acta oecologica 32 (2007) 3641

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Original article

Altitudinal and seasonal variation of protective and

photosynthetic pigments in leaves of the worlds highest
elevation trees Polylepis tarapacana (Rosaceae)
J.A. Gonzaleza,*, M.G. Gallardoa, C. Boeroa, M. Liberman Cruzb, F.E. Pradoc
a

Instituto de Ecologa Vegetal, Fundacion Miguel Lillo, Miguel Lillo 251, 4000 Tucuman, Argentina
Instituto de Ecologa, Universidad Mayor de San Andres, La Paz, Bolivia
c
Catedra de Fisiologa Vegetal, Fac. de Ciencias Naturales e IML, Miguel Lillo 205, 4000 Tucuman, Argentina
b

article info

abstract

Article history:

In the present study we analyzed both photosynthetic and UV-B absorbing pigment varia-

Received 24 February 2006

tions in Polylepis tarapacana (Rosaceae) during two contrasting seasons (winter and summer)

Accepted 12 March 2007

at two altitudes (4300 and 5000 m a.s.l.) in the Sajama volcano (Oruro, Bolivia). UV-B absorb-

Published online 26 April 2007

ing pigments, chlorophyll a, b and carotenoids contents as well as the chlorophyll a to chlorophyll b ratio showed clear differences in both seasons. UV-B absorbing pigments, total

Keywords:

chlorophyll and chlorophyll a contents as well as chlorophyll a/b values were higher in win-

UV-B absorbing compounds

ter than in summer at both altitudes, while chlorophyll b content and the total chlorophyll

Carotenoids

to carotenoids ratio showed an opposite pattern. Carotenoids content exhibited not only an

Chlorophyll

increase with altitude but also a significant variation between seasons, the highest value

Polylepis

being recorded in winter. We discuss the results in relation to the radiation regime of the

Radiation regime

Sajama region rather than to the water status of the plant studied, since the latter was sim-

Acclimation

ilar for both seasons and altitudes.

2007 Elsevier Masson SAS. All rights reserved.

1.

Introduction

Polylepis occurs naturally at altitudes higher than any other arborescent genus in the world. All known species of this genus
are confined to the South American Andes (Simpson, 1979).
This genus is exclusively arborescent (trees or shrubs) and
tends to form open to very dense shrubs and forests reaching
elevations over 5000 m a.s.l., well above the upper continuous
forest limit (timberline). To explain the altitudinal successful
distribution of Polylepis, some authors (Rauh, 1956; Troll, 1959;
Walter and Medina, 1969) consider that the success of this

species may be attributed to the special microclimatic conditions associated with the rocky protected habitat in which it occurs. However, other investigators (Rada et al., 1985, 1996, 2001;
Goldstein et al., 1994; Gonzalez et al., 2002) state that the success of Polylepis at high altitudes is not only a consequence of
microclimatic conditions but also depends on the special features of its carbon economy and frost resistance.
Polylepis tarapacana is an evergreen species that grows on
the Sajama volcano (Bolivia) from 4250 to 5200 m a.s.l. (Liberman Cruz, 1986). Due to its high altitudinal distribution, this
species is exposed in high tropical environments to wide

* Corresponding author.
E-mail address: lirios@cgcet.org.ar (J.A. Gonzalez).
1146-609X/$ see front matter 2007 Elsevier Masson SAS. All rights reserved.
doi:10.1016/j.actao.2007.03.002

