Functional

Growth, demography and carbon relations of Polylepis

Blackwell Publishing, Ltd.

Ecology 2005
19, 941–951 trees at the world’s highest treeline
G. HOCH† and C. KÖRNER
Institute of Botany, University of Basel, Schönbeinstrasse 6, CH-4056 Basel, Switzerland

Summary
1. Growth, reproductive success and non-structural carbon pools in Polylepis tarapa-
cana Philippi trees were examined across a transect between 4360 and 4810 m altitude
on Nevado Sajama, Bolivia.
2. The mean −10-cm soil temperature of 5·4 °C under trees at the treeline during the
265-day growing season matched the threshold temperature found at other subtropical
and tropical treelines. Beyond 4400 m Polylepis is restricted to the warmer and drier
equator-facing slopes, suggesting a direct thermal limitation of tree growth.
3. Maximum tree height, annual shoot increment and mean tree-ring width decreased
with altitude. Trees near the upper range limit reached a maximum tree height of 3·3 m
and a maximum stem diameter of 34 cm.
4. The smallest tree-height classes dominated populations at all altitudes, and the
uppermost site revealed the highest proportion of seedlings. Tree-size demography
indicates a critical phase for tree establishment during the sapling stage, when trees
emerge from sheltered niches near the ground.
5. No evidence of a depletion of mobile C stores (sugars, starch and lipids) was found
in any tissue type with increasing elevation, suggesting a limitation of C investment
(growth) rather than C acquisition (photosynthesis) at treeline.
Key-words: Andes, carbohydrates, forest limit, high elevation, temperature
Functional Ecology (2005) 19, 941–951
doi: 10.1111/j.1365-2435.2005.01040.x

rial treelines; Körner & Paulsen 2004). Despite these

Introduction
Although high-altitude treelines are a worldwide
phenomenon, ecophysiological studies at high eleva-
tions have mainly been conducted in the past at mid-
and high-latitude mountain ranges. Thus numerous
attempts at a functional explanation of treeline forma-
tion concern mechanisms tied to high-latitude climatic
conditions, especially the presence of a long, cold and
snow-rich winter season (for a summary of hypotheses
see Tranquillini 1979; Wardle 1993; Körner 1998;
Holtmeier 2003). For a unifying, globally valid theory
of treeline formation, data from tropical and subtropi-
cal regions are therefore needed.
Trees at low-latitude treelines experience climatic
conditions that differ substantially from those at
higher latitudes. Diurnal air temperature amplitudes
at low latitudes are often more pronounced than those
between seasons (Larcher 1975; Hardy et al. 1998),
and the duration of the growing season is markedly
longer than the duration of the dormant period (with
a maximum 365-day growing season at some equato-
© 2005 British †Author to whom correspondence should be addressed.
Ecological Society E-mail: guenter.hoch@unibas.ch
differences, the mean growing-season temperatures of
the vast majority of natural high-altitude treelines are
within the range 5·0–7·5 °C, with a global mean of
6·7 ± 0·8 °C (−10-cm soil temperatures; Körner &
Paulsen 2004). This suggests that annual minimum
and maximum temperatures, as well as the duration of
the growing season, are less decisive for the altitudinal
position of treelines than are average temperatures
during the period of active growth. Other climatic and
also edaphic determinants are of more regional signi-
ficance and are not really relevant on a global scale
(Körner 1998). Low rainfall and drought, for instance,
are not generally related to altitude and may limit tree
growth anywhere. However, it is remarkable that trees
reach their highest elevations globally in dry regions
such as in Tibet (Miehe et al. 2003) and especially in
the South American Andes (Braun 1997). Given that
the tree limit is often found close to vital upper mon-
tane forests, moisture is unlikely to be responsible for
an abrupt tree limit at similar altitudes across larger
areas of otherwise varied topography.
In the current study, we examined different parameters
related to tree growth (including the non-structural
carbon pools) in Polylepis tarapacana Philippi (Rosaceae:

