Elevational Variation of Leaf Traits in Montane Rain Forest Tree Species at La Chinantla, Southern...

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BIOTROPICA 34(4): 534–546 2002

Elevational Variation of Leaf Traits in Montane Rain Forest TreeSpecies at La Chinantla, Southern Mexico1

Noe Velazquez-Rosas, Jorge Meave 2

Departamento de Ecologıa y Recursos Naturales, Facultad de Ciencias, Universidad Nacional Autonoma deMexico, Mexico 04510, D.F., Mexico

and

Sonia Vazquez-Santana

Departamento de Biologıa Comparada, Facultad de Ciencias, Universidad Nacional Autonoma de Mexico,Mexico 04510, D.F., Mexico

ABSTRACTVariation in leaf traits of dominant tree species in six montane rain forest communities was analyzed along anelevational gradient ranging from 1220 to 2560 m within a single basin at La Chinantla, Oaxaca, Mexico. Threegroups of characters were used: morphological (leaf shape, margin, blade configuration, and phyllotaxy), morphometric(leaf area, leaf mass per area, stomatal density, and blade length/width ratio), and anatomical (thicknesses of blade,palisade [PP], and spongy [SP] parenchymae, PP/SP ratio, and epidermis and cuticle thicknesses). The variation ofmorphological characteristics was only evident at the highest elevations; in contrast, thickness of leaf blade, PP, SP, aswell as leaf mass per area clearly increased along the gradient, whereas leaf area was the only variable that significantlydecreased with elevation. Thicknesses of epidermis and of the two cuticles were not significantly correlated withelevation. A classification analysis based on a leaf trait matrix led to the distinction between low and high elevationcommunities, with an approximate limit between them at ca 2300 to 2400 m. The results are discussed in light ofenvironmental changes occurring along elevational gradients. Leaf characteristics of montane rain forest plants offerimportant insights about the complex roles of abiotic factors operating in these environments and supplement thetraditional physiognomic classification schemes for these communities.

RESUMENSe analizo la variacion de caracterısticas foliares de las especies arboreas dominantes en seis comunidades de bosquelluvioso de montana ubicadas a lo largo de un gradiente altitudinal comprendido entre 1220 y 2560 m s.n.m. dentrode una misma cuenca en la region de La Chinantla, Oaxaca, Mexico. Se utilizaron tres tipos de caracteres: morfologicos(forma de la hoja, tipo de margen, configuracion de la lamina y filotaxia), morfometricos (area foliar, masa foliar porunidad de area, densidad estomatica y cociente largo/ancho de la lamina), y anatomicos (grosor de la lamina, de losparenquimas en empalizada [PEm] y esponjoso [PEs], cociente PEm/PEs y grosor de la epidermis y de la cutıcula).La variacion de las caracterısticas morfologicas solo fue evidente en los sitios de mayor elevacion; por el contrario, losgrosores de la lamina foliar, el PEm y el PEs, ası como la masa foliar por unidad de area aumentaron claramente alo largo del gradiente. El area foliar fue la unica variable que mostro un decremento significativo con la altitud. Losgrosores de la epidermis y las dos cutıculas no se correlacionaron significativamente con la altitud. Un analisis declasificacion basado en una matriz de caracterısticas foliares permitio distinguir comunidades de baja y de alta altitud,cuyo lımite se ubica aproximadamente entre 2300 y 2400 m s.n.m. Los resultados son discutidos a la luz de loscambios ambientales que tienen lugar a lo largo de gradientes altitudinales. Las caracterısticas foliares de los bosquesmontanos lluviosos proporcionan claves importantes sobre el papel relativo de los factores abioticos que operan enestos ambientes y complementan los esquemas fisonomicos de clasificacion de estas comunidades.

Key words: adaptive morphology; elevational gradient; cloud forest; leaf anatomy; leaf characteristics; leaf morphology;Mexico; montane rain forest; Oaxaca.

CHANGES IN SPECIES COMPOSITION AND STRUCTURE OF

TROPICAL PLANT COMMUNITIES along elevational gra-

1 Received 16 April 2001; revision accepted 16 Septem-ber 2002.2 Author for correspondence; e-mail: [email protected]

dients have been amply recognized. Floristic rich-ness and diversity decrease toward higher elevations(Leigh 1975, Grubb 1977, Kappelle & Zamora1995, Kitayama 1995, Kappelle 1996, Liebermanet al. 1996, Richards 1996, Vazquez-G. & Givnish1998). Similarly, as elevation increases, reductionsin canopy height and increments in tree density are

Elevational Variation of Montane Forest Leaves 535

common. This latter change is usually accompa-nied by modest albeit noticeable increases in totalbasal area of the community (Lieberman et al.1996, Williams-Linera et al. 1996, Vazquez-G. &Givnish 1998).

Physiognomic variations along elevationalchanges have also been documented. For example,trees become shorter and their crowns tend to bemore compact with increasing elevation (Whit-more 1984). Among the different plant attributesthat have been studied, leaf characteristics appearto display the largest changes along this gradient:leaf size is reduced, varying from mostly mesophyllin the lowlands to notophyll and nanophyll in thehighlands, and leaf blade thickness tends to in-crease as leaf area decreases (Howard 1969, Grubb1977, Dolph & Dilcher 1980, Tanner & Kapos1982, Givnish 1984, Bruijnzeel et al. 1993). It isnoteworthy that the majority of these trends havebeen identified by comparing results from pointstudies conducted at different sites, most of whichwere located in regions far apart from each other,while the analysis of leaf attributes on the slopes ofsingle valleys or mountains are extremely scarce(Tang & Ohsawa 1999). The existence of partic-ular species pools in the different biogeographicalregions, as well as the preponderant influence oflocal factors on vegetational altidudinal gradients(Tang & Ohsawa 1999) precludes drawing conclu-sions with any level of generality.

