Journal of Tropical Ecology

http://journals.cambridge.org/TRO

Additional services for Journal of Tropical Ecology:

Email alerts: Click here

Subscriptions: Click here
Commercial reprints: Click here
Terms of use : Click here

Ecological traits of the tropical treeline species Polylepis quadrijuga (Rosaceae) in the Andes of
Colombia

Virginia Velez, Jaime Cavelier and Beatriz Devia

Journal of Tropical Ecology / Volume 14 / Issue 06 / November 1998, pp 771 - 787

DOI: 10.1017/S026646749800056X, Published online: 08 September 2000

Link to this article: http://journals.cambridge.org/abstract_S0266467498000568

How to cite this article:

Virginia Velez, Jaime Cavelier and Beatriz Devia (1998). Ecological traits of the tropical treeline species Polylepis quadrijuga
(Rosaceae) in the Andes of Colombia. Journal of Tropical Ecology, 14, pp 771-787 doi:10.1017/S026646749800056X

Request Permissions : Click here

Downloaded from http://journals.cambridge.org/TRO, IP address: 129.81.226.78 on 29 Apr 2016

 Journal of Tropical Ecology (1998) 15:771–787. With 7 figures
Copyright  1998 Cambridge University Press

Ecological traits of the tropical treeline species

Polylepis quadrijuga (Rosaceae) in the Andes of
Colombia

VIRGINIA VELEZ*, JAIME CAVELIER* and BEATRIZ DEVIA†

* Departamento de Ciencias Biológicas, and † Departamento de Quı́mica, Universidad de

los Andes, AA 4976, Bogotá, Colombia
(Accepted 27 June 1998)

ABSTRACT. Information is presented on the phenology, herbivory, phytochemis-

try and production of the tree species Polylepis quadrijuga. Leaf production was lower
during the dry season than during the wet season, when minimum temperatures
also occurred. Flower and fruit phenology were also seasonal. Herbivory was signi-
ficantly higher for leaves expanded during the wet season (20%) than during the
dry season (1%), and was also higher for younger leaves. Flavonoids, compounds
known as UV-B protectors, were found in high concentration in leaves of P. quadri-
juga. There was a significant positive relationship between monthly rainfall,
monthly minimum temperatures and flavonoid concentration, but no relationship
was found with leaf age. The annual fine litterfall for the Polylepis forest was estim-
ated to be 3.9 t ha−1 y−1, a high value when compared to other paramo and upper
montane rain forests in tropical mountains. High production was associated with
high leaf nitrogen concentration (3.0–3.5%), high rates of nitrogen retranslocation
(80% dry weight), and relatively low leaf longevity (8.4 mo). High production in P.
quadrijuga is probably a key factor in explaining the existence of this large woody
species in a paramo environment otherwise dominated by bunch grasses, cushion
plants and giant rosettes of the genus Espeletia.

KEY WORDS: Andes, Colombia, flavonoids, herbivory, leaf longevity, paramo,

phenology, phytochemistry, Polylepis, production

I N T R OD U C T I O N

Polylepis quadrijuga Bitter is a tree species that grows above the continuous
treeline and within the grassland matrix of the paramo vegetation in the high
tropical Andes (Simpson 1986). The species forms homogeneous forests, with
the understorey dominated by mosses. Several physiological adaptations to the
paramo environment have been documented for Polylepis sericea in Venezuela,
including supercooling, low leaf osmotic potential (Rada et al. 1985), high
stomatal conductance, high photosynthetic rates and high dark respiration