941
942 Sanguisorbeae) trees along an altitudinal transect at
G. Hoch & the volcano Sajama, Bolivia. Additionally, we recorded
C. Körner the first complete annual temperature course for this
treeline. Polylepis is a widespread evergreen genus of
the equatorial Andes, which includes about 20 species,
forming thickets and woodland commonly above
3500 m a.s.l. (Kessler 1995). It appears to be a poor
competitor, and with its inherent slow growth it loses
terrain to more vigorous species when the environment
becomes warmer or more humid. The highest-reaching
of all Polylepis species, P. tarapacana has a relatively
narrow geographical distribution, reaching from the
volcanic western Andean Cordillera in southern Peru
to the region of Potosi, southern Bolivia and to adjacent
Chile, and its distribution is restricted to volcanic
slopes between 3900 and 5100 m a.s.l. (Kessler 1995).
The high-altitude P. tarapacana forest belt, which
embraces the slopes of the volcano Nevado Sajama,
is of special interest for ecophysiological investigations
as it constitutes the world’s highest occurrence of
truly arborescent plant individuals.
The remarkably similar mean growing-season tem-
peratures of ≈6·7 °C at climatic treelines across the
globe indicate that temperature-driven mechanisms
dominate the formation of high-elevation treelines
worldwide. Following from previous studies, the low
temperatures at treeline probably first restrict growth
processes (meristem activities), while C acquisition
continues at more than sufficient rates (Grace, Bernin-
ger & Nagy 2002). This hypothesis of a sink limitation
of tree growth at climatic treelines (Körner 1998) has
gained support from recent surveys which reveal
ample provision of treeline trees with C-storage com-
pounds (Hoch & Körner 2003; Shi, Körner & Hoch,
2005), not congruent with a photosynthetic bottleneck
of tree growth in cold environments. Here we explore
the likelihood of C limitation for tree growth at an alti-
tude where the partial pressure of CO2 is nearly half
that at sea level.
Fig. 1. The Polylepis treeline ecotone at Nevado Sajama.
(a) Volcano Sajama (6542 m a.s.l.) with the Polylepis tarapacana
Materials and methods forest belt between 4200 and 5000 m. White arrows indicate
three sampling sites along the transect (see text). (b) Highest-
     growing ‘tree-like’ P. tarapacana individuals at 4810 m a.s.l.
Trees to the left are ≈3 m high. (c) Overview of the highest
We studied high-altitude populations of Polylepis tara- sampling site at 4810 m a.s.l. The area studied is marked by
pacana trees at the western front of Nevado Sajama the white trapezoid. White cross (×) indicates location of
(summit 6542 m a.s.l.) in Oruro province, Bolivia temperature loggers. Note the persons at the corners of the
(18°07′ S, 68°57′ W; Fig. 1). The climate is subtropical- marked plot as a size reference.
alpine with a wet, warm season during the southern
hemisphere summer from November to April and a dry,
cold season between May and October. Annual precipita- higher than 3 m are absent; Körner 2003). Shrub-sized
tion, which is very variable among years (Hardy et al. individuals of P. tarapacana are found at even higher
1998), averages at ≈330 mm [316 mm at 4220 m a.s.l., elevations up to 5100 m a.s.l. (Braun 1997 and refer-
1975 – 85 mean, cited by Hardy et al. (1998) and 347 mm ences therein), similarly to reports from northern Chile
at 4300 m a.s.l., 4-year mean, recorded by M. Liberman- (Troll 1973). Especially at the upper end of the forest
Cruz cited by Braun (1997)]. belt, P. tarapacana is absent from south-facing (pole-
© 2005 British
Ecological Society, On Nevado Sajama, P. tarapacana forms open for- facing) slopes, and highest stand densities are found on
Functional Ecology, est stands between 4200 and 4810 m a.s.l. (with the north- (equator-) to north-east-facing slopes (Braun
19, 941–951 treeline, defined here as the altitude above which trees 1997; Fig. 1a). Irrespective of altitude, P. tarapacana
943 Table 1. Site characteristics of the three investigated Polylepis tarapacana stands at Nevado Sajama
Polylepis at the
world’s highest Altitude (m a.s.l.) Aspect Inclination (°)
treeline
4360 NNW 30
4550 N 30
4810 N 25
*Estimated across all tree-size classes >5 cm.
tends to grow polycormic and forms open ‘dwarf’ for-
ests with tree height rarely exceeding 5 m, although
some monocormic individuals at lower altitudes reach
maximum heights of ≈7 m. Co-dominant plant species
are tussock grasses (Festuca orthophylla, Calama-
grostis curvula, Calamagrostis orbignyana); shrubs
(Baccharis incarum, Parastrephia lepidophylla, Parastrephia
quadrangularis); and cushion plants (Azorella com-
pacta, Pycnophyllum molle). Independent of exposure
and inclination, the vegetation cover is low and >50%
of the ground is bare soil of volcanic origin. Even at the
end of the dry season, we found moist soil at ≈30 cm
depth under a layer of dry, insulating volcanic dust, a
common feature at high altitudes in regions with low
rainfall (Körner 2003).
  
Soil temperatures at the treeline were continuously
recorded at hourly intervals for a full year from 25
August 2003 – 1 September 2004 by using completely
sealed, single-channel thermo-loggers (−5 to +50 °C,
Tidbit, Onset, Cape Cod, MA, USA). Following the
protocol of Körner & Paulsen (2004), two loggers were
buried at −10 cm soil depth beneath P. tarapacana trees
under full canopy shade at two sites, one at 4780 m
a.s.l. and the other at 4810 m a.s.l. (Fig. 1). As both
loggers revealed similar recordings, only mean temper-
atures for both sites are presented. The temperature
loggers were calibrated at the beginning and end of the
measurement period in an ice–water mix (0 °C refer-
ence point). As in the analyses by Körner & Paulsen
(2004), the beginning of the growing season was
defined as the date at which the daily mean soil tem-
peratures at −10 cm exceeded 3·2 °C, and the end of
the growing season as the date when daily mean soil
temperatures dropped below 3·2 °C. Short excursions
below 3·2 °C during the warm-rainy season were not
excluded. For physical reasons, the 3·2 °C daily mean
soil temperatures in shade at 10 cm depth approximate
a daily mean air temperature of 0 °C (Körner &
Paulsen 2004). We also mounted one sensor in the can-
opy of a tall tree at 4810 m a.s.l. 2 m above-ground.
The sensor was placed on the poleward facing side of
the stem under a thick canopy of branches to screen it
fully from sky radiation. This shaded sensor recorded
© 2005 British
Ecological Society, a canopy air temperature, which is co-affected by the
Functional Ecology, tree’s aerodynamic properties and solar canopy heat-
19, 941–951 ing. On 25 August 2003 soil temperature profiles were
Stand density* (trees ha−1) Basal area* (m2 ha−1)
1800 2·1
2400 2·3
1600 1·4
measured manually in open and tree-covered places on
a north- and south-facing slope, at 4550 m a.s.l., using
a 3 mm steel probe with a thermistor (Testoterm 110,
Testoterm, Lenzkirch, Germany). Here temperatures
are presented in °C and temperature differences in K,
to avoid confusion between them, as is the custom in
bioclimatology and applied physics.
    
