Effects of stem anatomical and structural traits onresponses to stem damage: an experimental studyin the Bolivian Amazon

Claudia Romero and Benjamin M. Bolker

Abstract: Persistence of tree species in a habitat depends on their ability to avoid and respond to disturbance-related dam-age. Responses to stem damage vary among species but typically include bark wound closure and prevention of xylem de-cay spread. These responses are associated with anatomical, structural, and physiological traits. This study explores howxylem (vessel size and (or) abundance, parenchyma abundance, ray width, and wood density) and phloem (bark thickness,proportion of live inner bark, ray width and (or) dilation, inter-ray distance, and tissue density) traits relate to responses tostem damage in seven species from the Bolivian Amazon. Rates of bark wound closure and radial xylem decay penetrationwere compared 2 years after experimental damage. A species that closed bark wounds rapidly (100% in Chorisia speciosaA. St.-Hil.) was not efficient at constraining xylem radial decay spread (1.7 mm). The opposite was true for Pseudolmedialaevis (Ruiz & Pav.) J.F. Macbr., a species that closed wounds slowly (30%) but efficiently controlled decay spread(0.5 mm). The relationship between anatomical and (or) structural traits and damage response variables revealed that spe-cies with favorable traits for rapid wound closure (e.g., widely dilating rays) had traits that favored xylem decay spread(e.g., low wood density). It is plausible that this apparent trade-off is based on physiological and phylogenetic constraints.

Resume : La persistance des especes d’arbres dans un habitat depend de leur capacite a eviter et a reagir aux dommagescauses par les perturbations. Les reactions aux blessures au tronc varient selon l’espece mais incluent typiquement la cica-trisation des blessures a l’ecorce et la prevention de la propagation de la carie dans le xyleme. Ces reactions sont associeesa des traits anatomiques structuraux et physiologiques. Cette etude examine de quelle facon les caracteristiques du xyleme(abondance et dimension des vaisseaux, abondance de parenchyme, largeur des rayons et densite du bois) et du phloeme(epaisseur de l’ecorce, proportion d’ecorce interne vivante, largeur ou dilatation des rayons, distance entre les rayons etdensite des tissus) sont reliees aux reactions aux blessures au tronc chez sept especes de l’Amazonie bolivienne. Les tauxde cicatrisation des blessures a l’ecorce et de penetration radiale de la carie dans le xyleme ont ete compares deux ans apresavoir fait des blessures experimentales. Une espece qui cicatrisait rapidement les blessures a l’ecorce (100 % chez Chorisiaspeciosa A. St.-Hil.) n’etait pas efficace pour enrayer la propagation radiale de la carie dans le xyleme (1,7 mm). Le contra-ire etait vrai pour Pseudolmedia laevis (Ruiz & Pav.) J.F. Macbr., une espece qui cicatrisait lentement (30 %) mais enrayaitefficacement la propagation de la carie (0,5 mm). La relation entre les caracteres anatomiques ou structuraux et les varia-bles de la reaction aux blessures revele que les especes dont les caracteres sont favorables a une cicatrisation rapide (p. ex.des rayons largement dilates) avaient des caracteres qui favorisent la propagation de la carie dans le xyleme (p. ex. une fai-ble densite du bois). Ce compromis est possiblement fonde sur des contraintes physiologiques et phylogeniques.

[Traduit par la Redaction]

Introduction

Tree stems play a variety of structural, physiological, andbiomechanical roles. In contrast to leaves, which can beshed when damaged, stems need to persist if the tree is tosurvive and thus avoiding and recovering from stem woundsis important. The most important responses to stem damageare wound closure and decay containment. Trees with stemtissues that do not heal properly after damage might beprone to pathogen invasion and further decay, with biome-chanical consequences that can lead to death. Thus, traits re-

lated to stem damage responses affect tree survival andtherefore should be influenced by natural selection.

There have been several studies describing the responsesof tree stems to damage (see references in the followingparagraph), but the relationships among traits associatedwith responses to stem damage have been less well ex-plored. Furthermore, the mechanisms governing these re-sponses are poorly known. In particular, allocation ofresources for repair and association of particular responsepatterns with specific disturbance regimes and in general,anatomical, structural, ecological, and physiological con-

Received 29 May 2007. Accepted 22 October 2007. Published on the NRC Research Press Web site at cjfr.nrc.ca on 29 February 2008.

