unit, Forest Manage-ment Support Centre, Kumasi) for compiling the forest in-ventory data used in this study. Peter Grubb, Ian Turner andOliver Phillips provided very helpful comments on a previ-ous version of this manuscript. This work was largely fund-ed by a University of Aberdeen Faculty studentship to TRB,who also acknowledges current financial support from theMax-Planck-Institut fr Biogeochemie, Jena, Germany.

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