Interciencia ISSN: 0378-1844 [email protected] Asociación Interciencia Venezuela

Azócar, Aura; Rada, Fermín; García-Núñez, Carlos Functional characteristics of the arborescent genus polylepis along a latitudinal gradient in the high andes Interciencia, vol. 32, núm. 10, octubre, 2007, pp. 663-668 Asociación Interciencia Caracas, Venezuela

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How to cite Complete issue Scientific Information System More information about this article Network of Scientific Journals from Latin America, the Caribbean, Spain and Portugal Journal's homepage in redalyc.org Non-profit academic project, developed under the open access initiative FUNCTIONAL CHARACTERISTICS OF THE ARBORESCENT GENUS Polylepis ALONG A LATITUDINAL GRADIENT IN THE HIGH ANDES

Aura Azócar, Fermín Rada and Carlos García-Núñez

SUMMARY

Polylepis is a genus restricted to the Andean Mountain cea avoids the less harsh conditions of its habitat through os‑ Range, naturally occurring above the upper continuous forest motic adjustments and cell wall elasticity changes. Mean CO2 limit. The purpose of this work was to integrate and compare assimilation rates were higher in P. australis (9µmol·m‑2·s‑1) functional characteristics in terms of water and carbon rela‑ campared to P. sericea (5µmol·m-2·s-1) and P. tarapacana tions and low temperature resistance mechanisms in different (3·µmol·m-2·s-1). Mean night leaf respiration rates were similar Polylepis species along a latitudinal gradient. The studied for all species (1-2·µmol·m-2·s-1). In terms of low temperature species were P. sericea in Venezuela, P. tarapacana in Bolivia resistance, P. sericea shows daily osmotic adjustments and a and P. australis in Argentina. Seasonal measurements of leaf moderate supercooling capacity (-9ºC). The other two spe‑ water and osmotic potentials, stomatal conductance, CO2 as‑ cies rely on freezing tolerance in order to survive the more similation and respiration rates, and injury and freezing tem‑ extreme low temperature conditions. The functional attributes peratures were compared. There is a gradient, in terms of described in this study for the different species in a wide en‑ functional attributes, along the environmental range. P. tarapa- vironmental range may explain some aspects of their success cana is the most tolerant species to water stress, while P. seri- along the latitudinal and altitudinal gradients.

limate is an impor- Thus, minimum absolute temperatures unhn (2006) reported 26 species, with tant factor for plant become an important variable in or- the highest diversity found in Peru (14 growth; it governs dis- der to establish the distribution limits species, 3 endemic) and Bolivia (13 tribution and sets limits for survival. of the major vegetation types (Wood- species, 4 endemic); only one species One important characteristic of high ward and Williams, 1987; Prentice et was recorded for Venezuela, 3 in Co- mountain environments is the low air al., 1992). In spite of this, the genus lombia (1 endemic), 7 in Ecuador (2 temperature, which limits plant growth Polylepis does not seem to respond endemic), 2 in Chile and 4 in Argen- and survival in these habitats (Sakai in their distribution to this regime of tina (1 endemic). and Larcher, 1987). On the other hand, low temperatures, since it presents a Regional forest distribu- tropical high mountain environments unique altitudinal distribution reaching tion seems to be related to areas where present large daily variations and much higher elevations than those of solar irradiance is controlled by the small seasonal changes in temperature, any other angiosperm tree in the world slope aspect (direction) and inclination and freezing temperatures occur al- (Liberman-Cruz, 1986). Additionally, (angle), and sun elevation influences lo- most every day of the year (Hedberg, it is an endemic genus in the Andean cal distribution (Braun, 1997). The ge- 1961; Azócar and Monasterio, 1980). Mountain Range, found from Vene­ nus creates a natural treeline well above Temperature and frost occurrence vary zuela in the north to Central Argentina the timberline (continuous forest line), with latitude, altitude and topography. in the south. Kessler and Schmidt-Leb- in some cases forming forest patches

KEY WORDS / Andean Mountain Range / Carbon Relations / Gas Exchange / Low Temperature Resistance / Photosynthesis / Water Relations / Received: 05/02/2005. Modified: 09/14/2007. Accepted 09/20/2007.