C. Romero.1 Department of Botany, University of Florida, 220 Bartram Hall, P.O. Box 118526, Gainesville, FL 32611-8526, USA.B.M. Bolker. Department of Zoology, University of Florida, 223 Bartram Hall, P.O. Box 118525, Gainesville, FL 32611-8525, USA.

1Corresponding author (e-mail: cromero@botany.ufl.edu).

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straints on compartmentalization and wound closure in dif-ferent species need investigating. Understanding these rela-tionships might help elucidate the differences observedamong tree species in their sensitivity to damage. Thepresent study relates bark and wood characteristics to re-sponses to mechanical stem damage and proposes explana-tions for the differences observed among tree species.

Damage to tree stems can occur in many different waysand even minor damage can have severe long-term conse-quences for wood quality and tree longevity (Mattheck andKubler 1995). For example, wind-thrown branches andwhole trees can scrape the bark from neighboring tree stems.Similarly, ice flows in riparian areas can rip open bark tis-sues (Filip et al. 1989). Animals also wound trees by feedingon inner bark, sap, or resins, and when they rub their bodiesor antlers on tree stems (Harcourt 1986; Akashi and Naka-shizuka 1999). Intentional human-induced stem damage isalso a horticultural practice (e.g., to improve fruit yield andquality; Layne and Flore 1991; Mataa et al. 1998) and silvi-culturists often thin stands by stem girdling, arboricide ap-plication, or a combination of the two (de Graaf et al. 1999;Pariona et al. 2003). Timber harvesting frequently results inunintentional damage to tree crowns, stems, and roots (Johnset al. 1996; Webb 1997; Feldpausch et al. 2005). Finally,bark harvesting for fibers, exudates, and medicines causesstem damage (e.g., dyes, rubber).

In general, tree species seem to have adapted to avoid ortolerate the sorts of damage to which they have been fre-quently exposed. For example, the presence of spines(Campbell 1986; Cooper and Ginnett 1998), symbiotic rela-tionships with herbivore-repelling ants (Janzen 1973), stickyexudates (Langenheim 2003), and toxic secondary com-pounds (Coley et al. 1985; Reichardt et al. 1990) are pre-sumably evolutionary responses to the pressures of differentdisturbance regimes.

Most studies on responses of tree stems to damage havefocused on xylem damage. Most prominently, the ‘‘compart-

mentalization of decay in trees’’ (CODIT) model of Shigoand collaborators (1984) elucidates the successive steps in-volved in preventing the advancement of wood decay.Although compartmentalization of decay in bark has not re-ceived as much attention (but see Mullick 1977; Biggs 1984;Trockenbrodt 1990), the process is essentially similar towood compartmentalization (Dujesiefken and Liese 1996)and is characterized by wound periderm formation after accu-mulation of lignin and suberin in existing tissues (Biggs 1985).

The CODIT model explains how tree stems contain theadvancement of decay. The process includes cellular modifi-cations (e.g., cell wall formation) as well as synthesis andtransport of chemical compounds induced by the action ofseveral hormones, including ethylene, that activate repairgenes. The associated genes start a cascade of events, suchas the induction of phytoalexins (i.e., antimicrobial substan-ces; Shain 1979, 1995) and the division and enlargement ofparenchyma cells (Lev-Yadun and Aloni 1992). Simultane-ously, conductive elements in xylem are clogged by gums,slime plugs, or tyloses, while the phloem conduits areplugged by callose. The vascular cambium adjacent to thewound also lays down a single-cell layer barrier zone, whichseparates the tissues formed before and after wounding andrestricts the growth of fungi and bacteria. This barrieragainst desiccation and infection by pathogens is further re-inforced by the suberization of parenchyma cells in the zoneadjacent to the wound (Biggs 1984, 1986a). Once this pri-mary barrier is formed, several other chemical and anatomi-cal boundaries develop (Pearce and Rutherford 1981).Elsewhere near the wound, phytoalexins and phenolic com-pounds are mobilized and accumulated, which further retardthe longitudinal and radial spread of fungal pathogens(Blanchette and Biggs 1992). Later, a new phellogen (i.e.,the cambium that produces bark tissues) differentiates adja-cent to the pre-existing phellogen in the surrounding bark,and a new vascular cambium forms beneath the phellogen.In species with exudates, insects and pathogens are often de-

Table 1. Bark characteristics of tree species that inhabit lowland forests in Amazonian Bolivia.