771

http://journals.cambridge.org Downloaded: 29 Apr 2016 IP address: 129.81.226.78

 772 VIRGINIA VELEZ, JAIME CAVELIER AND BEATRIZ DEVIA

rates (Goldstein et al. 1994). In spite of the great importance of this genus as
a source of fire-wood in the Andean paramos (Ellenberg 1958, Kessler 1995)
and as a marker in palynological studies (Van der Hammen 1974, Smit 1978),
little is known about its ecology.
Leaf and flower phenology can be controlled by environmental factors, such
as seasonal variations in temperature and moisture (Borchert 1983; Reich &
Borchert 1982, 1984), by biotic selection (Aide 1988, Janzen 1967), or can be
endogenously determined (Dugand 1978, Loubry 1994). In paramo environ-
ments, characterized by seasonal variation in rainfall and by lower minimum
air temperatures during the dry season (Sarmiento 1986), variations in water
and air temperatures regimes could be controlling plant phenology and produc-
tion (Cavelier et al. 1992, Smith 1981, Smith & Young 1987). Production is
known to decrease along altitudinal gradients in tropical mountains (Grubb
1977), and this has been explained in terms of environmental factors, like
decreasing air and soil temperatures, nutrient availability and partial pressure
of CO2 (Cavelier 1996). Plant related factors, such as low leaf nitrogen concen-
trations, have also been cited as possible causes of low production in tropical
mountains (Tanner 1977). Herbivory could also have a negative effect on pro-
duction by reducing total leaf area or by inducing changes in leaf growth and
development (Louda 1984, Marquis 1984). Plants in tropical seasonal environ-
ments can use phenological strategies to reduce damage by herbivores, like the
production of new leaves during the dry season when herbivore density is lower
(Aide 1992, 1993).
Another important factor in the high altitude tropical environment of P.
quadrijuga, is high levels of UV-B radiation (Caldwell 1971, Caldwell et al. 1980,
Robberecht et al. 1980). The accumulation of flavonoids, carbon-based second-
ary compounds, can be induced under high UV-B radiation (Caldwell et al.
1983, Hrazdina & Parsons 1982, Murali & Teramura 1986, Teramura 1983)
and may play a key role in the protection of leaf tissues from DNA damage
(Kootstra 1994). Flavonoid concentration can also vary under different climatic
and edaphic conditions (Flück 1963), and can be higher in either young
(Crawley 1983, Hatcher 1990, Rhoades & Cates 1976, Scriber & Slansky 1981)
or mature leaves (Coley 1980, Feeny 1976).
In the present study we wanted to know whether ecological traits such as
leaf and flower phenology, production and herbivory, as well as leaf chemistry,
may help explain the occurrence of P. quadrijuga forests in an ecosystem other-
wise dominated by grasses and giant rosettes.

S TU D Y S I T E A N D S P E C I E S

Field work was carried out at the P. quadrijuga forest of ‘Sietecuerales’, Rio La
Playa (3200 m) in the Parque Nacional Natural Chingaza (4°30′N; 73°45′W),
Department of Cundinamarca, Colombia. Mean annual rainfall at the nearest
weather station (La Playa) is 1415 mm (1971–1991) with a marked rainy season

http://journals.cambridge.org Downloaded: 29 Apr 2016 IP address: 129.81.226.78

 The neotropical treeline species Polylepis quadrijuga 773

from March to October (Repizzo 1993). Mean annual temperature is 8.8 °C

with minimum temperatures being lower during the drier part of the year
(December–March). Annual sunshine is 745 h, with lower values during the
wet season (Figure 1).

Figure 1. Seasonal variations of sunshine (G), mean (P) and minimum air temperatures (p), mean
monthly rainfall (m) and pan-evaporation (M) for the period 1971–1991, at the nearby weather station of
‘Golillas’, paramo of Chingaza, Cundinamarca, Colombia. The vertical lines on symbols represent the stand-
ard error of the mean.