Given the well-known adaptive value of leaftraits in various ecosystems (Dolph & Dilcher1980, Chabot & Hicks 1982, Givnish 1984, Roth1984), leaf attributes may be good indicators of therelationships between vegetation and elevationalgradients in tropical montane regions. Most studieson this topic, however, have been conducted in re-gions of low latitude, and information on leaf traitpatterns in montane rain forests near the fringes oftheir biogeographical range is lacking. The north-ern limit of montane rain forests in North Americais located in Mexico (Rzedowski 1978, Webster1995). Despite the scarcity of climatic data forthese areas, we suspect that temperature gradientsare steeper than at sites located closer to the equa-tor given the low angles of the sun in the sky (ca508 above the horizon) during winter months.Thus, at certain elevations phenomena such as frostor wind-related cooling may take place, whereas atlower latitudes these may be dampened or absentat the same elevation.

In this paper, we analyze patterns of leaf mor-phology and anatomy variation among dominantspecies of montane forest communities located

along an elevational gradient in La Chinantla, ahyper-humid region of southern Mexico. This wa-ter surplus may have complex consequences onother environmental factors; among them, soil fer-tility may be particularly affected through leachingand anaerobic conditions associated to soil per-manent saturation, and transpiration rates may bemuch lower than in less humid environments. Weaddressed the following questions: Do leaf traits ofdominant species change significantly along the ele-vational gradient within a single basin? If so, dothe different leaf characteristics display changes ofequivalent magnitude and direction?; and Are thesechanges analogous to those inferred from combin-ing the results from sites located at different ele-vations but in separate locations?

STUDY SITE

The study was conducted in the surroundings ofSanta Cruz Tepetotutla, located in the Sierra Norterange, Oaxaca State, southern Mexico (17838–178409N, 96832–968339W; Fig. 1). The region hasa very abrupt topography with slopes ranging be-tween 10 and 508. The shallow soils are derivedfrom metamorphic rocks and have high organicmatter, N, and P contents (Van der Wal 1998).The only climatic records, coming from a presentlyabandoned meteorological station located at 1450m elevation, indicate a transitional climate betweentemperate and tropical, with annual means of ca5800 mm for precipitation and 16.58C for tem-perature (Rzedowski & Palacios-Chavez 1977).The vegetation along the elevational range wherethe study was conducted (1200–2600 m) consistsof a mosaic of well preserved forest communities,mostly arranged by elevation, which were prelimi-nary classified as premontane and montane forests(Meave et al. 1994, 1996).

Although no climatic data specific for the studysites are available, field observations and generalprinciples on montane rain forest ecology allow tomake some speculations about the nature of theelevational changes of the environment. By usinglapse rates of 0.5 to 0.68C for every 100 m (Whit-more 1984, Ohsawa 1990, Cavelier 1996), we es-timated that temperatures of the highest sites couldbe on average 5 to 88C colder than the lowest ones.In addition, at higher sites mineral soils are verythin and covered by a thick layer of decomposingorganic matter, suggesting low decomposition andmineralization rates (Edwards & Grubb 1977, Tan-ner et al. 1998). Thus, fertility may also be differ-ential, with richer soils located at lower elevations,

536 Velazquez-Rosas, Meave, and Vazquez-Santana

FIGURE 1. Location of six montane rain forest communities at La Chinantla, Oaxaca, Mexico (S1 5 1220, S2 51830, S3 5 2010, S4 5 2260, S5 5 2430, and S6 5 2560 m elev).

and less fertile ones in the higher portions of themountain range. Estimating the magnitude and di-rection of rainfall variation with altitude is not asstraightforward. Our field observations stronglysuggest that rainfall in the mountains is greaterthan at adjacent lowland regions, where forestshave a larger degree of deciduousness (Hernandez-X. 1977; J. Meave, pers. obs.), but it remains un-known what portions of this elevational range re-ceive the largest and the smallest amounts of pre-cipitation.

MATERIALS AND METHODS

Data were gathered at six sites located on thenorth-facing (leeward) slopes of the Perfume Riverbasin, at the following elevations: S1, 1220; S2,1830; S3, 2010; S4, 2260; S5, 2430; and S6, 2560m elevation (Fig. 1). At each site, 32 fully expand-

ed, pathogen and herbivore damage-free leaveswere collected from the upper part of the canopiesof at least three different trees belonging to the tendominant species. Dominance had been previouslyassessed with the relative importance values (sumof relative basal area, frequency, and density by spe-cies), calculated in sampling units composed of tentransects totaling 0.1 ha per site (A. Rincon, pers.comm.). Mean percent basal area corresponding tothese species at the six sites was 82.3 6 13.9 per-cent (range: 61.6–97.8%), whereas mean (61 SD)percent density was 74.5 6 6.9 (range: 64.5–81.0%). Assuming a positive correlation betweenthese two variables, especially basal area and canopycover, the selected sets of ten dominant speciesprobably represent ca 75 percent of total cover ineach site. Some species were among the dominantgroup in more than one site; thus, the total numberof species in the entire sample was 43 (Appendix


1). Analyzing leaf traits of dominant species insteadof doing so for all species present at each site issomewhat limiting, as leaf traits of subordinate spe-cies may be the very cause of their minor contri-bution to forest structure; also, this approach doesnot allow identification of leaf types that are absentfrom (i.e., are nonfunctional in) certain environ-ments. The large numbers of species, particularlyat the lowest sites, made it impossible to includeall species in the study; however, the dominant spe-cies approach is worthwhile using because it allowsto identify general canopy properties along the ele-vational gradient.

We recognized three groups of traits: (1) mor-phological (N 5 30 leaves per species per site),including leaf blade shape (one of the four basicpatterns established by Hickey [1973]: elliptic,ovate, obovate, and oblong), leaf blade configura-tion (single vs. compound), type of margin (entirevs. non-entire), and phyllotaxy (alternate vs. op-posite); (2) morphometric (N 5 30 leaves per spe-cies per site): leaf area (measured with a leaf areameter, Delta Image Analysis System), leaf mass perunit area (g/m2), and blade length/width ratio; and(3) anatomic (N 5 2 leaves per species per site):leaf blade thickness, thicknesses of palisade (PP),and spongy (SP) parenchymae (and their ratio PP/PS), and thicknessess of both adaxial (upper) andabaxial (lower) cuticles and epidermis. Determina-tion of anatomical traits for each species was donein two transversal cuts performed in the centralpart of leaf blades. The leaf tissues were fixed inFAA (formalin, acetic acid, 96% ethanol, water 2:1:10:7). After dehydration in a gradual series ofethyl alcohol, the material was then infiltrated withParaplast, subsequently embedded in the same ma-terial, and then cut at 10 mm; these sections werestained with saphranin and fast green. The slideswere examined and anatomic measurements weredone on an Olympus CTH light microscope.