Polylepis tarapacana trees were studied at three eleva-
tions along an altitudinal transect covering 450 m of
altitude from 4360 to 4810 m a.s.l. (Table 1; Fig. 1). At
each site the number of tree individuals (excluding
seedlings <5 cm) was counted for a randomly chosen
area of 10 × 10 m at the lower and middle altitude, and
of 30 × 15 m at the uppermost site (Fig. 1), to calculate
stand density per hectare. Tree height and maximum
stem diameter (disregarding the loose outer bark), as
well as the annual length increment of leading
branches, were measured for 15 trees per elevation.
At each altitude, two stem cores were taken from
eight individual trees (>2 m high) using a 5 mm stem
corer (Suunto, Finland). Of each stem sampled, one
core was kept intact for later tree-ring analyses, while
the other was immediately separated into 1·5 cm seg-
ments, from the outermost tree ring towards the pith,
for chemical analyses. Analyses for starch and sugars
revealed strong decreasing concentrations of both
compounds from the outermost stem section towards
the pith (where concentrations were almost zero), clearly
characterizing P. tarapacana as a heartwood-forming
species (data not shown). For the current study, only the
results for the outermost (youngest) 1·5 cm segments
are presented, and are referred to as sapwood.
Finally, 5-year-old branchlets were collected from
the upper, well lit crown regions of 10 trees (>2 m) at
each site, and all leaves and the xylem (with bark and
phloem removed with a knife) were sampled separately
for chemical analyses. All tissues were sampled on two
consecutive days (24 and 25 August 2003) between
11.00 and 14.00 h, and dried at 70–80 °C within a
maximum 6 h from sampling.
After returning to the Basel laboratory, the intact
stem cores were smooth-cut with a razor blade and
tree-ring width (±0·01 mm) was measured using an
electronic analysis bench (LINTAB, TSAP, Heidelberg,
Germany). Because of the irregular growth of Polylepis
stems and the frequent occurrence of intermittent
944 layers of damaged tissue (perhaps from fire or fungal
G. Hoch & infections), we found it impossible to synchronize
C. Körner cores from those trees accurately. We therefore
refrained from analysing chronosequences of tree
rings, but still estimated the tree age and calculated
mean ring widths for each core. Stem cores were also
used for the gravimetric determination of sapwood
density (mg cm−3). For calculation of specific leaf area
(SLA; cm2 g−1) and leaf density (mg cm−3), 10 leaflets
were randomly chosen from each sampled branch and
dry weight, as well as leaf thickness, determined using
a handheld micrometer (±0·01 mm, Teclock Corp.,
Nagano, Japan). Finally, those leaves were rehydrated
in distilled water for 6 h before measuring the leaf area
on a photoplanimeter (LI-3050A, Li-Cor, Lincoln,
NB, USA). All tissue samples for chemical analyses
were re-dried at 75 °C until weight constancy, ground
to fine powder, and stored over silica gel at 4 °C until
analyses. Parts of the leaf powder were also used for
mass spectrometric stable-isotope analysis, in order to
assess the systemic water status of the trees.
 