Aura Azócar. Biologist, Universidad Central de Venezuela (UCV). Dr. in Ecology, University of Montpellier, France. Professor, Universidad de Los Andes (ULA), Venezuela. Dirección: Laboratorio de Ecofisiología, Instituto de Ciencias Ambientales y Ecológicas (ICAE), ULA, Mérida, Venezuela. e-mail: [email protected] Fermín Rada. Biologist, University of Maryland, USA. Dr. in Tropical Ecology, ULA, Vene­ zuela. Professor, ULA, Venezuela. e-mail: [email protected] Carlos García-Núñez. Forestry Engineer and Dr. in Tropical Ecology, Professor, ULA, Venezue­ la. e-mail: [email protected]

OCT 2007, VOL. 32 Nº 10 0378-1844/07/10/663-06 $ 3.00/0 663 between 4000 and 5200masl. In gen- Table I eral, Polylepis forests are restricted to Environmental characteristics and coordinates steep slopes in mid to low topographic of the study sites positions, although some species are Study site Species Coordinates Altitude Mean Mean also found on flat terrains. Polylepis (masl) annual annual dominates the upper strata of woodlands temperature precipitation and shrublands, together with other less (°C) (mm) abundant woody species of the genera Berberis, Gaultheria, Valeriana, among Piedras Blancas, P. sericea 9°N - 70°W 4200 3.7 800 others. These woody species occasion- Venezuela ally form dense stands that cover most Nevado Sajama, P. tarapacana 18°S - 68°W 4300 3.4 347 of the surface, often called forests, that Bolivia are usually intermingled with patches of tussock grasslands, ferns or rock out- Los Gigantes, P. australis 32° S - 66°W 2100 8.0 854 Argentina crops (Kessler, 2006). Despite their relatively small area cover, these forests represent unique ecological islands of biodiver- life form (Simpson, 1979), character- man-Cruz et al., 1997). The study site sity that are vanishing rapidly; Fjeldsa ized by twisted shapes, a thick, dense- is located at Nevado Sajama Nation- and Kessler (1996) indicate that only ly laminated and flaky bark with red- al Park, where P. tarapacana forms 2% of the original Polylepis forests re- dish color (Simpson, 1986), and small the world’s highest woody plant forest main in Perú and 10% in Bolivia, sug- green-gray leaves. The trees are 1-6m (Liberman-Cruz, 1986; Braun, 1997) gesting that human occupation in the in height and have crown diameters around the Sajama Volcano. Although Andean highlands has led to consider- of 3-5m. With respect to their distri- the study site is considered a semiarid able destruction of these forests. bution, the species occur in different tropical high mountain environment, its All species of the ge- ecological habitats associated with el- latitudinal position determines a marked nus are exposed to very harsh climatic evation and humidity. seasonal pattern in temperature and pre- conditions in both their altitudinal and Three species were com- cipitation regimes, with a cold dry sea- latitudinal distribution, indicating that pared a latitudinal distribution gradient: son during the austral winter (May-Oct) their survival depends on very special P. sericea Wedd, in Venezuela, P. tara‑ and a wet warmer season (Nov-Apr; adaptive characteristics that allow them pacana Philippi, in Bolivia and P. aus‑ Liberman-Cruz et al., 1997). Absolute to sustain freezing temperatures and a tralis Bitter, in Argentina. Table I shows maximum and minimum temperatures distinct water stress due to precipita- the environmental characteristics and registered at 4200m are 21 and -19ºC, tion regimes and drying winds. Nor- geographic coordinates for the different respectively (Liberman-Cruz, 1986). mally, these conditions would prevent study sites. P. australis is found tree growth; however, the presence of P. sericea, in the Ven- at the north extreme of Sierra Grande many Polylepis species above the tim- ezuelan Andes, may reach an altitude in Córdoba, Argentina, mainly associ- berline, forming forest islands along of 4600m (Arnal, 1983), well above ated with rock outcrops. This species broad temperature and water availability the treeline (3200masl) in this tropi- has to cope with altitude conditions in gradients, suggests a high diversity of cal area (Monasterio, 1980). Its dis- a temperate environment. Most (83%) functional attributes, which in turn play tribution is always associated to more rainfall occurs in the summer (Renison a fundamental role in their survival. favorable thermal conditions in areas et al., 2002). Absolute daily maximum In this work, some where large boulders accumulate to- and minimum temperatures of 27.1 and functional attributes of three Polylepis wards the base of glacial cirques (Wal- -12.8ºC were registered during this species along a wide latitudinal gra- ter and Medina, 1969; Azócar and study. dient are integrated and compared, in Monasterio 1980). This species has the order to establish functional responses widest latitudinal distribution, from Field and laboratory studies that help explain their wide geographi- Venezuela to northern Bolivia. Appar- cal distribution. Functional charac- ently, this species has spread through Mean air temperature teristics are compared in terms of re- the Andes in the last million years values were measured with copper- sistance mechanisms to freezing tem- as a consequence of climatic changes constantan thermocouples (n=3) con- peratures, leaf gas exchange and water (Simpson, 1986). P sericea´s study site nected to a digital thermometer. Rela- relations. In order to carry out this shows a 2.7ºC difference between the tive humidity was recorded with a dig- comparison, a revision and re-inter- coldest and the warmest month. Daily ital hygrometer (n=3). Plant response pretation of results obtained through- temperature fluctuations range from - parameters were obtained from daily out the last two decades (Rada et al., 3º to 15ºC during the rainy season and measurements of three mature leaves 1985, 1996, 2001; García-Núñez et al., -14º to 18ºC in the dry season (Monas- of each of three individual trees at 2004) was made, and more recent un- terio, 1986). the different studied sites. These pa- published results used. P. tarapacana forms fo­ rameters were CO2 assimilation (A) rests with an amazing altitudinal dis- and transpiration rates (E), stomatal Materials and Methods tribution (4200-5200m) in Bolivia. The conductance (Gs), night respiration lowest altitude represents the maximum (R) and minimum leaf water potential Studied species elevation for the growth of any shrub or ( ) for both dry and wet seasons. and site characteristics ΨLmin tree life-form, while the high extreme is Photosynthetically active radiation was All species of the practically the limit for plant growth in obtained from the leaf chamber inte- Polylepis genus have a tree or shrub the Andean region (Braun, 1997, Liber- grated to the gas exchange systems.