acta oecologica 32 (2007) 3641

diurnal and seasonal temperature fluctuations, frequent nocturnal frost, high radiant energy input and low CO2 partial
pressure. According to the daylight environment in the Sajama
volcano region and to the previous morphological and ecophysiological data of P. tarapacana such as smaller leaf area
and thicker cuticle (to reduce the transpiration rate), thicker
leaf, abundant leaf hairiness and CO2 assimilation rate, it could
be considered as a shade intolerant species (Braun, 1997;
Gonzalez et al., 2002; Garca-Nunez et al., 2004).
The altitudinal record of P. tarapacana is particularly important in relation to the ecophysiological mechanisms this species developed to protect the photosynthetic machinery
against the high solar (visible and UV-B) radiation existing in
that extremely unfavorable environment. According to this
viewpoint, we might expect this species to be relatively UV-B
tolerant with different strategies to achieve this tolerance.
With respect to UV-B radiation effects on plants, many
studies have been conducted under optimal growth conditions in growth chambers or greenhouses with various UV-B
lamp systems (Lavola et al., 1997; Kolb et al., 2001; Hilal
et al., 2004). However, there are not enough data available to
decide whether solar UV-B will have the same effect on plant
morphology as was observed in the laboratory, since a plant
growing under natural conditions is often subject to different
degrees of environmental stress due to different radiation regimes, water, nutrients or gas supply, among others. In addition, we found few studies of UV-B effects on trees in
natural ecosystems (Tevini and Teramura, 1989; Gonzalez
et al., 1993, 2002; Wand, 1995; Giordano et al., 2003). Also, there
is little evidence of UV-B effects on tropical tree species (Lovelock et al., 1992; Sullivan et al., 1994; Searles et al., 1995; Krause
et al., 2003). Consequently, according to Sullivan et al. (1994)
further information related to UV-B effects on trees and native
species is needed for an understanding of this problem. Thus,
the study of P. tarapacana may help to understand the adaptation mechanisms this species may have developed to grow
along altitudinal gradients. In this sense, we hypothesized
that relations between altitude, seasonal level of visible and
UV-B radiation and protective pigments might be good indicators of the adaptation degree of this species. Hence, the
purpose of this study was to compare protective and photosynthetic pigment contents of P. tarapacana in two contrasting
seasons (summer and winter) at two different altitudes (4300
to 5000 m a.s.l.).

2.

Material and methods

2.1.

Study site

The present study was performed at two altitudes (4300 and

5000 m a.s.l.) during summer and winter in the Sajama volcano
region in Oruro province, Bolivia (18 070 S, 68 570 W). Site characteristics were previously described by Gonzalez et al. (2002);
however, some climatic features of the area where P. tarapacana grows need to be commented. According to Liberman
Cruz (1986) the Sajama region (Sajama station at 4250 m
a.s.l.) could be characterized as a semiarid tropical high mountain environment with an annual mean temperature of 3.4  C

37

and a precipitation of 347.2 mm/year. Maximal and minimal

temperatures registered in summer and winter of the year
2002 were 21.0  C and -19.0  C, respectively. These values
were similar to those previously reported by Liberman Cruz
(1986) and to more recent measurements performed by Hoch
and Korner (2005). According to Koppens classification, the
climate of Sajama station corresponds to the following
nomenclature: Dw (micro thermal weather with dry winters).
In this region there are two well-differentiated seasons: winter
and summer. In February (summer), the average monthly
temperature was 4.2  C and the corresponding precipitation
99.3 mm, whereas in July (winter), they are 1.16  C and
0.4 mm, respectively.

2.2.

Radiation measurements

Visible radiation (PAR: photosynthetic active radiation) was

measured with a Quantum Sensor (LI-190SA) coupled to DataLogger (LI-1000) (Li-Cor, Lincoln, USA). UV-B radiation (UV-BB:
biologically effective UV-B radiation) was measured using
a Silicon photoelectric cell coupled to a Photometer/Radiometer (PMA2100, Version 1.17) (Solar Light Company, Inc., USA).
Measurements were performed using an identical pair of radiation testers for PAR and UV-B radiation, respectively. Each
tester pair was previously adjusted and calibrated according
to the manufacturers instructions. Measurements were taken
daily between 8 and 18 h at 30 min intervals during 5 days
including sunny and partially cloudy days to get a better
approach to the seasonal radiation. UV-B radiation flux density (kJ m2 day1) was calculated by integration of the curve
obtained from measurements between 8 and 18 h. For comparison of UV-B radiation, flux densities along an altitudinal
transect (4200 to 5000 m a.s.l.) using Greens semi-empirical
model (Green, 1983) were calculated. In contrast PAR radiation
measurements were obtained at 12:30 h, when solar radiation
over the canopy is more intense.