Polylepis quadrijuga, is one of the 15 species of the genus Polylepis. The genus
is distributed along the Cordillera of the Andes from Venezuela to northern
Chile and Argentina (Simpson 1979). P. quadrijuga is found only in the paramos
of the Departments of Santander, Boyacá and Cundinamarca on the Eastern
Cordillera of the Andes of Colombia. P. quadrijuga is an evergreen tree 1–10 m

http://journals.cambridge.org Downloaded: 29 Apr 2016 IP address: 129.81.226.78

 774 VIRGINIA VELEZ, JAIME CAVELIER AND BEATRIZ DEVIA

tall with compound leaves, twisted trunk and branches with a reddish bark that
peels continuously (Simpson 1979). This phenological trait may help reducing
the epiphytic load, particularly of mosses and lichens (J. Cavelier, pers. obs.).
Polylepis spp. currently grow in isolated patches restricted to steep and rocky
slopes (Arnal 1983). Two hypotheses have been proposed to explain this distri-
bution. Firstly, favourable microclimatic or edaphic conditions occur on rocky
slopes that allow the establishment and growth of the trees (Lauer 1981, Smith
1978, Walter & Medina 1969). Secondly, Ellenberg (1958) proposed that Poly-
lepis forests were once widely distributed and that human intervention by
means of fire, wood extraction and high altitude cattle ranching, reduced its
distribution to these isolated slopes. Regeneration of P. quadrijuga forests on
flat areas in the Natural Park of Paramo Chingaza, supports the latter hypo-
thesis (V. Velez, pers. obs.).

M ET H O D S

Phenology
Leaf phenology was studied in 10 trees (2–4 m tall), and in three branches
per tree (1–2 cm in diameter). Branches were selected from different sides of
the tree crown and the orientation of each branch measured with a compass
(± 5°). To measure leaf production (number of leaves/branch), newly emerged
leaves (2 cm long) were marked with pieces of plastic coated wire of different
colours every 30 d between December 1992 and December 1993. The monthly
count of the previously marked leaves allowed the calculation of the percentage
leaf survivorship as a function of time. Mean leaf life span (mo), was estimated
at 50% leaf survivorship. Flower and fruit phenology were studied in the same
ten trees used for the study of leaf production. The presence or absence of
inflorescenses and infructescenses for each tree was recorded every 30 d during
the same period.

Production
Leaf production (t dry weight ha−1 y−1) was calculated by multiplying the
average annual leaf production per branch of 1–2 cm in diameter (74.8 ± 7.74
leaves, n = 10 trees) by the average leaf dry weight (0.24 g ± 0.02 g, n = 10) by
the number of branches per tree (Y = 27.5X − 698; where Y is the number of
branches per tree and X is the tree dbh, r = 0.90, P < 0.01) and by the number
of trees per hectare (6.5 ± 0.9, in six 10 m × 10 m plots). Mean annual fine
litterfall (t dry weight ha−1 y−1) was calculated by subtracting the cumulative
percentage herbivory from the mean annual leaf production.

Nutrient retranslocation
Nitrogen retranslocation (R) was calculated as the difference in concentra-
tion between mature leaves and fine litterfall using the equation R = [(Cm-Cl)/

http://journals.cambridge.org Downloaded: 29 Apr 2016 IP address: 129.81.226.78

 The neotropical treeline species Polylepis quadrijuga 775

Cm] × 100, where Cm is the nitrogen concentration in mature leaves and Cl

is the concentration in fine litterfall (Del Arco et al. 1991). Nitrogen content
was determined with the micro-Kjeldahl technique.

Herbivory
Three leaves from each of the 10 trees used to measure leaf phenology
were selected at random to measure herbivory. Measurements were carried
out on leaves expanded during the wet (June) and dry season (January).
On each group of leaves (n = 10) herbivory was measured every 30 d over
7 mo. To measure the leaf area consumed every month, the number of mm2
of eaten tissue were counted using a millimetric plastic grid (Aide 1992).
The percentage area consumed by herbivores was calculated based on the
total mm2 per leaf.