Non-structural carbohydrates
Non-structural carbohydrates (NSC) were analysed
after Wong (1990), as described in more detail by Hoch
& Körner (2003). Non-structural carbohydrates are
defined here as the sum of the three most important
low molecular-weight sugars (sucrose, glucose and
fructose) plus starch. The low molecular-weight sugars
were determined photometrically after enzymatic conver-
sions with invertase and phosphoglucose-isomerase.
Following an enzymatic degradation of starch to
free glucose by a crude fungal amylase (‘Clarase’ from
Aspergillus oryzae, Enzyme Solutions Pty Ltd, Crydon
South, Victoria, Australia), the sum of free sugars plus
starch (NSC) was determined in a separate analysis.
The concentration of starch was calculated as NSC
minus the free sugars.
Lipids
Lipids (acylglycerols) were determined following the
method of Eggstein & Kuhlmann (1974) as described
in detail by Hoch & Körner (2003). Following saponi-
fication of lipids by extraction of ≈10 mg plant powder
in aqueous NaOH for 30 min, the amount of liberated
glycerol was determined after enzymatic conversion of
glycerol to glycerol-3-phosphate in a 96-well micro-
plate reader. To enable direct comparison of the quan-
titative contribution of lipids to the whole mobile C
pool, we assumed that almost the entire acylglycerols
in wood are triacylglycerols, and converted the meas-
ured glycerol concentrations to percentage lipids per
© 2005 British
Ecological Society, dry biomass, using a mean triacylglycerol molecular
Functional Ecology, weight of 875 (conservatively assuming the proportion
19, 941–951 of C17 : C18 fatty acids to be 1 : 1).
Gas chromatography
Gas-chromatography was applied to estimate the
contribution of all low molecular-weight carbohydrates
(and sugar alcohols) other than those covered by the
NSC method. The samples were extracted in methanol :
chloroform : water (12 : 5 : 3) at 60 °C for 30 min. After
phase separation by addition of water and chloroform,
aliquots of the aqueous phases were vacuum dried,
silylized with bis(trimethylsilyl)-trifluoroacetamide
(BSTFA) and trimethylchlorosilane (TMCS) and
analysed on a capillary column (HP1, 30 m × 0·20 mm
i.d., 0·2 µm film thickness) on a HP 8690 gas chro-
matograph (Agilent, CA, USA; detector: FID; analysis
software: HP ). Phenyl-β-glucopyranosid
was used as internal standard.
Nitrogen
Total N concentrations were determined in dried sam-
ples with a CHN elemental analyser (Vario EL III,
Elementar Analysesyteme, Hanau, Germany).
   
Compound concentrations are given on a dry matter
(% DM) as well as on a volume (mg cm−3) basis, as
higher tissue densities ‘dilute’ non-structural cell com-
pounds on a dry matter basis by a higher proportion of
structural compounds. Results for NSC were log-
transformed to meet the requirements of normal distri-
bution prior to analyses. All other values were a priori
normally distributed and so were computed untrans-
formed. Influence of elevation was analysed by Type III
 with altitude as fixed factor. A Tukey–Kramer
Honest Significant Difference (HSD) test was used
to test for significant differences between altitudes.
All statistical tests were performed with  3·2·2
(SAS institute, Cary, NC, USA).
Results
  
The −10 cm soil temperature at treeline (mean for
4780 and 4810 m a.s.l.) exhibited a clear seasonality,
with warmer temperatures from October to April and
cooler temperatures from May to September. The mid-
summer reduction of temperature (2·5 months) is typ-
ically associated with clouds and rain, and we presume
that most of the growth of P. tarapacana occurs after
this period in March and April. By our purely meteor-
ological definition (see Materials and methods), the
growing season lasted for 265 days in 2003/04 (from
29 August 2003 to 21 May 2004; Fig. 2). The mean
−10 cm soil temperature during this 265-day period was
5·4 ± 0·1 °C. The minimum and maximum daily means
during that period were 2·2 °C (13 February 2004) and
8·9 °C (9 December 2003). The absolute minimum
945
Polylepis at the
world’s highest
treeline
Fig. 2. Long-term temperature curves at the Polylepis tarapacana treeline. Above:
characteristic diurnal crown air-temperature curves at 4810 m a.s.l. during three
selected periods: early warm season (1– 4 November 2003); peak warm season (6–9
February 2004); peak cold season (4 – 7 July 2004). Air temperatures were measured in
full canopy shade. Note that temperatures < −5 °C were not recorded. Below: root-
zone temperatures (−10 cm) under full canopy shade (mean of two independent
measurements between 25 August 2003 and 1 September 2004 at 4780 and 4810 m
a.s.l.). Black curve, daily mean temperatures; grey area, daily temperature amplitudes
(diurnal minimum and maximum temperatures). Histogram shows frequency
distribution of daily mean soil temperatures across the growing season.
daily mean soil temperature for the entire year was
0·4 °C, recorded on 14 July 2004.
Diurnally and annually, the canopy air temperatures
at the treeline oscillated at a much greater amplitude
than soil temperatures (Fig. 2). During the afternoon
air temperatures, which were always recorded in full
shade, regularly reached more than 20 °C on sunny
days, mainly during the growing season, but also on
warmer days from May to September (Fig. 2). The wet
period from the end of December to the beginning of
March was characterized by quite cold canopy tem-
peratures (mean 4·2 °C) and a strongly reduced daily
amplitude, with night-time minimum temperatures
rarely below 0 °C. Freezing temperatures during at
least 1 h per day were recorded on 303 days, hence
night-time freezing within the canopy occurred almost
every day except during the middle of the wet season.
Hourly temperature minima below −5 °C were meas-
ured on 91 days, and on 16 days the daily mean crown
air temperature was below 0 °C.
© 2005 British
Ecological Society, The soil temperature profiles on south- and north-
Functional Ecology, facing slopes clearly revealed strong slope effects, with
19, 941–951 morning temperatures below 5 cm being ≈6 K higher
Fig. 3. Temperatures along three soil profiles at sites with
different slope aspects [north-facing (N-) and south-facing
(S-) slopes] and vegetation cover (with and without canopy
shadow of Polylepis). Records were taken between 9.50 and
10.20 am at 4550 m a.s.l. (25 August 2003; air temperature
5·2 °C).
on north-facing slopes, where P. tarapacana grows
(Fig. 3). Soil temperatures under P. tarapacana and
under grass tussocks on the north-facing slope revealed
no differences near the surface, but soils under trees
were ≈1 K colder below 20 cm soil depth (Fig. 3).
    