2.3.
Analysis of photosynthetic and UV-B
absorbing pigments
Leaf samples were obtained from flowering plants. Ten different plants were selected for each altitude and season. Fifty
leaves per plant were collected for chemical analyses. For
UV-B absorbing compounds 50 leaf discs (equivalent to
0.3925 cm2) per plant were extracted in the dark with 2 ml of
acidified methanol (methanol/water/HCl, 79:20:1) following
the procedure of Mirecki and Teramura (1984). Absorbance
was measured at 300 nm. Chlorophyll and carotenoids from
50 leaf discs were extracted using 2 ml dimethyl sulfoxide
(12 h in the dark at 45  C) as described by Chapelle and Kim
(1992). Photosynthetic pigments content was calculated from
absorbance at 664, 648 and 472 nm according to Wellburn (1994).

2.4.

Other analyses

Relative water content (RWC) and leaf mass per area (LMA)
were calculated according to the method described in a previous paper (Gonzalez et al., 2002).

38

Statistical analysis

Statistical differences were determined by Student t-test at

P < 0.05. For comparisons among means an analysis of variance was used.

3.

Results

3.1.

PAR and UV-B radiation

UV-B absorbing compounds showed a clear relationship between season-independent content and altitude. Thus, plants
at the highest site exhibited the highest values (34.5% and
32.2%) in winter and summer, respectively (Fig. 2). Absorbance values for winter were higher than summer ones at
both altitudes. The differences between seasons and elevations were similar on a leaf area (LA) basis because LMA did
not differ between sites and seasons (data not shown). In relation to photosynthetic pigments, Table 2 shows that total
chlorophyll, chlorophyll a and chlorophyll b contents and chlorophyll a to chlorophyll b ratio did not change with altitude in
either season. However, highest values for total chlorophyll,
chlorophyll a and chlorophyll a/b (nearly 5%, 42% and
80%, respectively) were observed in winter, while chlorophyll
b content showed the highest value in summer (nearly 28%).
Carotenoids content revealed not only an increase with altitude, but also a significant variation between seasons, with
the highest values in winter (32.7% and 32.6% at 4300 and
5000 m a.s.l., respectively). On the other hand, total chlorophyll
to carotenoids ratio was lower in winter at both sites (Table 2).
However, this reduction was more pronounced at 4300 m a.s.l.,
10.0 versus 7.9 for summer and winter, respectively.

Table 1 PAR and UV-B radiation flux density at 4300 and

5000 m a.s.l. in Sajama volcano region. Values are the
mean SD of 5 independent determinations

4300
5000

PARa (mmol m2 s1)

60

Winter
Summer

40
20

4500

4200

UV-B absorbing and photosynthetic pigments

Altitude
(m a.s.l.)

80

Highest values of PAR and UV-B radiation flux density in both

seasons were observed at 5000 m a.s.l. (Table 1). However, at
both altitudes winter values were higher than summer ones.
In order to assert the results, UV-B radiation flux densities calculated from field data were compared with those obtained
with Greens semi-empirical model (Fig. 1). In both altitudes
and seasons values of UV-B radiation flux density were
coincident.

3.2.

UV-B (kJ m-2 day-1)

100

UV-B (kJ m2 day1)

Summer

Winter

Summer

Winter

1927  124a
2276  112b

2260  103b
2493  97d

51.8  5.4a
60.7  4.6b

61.7  2.4b
70.0  3.0d

Values followed by the same letter are not significantly different at

P  0.05.
a Correspond to measurements performed at 0.30 p.m when solar
radiation over the canopy is more intense.

4700

5000

Altitude (m a.s.l.)
Fig. 1 UV-B radiation flux density (kJ mL2 dayL1) along an
altitudinal transect (4200 to 5000 m a.s.l.) in the Sajama
volcano (18 070 S, 68 570 W) in winter and summer
calculated according to Greens semi-empirical model.

3.3.

Relative water content (RWC) leaf mass area (LMA)

Relative water content (RWC) and leaf mass per area (LMA)
values did not show significant differences (P < 0.05) (Table 3).

4.