Phytochemistry
In a preliminary qualitative analysis based on colorimetric and precipitation
reactions following the methods in Dominguez (1973) and Sanabria (1983);
quinones, tannins, steroids and flavonoids were found. There were no alkaloids
or triterpenes. Flavonoids gave the strongest reaction, and were analyzed
quantitatively in leaves of five age classes, expanded during the dry and wet
season. Three replicates per sample were used for a total of 30 samples. The
flavonoids were isolated and two of them identified by spectrophotometry, thin
layer chromatography (TLC) and comparison with standards, either obtained
in the laboratory or previously published (Geissman 1962, Harborne 1973,
Mabry 1969).
To determine the concentration of total glycosides of flavonoids, the meth-
anol plant extract was mixed with 5 % AlCl3 in methanol and the absorbance
measured at 421 nm. The total flavonoid content was calculated using ε =
29 200. The extraction and separation of the flavonoid compounds were carried
out using the following methods. First, 50 g of dry leaves (40 °C for 24 h) were
ground in a mortar and refluxed in 90 % ethanol for 5 h. Second, the extract
was filtered, concentrated in a rotatory evaporator, and washed with petroleum
ether to eliminate lipids and pigments. Third, the extract was hydrolyzed with
10 % HCl to eliminate sugars (Harborne 1973), and neutralized with a satur-
ated solution of sodium bicarbonate to precipitate aglycones. Finally, flavonoids
were extracted with ethyl acetate (Harborne 1973).
The ethyl acetate extract was chromotographed by TLC on silica gel plates
(F254 ref. 5567) in a benzene-ethyl acetate 1 : 1 mixture, using ammonia
vapours as the developing reagent. By means of preparative chromatography
the two most abundant flavonoid compounds were obtained and analyzed by
UV-Vis spectroscopy (Harborne 1973). The flavonoid compounds were identi-
fied based on their Rf (migration rate) and colour derived from the TLC plates
and their absorption spectra.

http://journals.cambridge.org Downloaded: 29 Apr 2016 IP address: 129.81.226.78

 776 VIRGINIA VELEZ, JAIME CAVELIER AND BEATRIZ DEVIA

Data analysis
A two-way analysis of variance was carried out to determine the significance
(P < 0.05) of the seasonal variation in leaf production. Data were squared-root
transformed to normalize the distribution before carrying out the ANOVA.
Tukey’s Studentized range test was carried out to detect differences between
the levels of trees and months. A repeated ANOVA was carried out to analyze
variation in percentage herbivory between seasons and leafage. Percentage
herbivory was arcsine-transformed. The repeated analysis was used because in
the sphericity test, chi-squared was rejected (χ2 = 31.21, df = 9, P < 0.001). A
two-way ANOVA was carried out to analyze the variation in flavonoid
concentration between seasons and leaf age. No transformation of the original
data was necessary for this analysis. The range test was again used to detect
differences between the levels of the months and seasons. Regressions between
monthly leaf production and weather variables (monthly rainfall, humidity,
sunshine (hours), and mean, maximum and minimum temperatures)
were calculated using step-wise multiple regression analyses in SYSTAT
(1992).

R ES U L T S

Phenology, leaf production, leaf longevity and nutrient retranslocation

Leaf production showed monthly variation (F = 22.6, df = 9, 11; P < 0.001),
with the highest values during September (8.5 ± 1.2 leaves per branch) and the
lowest during February (2.3 ± 0.5 leaves per branch) (Figure 2). Tukey’s test,
showed statistically significant differences (P < 0.05) between leaf production
during February and the rest of the months. No relationship was found between
angle of exposure of branches (degrees) and leaf production (r = 0.04, df = 29,
P > 0.05). The multiple regression analysis showed that the only predictor of
monthly leaf production was mean monthly minimum temperature (F = 8.22,
df = 1, 10; P < 0.05; Figure 3a). The analysis also showed positive, but not
predictive, relations between leaf production and monthly rainfall. On inde-
pendent analysis, a significant second order regression was found between
monthly leaf production and rainfall (Figure 3b).
Flowering and fruiting were both unimodal, with peaks during August
(mid-wet season) and October (end of the wet season), respectively. Only 60 %
of the trees sampled produced both flowers and fruits (Figure 4).
At the stand level, leaf production and fine litterfall were 5.0
(± 1.1) t ha−1 y−1 and 3.9 (± 0.8) t ha−1 y−1, respectively. Percentage herbivory
accounted for 21% of leaf production.
Mean leaf longevity was 8.4 mo and there was only a small difference
between the longevity of leaves expanded during the wet (8.8 mo) and during
the dry season (8.1 mo). Leaves expanded during the dry season, started to fall
and completely disappeared 2 mo before those expanded during the wet season
(Figure 5).

