Spatial heterogeneity and its influence on Copaifera langsdorffii Desf. (Caesalpiniaceae)

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Brazilian Archives of Biology and Technology

Vol.46, n. 3 : pp. 405-414, June 2003ISSN 1516-8913 Printed in Brazil %5$=,/,$1�$5&+,9(6�2)

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.H\�ZRUGV��Gallery forest; seedling; recruitment, mortality, growth, saplings

∗ Author for correspondence

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Gallery forests follow streams and drainage linesin the savannas of Central Brazil. They grow onhydromorphic soils, have different degrees ofdeciduousness and may appear along one or bothmargins of the watercourse (Mantovani, 1989).Most gallery forests are subject to periodicflooding. Overbank flooding is common in therain season, when large rain events cause anincrease of flux of water. The topography(depression in some places), the soil feature(hydromorphic soil) and water table fluctuationscause a second type and more durable floodingeffect, during the entire rainy season, thisprolonged flooding and its effect is explored in

this work. The light conditions associated withdifferent susceptibility to flooding determinedifferent habitat types in the gallery forests(Schiavini, 1992). Due to these particularcharacteristics, gallery forests are useful models tostudy spatial heterogeneity in the environment andthe influence of this heterogeneity on populationstructure and dynamics of forest communities(Schiavini, 1992; Oliveira - Filho et al., 1994).How natural plant populations seem to beregulated by density dependent processes(Antonovics and Levin, 1980; Crawley, 1990;Condit et al., 1994) in association withenvironmental heterogeneity in space and time(Fowler, 1988), gallery forests could be used totest hypotheses of populations regulation.

Resende, J. C. F. et al.


406

Studies of density and its effects have been limitedto the direct interference between intraspecificneighbors (Mithen et al., 1984) through limitationof resources such as light or nutrients (Berntsonand Wayne, 2000). However, low density treepopulations in tropical forests is common, andneighbors are seldom conspecifics. Densitydependent processes may be detected mainly byincrease in density of natural enemies. However,intraspecific density dependent processes aredifficult to detect in field conditions, sinceenvironmental heterogeneity obscures theseeffects. One way to circumvent this difficulty is tomeasure performance (mortality, growth andrecruitment) of individual plants under differentenvironmental conditions (Condit et al., 1994).Spatial distribution is an important demographiccomponent as it reflects several factors such asparental distribution, seed dispersal, predation andherbivory, and the distribution of safe-sites(Hutchings, 1986). The association of periodicflooding, with either intolerance or toleranceflooding may determine the distribution of plantsin gallery forests. The increase of light to theforest floor, mainly at the edge (adjacent to thesavanna), associated with flood may determine theavailability of safe-sites, and in turn the plantestablishment and growth. Spatial distribution ofgallery forests tree species between habitats andwithin habitats should reflect the distribution ofthese safe-sites.We studied the effect of flooding and lightconditions in spatial distribution, size structure,growth rates, recruitment and mortality ofseedlings and saplings of &RSDLIHUD� ODQJVGRUIILLDesf., a late successional, flood intolerant,common and widespread tree. We assumed as ourhypotheses: 1 – the distribution of &�� ODQJVGRUIILLseedlings and saplings was clumped on the dryareas (less prone to flooding); 2 – the growth ofseedlings and saplings of &�� ODQJVGRUIILL wasdirectly related to canopy cover; 3 – the density ofintraspecific seedlings and saplings was negativelyrelated to growth; 4 – The mortality rates ofseedlings and saplings could be higher in theflooded habitat.