664 OCT 2007, VOL. 32 Nº 10 Table II Non-parametric tests Minimum registered air temperature, injury and for comparison between two samples freezing temperatures and low temperature and between three samples were used. resistance mechanisms during wet and dry seasons For the comparison of ecophysiological for the three Polylepis studied species parameters between seasons and for avoidance or tolerance mechanisms the Species Dry season temperatures (ºC) Wet season temperatures (ºC) RM U-Mann-Whitney test was used. For comparison between the three species Tmin Injury Freezing Tmin Injury Freezing a Kruskall-Wallis test was used. P. sericea -4.5 -9.0 ±0.5 a -8.5 ±0.5 a -2.0 -8.0 ±0.9 a -8.0 ±0.3 a A Results P. tarapacana -13.0 -20.0 ±0.5 a -3.5 ±0.5 b -6.0 -21.0 ±1.2 a -9.2 ±0.6 b T P. australis -13.5 -24.0 ±1.0 a -7.0 ±0.2 b -2.0 -18.0 ±2.0 a -6.0 ±0.2 b T Freezing temperature resistance mechanisms Minimum registered air temperature (Tmin), injury and freezing temperatures and low temperature resistance mechanisms (RM, A = avoidance through supercooling capacity and T = freezing tolerance) Injury temperatures were during wet and dry seasons for the three Polylepis studied species. Different letters represent signifi- cant differences (P<0.05) between injury and freezing temperatures for each of the species. similar in P. tarapacana for both dry and rainy seasons (Table II), but the temperature at which the freezing pro- Three 24h courses were carried out for respiration rates were used to obtain cess began showed significant differenc- each season and at every site, with 7 integrated curves for the assimilation/ es, with values of -3.5 and -9°C during measurements during day hours and 3 respiration ratio (A/R) at leaf level. wet and dry seasons, respectively. P. to 4 at night. Furthermore, water re- Freezing temperature (initiation of the australis showed lower injury tempera- lations parameters such as turgor loss ice nucleation process) was determined tures for the dry season but the freez- potentials (Ψπ, n=5) obtained from as the appearance of a low tempera- ing temperatures were similar in both pressure-volume curves and low tem- ture exotherm in ten to fifteen samples seasons. Differences between frost for- perature resistance mechanisms (freez- subjected to thermal analysis in a con- mation (i.e. supercooling capacity) and ing and injury temperatures) were trolled bath; the system recorded exo- injury temperature for these two species also obtained in the laboratory for all therms as plant tissue was cooled at a point to freezing tolerance in leaf tis- species. A portable gas exchange sys- rate of 9ºC·h-1 from 5 to -25ºC. Low sues. In contrast, P. sericea showed no tem (LCA-2 for P. sericea and LCA- temperature injury was determined significant differences between freezing 4 for P. tarapacana and P. australis, quantitatively with the triphenyl tetra- and injury temperatures during either ADC, Hoddesdon, England) was used zolium chloride method (TTC) in three season, indicating frost avoidance as its for gas exchange measurements com- different samples; respiring tissues re- resistance mechanism to freezing tem- prising leaf conductance, transpira- duce TTC, changing from clear to a peratures. tion, CO2 assimilation and respiration red color that was quantified through rates. Water relation parameters were spectrometry. A full description of the Water and carbon relations measured with a pressure bomb (PMS methods used may be found in Rada Instruments Co., Oregon, USA). Day- et al., (1985, 1996, 2001) and García- The three species re- time CO2 assimilation and nighttime Núñez et al., (2004). sponded differentially to temperature