Discussion

Previous papers (Rada et al., 2001; Gonzalez et al., 2002; GarcaNunez et al., 2004) have reported some ecophysiological aspects such as water relations, gas exchange and soluble sugar
contents of Polylepis tarapacana (quenua or qewina) growing at extreme altitudes in the Bolivian Andes. In this paper we
report the altitudinal and seasonal variations of the UV-B
absorbing and photosynthetic pigments in the same species
growing at two different altitudes: 4300 and 5000 m a.s.l. P. tarapacana showed an increase in UV-B absorbing pigments and
carotenoids contents not only with increasing altitude but
also between seasons. Independently of the season, the highest values were found at 5000 m a.s.l. However, chlorophyll
content did not show any change between altitudes. These
results can be related to the light regime in the Sajama volcano region. Thus, according to our data, PAR and UV-B solar
radiation increased significantly between 4300 and 5000 m

Absorbance (300 nm g-1 DW)

2.5.

acta oecologica 32 (2007) 3641

80
70
60
50

Winter
Summer

40
30
20
10
0
4300

5000

Altitude (m a.s.l.)
Fig. 2 UV-B absorbing compounds contents of
P. tarapacana leaves at two different altitudes and seasons.
Vertical bars represent the mean SD of 5 different plants.

acta oecologica 32 (2007) 3641

Table 2 Total chlorophyll (Total Chl), chlorophyll a

(Chl a), chlorophyll b (Chl b), chlorophyll a to chlorophyll
b ratio (Chl a/b), carotenoids (Carot) and total chlorophyll
to carotenoids ratio (T. Chl/Carot) in leaves of
P. tarapacana at different altitudes and seasons. Each
value is the mean SD of 5 different plants
Altitude (m a.s.l.)

4300

5000

1221  42a
1278  37cb

1249  29ab
1323  14c

512  12a
735  12b

536  15a
756  11b

709  16a
543  14b

713  18a
567  19b

0.72a
1.35b

0.75a
1.33b

1

Total Chl (mg g DW)

Summer
Winter
Chl a (mg g1 DW)
Summer
Winter
Chl b (mg g1 DW)
Summer
Winter
Chl a/b
Summer
Winter
Carot (mg g1 DW)
Summer
Winter
T. Chl/Carot
Summer
Winter

122  7a
162  9.5c

138  6b
183  16d

10.0a
7.9b

9.0a
7.6b

Values followed by the same letter are not significantly different at

P  0.05.

a.s.l. in winter and summer, respectively (Table 1). The mean

altitude effects for both radiation ranges were 13.5%/1000 m
(PAR) and 10.7%/1000 m (UV-B). These results are consistent
with those recorded at other places in the world (Blumthaler
et al., 1994) and with the measurements performed in the Central Andes in Bolivia and Chile (Andrade et al., 1998; Piazena,
1996). Together with the increase in UV-B and PAR irradiance
with altitude, an increase is expected in protective radiation
compounds such as flavonoids and carotenoids. Data from
Fig. 2 and Table 2 show a significant increase in UV-B absorbing pigments and carotenoids contents with altitude in both
seasons, while chlorophyll content did not show a significant
variation between elevations. In every case, except for chlorophyll b, the highest values were found in the winter season in
agreement with those in UV-B and PAR radiation. In relation to
this fact, chlorophyll b is known to be more sensitive to UV-B
radiation than chlorophyll a (Strid and Porra, 1992). Thus, the
highest UV-B radiation detected in Sajama during winter is
most likely the cause of chlorophyll b depletion. On the other

Table 3 Relative water content (RWC) and leaf mass per

area (LMA) in P. tarapacana leaves at two altitudes in
winter and summer. Values of RWC and LMA are the
mean SD of 10 different plants
Altitude (m a.s.l.)

RWC (%)
Summer

4300
5000

Winter

LMA (mg cm2)

Summer

Winter

75.7  2.3a 78.5  4.3a 35.4  1.3b 33.6  3.8b

78.9  1.4a 79.0  3.3a 33.8  1.7b 32.6  2.5b

Values followed by the same letter are not significantly different at

P  0.05.