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6SHFLHV� GHVFULSWLRQ� DQG� VWXG\� VLWH�� Copaiferalangsdorffii (Caesalpiniaceae) is a typical galleryforest tree that may also occur in adjacent savannacommunities (Cerrado) in Central Brazil. It canreach 25 m in height in the forest (it is smaller inthe savanna). Seeds have an aril and are dispersedthrough animals, particularly by birds. Theirseedlings do not survive prolonged floods (2 to 7days to die) (Barbosa et al., 1992). Topographyand soil characteristics result in different degreesof flooding in the forest. Three habitats wererecognized, associated with the nature andduration of the flooding, soil features, lightconditions and floristic composition (Schiavini,1992): 1) Dike: a 10 m wide zone near thewatercourse, which was characterized bydeposition of alluvial sandy sediments, and wasless prone to periodic flooding. 2) Middle: thedepression after the Dike that was roughly parallelto the watercourse, with hydromorphic soil; it wasmore prone to periodic flooding. 3) Edge: theboundary zone adjacent to the open savanna,characterized by moderate hydromorphic soil andhigher incident light than the other habitats. Theplant community of gallery forests includedspecies that were tolerant and intolerant to theperiodic flooding (Schiavini, 1992; Walter, 1995).Seedlings and saplings of &�� ODQJVGRUIILL weresampled at the Panga Ecological Station located inUberlândia, Minas Gerais, Brazil. The station hasa total area of 400 ha and comprises severalvegetation types including forests, cerradograsslands and woodlands (Fig. 1). The regionalclimate is of Aw type (Köppen) with dry winters(from May through September) and rainy summers(from October to April). The average annualprecipitation is 1500 mm. The studied area was10,000 m2 of forest. The gallery forest forms acontinuous forest along the river. The sample areawas 3,000 m2, divided into 120 plots of 5 x 5 m.Forty plots were allocated for each habitat, theDike, Middle and the Edge (Fig. 1). Annualsurveys were conducted in 1993, 1994, 1995 and1996. For each survey, all plants of &��ODQJVGRUIILLin each of the 120 plots were individually tagged,measured for height and diameter at base.

'HPRJUDSK\� DQG� 6SDWLDO� GLVWULEXWLRQ�� Allseedlings and saplings of &�� ODQJVGRUIILL found in

Spatial Heterogeneity and its Influence on &RSDLIHUD�ODQJVGRUIILL Desf. (Caesalpiniaceae)


407

the 120 plots were mapped. Their pattern ofspatial distribution in each habitat was describedby comparing the 1993 survey, using the index ofdispersion:

ID = s2

xwhere: s2 = variance

x = meanand Green’s index (Ludwig and Reynolds, 1988):

GI = (s2/x) - 1N - 1

where: s2 = variancex = meanN = number of individuals.

We found a different N of seedling and saplingbetween the habitats types. The index ofdispersion is dependent on sample size, sinceGreen’s index is more appropriate forcomparisons of the degree of clustering (Ludwigand Reynolds, 1988).Size classes were determined using the relationA/k, where A was the amplitude and k wasSturges algorithm, 1+ 3.3log N, N being thenumber of individuals (Gerardi and Silva, 1981).The Komolgorov - Smirnov test compared thedifferences between the 1993 and 1996frequencies in the size structure curves.Differences in mortality and recruitment betweensurveys and habitat types (Dike, Middle and Edge)were tested using chi-square.

7KH� LQIOXHQFH� RI� KDELWDW�� FDQRS\� FRYHU� DQGGHQVLW\�RQ�JURZWK� Growth was estimated usingthe final/initial height ratio or the final/initialdiameter ratio. This allowed us to comparedifferences in growth between size classes andhabitats. Differences were tested with the Kruskal- Wallis test (Sokal and Rohlf, 1981). Theinfluence of cover on growth was examined usingcanopy pictures of each plot. The pictures weretaken with black and white 35 mm film, iso 400,with a SLR camera fitted with a 35 mm wide -angle lens. The diaphragm was set for sub-exposition, in order to maximize the contrast

between light and dark areas in the pictures. Onepicture was taken in the center of each plot, at 55cm above ground. Data collection took 15 days inJuly 1996, between 10 a.m. and 2 p.m.. Thepictures were digitized using a scanner (200 - dpiresolution); dark and white areas were quantifiedto calculate a relative index of canopy cover. Therelationship between canopy cover index andgrowth of plants of &�� ODQJVGRUIILL was testedusing the Spearman Rank Order Correlation.Density of seedlings and saplings of &�ODQJVGRUIILL in the plots was also correlated withgrowth by the Spearman Rank test.