Table III MEAN PHOTOSYNTHETICALLY ACTIVE RADIATION, AIR TEMPERATURE, RELATIVE HUMIDITY AND PLANT RESPONSE PARAMETERS FOR WET AND DRY SEASON DAILY COURSES IN THREE Polylepis SPECIES Species Season PAR Ta RH Gs A R A/R

P. sericea Wet 1042 ±168 a1 11.6 ±1.2 a1 84.2 ±1.4 a1 90.6±15.4 a1 4.60±0.6 a 1 2.0 2.3 (1700) (21.5/-0.7) (100-64) (213) (7.4) Dry 1146 ±256 a1 13.4 ±1.7 a1 52.2 ±2.1 b1 63.3±6.0 b1 3.6±0.5 a 1 1.6 ±0.3 1 2.3 (1900) (24.5/-2.7) (98-32) (93) (5.8) (2.7) P. tarapacana Wet-warm 721 ±182 a2 7.9 ±1.1 a2 73.4 ±4.0 a2 58.9±10.4 a1 2.8±0.4 a 2 1.3 ±0.1 1 2.2 (1369) (12.5/-4.5) (92-46) (128) (6.8) (2.6) Dry-cold 1443 ±152 b1 7.5 ±1.2 a2 38.6 ±5.2 b2 33.5±4.6 b2 2.5±0.4 a 1 - - (2052) (12.5/-14.0) (76/15) (65.0) (4.7) P. australis Wet-warm 1034 ±126 a1 7.7 ±0.8 a2 56.0 ±3.0 a3 65.5±10.6 a1 7.3±0.4 a 3 1.8 ±0.1 a 2 4.1 (1943) (15.3/-2.8) (82/29) (92) (14.4) (2.3) Dry-cold 1246 ±133 a1 8.5 ±1.4 a2 53.4 ±5.7 a1,2 43.7±8.5 a2 9.0±0.3 b 2 1.6 ±0.1 a 1 5.6 (2231) (15.3/-12.8) (89/25) (75) (12.3) (1.9)

-2 -1 PAR: mean photosynthetically active radiation, Ta: mean air temperature (°C), RH: relative humidity (%), Gs: stomatal conductance (mmol·m ·s ), A: CO2 assimilation rate (μmol·m-2·s-1), and R: respiration rate (μmol·m-2·s-1). Values in parenthesis are maximum for PAR, maximum and minimum for Ta and RH, and maximum for Gs and A. Different letters correspond to significant differences (P<0.05) for the measured parameters between seasons for each species. Different superscript numbers correspond to significant differences (P<0.05) for measured parameters between species during the same season.