Stand density (here defined as number of trees
>5 cm ha−1), as well as the basal stem area per hectare,
were highest at the middle stand and lowest at the
treeline (Table 1). The relative frequencies of tree-height
classes show that the smallest height class (0·05–0·5 m)
accounted for the largest fraction (between 22 and
38%) at all three altitudes, indicating successful regen-
eration across the entire transect (Fig. 4). Surprisingly,
the uppermost stand was particularly rich in tiny
(<5 cm) Polylepis seedlings (not included in the demo-
graphic survey) and exhibited the most pronounced
pyramid-shaped height-class distribution, which may
point towards regular regeneration success at the treeline.
We cannot exclude that herbivory had affected the
patterns found, although we saw no browsing damage,
but trampling by llamas, alpacas and humans may
have diminished the number of small seedlings at the
lower sites.
The average tree height of adult trees (>1 m high)
decreased significantly by one-third from the lowest to
the uppermost site, while there was no significant
change in average stem diameter with elevation
(Fig. 5). The mean tree-ring width in the cored (>2 m)
trees decreased towards the treeline by 20% (Fig. 5),
but due to the large interannual variations in tree-ring
growth within a single stem (from ≈0·1–3 mm year−1),
as well as the large within-site differences among tree
individuals, this reduction of annual increment was
not significant across the transect. However, sapwood
density increased significantly with altitude by almost
946
G. Hoch &
C. Körner

Fig. 4. Frequency distributions of tree-height classes of Polylepis tarapacana stands at

three different altitudes across the treeline ecotone. Numbers of trees measured (n) are
given. Numerous tiny seedlings of P. tarapacana were found at the uppermost site but
were not counted for the demographic survey.

10%, probably as a consequence of the reduced tree-

ring widths at the highest elevation (Fig. 5). As the alti-
tudinal trend of stem diameter paralleled that of mean
tree-ring width, the mean stem age of the largest trees
is approximately the same at all sites along the
transect. A coarse estimate revealed ages between 130
and 160 years, but rootstocks may be much older. Neither
SLA nor leaf-volume density changed significantly
with elevation, although SLA tended to decrease
towards the treeline (Fig. 5).
The annual increment of leading shoots did not dif-
fer between the lowest and the middle stand, but was
significantly smaller for the uppermost trees for both
growing seasons investigated (2001/02 and 2002/03; Fig. 5. Tree-growth parameters of Polylepis tarapacana at
Fig. 6). The decrease in shoot growth between the low- three altitudes along the transect. (a) Mean tree height (n =
est and the uppermost stand was more pronounced for 15 –32 per altitude) and stem diameter (n = 8 per altitude); (b)
mean sapwood density and tree-ring width (n = 8 per
the 2001/02 growing season (−40%) than for the 2002/
altitude); (c) specific leaf area (SLA) and leaf density (n = 10
03 season (−25%). per altitude). Different letters show significant differences at
the 0·05 level by the Tukey–Kramer test.

- , 

   
Irrespective of altitude and tree organ, low molecular-
weight carbohydrates accounted for the largest frac-
tion of NSC (Fig. 7). The starch fraction of the NSC
pool was smallest in branch sapwood (17% of total
NSC pool) and highest in stem sapwood (32%). Within
the low molecular-weight carbohydrate fraction,
the sugars analysed by the NSC method (glucose,
fructose and sucrose) covered >90% of the total pool
in all organs (Fig. 7). In addition to the three sugars
mentioned above, only raffinose and the cyclitol
myo-inositol were present at concentrations measurable
by gas chromatography. Other carbohydrates such as
© 2005 British
Ecological Society, galactose and stachyose were detectable in traces,
Functional Ecology, while sorbitol was completely lacking in all samples
19, 941–951 investigated.
The altitudinal differences in NSC, as expressed on
a dry mater basis, were generally small in all three
organs investigated (Fig. 8). Free sugars increased
with elevation in all organ types (significant in leaves
and branch sapwood but not in stem sapwood;
Table 2). The smaller starch fractions decreased from
the lowest to the highest site (not significant in leaves;
Table 2). The combination of both compound groups
(NSC) resulted in a significant increase with elevation
in leaves, and no significant difference in branches and
stem sapwood (Fig. 8; Table 2).
When expressed on a volume rather than a dry mat-
ter basis (avoiding the bias introduced by tissue density
differences), the overall NSC trends with altitude did
not change (Fig. 8). However, as the wood density
increased significantly towards the treeline, NSC
947
Polylepis at the
world’s highest
treeline