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The total number of seedlings and saplings of &�ODQJVGRUIILL decreased from 481 in 1993 to 454 in1996, the mean density of seedlings and saplingswas 0.16 and 0.15 individuals/m2, respectively.There was a clear concentration of seedlings andsaplings on the Dike, corresponding to an averageof 61 % of all plants sampled during the fouryears. The Middle had 21.5 % and the Edge 17.5% of the plants. Both the dispersion coefficientand Green’s index indicated an aggregateddistribution for the three gallery forest habitats(Table 1). The flooded habitat (Middle) presenteda higher degree of cluster than the Dike and Edge.

7DEOH�� Dispersion and Green’s index of individualsof &RSDLIHUD� ODQJVGRUIILL in the three habitats of agallery forest in Panga Ecological Station for the 1993and 1996 surveys. Values for three microhabitats ofgallery forest. All values of dispersion index aresignificantly different from 1 at 5 % level in the chi-square test. ID = Index of Dispersion, GI = Green’sIndex.+DELWDW ��

ID GI ID GI

Dike 4.77 0.0133 5.12 0.0149

Middle 8.19 0.0672 5.81 0.0506

Edge 2.88 0.0229 2.43 0.0183



408

)LJXUH�� Map of the plant communities in Panga Ecological Station, below study area with plotlocation, Uberlândia, Minas Gerais, Brazil (Adapted from Schiavini, 1992).

No significant difference in mortality (P = 0.08)and recruitment (P = 0.37) was found betweenhabitats, but mortality was significantly higherthan recruitment during the four year period (P <0.005). Recruitment decreased over time, whilemortality remained constant (Table 2).Mortality was concentrated in the first threediameter classes, of the 69 plants that died duringthe study period, 60 were in the smallest size class(diameter between 1 - 3.3 mm).Size frequency distribution followed a typicalreversed “J”, for both height and diameter, witha high concentration of plants in the first class(Fig. 2). The Kolmogorov - Smirnov test showed asignificant difference between the 1993 and the

1996 surveys for height in the Edge Habitat (P <0.001) (data not presented) and for diameter in theDike Habitat (P < 0.01) (Fig. 2 B), Edge Habitat(P < 0.004) (Fig. 2 D) and for the total population(P < 0.001) (Fig. 2 A). The modification of sizeclasses between years was caused by concentratedmortality in the first three classes associated withlow recruitment during the period.There was highly significant difference in growthbetween habitats to the seedlings and saplings of&�� ODQJVGRUIILL (Fig. 3). Plants in the Edge had alarger growth ratio than plants in the Dike and theMiddle Habitat for height (P < 0.001) anddiameter (P < 0.001). Growth differed alsobetween diameter classes (P < 0.01). The first



409

diameter class had the highest growth ratio andthere was a tendency reducing growth ratio on thelarger diameters (data not presented). There wasrelationship between canopy cover and growthratio (Table 3). A significant correlation wasfound between diameter growth ratio and canopycover in the Middle habitat (r = 0.533, P < 0.01 inSpearman Correlation). Low correlation alsooccurred between growth ratio of seedling andsaplings of &�� ODQJVGRUIILL and plot density ofconspecifics. A significant negative correlationwas found between diameter growth ratio to allseedlings and saplings and density of conspecifcsplot density (r = -0.2, P = 0.04 in SpearmanCorrelation).

7DEOH� �� Spearman Rank Order Correlation betweengrowth ratio and canopy cover, for &RSDLIHUDODQJVGRUIILL in the Panga Ecological Station. ( )Indicates significant difference at the 5 % level.

*URZWK�UDWLR�;�&DQRS\�FRYHU+DELWDW+HLJKW 'LDPHWHU

Dike -0.236 -0.003Middle 0.071 0.533*Edge 0.202 0.033Total Population -0,003 0.134

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The most important determinant of tree spatialdistribution in gallery forest seems to be theperiodic flooding and the species tolerance to thiscondition (Walter, 1995). Adult individuals of &�ODQJVGRUIILL have been restricted to areas notsubjected to flooding, which led some authors toclassify the species as intolerant to flooding(Schiavini, 1992; Walter, 1995). In this study, weobserved that seedlings and saplings of &�ODQJVGRUIILL were found mainly in the driesthabitat (the Dike). The spatial distribution of