Comparisons of morphological traits werebased on the frequencies of the different categoriesat the six sites, while morphometric and anatomicalcharacteristics were compared with one-way ANO-VAs. When results were significant, a least signifi-cant differences test (LSD; Zar 1999) was applied.We calculated Pearson product–moment correla-tions between elevation and both morphometricand anatomical characteristics. A numeric classifi-cation based on the leaf traits assessed was obtainedby using the unweighted pair–group average meth-od (UPGMA; Gauch 1982) with Euclidean dis-tances; to avoid biases due to the different magni-tudes of the assessed variables, these were standard-

ized in all cases. Based on the results of the classi-fication, a x2 test for contingency tables wasconducted to determine the association betweenmorphological characteristics and elevationalgroups.

RESULTS

MORPHOLOGY. Changes in morphological traitsalong the elevational gradient are shown in Figure2. Elliptic leaves prevailed at five sites (Fig 2a; fre-quency range: 70–90%), with the exception of S5and S6, where ovate leaves had the only high valuesamong all sites (50%). Obovate shapes occurred atall sites albeit with constantly low frequencies,whereas oblong leaves were almost always absent(Fig. 2a). Leaves with entire margins prevailed atall sites, but at high elevation sites (S5 and S6) theirfrequency decreased slightly (from 70–80% to60%; Fig. 2b). Simple leaves were the commonestin all sites, and in fact were the only type found athigher elevations (Fig. 2c). The most distinct dif-ferences between low and high elevation sites wereobserved for phyllotaxy: although alternate leavesprevailed at all sites (except at S2), they were theonly type present at higher elevations (Fig. 2d).

MORPHOMETRY. Among morphometric character-istics only leaf area varied with elevation (Fig. 3).A significant, negative correlation was found be-tween these two variables (r 5 20.34; df 5 67; P, 0.05). Despite apparent increasing trends for leafmass per area and stomatal density, these variableswere not significantly correlated with elevation, andno significant differences for them were foundamong sites.

ANATOMY. Some anatomical characters were themost sensitive ones to the elevational gradient (Fig.4). Blade thickness (Fig. 4a) and thicknesses of pal-isade and spongy parenchymae (Fig. 4b, c) werepositively correlated with elevation (r 5 0.45, P ,0.001; r 5 0.5, P , 0.0001, and r 5 0.26, P ,0.05, respectively, with df 5 57 in all cases). In thisincreasing pattern, S5 had the highest values forleaf blade and palisade parenchyma thicknesses(322 mm; F 5 3.06, P , 0.05; and 125 mm; F 59.17, P , 0.001, respectively). Thicknessess of epi-dermis and cuticles (both adaxial and abaxial; Fig.4e–h) were similar among all sites and were notsignificantly correlated with elevation.

CLASSIFICATION ANALYSIS. In the classificationbased on all leaf traits studied (Fig. 5), a clear group


FIGURE 2. Leaf morphology traits of the ten dominant tree species in six forest communities at La Chinantla,Mexico. (a) form (elliptic [white], obovate [black], ovate [dashed], oblong [gray]); (b) margin (entire [white], non-entire [black]); (c) blade configuration (simple [white], compound [black]); and (d) phyllotaxy (alternate [white],opposite [black]).

containing all sites between 1220 and 2260 m wasformed, with the core of highest similarity betweenS3 and S4. In contrast, the two sites located athigher elevations remained unclustered. The rec-ognition of a low elevation group allowed a statis-tical comparison of the frequencies of morpholog-ical traits between it and the two high sites. Fre-quencies of shape, margin, and phyllotaxy typeswere significantly associated with the elevationalposition (shape x2 5 6.9, P , 0.01; margin x2 53.9, P , 0.01; phyllotaxy x2 5 4.9, P , 0.05);ovate and obovate leaves with non-entire marginsand with alternate phyllotaxy were significantlymore frequent at sites with higher elevations.

DISCUSSION

RELATIONSHIPS BETWEEN LEAF TRAITS AND ENVIRON-MENT AT LA CHINANTLA. The adaptive significanceof the leaf traits studied here has been little ex-plored for tropical montane forest plants. The re-sults of this study show that in general leaf traitsrespond clearly to the elevational gradient at LaChinantla, and that the observed patterns show an

overall good correspondence with those inferredfrom the comparison of several sites distributedover a range of elevations in different locations ofthe tropical world. Among the three groups ofstudied traits, the largest elevation-related variabil-ity was found for some anatomical characteristics(namely leaf blade, palisade, and spongy parenchy-mae thicknesses). These were followed by morpho-metric variables (in particular, leaf area), whereasthe differentiation of morphological characteristicswas rather limited to the highest elevations.

The observed significant decreases in leaf areawith elevation may be primarily associated to tem-perature reductions, as has been found for manytropical montane plant communities (Dilcher1973, Leigh 1975, Dolph & Dilcher 1980, Oh-sawa 1990, Tang & Ohsawa 1999). The low tem-peratures of these environments have profound ef-fects on plant metabolism, and they have been sin-gled out as an overriding factor in determiningtheir structural and physiognomic patterns (Leigh1975, Grubb 1977, Whitmore 1984, Jones 1992,Cavelier 1996). Leigh (1975) claimed that lowertemperatures reduce cell growth, producing an


FIGURE 3. Leaf morphometry traits of dominant treespecies in six montane forest communities at La Chi-nantla, Mexico.

overall decrease in leaf size; however, it has beenshown that although low temperatures affectgrowth rates at the whole-plant level, they do notreduce cell expansion (Korner 1999). A second en-vironmental factor recognized to influence leaf sizealong elevational gradients in tropical mountains issoil fertility (Grubb 1977, Tanner & Kapos 1982);in particular, strong deficits in soil N have beeninvoked as the cause of the existence of small,thick, nutrient-conserving leaves at higher eleva-tions (Tanner et al. 1998). Unfortunately, we lackdata showing such changes in N availability alongthe studied gradient to examine this hypothesis. Fi-

nally, leaf size may also be related to wind exposure,as smaller leaves are less prone to wind damage(Dolph & Dilcher 1980, Sugden 1982, Kappelle1996). This relationship could be in part respon-sible for the irregular changes observed along thealtitudinal gradient. In particular, S5 was more ex-posed to winds and accordingly its average leaf sizewas smaller than expected on the basis of its ele-vation.