Fig. 6. Mean length of annual shoot growth of Polylepis

tarapacana across the altitudinal transect for the growing
Fig. 7. Relative proportion of (a) starch and free sugars
seasons 2001/02 and 2002/03 (n = 15 shoots per elevation).
within the whole non-structural carbohydrate (NSC) pool;
Different letters show significant differences (P < 0·05) among
(b) sugars within the low molecular-weight sugar pool in
the altitudinal categories for each season. Drawing (right)
different organs of Polylepis tarapacana. Glc, glucose; Fru,
shows terminal 2-years increments of a P. tarapacana
fructose; Sacc, sucrose; Raff, raffinose; myo-I, myo-inositol.
shoot.
Values are means across all three altitudinal categories
(n = 30 for leaves and branches; n = 24 for stem sapwood).

concentrations in stemwood on a volume basis were
enhanced in the uppermost trees relative to the lowest
site (Table 2). Even in leaves, in which volume density
did not change significantly across the transect (Fig. 5),
the increase in NSC concentrations with elevation
became more pronounced on a leaf-volume basis than
on a leaf dry matter basis (Table 2).
Total lipid concentrations were low compared with
NSC, and hardly exceeded 0·5% DM in branch and
stem sapwood. Neither the twofold altitudinal increase
of lipid concentrations in branchwood, nor the altitu-
dinal decrease of lipids by 30% in stem sapwood, was
significant when expressed as % DM (Fig. 9). How-
ever, when accounting for the increased wood density
of trees at the tree limit, the lipid concentrations in
branchwood were significantly higher at the upper-
most site on a volume basis (Fig. 9). Total leaf N con-
centrations increased significantly with elevation on a
dry matter basis, but only insignificantly when calcu-
lated per unit leaf volume (mg N cm−3; Fig. 10).
Stable C isotope data for leaves of P. tarapacana
sampled between 4320 and 4810 m a.s.l. revealed an
altitudinal increase of δ13C, reaching from −23·9‰ at
the lowest site to −23·3‰ at the treeline. The calculated
linear regression is δ13C = −28·13 + 0·00104 × altitude
(r2 = 0·699), which yields an approximate 1·0‰ increase
per altitudinal km, and a hypothetical sea-level refer-
ence of −28·13‰.
Discussion
The mean 5·4 °C growing season soil temperature
measured in the current study at the upper edge of the
Sajama treeline ecotone matches well with the world-
wide pattern described previously (Körner 2003). For
instance, an average growing season mean temperature
of 5·4 °C was measured at different treelines on Mexi-
can volcanoes, 19° N (Hoch & Körner 2003). Tropical
and subtropical treelines (with mean growing season
temperatures of 5–6 °C) generally appear to operate at
temperatures 1–2 K cooler than temperate and boreal
zone treelines (≈7 °C growing season mean tempera-
tures), which led to a global mean for 46 treelines of
6·7 ± 0·8 °C (Körner & Paulsen 2004). The treeline

Table 2. Relative differences of non-structural carbohydrate (NSC) concentrations between the lowest and uppermost sampling sites, and results of an 
for elevation effects on NSC concentrations among all three altitudes. Results for each organ are given as percentage dry matter (% DM) and mg per volume