saplings and seedlings seems to reflect theflooding conditions found in each habitat.The Dike population had the smallest degree ofclumping, possibly due to its dry sandy soil andmicrotopographic characteristics, which preventedprolonged inundation (Schiavini, 1992). TheMiddle population had the highest degree ofclumping. This habitat has hydromorphic soil andis characterized by a depression that suffersperiodic and prolonged flooding (Schiavini, 1992).Distribution of &�� ODQJVGRUIILL in the Middle islimited to areas where alluvial sedimentdeposition creates small mounds (personalobservation). The presence of these moundsmodified germination rate and seedling survival,as has been shown in studies of other floodplainsystems (Jones et al., 1994), possibly influencing&�� ODQJVGRUIILL distribution. The Edge populationshowed an intermediate degree of clumping andthis habitats been influenced by indirect light fromthe open savanna (Schiavini, 1992).Survival and recruitment were similar and couldnot explain the high differences in abundancebetween habitats. The factors determiningdistribution probably acted during seed dispersaland seedling establishment. Parent plants wereconcentrated on the Dike (Schiavini, 1992), andprobably contributed a larger input of seeds to thishabitat than the others, which would increaseestablishment. After dispersion, the density ofseeds was higher near the parent plant anddecreased with distance (Janzen, 1970; Whitmore,1988). The association between spatial andtemporal heterogeneity brought about by waterlevel fluctuations, erosion and sedimentationmight create differential site suitability betweenhabitats for seedling establishment (Bertoni andMartins, 1987).

7DEOH�� Mortality and recruitment of seedlings and saplings of &RSDLIHUD�ODQJVGRUIILL in the gallery forest of PangaEcological Station between 1993 and 1996 surveys. mort = mortality; recr = recruitment.+DELWDW �� $QQXDO� DYHUDJH

��mort recr mort recr mort Recr mort Recr

Dike 14 (4.8%) 20 (6.9%) 12 (4.1%) 7 (2.4%) 13 (4.5%) 2(0.7%) 4.5 3.5Middle 10 (9.2%) 4 (3.7%) 7 (6.8%) 4 (3.9%) 5 (5.0%) 1 (1.0%) 6.8 2.8Edge 2 (2.4%) 3 (3.6%) 1 (1.2%) 1 (1.2%) 5 (6.5%) 0 (0.0%) 3.2 1.6Total 26 (5.4%) 27 (5.6%) 20 (4.1%) 12 (2.5%) 23 (4.8%) 3 (0.6%) 4.8 2.9



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)LJXUH�� Diameter frequency distribution of &RSDLIHUD�ODQJVGRUIILL for Total population (A), Dike (B), Middle (C)and Edge (D) of a gallery forest in the Panga Ecological Station. Diameter class in mm, �: 1 - 3,29; �: 3,3- 5,59; �: 5,6 - 7,89; �: 7,9 - 10,19; �: 10,20 - 12,49; �: 12,50 - 14,79; �: 14,80 - 17,09; �: 17,10 - 19,39;�: 19,40 - 21,69; ��: 21,70 - 23.99; ��: 24 - 26,29; ��: 26,30 - 28,59; ��: 28,60 - 30,89; ��: 30,90 -33,19; ��: 33,20 - 35,50.



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)LJXUH� �� Growth ratios of seedlings and saplings of &RSDLIHUD� ODQJVGRUIILL for the three habitats and totalpopulation. Growth was measured as the ratio between final size (1996 survey) and initial size (1993survey) as measured by both height and diameter. Means with one standard error.

In undisturbed forests, tree losses are continuouslyreplaced by new recruits in “steady-state”populations (Swaine et al., 1987), even thoughconstant recruitment and mortality rates,commonly used in population dynamics’ modelsare probably unrealistic (Crawley, 1990), as hasbeen the case of &��ODQJVGRUIILL.During the study period, the mortality was higherthan recruitment because adult trees did not

produce seeds in the area (personal observation).&�� ODQJVGRUIILL usually produced seeds at three-year intervals (Leite and Salomão, 1992). It hasbeen reported that in tropical forests recruitmentvaried from years of large seed production (mastyears) to years of low seed production andrecruitment (De Steven, 1994).In tropical forests, mortality varied within localsites and between successive periods (Swaine et