The reduction of the proportion of species withentire margins with altitude was modest at La Chi-nantla. This result neither matches the findings byBrown (1919, cited in Howard 1969) and Dilcher(1973), nor corresponds to the generalization madeby Wolfe (1971) that serrate margins are morecommon at sites with lower temperatures. Accord-ing to this latter author, serrate margins induce abreakage of the boundary layer around leaves, al-lowing drier air to come into the leaf vicinity andthus enhancing transpiration. Therefore, serratemargins should be more common in forests with aconstantly high atmospheric humidity. Althoughwe lack a satisfactory explanation for the rarity ofthis trait even in high altitude sites at La Chinantla,our results cast some doubt on the generality ofthis adaptive value.

One of the clearest changes with elevation atLa Chinantla was the increase in mesophyll thick-ness. It has been suggested that the prevailing an-atomical traits in tropical montane forests shouldbe interpreted as direct responses to soil nutritionalstatus (Small 1972, Grubb 1977, Tanner 1977,Tanner & Kapos 1982, Givnish 1984, Medina etal. 1990, Leal & Kappelle 1994, Turner 1994).Plants growing in soils with low P and N avail-ability usually bear thick leaves, with well devel-oped mesophyll and cuticles (Chabot & Hicks1982). The results obtained for the mesophyll, butnot for the cuticles, point out to the possibility ofnutrient deficiencies at the higher sites.

The elevational increase of mesophyll thickness,especially for the palisade parenchyma, may be alsorelated to CO2 fixation. Tropical montane forestsare also known as cloud forests precisely because ofthe almost permanent cloud layer that covers themduring extended periods of time. This phenome-non causes a low radiation balance in these systems,ultimately affecting photosynthetic rates (Bayton1968). These negative effects may be compensatedfor by having a more efficient photosynthetic ap-paratus that allows plants to benefit from the in-frequent sunny periods (Grubb 1977, Cavelier1996). Although it may be argued that the presenceof thick parenchymae is paradoxical in N-limited


FIGURE 4. Leaf anatomy traits of dominant tree species in six montane forest communities at La Chinantla, Mexico.In all graphs the plotted variable is thickness of the named tissue, except for PP/SP ratio.

environments, one must consider the fact that insuch places leaves usually have very long life spans(Tanner et al. 1998). Thus, despite the relativelylarge costs of constructing leaves with thick pa-renchymae in oligotrophic habitats, the N investedin them may be used more efficiently, as leaves re-main active for longer periods of time (Medina etal. 1990). In addition, there are indications that ininfertile habitats high translocation rates are morefrequent than in fertile ones (Chabot & Hicks1982). Incidentally, the lack of response of the cu-ticles to elevation was surprising, as thick cuticleshave been suggested to be a protective featureagainst lixiviation of nutrients from the leaves andthe negative effects of UV radiation on internal

tissues at higher elevations (Grubb 1977, Jones1992, Flenley 1995, Cavelier 1996).

At the three high sites, all species had alternateleaves. Although the adaptive value of phyllotaxy iscontroversial, Givnish (1984) proposed that it af-fects the amount of radiation received by the leaves.Before drawing more definite conclusions aboutthe implications of the observed pattern for thistrait at La Chinantla, it would be necessary to dis-card the possibility that the differences between lowand high elevations simply result from the phylo-genetic constraints associated to the biogeographi-cal affinities of the differential familial compositionof these forests.

One of the benefits of examining leaf traits


FIGURE 5. Classification of six montane rain forestsites at La Chinantla, Mexico, based on a matrix of leaftraits. The dendrogram was obtained with the UPGMAmethod and using Euclidean distances.

TABLE 1. Summary of leaf morphology traits in several montane forest communities. LMRF 5 lower montane rain forest;UMRF 5 upper montane rain forest; MMF 5 mesophyll montane forest; and MRF 5 montane rain forest.When available, percentages in parentheses indicate the proportion of total leaf sample analyzed that correspondsto a given specific category. Sites are arranged in increasing elevational order, except La Chinantla, as it comprisesseveral elevations.

Site, forest type,and elevation

Dominantleaf size

(%)

Dominantblade

configur-ation (%)

Dominantmargin

type (%)Dominantshape (%) Source

Macuira, ColumbiaCloud forest (865 m) Microphyll Simple — Elliptic Sugden 1982Pico del Oeste, Puerto RicoElfin Forest (1050 m)

Microphyll(57)

Simple Entire(70)

— Howard 1969

Omiltemi, MexicoMMF (2100 m)

Mesophyll(81)

Simple(81)

Entire(63)

— Meave et al. 1992

New GuineaLMRF (2500 m)

Notophyll Simple — — Grubb 1977

VenezuelaCloud Forest (2550–2650 m)

Notophyll(31)

Simple — — Kelly et al. 1994

Talamanca, Costa RicaUMRF (2975 m)

Notophyll(47)

Simple(85)

Entire(70)

Elliptic(50)

Kappelle & Leal 1996

New GuineaUMRF (3300 m)

Microphyll Simple — — Grubb 1977

La Chinantla, MexicoMRF (1220–2560 m)

Microphyll(39)

Simple(85)

Entire(60)

Elliptic(66)

This study

along an elevational gradient within the same basinis the possibility of discriminating between twophenomena potentially responsible of the observedchanges. On one hand, individual species withbroad elevational distributions may show plastic re-sponses by having different physiologies and evenmorphologies (Geeske et al. 1994, Velazquez-Rosas2000). On the other, elevational patterns in leafmorphology may be only related to changes in flo-ristic composition that always exist along mountainslopes. Our data show a large turnover amongdominant species, and it is reasonable to assume

that at each elevation plants have different adap-tations to those specific environmental conditions;however, a few dominant species and some otherssuch as Drimys granadensis, which were dominantat some sites but not in others (A. Rincon, pers.comm.), showed a large variation in leaf size alongthe gradient. Vaccinium consanguineum provides anexample of this variation (Appendix 1). This spe-cies had relatively large leaves at its lower location(mean leaf area 5 3.5 cm2), much smaller at thehighest one (2.2 cm2), but its largest leaves (5.0cm2) occurred at an intermediate elevation. In ad-dition, thicknesses of leaf blade and of both pa-renchymae increased with elevation.