OCT 2007, VOL. 32 Nº 10 665 In relation to mini- temperature may be below -10ºC, tis- mum leaf water potentials sue freezing occurs at relatively high (Figure 1) P. sericea and temperatures (-3.5ºC) determining a P. tarapacana showed freezing tolerance range. During the a decrease towards the wet and warmer season, night air tem- dry season. P. austra‑ peratures never reach tissue freezing lis showed a tendency to temperatures (-9ºC). This seasonal maintain similar poten- differentiation is a consequence of an tials between seasons. increase in total soluble carbohydrates With respect to turgor and proline during the wet warm sea- loss, both P. tarapacana son, determining an increase in super- and P. australis main- cooling capacity (Rada et al., 2001). tain similar values be- Freezing tolerance provides plants a tween seasons. On the better protection against cold injury other hand, P. sericea and this increase in supercooling ca- decreased its turgor loss pacity may be advantageous to this point during the dry sea- species since it would permit an ear- son, indicating a signifi- lier start in photosynthetic activity. cant capacity for osmotic In spite of the differ- adjustment. ent degrees of water stress found at the sites, there are no marked effects Discussion on carbon gain at the leaf level. In Figure 1. Minimum leaf water potentials (ΨLmin) for dry and wet seasons 0 general, mean CO assimilation rates and osmotic potential at turgor loss point (Ψπ ) during dry and wet sea- 2 sons for the three Polylepis species along a latitudinal gradient. Different Freezing damage may oc- for the three species studied are com- letters represent significant differences (P <0.05) between species. cur any night of the year parable to or higher than those re- in tropical and subtropi- ported for other tropical alpine plants and/or seasonal water availability (Ta- cal high altitude environments, but (Schulze et al., 1985; Goldstein et al., ble III). P. sericea showed clear dif- some authors (Sakai and Larcher, 1987; 1994) and timberline species (Meinzer ferences between seasons; mean air Goldstein et al., 1994) indicate that it et al., 1984; Aylett, 1985). The stud- temperature increased by 2ºC, while is rather improbable that frost damage ied species showed a coupling of gas leaf conductance and CO2 assimila- plays a decisive role in the survival exchange characteristics to the extreme tion were lower during the dry season. of trees in these regions. The three daily and seasonal conditions of their Air temperatures below zero occurred studied species respond in contrasting respective environments. in both seasons. P. tarapacana also manners to the different thermal con- In terms of water re- showed some differences in gas ex- ditions of their specific habitats. P. lations, even though P. tarapacana is change characteristics between seasons sericea, growing in less extreme envi- subjected to the most extreme condi- (Table III). Even though a large (43%) ronments, showed no significant dif- tions, minimum leaf water potentials drop in leaf conductance was found ferences between injury and freezing for the dry season are similar to those from the wet to the dry season, only a temperatures, indicating that when the of P. australis and P. sericea. This is small (11%) drop in CO2 assimilation freezing process begins, injury will si- an indication that under the arid char- was detected during the latter. Mean multaneously occur and, therefore, this acteristics of its habitat, this species air temperatures were similar for both species does not resist ice formation in relies on a greater stomatal control. seasons and lower compared to P. seri‑ its tissues. However, although freez- At the other end, P. sericea avoids the cea; however, minimum temperatures ing takes place at moderate tempera- less harsh water stress conditions of were much lower during the dry sea- tures (-9ºC), this suprcooling avoid- its habitat through osmotic adjustments son. P. australis had a substantially ance mechanism seems to be enough and wall elasticity changes (Rada et different response to the two previous to withstand mild, short duration low al., 1996). species; means for most of the ana- temperatures present in the Venezuelan The results support the lyzed parameters showed no significant Andes throughout the year (Rada et statement by Goldstein et al. (1994) differences between the two measure- al., 1985). In contrast, P. tarapacana that high photosynthetic efficiency and ment periods. It is interesting to note and P. australis show significant dif- frost resistance are the main physi- that the assimilation rate increased to- ferences between freezing and injury, ological explanations for the Polylepis wards the dry-cold season, even though indicating that once the freezing pro- phenomenon. However, controversy still leaf conductance tended to decrease cess occurs, the tissues remain undam- persists about its restricted distribution, (no significant differences). aged down to much lower tempera- always at altitudes above the natural In general, mean CO2 tures. This corresponds to a freezing altitudinal limit of tree growth, asso- assimilation rate (A) was higher in P. tolerance mechanism, as a response to ciated with rock outcroppings, along australis during both seasons, as com- more extreme temperature conditions streams and, in the case of P. tarapa‑ pared to the other two species. On the of their habitats (Azócar et al., 1988; cana, around a volcano suggesting the other hand, dark respiration rates were Squeo et al., 1991). need of special soil conditions. This lower in P. tarapacana during the wet Differences between sea­ apparent preference has been explained season, as compared to P. australis sons in supercooling capacity in P. by the existence of a favorable micro- and P. sericea (Table III). All three tarapacana suggest differences in re- climate at these sites, which permits species showed a positive diurnal leaf sistance mechanisms when thermal tree survival in an unfavorable envi- carbon balance throughout the year, al- conditions change (Rada et al., 2001). ronment (Walter and Medina, 1969; though more favorable in P. australis. During the cold-dry period, when air Troll, 1973; Simpson, 1979, 1986; Azó-