412

al., 1987), even though this was not true for &�ODQJVGRUIILL� during the duration of this study.Seedling and sapling mortality was similarbetween habitats and possibly caused by similaragents, such as resource limitation and inter andintraspecific competition. Catastrophic eventssuch as “drought” were not the main mortalityfactor in this tree population as been reported inother studies (Condit et al., 1995), since no largefluctuations in population size were seen. In theabsence of catastrophic mortality, populationfluctuations should follow years of high seedproduction, when recruitment rates are expected tobe higher than in subsequent years. Thus,fluctuations in the population of &�� ODQJVGRUIILLshould be directly linked to its multi-annualreproductive cycle, a pattern reported by DeSteven (1994) for tropical trees in which highrecruitment rates were a consequence of increasedinput of seeds, followed by declines caused bymortality and low seed production and lowrecruitment.The relatively higher growth found in the Edgehabitat could be related to the high mortality rateof the Edge pioneer tree 0LFRQLD� WKDH]DQV�(80 %of the mature plants have died in the last fiveyears - Schiavini, unpublished data). This speciesforms dense clumps, but mature trees suffer highmortality and form gaps in the canopy. Seedlingsand saplings of &�� ODQJVGRUIILL could havebenefited from the low competitive influence andconsequently had higher growth than in the otherhabitats, a response also seen for other tropicaltree species in canopy gaps (Denslow, 1987;Martinez-Ramos et al., 1988; Whitmore, 1988; DeSteven, 1994; Forget, 1994).Canopy cover was not the only factor affectinggrowth in &��ODQJVGRUIILL, as suggested by the lowrelationship found between growth and coverindex. Specific site conditions such as number andsize of neighbors, soil fertility, grazing, andgenetic variability might have influenced theresults. Conspecific neighbors may alter thegrowth of plants by depleting limited resources, byproducing toxins and by influencing the behaviorof natural enemies (Harper, 1977). Studies ofintraspecific density dependent effects usuallytake into consideration the direct effects ofcompetition for light and nutrients that areimportant factors on intraspecific competition(Liddle et al., 1982, Mithen et al., 1984; Weiner

and Thomas, 1986), but often they do not considerthe effect of increase in concentration of naturalenemies (Janzen, 1970; Isaacs et al., 1996) andherbivory (Angulo-Sandoval and Aide, 2000;Silva Matos, 2000). Since the population densityof seedling and saplings of &�� ODQJVGRUIILL waslow, usually 1 plant/m2 in the densest plots, theintraspecific density effect on growth of thistropical tree would be minimal and be relatedmore to the concentration of natural enemies.Grazing and fungal attacks have been observed,but not quantified in the field (personalobservation). Even at low intraspecific densities anegative effect of density, due to concentration ofnatural enemies, may occur in tropical trees(Condit et al., 1994).Structured populations with ample longevity oftheir individuals and repeated, sometimes yearly,recruitment have age differences between plantswhich are the main causes of height distributions(Weiner, 1988). The reversed “J” curve of sizedistributions has been found for several tropicaltrees in Brazil and indicated a consistentrecruitment and growth of populations (Leite andSalomão, 1992; Schiavini, 1992). Despite otherpossible marginal causes of the reversed “J”curve, the data presented here suggests that &�ODQJVGRUIILL presented local regeneration.

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We appreciate comments by Paulo EugênioOliveira, John Du Vall Ray and Raimundo P. B.Henriques. CAPES supported this research.

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A estrutura e a dinâmica dos indivíduos jovens daespécie &RSDLIHUD� ODQJVGRUIILL Desf.(Caesapiniaceae) foi estudada na mata de galeriada Estação Ecológica do Panga (Uberlândia, MG -Brasil). A mata de galeria neste estudo foi descritacomo apresentando 3 ambientes: Dique, Meio eBorda. O trabalho de campo consistiu de quatrolevantamentos, realizados anualmente entre 1993 e1996. A população foi caracterizada comoagrupada nos três ambientes. A estrutura detamanho da população se apresentou como umacurva em “J” invertido, indicando regeneração



413

local. As taxas de mortalidade foram constantes ebaixas durante os quatro anos (4,8 % por ano), jáas de recrutamento sofreram um declínio durante omesmo período (2,9 % por ano). A densidadeintraespecífica das plântulas e indivíduos jovensde &�� ODQJVGRUIILL tem um efeito negativo nastaxas de crescimento, possivelmente devido a açãode herbívoros e patógenos.