COMPARISON WITH OTHER MONTANE FORESTS. Mor-phological descriptions of the leaves of montaneforests species are scarce, and they seldom includethe existing variability along local elevational gra-dients. Despite these limitations, we made an gen-eral comparison between the overall leaf trait pat-terns found at La Chinantla and those from othersites (Tables 1 and 2). Apart from changes alongthe elevational gradient, leaf morphology at LaChinantla was generally more similar to that foundin other montane forests than we originally ex-pected (Table 1), considering its marginal locationat the northern boundary of its geographical range.

Shared leaf traits between La Chinantla and


TABLE 2. Summary of anatomical leaf traits in several montane forests. LMRF 5 lower montane rain forest; UMRF 5upper montane rain forest; PP 5 palisade parenchyma; SP 5 spongy parenchyma; and n.d. 5 no data. Figuresin bold are from this study.

Site andforest type

Eleva-tion (m)

Leafbladethick-ness(mm) PP/SP

Uppercuticlethick-ness(mm)

Lowercuticlethick-ness(mm) Source

Pico del Oeste, Puerto RicoElfin forest

La Chinantla Mexico, S1Jamaica, UMRFLa Chinantla, Mexico, S2La Chinantla, Mexico, S3La Chinantla, Mexico, S4La Chinantla, Mexico, S5New Guinea, LMRFLa Chinantla, Mexico, S6Talamanca, Costa Rica

UMRFNew Guinea, UMRF

105012201500183020102260243025002560

29753300

380186237235237242322300280

220376

2.01.52.12.11.51.71.1n.d.1.2

1.43.5

6.43.55.43.92.43.75.95.54.2

n.d.7.4

3.31.84.32.11.62.43.22.61.8

4.33.5

Howard 1969This studyTanner & Kapos 1982This studyThis studyThis studyThis studyGrubb 1977This study

Leal & Kappelle 1994Grubb 1977

other montane forest sites are simple leaves (all sitesin Table 1), entire margins (Pico del Oeste, PuertoRico [Howard 1969]; Omiltemi, Mexico [Meave etal. 1992]; Talamanca, Costa Rica [Kappelle & Leal1996]), and elliptic shape (Sierra de Macuira, Co-lombia [Sugden 1982]). In relation to leaf size, themicrophyll class was dominant in our area, as itwas in upper montane communities in New Guin-ea (Grubb 1977), Pico del Oeste (Howard 1969),and Sierra de Macuira (Sugden 1982; Table 1). Theabundance of small leaves in these forests is one ofthe features that better distinguishes them fromtypical lowland tropical forests (Howard 1969,Grubb 1977, Dolph & Dilcher 1980, Tanner &Kapos 1982, Whitmore 1984).

With respect to elevational changes of anatom-ical leaf traits, some findings at La Chinantlashowed a good agreement with other sites (Table2). Decreases in leaf area and increases in leaf bladethickness toward higher elevations, both found tobe significant changing trends at La Chinantla, arecommon in montane forests. For given elevations,however, cuticle thicknesses and SP/PP ratio valuesobtained by us were smaller than in most othersites where these variables have been assessed, sug-gesting that they show a more limited response toelevation. Unfortunately, there is a tremendousdearth of data in the literature to make these kindsof comparisons, and among the few existing stud-ies, only a minority have published data separatedby species (Howard 1969, Leal & Kappelle 1994).

CONCLUDING REMARKS. The large heterogeneity ofplant communities in tropical mountain regions

has driven many authors to propose classificationschemes for the vegetation that develops along theirslopes. These are usually based on structural andcompositional criteria, while much less importancehas been given to plant morphology and overallphysiognomy. Nonetheless, the study of morphol-ogy, particularly that of the leaves, may be a usefultool for classification purposes (Tang & Ohsawa1999).

In this study, a numerical classification basedon a leaf traits matrix allowed us to distinguish aclear group of low elevation sites from the twohigher ones. This result indicates that at La Chi-nantla, a distinction can be made between lowerand upper montane forests around an elevation of2300 to 2400 m. This limit at La Chinantla isvirtually identical to that identified by Kappelle(1996) for the Talamanca montane oak forests (ca2300 m). In contrast, in regions located closer tothe equator, the limits between these two foresttypes are usually found at much higher elevations,sometimes as high as 3050 m in New Guinea(Grubb 1977).

Our results provide some insight in relation tothe question of whether or not montane rain for-ests at their distributional fringes differ from sim-ilar forests located closer to the core of their rangeat equatorial latitudes. Morphologically, the leavesof dominant trees at La Chinantla were virtuallyindistinguishable from those in other forests, al-though relatively larger differences existed for an-atomical traits. Although it could be argued thatthe observed trends are not indicative of a steeper


thermal gradient as was expected for La Chinantlafrom its northern location, drawing such a conclu-sion will have to wait until similar data for singlebasins are available for several tropical mountainlocations at lower latitudes. In fact, much moreresearch is needed on leaf characteristics of mon-tane rain forest trees and their elevational patternswithin single basins; these plant traits offer impor-tant insights on the complex roles played by abioticfactors operating in these environments and sup-plement the traditional physiognomic classificationschemes for these communities.

ACKNOWLEDGMENTS

We are grateful to C. Gallardo, A. Rincon, A. Osorio,and B. Osorio for assistance during fieldwork. S. Men-doza and M. A. Romero helped with statistical analysis,computational work, and preparation of figures. This pa-per greatly benefited from the valuable comments of Drs.Frans Bongers, Lourens Poorter, Augusto Cesar Franco,and two anonymous reviewers on an earlier version. Thisstudy was partially funded by the Comision Nacionalpara el Conocimiento y Uso de la Biodiversidad (projectno. FB053/P069/93), and by a scholarship from the Na-tional Autonomous University of Mexico to N. V. R.

LITERATURE CITED

BAYTON, H. W. 1968. The ecology of an elfin cloud forest in Puerto Rico. 2. The microclimate of Pico del Oeste. J.Arnold Arbor. 49: 419–430.