39

hand, the fact that the chlorophyll a to chlorophyll b ratio

shows differences between seasons but not at different altitudes should be pointed out. Chlorophyll a/b has been frequently used as an indicator of plant response to light
intensity (Hendry and Price, 1993).
In addition to the sensitivity of the photosynthetic machinery to UV-B radiation (Nogues and Baker, 1995; Baker et al.,
1997; Sharma et al., 1998), exposure to high levels of PAR radiation could be hazardous to plant photosynthesis (Asada, 1999;
Rokka et al., 2000). Thus, plants have evolved a variety of mechanisms to cope with UV-B and PAR radiation damage (Jordan,
1996; Maxwell et al., 1997; Kolb et al., 2001). In relation to PAR
radiation, we observed that total chlorophyll to carotenoids ratio was lower in winter at both altitudes. This fact suggests that
both synthesis and accumulation of carotenoids are very significant in this season. Carotenoids content increase is not
only related to their essential role in the photosynthetic process, but also to their significant role in the photoprotection
of photosynthetic membranes against the large amounts of
solar energy absorbed by photosynthetic pigments (DemmigAdams and Adams, 1996; Havaux, 1998; Asada, 1999). Consequently, carotenoids increase can be thought of as a safety
valve venting the excessive PAR energy before it can damage
the photosynthetic system (Gilmore, 1997). Thus, the highest
chlorophyll a/b as well as the lowest total chlorophyll/carotenoids values observed in the winter season may indicate a better
acclimation of P. tarapacana to high solar radiation.
On the other hand, the absence of variation in the chlorophyll content between altitudes probably represents an
adaptive growth strategy of P. tarapacana to maintain its photosynthetic capacity along an altitudinal gradient. In this sense,
data reported by Garca-Nunez et al. (2004) for P. tarapacana
showed that the maximum CO2 assimilation rate did not reveal
a significant difference between summer and winter. Similar
results were obtained for P. sericea in Venezuela (Venezuelan
Paramos) at 4000 m a.s.l. (Rada et al., 1996). In agreement with
this fact, our results did not show significant changes in LMA
values between seasons (Table 3). Likewise, Ziska et al. (1992)
demonstrated that plants from higher elevations did not show
significant alterations in maximal photosynthetic capacity
with increasing UV-B radiation. Thus, our results agree with
this assertion and are probably related to photorepair mechanisms mediated by UV and visible radiation (Fernbach and
Mohr, 1992; Ziska et al., 1992; Giordano et al., 2003).
The relationship between water stress and UV-B radiation
is still unclear for the time being. Many researchers found that
water limitations can decrease UV-B sensitivity (Teramura
et al., 1990; Balakumar et al., 1993). On the contrary, other
authors hypothesized that water stress can exacerbate UV-B
effects (Drilias et al., 1997; Hofmann et al., 2003). In P. tarapacana our results in winter and summer showed that RWC did
not change significantly with altitude (Table 3). In addition
and in agreement with these results, Hoch and Korner (2005)
found that there is no indication of water stress in the leaves
of P. tarapacana growing in the Sajama volcano. In addition,
the same investigators found that soil moisture up to 30 cm
below the surface did not change with altitude in either season (Hoch and Korner, 2005). Therefore, the probable relationships between UV-B absorbing pigments and carotenoids
increase in the leaves of P. tarapacana and water stress may

40

acta oecologica 32 (2007) 3641

be discarded. Nevertheless, these results do not agree with

those reported by Hofmann et al. (2003), who demonstrated
that UV-B radiation increased leaf water potential and UV-B
absorbing pigments under drought.
Although leaf thickness increase in response to UV-B radiation has been interpreted as alleviating the deleterious effects
by reducing radiation penetration (Warner and Caldwell, 1983;
Flint et al., 1985), previous anatomical data showed that P. tarapacana leaf thickness was almost constant at different
altitudes (Gonzalez et al., 2002). Thus, we consider that P. tarapacana adaptations to prevent the deleterious effects of high
solar (UV-B and PAR) radiation can be related to the presence
of UV-B absorbing pigments and carotenoids rather than to
leaf thickness. However, other strategies such as morphological adaptations or metabolic events may have also been
developed for P. tarapacana to persist in that extremely unfavorable environment.

Acknowledgments
We thank S. Urcullo, J. Chincheros and F. Velazco for their assistance in the Laboratory of Environmental Quality, Ecology
Institute (La Paz, Bolivia). We also acknowledge the support
of RICAS project (CRN 040).

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