Density (g/cm3)

Species (family) Bark descriptionTotal barkthickness (cm) Exudate Wood Bark

Innerbark

Outerbark

Ampelocera ruizii(Klotzsch) (Ulmaceae)

Fluted trunk with long shallow fissures,bark fibrous and soft, vascular cambiumwhite; dry blaze

0.5 (very thin) None 0.69 0.31 — —

Pseudolmedia laevis (Ruiz &Pav.) J.F. Macbr.(Moraceae)

Surface smooth with abundant reddishbrown lenticels; inner bark reddish,wet blaze

0.7 (thin) Abundant stickylatex (cafe-au-lait)

0.68 0.35 — —

Pouteria nemorosa(Baehni) (Sapotaceae)

Shallow fissured bark, hard, dry blaze 0.95 (thick) Abundant whitesticky latex

0.72 — 0.25 0.23

Hura crepitans L.(Euphorbiaceae)

Rugose bark with prickles; fibrous texture;wet blaze; tags nailed into bark wereejected and found at tree base

1.1 (thick) Abundant viscousopaque latex

0.42 — 0.22 0.35

Chorisia speciosaA. St.-Hil. (Bombacaceae)

Smooth, green, abundant prickles; innerbark red and fibrous; photosynthetictissues inside cracks

1.1 (thick) Clear 0.21 0.22 — —

Cyclolobium blanchetianum(Tul.) (Leguminosae)

Deeply longitudinal fissured, corky texture 1.3 (very thick) None 0.66 — 0.35 0.27

Cavanillesia hylogeiton (Ruiz& Pav.) (Bombacaceae)

Smooth green bark; translucid periderm;inner bark white and fibrous

1.6 (very thick) Clear 0.18 0.22 — —

Note: Density is defined as dry mass / fresh volume (n = 5 samples/species). Bark thickness corresponds to the estimated value of a 20 cm DBH tree, afterfitting a line to a data set that included 35 individuals/species of a range of DBH. Bark terminology according to Junikka (1994).

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Table 2. Means of anatomical and functional traits of seven tree species from Amazonian Bolivia.

(a) Xylem

SpeciesVessel diameter(mm)

Vessel density(mm/mm2)

Ray width(mm)

Axial parenchymacell diameter (mm)

Axial parenchyma celldensity (mm/mm2)

A. ruizii 249.3 13.3 148.2 105.9 118.6P. laevis 300.1 18.7 105.2 17.7 146.2P. nemorosa 323.3 6.8 50.7 22.0 37.6H. crepitans 344.2 3.4 31.3 35.0 71.4C. speciosa 412.5 2.3 175.7 77.1 112.6C. blanchetianum 236.3 15.8 50.7 20.5 73.8C. hylogeiton 365.8 3.0 182.5 67.2 156.6

(b) Phloem

SpeciesRay width(mm)

Max. ray width(mm)

Ray distance(mm) Live bark (%) Inner bark (%)

A. ruizii 271.32 271.32 358.68 95.13 49.8P. laevis 104.16 331.52 201.6 81.93 50.6P. nemorosa 53.2 179.76 172.76 33.46 34.6H. crepitans 31.64 31.64 147.84 100 74.2C. speciosa 178.64 1062.6 495.6 62.59 88.8C. blanchetianum 55.44 222.32 120.68 34.66 25.6C. hylogeiton 175.84 835.56 368.48 42.66 90.4

Note: Distance between phloem rays corresponds to the average of 3 points along the non-dilated portions. For all traits, n = 5 individuals/species and 3 sections/individual (see text for explanation).

Fig. 1. Results of principle components analysis (PCA) of xylemanatomical and structural traits for seven tree species from the low-land in Amazonian Bolivia. Traits measured were vessel diameter(VEDI) and abundance (VEDEN), ray width (RAWI), axial parench-yma cell diameter (AXDA) and abundance (AXDE), and wood den-sity (DEN; n = 5 individuals/species). Am, Ampelocera ruizii; Ca,Cavanillesia hylogeiton; Sp, Chorisia speciosa; Ps, Pseudolmedialaevis; Ne, Pouteria nemorosa; Cy, Cyclolobium blanchetianum; Hu,Hura crepitans. Numbers in parentheses indicate proportion of var-iance explained by each axis.

Fig. 2. Results of PCA of phloem anatomical traits on seven treespecies from from the lowland in Amazonian Bolivia. Traits exam-ined were ray width (RAWI), maximum ray width (MAXRAWI),inter-ray distance (RADIST), percentage of inner bark (IN), andproportion of live inner bark (LIVEIN; n = 5 individuals/species).For an explanation of abbreviations see Fig. 1. Numbers in par-entheses indicate proportion of variance explained by each axis.