BRUIJNZEEL, L. A., M. J. WATERLOO, J. PROCTOR, A. T. KUITERS, AND B. KOTTERINK. 1993. Hydrological observationsin montane rain forest on Gunun Silam, Sabah, Malaysia, with special reference to the ‘‘Massenerhebung’’effect. J. Ecol. 81: 145–167.

CAVELIER, J. 1996. Environmental factors and ecophysiological processes along altitudinal gradients in wet tropicalmountains. In S. S. Mulkey, R. L. Chazdon, and A. P. Smith (Eds.). Tropical forest plant ecophysiology, pp.399–436. Chapman and Hall, New York, New York.

CHABOT, F. B., AND D. J. HICKS. 1982. The ecology of leaf life spans. Annu. Rev. Ecol. Syst. 13: 229–259.DILCHER, D. L. 1973. A paleoclimatic interpretation of Eocene floras of southeastern North America. In A. Graham

(Ed.). Vegetation and vegetational history of northern Latin America, pp. 39–59. Elsevier, Amsterdam, TheNetherlands.

DOLPH, G. E., AND D. L. DILCHER. 1980. Variation in leaf size with respect to climate in Costa Rica. Biotropica 12:91–99.

EDWARDS, P. J., AND P. J. GRUBB. 1977. Studies of mineral cycling in a montane rain forest in New Guinea. 1. Thedistribution of organic matter in the vegetation and soil. J. Ecol. 65: 943–969.

FLENLEY, J. R. 1995. Cloud forest, the Massenerhebung effect and ultraviolet insolation. In L. S. Hamilton, J. O.Juvik, and F. N. Scatena (Eds.). Tropical montane cloud forests, pp. 150–155. Springer-Verlag. New York,New York.

GAUCH, H. G. 1982. Multivariate analysis in community ecology. Cambridge University Press, New York, New York.GEESKE, J., G. APLET, AND P. M. VITOUSEK. 1994. Leaf morphology along environmental gradients in Hawaiian

Metrosideros polymorpha. Biotropica 26: 17–22.GIVNISH, T. J. 1984. Leaf and canopy adaptations in tropical forests. In E. Medina, H. A. Mooney, and C. Vazquez-

Yanes (Eds.). Physiological ecology of plants of the wet tropics, pp. 51–54. Dr W. Junk Publishers, The Hague,The Netherlands.

GRUBB, P. J. 1977. Control of forest growth and distribution on wet tropical mountains: with special reference tomineral nutrition. Annu. Rev. Ecol. Syst. 8: 83–107.

HERNANDEZ-X., E. 1977. Vegetacion. In J. L. Tamayo and E. Beltran (Eds.). Recursos Naturales de la Cuenca delPapaloapan. Tomo I, pp. 293–388. Instituto de Recursos Naturales Renovables. Mexico D.F., Mexico.

HICKEY, J. L. 1973. Classification of the architecture of dicotyledonous leaves. Am. J. Bot. 60: 17–33.HOWARD, R. A. 1969. The ecology of an elfin forest in Puerto Rico. 8. Studies of stem growth and form, and of leaf

structure. J. Arnold Arbor. 50: 225–267.JONES, H. G. 1992. Plants and microclimate. A quantitative approach to environmental plant physiology. Cambridge

University Press, Cambridge, England.KAPPELLE, M. 1996. Los bosques de roble (Quercus) de la Cordillera de Talamanca, Costa Rica: Biodiversidad, ecologıa,

conservacion y desarrollo. Instituto de Biodiversidad y Universidad de Amsterdam, Wageningen, The Neth-erlands.

———, AND M. E. LEAL. 1996. Changes in leaf morphology and foliar nutrient status along a successional gradientin a Costa Rican, upper montane Quercus forest. Biotropica 28: 331–344.

———, AND N. ZAMORA. 1995. Changes in woody species richness along an altitudinal gradient in Talamaca montaneQuercus forests, Costa Rica. In S. P. Churchill, H. Balslev, E. Forero, and J. L. Lutein (Eds.). Biodiversity andconservation of Neotropical montane forests, pp. 135–148. New York Botanical Garden Press, Bronx, NewYork.

KELLY, D. L., E. V. J. TANNER, E. M. NICLUGHADHA, AND V. KAPOS. 1994. Floristics and biogeography of a rain forestin the Venezuelan Andes. J. Biogeogr. 21: 421–440.

KITAYAMA, K. 1995. Biophysical conditions of the montane cloud forest of Mount Kinabalu, Sabah, Malaysia. In L.


S. Hamilton, J. O. Juvik, and F. N. Scatena (Eds.). Tropical montane cloud forests, pp. 183–197. Springer-Verlag, New York, New York.

KORNER, C. 1999. Alpine plant life: Functional plant ecology of high mountain ecosystems. Springer-Verlag, Berlin,Germany.

LEAL, M. E., AND M. KAPPELLE. 1994. Leaf anatomy of a secondary montane Quercus forest in Costa Rica. Rev. Biol.Trop. 42: 473–478.

LEIGH, E. G. 1975. Structure and climate in tropical rain forest. Annu. Rev. Ecol. Syst. 6: 67–86.LIEBERMAN, D., M. LIEBERMAN, R. PERALTA, AND G. HARTSHORN. 1996. Tropical forest structure and composition on

a large scale altitudinal gradient in Costa Rica. J. Ecol. 84: 137–152.MEAVE, J., C. GALLARDO, AND A. RINCON. 1996. Plantas raras del bosque mesofilo de montana. II. Ticodendron

incognitum Gomez Laurito & Gomez P. (Ticodendraceae). Bol. Soc. Bot. Mexico 59: 149–152.———, ———, ———, A. OTERO, AND G. IBARRA-MANRIQUEZ. 1994. La vegetacion de La Chinantla, Oaxaca,

Mexico. In Libro de Resumenes, VI Congreso Latinoamericano de Botanica, p. 749. Mar del Plata, Argentina.———, M. A. SOTO, L. M. CALVO-IRABIEN, H. PAZ-HERNANDEZ, AND S. A. VALENCIA. 1992. Analisis sinecologico del

bosque mesofilo de montana de Omiltemi, Guerrero. Bol. Soc. Bot. Mexico 52: 31–57.MEDINA, E., V. GARCIA, AND E. CUEVAS. 1990. Sclerophylly and oligotrophic environments: relationship between leaf

structure, mineral nutrient content, and drought resistance in tropical rain forest of the Upper Rıo Negroregion. Biotropica 22: 51–64.