Sugars Starch Non-structural carbohydrates

Difference Difference Difference

Plant part Parameter df (%) F P (%) F P (%) F P

Leaves (% DM) 2 +22 7·0 0·004 −15 1·0 0·369 +10 5·7 0·009
(mg cm−3) 2 +27 9·5 0·001 −12 0·8 0·466 +15 7·0 0·004
Branches (% DM) 2 +19 5·9 0·047 −36 7·4 0·003 +5 0·5 0·641
(mg cm−3) 2 +30 6·0 0·007 −30 6·0 0·007 +15 1·9 0·171
© 2005 British
Stemwood (% DM) 2 +3 0·4 0·657 −49 4·0 0·036 −19 1·8 0·192
Ecological Society,(mg cm−3) 2 +13 1·2 0·335 −44 3·2 0·063 −11 0·8 0·465
Functional Ecology,
Significant
19, 941–951differences (P < 0·05) are in bold.
948
G. Hoch &
C. Körner
Fig. 8. Concentrations of non-structural carbohydrates (NSC) in leaves, branch
sapwood and stem sapwood of Polylepis tarapacana along the altitudinal transect
(n = 10 for leaves and branches; n = 8 for stem sapwood). Values are given as
percentage dry matter (left) and as mg cm−3 of the respective tissue (right). Different
letters show significant differences at the 0·05 level among altitudes by the Tukey–
Kramer test. Note the different y axes.
of Nevado Sajama is not an exception from other
subtropical or tropical treelines, and thermally fits the
global patterns. Other environmental factors may
modulate year-to-year growth variations, but in the
light of these data, effects other than those by temper-
ature seem irrelevant for the actual position of the
uppermost trees in this area. For instance, Morales
et al. (2004) had shown that moisture availability can
influence annual tree-ring width in the Andes, but
moisture is certainly not the decisive factor for the
rather abrupt Polylepis treeline, for several reasons. (1)
There is no indication of water stress in δ13C data from
P. tarapacana leaves. The measured δ 13C increase
of 1·0‰ km−1 does not deviate from the elevational
gradients found in a global survey, which revealed an
average of +1·2‰ km−1 for a within-species comparison
of 12 herbaceous plants, and +0·9‰ km−1 for an inter-
© 2005 British
Ecological Society, specific comparison of 25 tree species (Körner et al. 1988).
Functional Ecology, (2) Despite the low annual precipitation of ≈330 mm,
19, 941–951 we found soils moist at 30 cm below the surface at the
Fig. 9. Lipid concentrations in stem and branch sapwood of
Polylepis tarapacana at the three altitudes of the transect
(n = 10 for branches; n = 8 for stems). Values are given as
percentage dry matter and as mg cm−3. Different letters show
significant differences (P < 0·05) among altitudes by the
Tukey–Kramer test.
end of the dry season. Similar situations are reported
for sites above 4200 m a.s.l. in Argentina (Körner
2003), and reflect a combination of low potential eva-
potranspiration and storage of runoff from higher ele-
vations. Functionally humid and mesic climates are
abundant at annual precipitations well below 350 mm
at high altitudes and latitudes (Walter & Breckle 1994).
(3) Polylepis tarapacana reaches the highest altitudes
on warm and dry equator-facing slopes, with no trees
on the more humid, poleward-facing slopes. If the
trees’ distribution were water-limited, we would expect
them to be restricted to the cooler, south-facing slopes.
Crown air temperatures revealed characteristic pat-
terns of the subtropical alpine climate, with harsh con-
ditions for prostrate growing at the treeline. First, on
more than 80% of days recorded, night-time air tem-
peratures fell below 0 °C. Rada et al. (2001) pointed
out that P. tarapacana is probably frost-tolerant during
the major part of the year, but may switch to frost
avoidance by accumulating low molecular-weight
949
Polylepis at the
world’s highest
treeline
Fig. 10. Altitudinal trend of total leaf nitrogen concentrations
in 1-year-old leaves of Polylepis tarapacana along the transect.
Values are given as percentage dry matter and as mg cm−3.
Different letters show significant differences (P < 0·05) among
altitudes by the Tukey–Kramer test.
sugars at the peak warm and wet season (January and
February), when temperatures rarely fall below freez-
ing. On the other hand, as the coldest nights occur
when skies are clear, they are generally followed by the
warmest daytime temperatures, resulting in extreme
high diurnal amplitudes between minimum and maxi-
mum air temperatures, which can reach more than
30 K. The very high afternoon canopy air temperatures
measured in the current study probably resulted from
special microclimatic properties of Polylepis crowns,
which may trap heat fluxes from the surrounding bare
soils. It has been shown for Polylepis sericea stands that
mean air temperatures within the forests are generally
above that of the free atmosphere (Goldstein, Meinzer
& Rada 1994).
The high temperature difference between north- and
south-facing slopes (>6 K) underlines the significance
of slope exposure. Braun (1997) reported similar expos-
ure effects for Nevado Sajama at 4500 m a.s.l., where
the temperature difference even increased towards
© 2005 British
Ecological Society, late afternoon. According to Braun, the distribution of
Functional Ecology, P. tarapacana is related to moisture on a very broad
19, 941–951 geographic scale across the Western Cordillera, while
on a local scale its distribution is predominantly driven
by solar irradiance and slope aspect, with trees clearly
restricted to the warmer and presumably even drier
sites. Such pronounced slope exposure effects on
treeline position and soil temperature are rare, and
seem to reflect the largely bare volcanic ground and the
very steep slopes. With less steep terrain and denser
ground cover, no direction effect on treeline position
was found on Mexican volcanoes (Beaman 1962) or in
the Alps (Paulsen & Körner 2001; Körner & Paulsen
2004). Further, no clear slope effect on the distribution
of P. sericea trees was found in the Venezuelan Andes
(Goldstein et al. 1994).
Tree seedling mortality exceeding that of other taxa
due to frost events during the growing season has been
discussed as a primary determinant of treeline position
at high altitudes (Smith et al. 2003; Wang et al. 2004),
although there is no evidence that trees are less capable
than other life forms of resisting low temperatures
(Sakai & Larcher 1987). The analyses of tree height
along the current transect revealed that the smallest
(<0·5 m) tree height class is most abundant. Provided
that tree height correlates at least loosely with tree age,
this points at a dominance of young trees at all three