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terred when these substances are exuded onto exposed sur-faces after damage.

Responses to stem damage vary primarily with the tissuesaffected and the extent of damage (Guariguata and Gilbert1996; Pinard and Huffman 1997; Pariona et al. 2003;Schoonenberg et al. 2003). Season of wounding can also beimportant, owing to variations in cambial activity (Duje-siefken and Liese 1990) and tissue moisture content (Puritchand Mullick 1975).

This research focuses on the response patterns to damageto tree stems as influenced by wood and bark characteristics.Based on the reactions to stem wounding of a diversity oftropical tree species, we explore stem-wounding response asa functional trait that affects tree fitness.

Materials and methods

The study was carried out in La Chonta Limitada TimberConcession in Guarayos Forest Reserve (15845’S, 62860’W)in the Department of Santa Cruz, Bolivia. This forest is clas-sified as a humid tropical forest (200–400 m a.s.l.; meanannual temperature = 24.5 8C; mean annual rainfall =1400 mm).

Seven tree species with contrasting bark characteristicsand similar girths (Table 1; n = 10 individuals/species; 25–35 cm diameter at breast height (DBH)) were selected fortreatment from a list of 120 species surveyed for responsesto manual and chemical girdling (Pariona et al. 2003). Spe-cies were selected to represent a range of bark thicknesses(i.e., inner and outer) and the presence or absence of exu-dates. The stem damage experiment involved removing rec-tangular sections (approximately 8 cm2) penetrating beyondthe vascular cambium with a hammer and chisel; only trees

with no evidence of earlier damage were used. For latex-producing species an additional treatment was carried out inwhich latex was wiped from the exposed wound until itstopped flowing.

Trees were harvested with a chainsaw 2 years after wound-ing, and cross-sections of the damaged site were made. Wemeasured the proportion of the initial wound that hadclosed and the maximum extent of radial decay penetrationinto the xylem. Samples of the most recently formed wood,inner bark, and outer bark were collected to determine den-sity (dry mass / fresh volume) by water displacement anddrying for 72 h at 80 8C (n = 5 samples/species). Materialfor histological studies and measurements from the mostrecent wood and bark was preserved in formalin-aceticacid (FAA).

Anatomical studiesAfter fixing in FAA, xylem and phloem samples were

rinsed with distilled water and stored in 70% ethanol. Inpreparation for microscopic evaluation, samples were againrinsed in distilled water and soaked in Aerosol OT (Merck)for 36 h, sectioned at 20–30 mm with a sliding microtome(n = 3 sections/individual; n = 5 individuals/species), stainedwith Toluidine blue 0.05%, and measured with a stage mi-crometer at various magnifications. We measured meanmaximum xylem vessel diameters and densities, ray widths,and the diameters and densities of axial parenchyma cells. Inthe phloem, we measured the thickness of inner and outerbark, ray widths (midpoints and maxima), distance betweenrays (average of 3 points along the non-dilated portion), andproportion of live and dead tissues in the inner bark. Thesetraits were measured on 10 linear transects/section.

Fig. 3. Wound closure rates of seven tree species from the lowlandin Amazonian Bolivia (n ‡ 10 individuals/species). Circle sizes re-present the number of overlapping individual observations. /L indi-cates that latex was not removed.

Fig. 4. Extent of radial xylem decay penetration in seven tree spe-cies from the lowland in Amazonian Bolivia after experimentalstem damage (n ‡ 10 individuals/species). /L indicates that latexwas not removed.

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Data analysesLikelihood methods were used for most data analyses.

These methods permit consideration of the application ofdifferent models to the same data, with the null model beingthat all species respond the same way. Formulation of a ser-ies of models permits examination of different assumptionsregarding how a particular system operates and allows incor-poration of a diversity of data, thus facilitating identificationof the prominent traits of the system (Hilborn and Mangel1997). Between-species comparisons of percent wound clo-sure and decay penetration were made with one-way ANOVA.Permutation tests were carried out to further explore re-sults. Statistical tests were performed in R (R DevelopmentCore Team 2005) and reported at p < 0.05. We tested fordifferences among all the species, differences among spe-cies with particular attributes such as thick bark or latexpresence, and the effects of latex removal. The Pearsonproduct moment correlation between percent wound closureand radial decay penetration (species means) was calculatedusing SAS Version 8e (SAS Institute Inc., Cary, N.C.). Re-siduals were examined independently for percent woundclosure and extent of radial xylem decay penetration asfunction of tree diameter, to determine the effect of treegirth on the response variables. Principal component analy-sis (PCA) was used to investigate relationships betweenxylem and phloem anatomical variables independently. Re-gression analyses were carried out using the PCA scoresfor the first axis for xylem and phloem on radial decaypenetration and percent wound closure, respectively, to in-vestigate the explanatory value of anatomical traits withthe response variables.