OHSAWA, M. 1990. An interpretation of altitudinal patterns of forest limits in south and east Asian mountains. J.Ecol. 78: 326–339.

RICHARDS, P. W. 1996. The tropical rain forest. An ecological study, 2nd edition. Cambridge University Press, Cam-bridge, England.

ROTH, I. 1984. Stratification of tropical forest as seen in leaf structure. Dr W. Junk Publishers, The Hague, TheNetherlands.

RZEDOWKSI, J. 1978. La vegetacion de Mexico. Limusa, Mexico D.F., Mexico.———, AND R. PALACIOS-CHAVEZ. 1977. El bosque de Engelhardtia (Oreomunnea) mexicana en la region de La

Chinantla (Oaxaca, Mexico): una reliquia del Cenozoico. Bol. Soc. Bot. Mexico 36: 93–123.SMALL, E. 1972. Photosynthetic rates in relation to nitrogen recycling as an adaptation to nutrient deficiency in peat

bog plants. Can. J. Bot. 50: 2227–2233.SUGDEN, A. M. 1982. The vegetation of the Serranıa de Macuira, Guajira, Colombia: a contrast of arid lowlands and

an isolated cloud forest. J. Arnold Arbor. 63: 1–30.TANG, C. Q., AND M. OHSAWA. 1999. Altitudinal distributions of evergreen broad-leaved trees and their leaf-size

patterns on a humid subtropical mountain, Mt. Emei, Sichuan, China. Plant Ecol. 145: 221–233.TANNER, E. V. J. 1977. Four montane rain forests of Jamaica: a quantitative characterization of the floristics, the soils

and the foliar mineral levels, and a discussion of the interrelations. J. Ecol. 65: 883–918.———, AND V. KAPOS. 1982. Leaf structure of Jamaican upper montane rain forest trees. Biotropica 14: 16–24.———, P. M. VITOUSEK, AND E. CUEVAS. 1998. Experimental investigation of nutrient limitation of forest growth on

wet tropical mountains. Ecology 79: 10–22.TURNER, I. M. 1994. Sclerophylly: primarily protective? Funct. Ecol. 8: 669–675.VAN DER WAL, H. 1998. Chinantec shifting cultivation and secondary vegetation. A case study on secondary vegetation

resulting from indigenous shifting cultivation in the Chinantla, Mexico. Bos Foundation, Wageningen, TheNetherlands.

VAZQUEZ-G., J. A., AND T. J. GIVNISH. 1998. Altitudinal gradients in tropical forest composition, structure, and diversityin the Sierra de Manantlan. J. Ecol. 86: 999–1020.

VELAQUEZ-ROSAS, N. 2000. Estudio de los patrones arquitectonicos de especies arboreas de bosque humedo de montanaa traves de un gradiente altitudinal. M.Sc. thesis. Facultad de Ciencias, Universidad Nacional Autonoma deMexico, Mexico D.F., Mexico.

WEBSTER, G. L. 1995. The panorama of Neotropical cloud forests. In S. P. Churchill, H. Balslev, E. Forero, and J.L. Lutein (Eds.). Biodiversity and conservation of Neotropical montane forests, pp. 53–77. New York BotanicalGarden, Bronx, New York.

WHITMORE, T. C. 1984. Tropical rain forest of the Far East. Clarendon Press, Oxford, England.WILLIAMS-LINERA, G., I. PEREZ-GARCIA, AND J. TOLOME. 1996. El bosque mesofilo de montana y un gradiente altitudinal

en el centro de Veracruz, Mexico. Cien. Hombre 23: 149–161.WOLFE, J. A. 1971. Tertiary climatic fluctuations and methods of analysis of tertiary floras. Palaeogeogr. Palaeoclimatol.

Palaeoecol. 9: 27–57.ZAR, J. H. 1999. Biostatistical analysis, 4th edition. Prentice Hall, Upper Saddle River, New Jersey.


AP

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1112

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n.d.

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1.9

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n.d.

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17.6

21.5

19.5 7.8

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54.6

n.d.

n.d.

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7.8

11.7

11.7

11.7 7.8

15.6

27.3

n.d.

n.d.

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3.2

3.2

4.0

4.8

5.6

1.6

2.4

n.d.

n.d.

1.6

1.6

1.6

1.6

1.6

4.8

1.6

1.6

n.d.

n.d.

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830

m)

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AL

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OP

OP

AL

OP

10.9

60.6

107.

215

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18.2

23.5

70.3

44.1

Mi

No

Me

Mi

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Mi

Mi

No

Me

No

121.

711

8.9

79.5

94.0

113.

910

0.6

36.4

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92.4

55.2

4.9

3.5

2.4

2.4

2.3

2.9

3.7

2.9

2.9

2.9

n.d.

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n.d.

395

115

n.d.

n.d.

377

n.d.

n.d.

142.

541

4.0

242.

322

7.5

331.

123

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98.4

303.

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9.5

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8

91.7

91.7

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15.6

255.

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132.

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0.2

153.

129

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8.7

79.9

80.0

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2.8

4.7

2.3

1.4

2.9

0.9

4.1

0.9

1.6

15.6

25.2

37.1

19.5

47.8

14.6

19.5

71.2

21.5

14.6

14.6

27.3 9.8

11.7

20.5 6.8

15.6

14.6 9.8

8.8

3.2

6.4

2.0

3.2

2.4

3.2

n.d. 2.4

15.2 1.2

1.6

4.8

1.6

1.6

1.6

2.0

n.d. 1.6

6.4

n.d.

Site

3(2

010

m)

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AL

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11.5

19.5

15.8

16.8

73.8

106.

3

Mi

Me

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Mi

Mi

Mi

Mi

Mi

Me

Me

88.5

91.2

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611

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90.6

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512

4.7

94.1

134.

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6.9

2.6

2.3

3.1

2.5

1.9

4.1

2.8

3.2

2.1

1.9

404

n.d.

213

455

653

379

239

376

n.d.

n.d.

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1.3

292.

824

0.1

215.

126

3.2

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123

4.5

213.