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CARACTERíSTICAS FUNCIONALES DEL GÉNERO ARBORESCENTE Polylepis EN UN GRADIENTE LATITUDINAL EN LOS ALTOS ANDES Aura Azócar, Fermín Rada y Carlos García-Núñez

RESUMEN

Polylepis es un género restringido a la Cordillera de los Andes, evade condiciones menos severas de su habitat a través de ajuste encontrándose de forma natural por encima del límite superior de osmótico y cambios en la elasticidad de las paredes celulares. Las bosque continuo. El propósito de este trabajo fue integrar y com‑ tasas promedios de asimilación de CO2 fueron mayores en P. aus- parar las características funcionales, en términos de relaciones hí‑ tralis (9µmol·m-2·s-1) que en P. sericea (5µmol·m-2·s-1) y P. tarapaca- dricas y de carbono y mecanismos de resistencia a bajas tempera‑ na (3µmol·m-2·s-1). La tasa promedio de respiración foliar nocturna turas, en diferentes especies de Polylepis a lo largo de un gradiente fue similar para todas las especies (1-2µmol·m-2·s-1). En términos de latitudinal. Las especies estudiadas fueron P. sericea en Venezuela, resistencia a bajas temperaturas, P. sericea muestra ajuste osmóti‑ P. tarapacana en Bolivia y P. australis en Argentina. Se compararon co diario y capacidad moderada de sobreenfriamiento (-9ºC). Las medidas estacionales de potencial hídrico y osmótico foliares, con‑ otras dos especies dependen de la tolerancia al congelamiento para ductancia estomática, asimilación de CO2 y respiración, y tempera‑ soportar las temperaturas bajas más extremas. Los atributos fun‑ tura de congelamiento y daño. Se evidencia un gradiente de atri‑ cionales descritos para las diferentes especies en un amplio rango butos funcionales a lo largo del rango ambiental. P. tarapacana es ambiental pueden explicar algunos aspectos de su éxito en los gra‑ la especie más resistente al estrés hídrico, mientras que P. sericea dientes latitudinales y altitudinales.

CARACTERÍSTICAS FUNCIONAIS DO GÊNERO ARBORESCENTE Polylepis EM UM GRADIENTE LATITUDINAL NOS ALTOS ANDES Aura Azócar, Fermín Rada e Carlos García-Núñez

RESUMO

Polylepis é um gênero restringido a Cordilheira dos Andes, ras de seu habitat a través de ajuste osmótico e mudanças na encontrando-se de forma natural por encima do limite superior elasticidade das paredes celulares. As taxas médias de assimi‑ -2 -1 de bosque contínuo. O propósito deste trabalho foi integrar e lação de CO2 foram maiores em P. australis (9µmol·m ·s ) que comparar as características funcionais, em termos de relações em P. sericea (5µmol·m-2·s-1) e P. tarapacana (3µmol·m-2·s‑1). A hídricas e de carbono e mecanismos de resistência a baixas taxa média de respiração foliar noturna foi similar para todas temperaturas, em diferentes espécies de Polylepis ao longo de as espécies (1-2µmol·m-2·s-1). Em termos de resistência a baixas um gradiente latitudinal. As espécies estudadas foram P. sericea temperaturas, P. sericea mostra ajuste osmótico diário e capa‑ na Venezuela, P. tarapacana na Bolivia e P. australis na Argenti‑ cidade moderada de super-resfriamento (-9ºC). As outras duas na. Compararam-se medidas estacionais de potencial hídrico e espécies dependem da tolerância ao congelamento para supor‑ osmótico foliares, condutância estomática, assimilação de CO2 tar as temperaturas baixas mais extremas. Os atributos funcio‑ e respiração, e temperatura de congelamento e dano. Eviden‑ nais descritos para as diferentes espécies em uma ampla faixa cia-se um gradiente de atributos funcionais ao longo da faixa ambiental podem explicar alguns aspectos de seu sucesso nos ambiental. P. tarapacana é a espécie mais resistente al estresse gradientes latitudinais e altitudinais. hídrico, enquanto que P. sericea evade condições menos seve‑

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