Results

Anatomical dataThe species studied varied widely in stem characteristics.

Species differences in bark thickness and external aspectwere consistent with differences in phloem and xylem ana-tomical traits (Tables 2a, 2b). The proportion of live bark(i.e., between the vascular cambium and the last-formedperiderm) ranged from 33% in P. nemorosa to 100% inH. crepitans. Ray dilation was pronounced in Bombacaceaespecies. Distance between rays also varied substantiallyamong species, from 121 mm in C. blanchetianum to496 mm in C. speciosa. In the xylem, vessel diameter variedfrom 237 mm in C. blanchetianum to 412 mm in C. speciosa.Xylem ray width ranged from 31 mm in H. crepitans to182 mm in C. hylogeiton, and phloem ray width rangedfrom 53 mm in P. nemorosa to 271 mm in A. ruizii(Table 2a). The species studied can be grouped into high

(P. nemorosa, A. ruizii, P. laevis and C. blanchetianum;*0.70 g/cm3) and low (C. speciosa and C. hylogeiton;*0.20 g/cm3) wood density classes, with H. crepitans hav-ing an intermediate value (0.42 g/cm3). Eigenvalues for axis1 and axis 2 of the PCA of xylem anatomical traits ex-plained 52% and 29% of the total variation, respectively(Fig. 1). The first component was positively associated withray width and mean maximum vessel diameter. The secondcomponent was positively loaded by axial parenchyma den-sity and negatively loaded by high vessel density.

For PCA of the phloem traits, eigenvalues for axis 1 andaxis 2 explained 57% and 23% of the total variation, respec-tively (Fig. 2). The first component was positively loaded bymaximum ray width and negatively loaded by mean inter-ray distance; whereas, the second axis was heavily loadedby the proportion of axial parenchyma (Table 2b).

Residual examination demonstrated there were no signifi-cant effects of DBH on the response variables (i.e., percentwound closure and extent of radial decay penetration).

Responses to stem damageSpecies differed in the rates of wound closure as meas-

ured 2 years after damage (F[9] = 11.9; p < 0.001; Fig. 3).Percent wound closure varied among species and treatments,with C. speciosa and H. crepitans with latex removed show-ing the most rapid closure (100%) and P. laevis with latexpresent the slowest (22%).

Species also differed in the extent of xylem decay penetra-tion (F[9] = 7.2; p < 0.001; Fig. 4). Radial decay penetrationranged from 0.5 mm in P. nemorosa with latex present to1.9 mm in C. hylogeiton. There was a strong positive rela-tionship between xylem PC1 scores and radial decay pene-tration (p < 0.001; Table 3), implying that species withlow-density wood and wide rays suffered more radial decaypenetration in the xylem than species without those traits.In the phloem, there was a positive relationship betweenPC1 scores and wound closure (p < 0.05), suggesting thatspecies with large dilating rays closed wounds more rap-idly than species with thin closely spaced rays (Table 3).

There was a positive significant correlation between spe-cies means of percent wound closure and radial extent ofxylem decay penetration (r = 0.81; p < 0.001). In otherwords, species that closed wounds rapidly suffered a largeamount of radial decay penetration (Fig. 5). Finally, the pos-itive correlation between the first axes of the xylem andphloem PCAs (r = 0.87; p < 0.001) indicates that the speciesstudied had anatomical traits that favored either betterwound closure or ability to compartmentalize decay, but notboth.

Table 3. Results of regression of the scores of the first two principal component analysis (PCA) axes for xylem and phloem onradial decay penetration and wound closure, respectively.

Variable dfParameterestimate SE T Pr > [T]

Xylem anatomical traits PCA scores on radial decay penetration prin1 1 0.26 0.04 6.28 <0.0001*prin2 1 0.08 0.05 1.57 0.12

Phloem anatomical traits PCA scores on percent wound closure prin1 1 8.80 3.75 2.35 0.02*prin2 1 0.44 5.98 0.07 0.94

Note: Pr, probability; *, significant at 0.05.