617

7.1

62.4

66.3

64.4

70.2

93.6

11.2

93.6

63.4

81.9

79.0

156.

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7.2

126.

887

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7.9

124.

881

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.3

2.5

1.1

2.9

1.8

0.9

0.9

1.7

2.0

1.0

0.9

22.4

38.0

23.4

23.4

19.5

28.3

19.5

28.3

37.1

11.7

15.6

10.7

11.7

10.7

11.7

14.6

15.6

11.7

11.7

11.7

3.2

n.d. 1.6

4.0

n.d. 5.6

3.2

2.8

n.d. 4.0

1.6

n.d. 1.6

3.2

1.6

3.2

1.6

1.6

n.d. 1.6


AP

PEN

DIX

.C

onti

nued

.

Spec

ies

12

34

56

78

910

1112

1314

1516

17

Site

4(2

260

m)

Bei

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NE

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E E E

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AL

AL

AL

AL

AL

AL

AL

AL

AL

AL

97.4

69.3

67.4

18.7

54.7

21.8

20.5

19.1

46.2

38.6

Me

Me

Me

Mi

Me

No

No

Mi

Me

No

101.

710

5.5

123.

610

3.9

88.9

71.6

107.

813

6.6

88.5

97.7

2.2

3.1

2.5

3.1

2.4

3.0

3.2

2.5

3.3

3.7

n.d.

172

n.d.

236

n.d.

299

n.d.

392

299

223

172.

012

6.6

173.

535

0.8

398.

626

3.8

330.

824

7.0

209.

616

4.1

69.2

40.0

45.8

117.

085

.353

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9.9

99.5

70.2

164.

1

56.6

60.5

84.8

97.2

255.

617

3.6

163.

810

7.3

111.

262

.4

0.8

1.5

1.9

1.6

3.0

3.2

1.4

1.1

1.6

1.4

29.3

11.7

33.2

23.4

19.5

19.5

18.5

17.6

11.7

33.2

9.8

7.8

7.8

17.6

21.5

10.7

17.6

13.7 7.8

17.6

1.6

2.0

n.d. 1.6

5.6

1.6

6.4

4.8

4.0

2.4

1.6

2.0

n.d. 1.6

5.6

1.6

3.2

3.2

3.2

2.4

Site

5(2

430

m)

Vacc

iniu

mco

nsan

guin

eum

Wei

nman

nia

tuer

ckhe

imii

Vib

urnu

mac

utifo

lium

Sym

ploc

osve

rnic

osa

Tern

stroe

mia

hem

sleyi

Gau

lther

iaod

orat

aC

leth

raga

leot

tian

aTa

xus

glob

osa

Cle

yera

inte

grifo

liaPr

unus

brac

hybo

tria

Ov

O Ov

E O Ov

O Ob

E Ov

NE

NE

E NE

E E NE

E E E

S S S S S S S S S S

AL

AL

AL

AL

AL

AL

AL

AL

AL

AL

5.0

10.7

22.4

14.7

19.3

16.7

41.6 0.6

20.9

26.5

Mi

Mi

No

Mi

Mi

Mi

No

No

No

No

89.9

124.

275

.175

.816

9.9

185.

910

5.5

76.3

107.

912

1.4

2.7

2.6

2.3

2.7

2.6

2.5

2.9

13.1 2.8

2.9

261

532

350

462

207

497

n.d.

226

n.d.

529

287.

930

2.4

303.

130

3.5

295.

937

6.5

259.

239

5.4

376.

233

3.3

118.

910

1.4

137.

510

4.3

136.

514

5.3

93.6

140.

414

0.4

132.

6

128.

712

4.8

118.

915

9.9

120.

916

5.8

87.8

168.

717

3.6

142.

4

1.1

1.2

0.9

1.5

0.9

1.1

0.9

1.2

1.2

1.1

19.5

59.5

21.6

22.4

17.6

38.0

64.4

44.9

31.2

23.4

11.7

10.7

15.6

11.7

13.7

12.7 7.8

19.5

23.4

19.5

4.8

3.2

5.6

2.0

4.8

10.4 4.8

11.2 4.8

8.0

3.2

1.6

3.2

1.6

1.6

3.2

n.d. 9.6

1.6

6.4

Site

6(2

560

m)

Que

rcus

euge

niifo

liaC

leth

raga

leot

tian

aTe

rnstr

oem

iahe

msle

yiC

leye

rain

tegr

ifolia

Wei

nman

nia

tuer

ckhe

imii

Vacc

iniu

mco

nsan

guin

eum

Sym

ploc

osve

rnic

osa

Que

rcus

aff.

oleo

ides

Cin

nam

omum

zapa

tae

Den

drop

anax

arbo

reus

E O O E Ov

Ov

E E E E

E NE

E E NE

NE

NE

E E NE

S S S S S S S S S S

AL

AL

AL

AL

AL

AL

AL

AL

AL

AL

19.9

49.1

18.2

24.3

13.2 2.2

18.9 9.4

28.6

27.6

Mi

Me

Mi

No

Mi

Mi

Mi

Mi

No

No

126.

813

9.7

157.

211

7.7

117.

919

3.3

87.2

146.

092

.863

.2

3.1

1.9

2.3

2.7

2.6

2.8

2.9

1.9

2.6

3.4

n.d.

n.d.

213

271

395

280

188

471

374

372

253.

917

5.2

339.

125

5.6

309.

253

6.3

267.

224

8.4

238.

424

3.3

134.

674

.114

2.4

99.5

101.

416

9.7

72.3

122.

998

.582

.9

87.8

58.5

156.

056

.614

7.2

325.

515

8.0

99.5

95.6

122.

9

0.65

0.79

1.10

0.56

1.45

1.92

2.19

0.81

0.97

1.48

11.7

31.2

15.6

21.5

43.9

22.4

19.5

11.7

21.5

19.5

13.7 5.9

13.7

15.6

11.7

11.7

11.7 7.8

11.7

14.6

4.0

4.8

8.0

4.0

2.8

4.0

2.4

2.8

7.2

2.4

1.6

n.d. 2.4

2.0

1.6

1.6

1.6

1.6

3.2

n.d.

Elevational Variation of Leaf Traits in Montane Rain Forest Tree Species at La Chinantla, Southern...

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