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Angulo-Sandoval, P. and Aide, T. M. (2000), Effect ofplant density and light availability on leaf damage inManilkara bidentata (Sapotacea). -RXUQDO�RI�7URSLFDO(FRORJ\, ��, 447-464.

Antonovics, J. and Levin, A. L. (1980), The ecologicaland genetic consequences of density - dependentregulation in plants. $QQXDO� 5HYLHZ� RI� (FRORJ\� DQG6\VWHPDWLFV, ��, 411-452.

Barbosa, L. M.; Asperti, L. M.; Bedineli, C.; Barbosa, J.M.; Belasque, E. F. and Pirré, E. (1992), ,QIRUPDo}HV%iVLFDV� 3DUD� 0RGHORV� GH� 5HFXSHUDomR� GH� ÈUHDV'HJUDGDGDV�GH�0DWDV�&LOLDUH. 2o Congresso NacionalSobre Essências Nativas. São Paulo.

Berntson, G. M. and Wayne, P. M. (2000),Characterizing the size dependence of resourceacquisition whitin crowded plant populations.(FRORJ\, ��, 1072-1085.

Bertoni, J. E. A. Martins, F. R. (1987), Composiçãoflorística de uma floresta ripária na Reserva Estadualde Porto Ferreira. $FWD� %RWDQLFD� %UDVLOLFD, � : (1),17-26.

Condit, R.; Hubbell, S. P. and Foster, R. B. (1994),Density dependence in two understory tree species ina neotropical forest. (FRORJ\, �� : (3), 671-680.

Condit, R.; Hubbell, S. P. and Foster, R. B. (1995),Mortality rates of 205 neotropical tree and shrubspecies and the impact of severe drought. (FRORJLFDO0RQRJUDSKV, �� : (4), 419-439.

Crawley, M. J. (1990), The population dynamics ofplants. 3KLORVRSKLFDO� 7UDQVDFWLRQV� RI� WKH� 5R\DO6RFLHW\�RI�/RQGRQ, ��, 125-140

Denslow, J. S. (1987), Tropical rainforest gaps and treespecies diversity. $QQXDO� 5HYLHZ� RI� (FRORJ\� DQG6\VWHPDWLFV, ��, 431-451.

De Steven, D, (1994), Tropical tree seedling dynamics:recruitment patterns and their populationconsequences for three canopy species in Panama.-RXUQDO�RI�7URSLFDO�(FRORJ\, ��, 369-383.

Forget, P. M. (1994), Recruitment pattern of9RXDFDSRXD� DPHULFDQD (Caesalpiniaceae), a rodent-dispersed tree species in French Guiana. %LRWURSLFD,�� : (4), 408-419.

Fowler, N. (1988), The effects of environmentalheterogeneity in space and time on the regulation ofpopulations and communities. In: Davy, A. J.;Hutchings, M. J. and Watkinson, A. R. (eds.). 3ODQWSRSXODWLRQ� HFRORJ\. Blackwell ScientificPublications, London, pp. 249-269.

Gerardi, M. M. and Silva, B. C. N. (1981),4XDQWLILFDomR�HP�JHRJUDILD. Ditel, São Paulo.

Harper, J. L. (1977), 7KH�SRSXODWLRQ�ELRORJ\�RI�SODQWV�Academic Press, London.

Hutchings, M. J., (1986), The structure of plantpopulations. In: Crawley, M. J. (ed.). 3ODQW� HFRORJ\Blackwell Scientific Publications, London, pp. 97-136.

Isaacs, R.; Gillman, M. P.; Johnston, M.; Marsh, F. andWood, B. C. (1996), Size structure of dominantNeotropical forest tree species, 'LF\PEH� DOWVRQLL, inGuyana and some factors reducing seedling leaf area.-RXUQDO�RI�7URSLFDO�HFRORJ\, ��, 599-606.

Janzen, D. H. (1970), Herbivores and the number oftree species in tropical forests. $PHULFDQ� 1DWXUDOLVW,��, 501-528.

Jones, R. H.; Sharitz, R.R.; Dixon, P. M.; Segal, D. S.and Shneider, R. L. (1994), Wood plant regenerationin four floodplain forests. (FRORJLFDO� 0RQRJUDSKV,�� : (3), 345-367.