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Discussion

The Amazonian tree species we studied differed in theirresponses to stem damage, particularly in wound closurerates. Species also varied in bark thickness, exudate produc-tion, and in many structural, morphological, and anatomicaltraits. Species with exudates (H. crepitans, P. nemorosa,P. laevis, C. speciosa, and C. hylogeiton), trunk thorns(H. crepitans and C. speciosa), thick live bark (H. crepitans,C. hylogeiton, and C. speciosa), or thick bark (H. crepitans,C. speciosa, C. hylogeiton, and C. blanchetianum) weremore efficient at responding to stem wounding than specieslacking these traits (A. ruizii). Species differences are corre-

lated with inner and outer bark physiology (i.e., species thatclosed wounds efficiently produced some kind of exudate),morphology (i.e., thick live bark species closed the woundbetter than those with thin live barks), and anatomy (i.e.,species with dilating rays or abundant axial parenchymaclosed wounds better than species without these traits).These results confirm previous reports of the ability of pa-renchyma cells surrounding wounds to become meristematic(Zimmermann and Brown 1971) and the role of rays inwound phellogen formation (Miller and Barnett 1983).Thus, knowledge of specific bark traits can be used to pre-dict the rates of wound closure.

The extent of xylem decay spread was positively corre-

Fig. 5. Comparison of anatomical traits of species presenting either of two responses to stem damage: efficient wound closure or efficientcompartmentalization of xylem decay. Scale bars indicate 200 mm for C. speciosa and 100 mm for P. laevis.

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lated with specific traits, such as low density wood with lowfiber content, wide dilating rays, and large vessels. These re-sults agree with previous research that indicated that afterthey are cut, large diameter vessels expose large surfaceareas, thus facilitating moisture loss and air access, whichlead to decay propagation (Eckstein et al. 1979). The largewithin-species variation we observed in xylem decay spreadsuggests that traits affecting species responses (e.g., suberinaccumulation in wounded areas) might be heritable, whichsuggests that developing resistance to particular pathogensmight take different paths (Biggs et al. 1992). Likewise, in-dividual variation in decay spread within a species might beinfluenced by individual vigor, which might be affected byresource availability. Therefore, it seems reasonable to ex-tend predictions about allocation to defense as a function ofgrowth rate (i.e., higher growth rate and less allocation todefense and vice versa; Bryant et al. 1983; Coley et al.1985) to stem responses to damage.

Our results indicate that the species studied are unable toboth close wounds efficiently and control the advancementof xylem decay. The differential ability of xylem and phloemtissues to respond to a particular pathogen was reported byBiggs (1986b). The apparent trade-off (i.e., species withtraits that promote efficient decay compartmentalization inxylem have traits that do not favor bark wound closure)suggests the need to consider morphological (e.g., allome-try), physiological (e.g., allocation), and evolutionary (e.g.,phylogenetic) constraints when examining responses tostem damage.

The results from this experiment are confined to the spe-cies selected for study, a limitation that is common to mostecological and evolutionary studies (Ackerly and Donoghue1998). Nevertheless, given that the species studied display awide range of bark morphologies and xylem characteristicsand represent a wide range of phylogenetic lineages, the re-sponses observed may represent general patterns.

Given that wood density is a good predictor of the abilityto compartmentalize decay and that wood density generallydecreases with fertility, rainfall and disturbance dependence(Muller-Landau 2004; Baker et al. 2004), we expect thatmany trees characteristic of areas with nutrient-rich soilsand plentiful rainfall are poor at stem decay compartmental-ization. Similarly, variations in life-history strategies shouldalso correspond to specific patterns of responses to stemdamage (e.g., pioneers vs. shade-tolerant species). Followingthe same logic, we predict that within species fast-growingindividuals are less able to compartmentalize decay thanslow-growing individuals.

This study on seven species of Amazonian tree speciesdemonstrated the influence of anatomical and structuraltraits on responses to stem damage. The differences ob-served in these responses among species sharing the samehabitat suggest that there are a variety of ways to cope withstem damage. Additional insights about the evolutionaryconstraints on traits associated with responses to stem dam-age will emerge from studies in which responses to stemdamage are compared in closely related species inhabitingcontrasting disturbance regimes.

AcknowledgementsWe thank the BOLFOR-USAID project for financial

support for this study. Assistance in the field was providedby Eugenio Martınez. We appreciate comments to previousversions of the manuscript by S. Mulkey, T. Martin, D. Jones,D. King, and L. Poorter. Critical feedback to this workwas also provided by F. Putz and members of the PEERSEcology Group at the Department of Botany, University ofFlorida.

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