elevations, most pronounced at the highest site. The
‘healthy’ demographic pyramid at 4810 m a.s.l. sug-
gests constant recruitment events and sufficient seed-
ling survival during the past decades. Additionally,
numerous tiny seedlings were found at the uppermost
site but not at the lower elevations. Hence it seems
highly unlikely that a lack of seedlings determined the
treeline on Nevado Sajama. Similarly, Byers (2000)
described high seedling numbers and good regenera-
tion of a subalpine Polylepis forest in the upper Pisoc
Valley in Peru. The critical constraints must affect later
life stages, when trees transform from shrub to tree
stature and the apical meristems protrude from the
warmer air layer near the soil surface, coupling crown
temperatures more closely to the climatic conditions of
the free atmosphere (Grace & Norton 1990). Accord-
ingly, annual shoot growth in mature P. tarapacana
crowns was small, and trees higher than 3·5 m were
absent at the uppermost site in the current study.
The comparatively low starch concentrations found
in all tree organs and sites may reflect the time of sam-
pling near the end of the cold-dry season. Temperate
evergreen conifers, for example, also exhibit lowest
starch concentrations towards the end of the dormant
season, but a pronounced starch accumulation imme-
diately prior to the flushing of new shoots (Schaberg
et al. 2000; Hoch, Richter & Körner 2003). Similarly
to our study, Rada et al. (2001) found free sugar con-
centrations to be more than three times higher than the
concentrations of starch in leaves of P. tarapacana at
the beginning of September. The complete absence
of sorbitol in P. tarapacana is in line with previous
findings of Wallaart (1980), who described this sugar
alcohol to be lacking in most phylogenetic tribes of
the subfamily Rosoideae (which includes the genus
950 Polylepis), while it resembles an important form of C
G. Hoch & transport in all other subfamilies within the Rosaceae.
C. Körner There was no evidence for a depletion of mobile C
pools in P. tarapacana with altitude. Although the dif-
ferences in NSC and lipid concentrations were small,
and most of the time insignificant, among the sites, we
found significantly higher concentrations of NSC in
leaves and lipids in branches at the uppermost eleva-
tion. Because NSC, as well as lipids, decrease from the
youngest tree rings towards the pith in heartwood-
forming trees (Magel et al. 1997; Piispanen & Saran-
pää 2002), the sampling procedure used for the current
study probably influenced the elevational trends in the
stemwood of P. tarapacana. At all three elevations,
stem sapwood was sampled as the outer 1·5 cm stem
core segment. Thus the slightly greater tree-ring width
at lower elevations may have contributed to the (not
significant) NSC reduction in stem sapwood towards
the treeline. In branchwood tissue, which was exactly 5
years old at each elevation, the mobile C pools tended
to increase towards the treeline.
The evidence that mobile C compounds are not
becoming increasingly rare in tissues of P. tarapacana
at the tree limit does not support the C-limitation
hypothesis (Stevens & Fox 1991; Johnson, Germino &
Smith 2004). In a recent study, low but clearly positive
net photosynthetic rates were measured in both the dry
and the cold season for P. tarapacana growing at
4300 m a.s.l. at Nevado Sajama (Garcia-Nunez et al.
2004). Goldstein et al. (1994) and Rada et al. (2001)
demonstrated strongly positive net assimilation rates
of P. sericea at its upper distribution limit in Venezuela,
making C shortage for this species highly unlikely.
Plants at high altitudes operate at very high photo-
synthetic capacity, and thus, together with increased
diffusivity, compensate for the elevational reduction
of partial CO 2 pressure (Körner 2003). Previous
studies revealed no change in maximum photo-
synthetic rates at local partial pressure of CO2 over 2–
4 km elevation (Körner & Diemer 1987; Terashima
et al. 1995). It seems more likely that growth drops so
abruptly, and thus leads to the altitudinal tree limit,
because temperatures fall too low for meristematic
activity (sink limitation). The results are therefore in
line with previous studies at northern hemisphere
climatic treelines at different latitudes, all of which
revealed increasing C-charging of tree tissue with
increasing altitude (Hoch & Körner 2003; Shi 2005).
The small altitudinal increase of N concentration in
leaf tissue follows global trends (Körner 1989; Mitchell
et al. 1999), and seems to be associated with enhanced
photosynthetic capacity at high elevations (Körner &
Diemer 1987).
In conclusion, we found no evidence that the ‘world-
record’ treeline elevation of P. tarapacana at Nevado
Sajama is the result of increasing C shortage, water
© 2005 British
Ecological Society, limitation or recruitment problems at high elevations.
Functional Ecology, The mean 5·4 °C soil temperature during the growing
19, 941–951 season places this treeline perfectly within the thermal
range of other tropical and subtropical treelines
worldwide, which occur at lower altitudes (Körner &
Paulsen 2004). The reason why P. tarapacana reaches
such exceptional elevations in this part of the Andes is
associated with the regional climatic peculiarities (e.g.
the ‘Massenerhebungseffect’, low degree of cloudiness,
solar warming of the bare volcanic soils). There is no
evidence that the physiology of P. tarapacana places
this species in an exceptional position compared with
other treeline-forming species, although evolution has
certainly selected for traits that are particularly suita-
ble for life in this environment, such as high year-
round frost tolerance of leaves.
Acknowledgements
We would like to thank M. Liberman (University
Mayor de San Andres, La Paz), F. Guzmán (Parque
Nacional Sajama) and S. Beck (Herbario Nacional de
Bolivia) for their great support in Bolivia, R. Körner and
E. Spehn for field assistance, J. Paulsen for processing
the temperature data, O. Bignucolo for CHN analyses,
and S. Peláez-Riedl for drawing and help with the fig-
ures. We further thank A. Richter and G. Hertenberger
(both University of Vienna, Austria) for GC analyses
of low molecular-weight sugars, and S. Keel and M. Jäggi
(both Paul Scherrer Institute, Switzerland) for δ13C
analyses.
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Received 18 April 2005; revised 1 July 2005;
accepted 4 July 2005