Leite, A. M. C. and Salomão, A. N. (1992), Estruturapopulacional de regenerantes de copaíba (&RSDLIHUD/DQJVGRUIILL Desf.) em mata ciliar do Distrito Federal.$FWD�%RWDQLFD�%UDVLOLFD, � : (1), 123-134.

Liddle, M. J.; Budd, C. S. J. and Hutchings, M. J.(1982), Population dynamics and neighborhoodeffects in establishing swards of festuca rubra. 2LNRV,��, 52-59.

Ludwig, J. A. and Reynolds, J. F. (1988), 6WDWLVWLFDOHFRORJ\��$� SULPHU� RQ�PHWKRGV� DQG� FRPSXWLQJ. JohnWiley and Sons, New York.

Mantovani, W. (1989), &RQFHLWXDomR� H� IDWRUHVFRQGLFLRQDQWHV� Anais do Simpósio Sobre MataCiliar, Fundação Cargil, Campinas, São Paulo.

Martinez-Ramos, M.; Sarukhán, J. and Piñero, D. (1988),The demography of tropical trees in the context offorest gap dynamics; the case of $VWURFDU\XPPH[LFDQXP at Los Tuxtlas tropical rain forest. In:Davy, A. J.; Hutchings, M. J. and Watkinson, A. R.(eds.). 3ODQW� SRSXODWLRQ� HFRORJ\. Blackwell ScientificPublications, London. pp. 293-313.

Mithen, R.; Harper, J. L. and Weiner, J. (1984), Growthand mortality of individual plants as a function of“available area”. 2HFRORJLD, ��, 57-60.

Oliveira Filho, A. T.; Vilela, E. A.; Carvalho, D. A. andGavilanes, M. L. (1994), Effects of soils andtopography on the distribution of tree species in atropical riverine forest in south - eastern Brazil.-RXUQDO�RI�7URSLFDO�(FRORJ\, ��, 483-508.



414

Schiavini, I. (1992), (VWUXWXUD� GH� FRPXQLGDGHVDUEyUHDV� GH� PDWD� GH� JDOHULD� GD� (VWDomR� (FROyJLFDGR� 3DQJD� �8EHUOkQGLD�� 0*�� Tese de Doutorado,Unicamp, Campinas, Brazil.

Silva Matos, D. M. (2000). Herbivore and plantdemography: a case study in a fragment of semi-deciduous forest in Brazil. -RXUQDO� RI� 7URSLFDO(FRORJ\, ��, 159-165.

Sokal, R. R. and Rohlf, J. F. (1981), %LRPHWU\. W. H.Freeman and Company, New York.

Swaine, M. D.; Lieberman, D. and Putz, F. E. (1987),The dynamics of tree populations in tropical forest: areview. -RXUQDO�RI�7URSLFDO�(FRORJ\, �, 359-366.

Walter, B. M. T. (1995), 'LVWULEXLomR� HVSDFLDO� GHHVSpFLHV�SHUHQHV�HP�XPD�PDWD�GH�JDOHULD� LQXQGiYHOQR�'LVWULWR�)HGHUDO��IORUtVWLFD�H�ILWRVVRFLRORJLD� Tesede Mestrado, Universidade de Brasília, Brasília, Brazil.

Weiner, J. (1988), Variation in the performance ofindividuals in plant populations. In: Davy, A. J.;Hutchings, M. J. and Watkinson, A. R. (eds.). 3ODQWSRSXODWLRQ� HFRORJ\. Blackwell ScientificPublications, London, pp. 59-82.

Weiner, J. and Thomas, S. C. (1986), Size variabilityand competition in plant monocultures. 2LNRV, ��,211-222.

Whitmore, T. C. (1988), The influence of treepopulations dynamics on forest species composition.In: A. J. Davy, M. J. Hutchings and A. R. Watkinson(eds.). 3ODQW�SRSXODWLRQ�HFRORJ\� London : BlackwellScientific Publications. pp. 271-291.

Received: July 11, 2001;Revised: February 20, 2002;

Accepted: May 06, 2003.

Spatial heterogeneity and its influence on Copaifera langsdorffii Desf. (Caesalpiniaceae)

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