http://journals.cambridge.org Downloaded: 29 Apr 2016 IP address: 129.81.226.78

 The neotropical treeline species Polylepis quadrijuga 777

Figure 2. Seasonal variations in leaf production (number of leaves per branch) in Polylepis quadrijuga in
1993 in the paramo of Chingaza, Colombia. Each value is the mean (± SE) of 10 trees.

Leaf nitrogen concentrations were 3.43, 3.36, 3.45, 3.08 and 3.43 % in leaves
1 to 5 mo old, respectively, and fell to 0.70 % in fine litterfall. Nitrogen retrans-
location was 80 %.

Herbivory
There was seasonal variation in leaf herbivory (F = 3.30, df = 1, 9; P < 0.05)
with higher rates in leaves expanded during the wet (20 %) than during the
dry season (1 %) (Figure 6a). In both cases, maximum herbivory occurred in
leaves 3 mo old (Figure 6b). Herbivores included strip-mining larvae belonging
to the orders Coleoptera and Lepidoptera. Although abundant Membracidae
(Maturnaria sp. nov; R. Restrepo, pers. comm.) were observed on young leaves of
P. quadrijuga, membracids could not have produced the observed damage
because they are leaf sap-suckers (Maxwell-Lefroy 1923).

Phytochemistry
Total flavonoid concentration was higher in leaves expanded during the
wet (0.137 ± 0.012 µmol g−1 dry weight) than during the dry season (0.078
± 0.008 µmol g−1 dry weight) (F = 78.6, df = 1, 4; P < 0.001), but no relationship
was found between flavonoid concentration and leaf age (Figure 6c). There
were significant positive relations (P < 0.01) between monthly rainfall and fla-
vonoid concentration (Figure 7a) and between average monthly minimum tem-
peratures and flavonoid concentration (Figure 7b).

http://journals.cambridge.org Downloaded: 29 Apr 2016 IP address: 129.81.226.78

 778 VIRGINIA VELEZ, JAIME CAVELIER AND BEATRIZ DEVIA

Figure 3. Relationships between (a) mean monthly minimum temperature and leaf production
(Y = 1.18X + 4.41; r = 0.67, df = 11, P < 0.05), and (b) monthly rainfall and leaf production
(Y = 2.00 − 0.00016X + 0.0597X2; r = 0.66, df = 10, P < 0.05) in Polylepis quadrijuga in the paramo of Chingaza,
Colombia.

The two flavonoids, identified by TLC and UV-Vis spectroscopy, were a

flavone and a catechin. While the flavone showed a pale yellow colour in the
chromatogram (Rf = 0.89) and absorbance peaks at 335 and 270 nm in the
spectrum, the catechin showed a grayish-blue colour (Rf = 0.35) and a single
peak at 285 nm.

D I S C US S I O N

Leaf, flower and fruit phenology

P. quadrijuga showed a seasonal variation in leaf production. Although there
was a minimum leaf production during the dry season (i.e. February), monthly
leaf production correlated better with mean minimum monthly temperature,

http://journals.cambridge.org Downloaded: 29 Apr 2016 IP address: 129.81.226.78

 The neotropical treeline species Polylepis quadrijuga 779

Figure 4. Seasonal variation in the percentage of flowering and fruiting trees (n = 10) for Polylepis quadrijuga
in the paramo of Chingaza during 1993.

Figure 5. Percentage survivorship of leaves expanded during the wet (P) (n = 173) and dry (p) (n = 69)
seasons, of Polylepis quadrijuga in the paramo of Chingaza, Colombia.

http://journals.cambridge.org Downloaded: 29 Apr 2016 IP address: 129.81.226.78

 780 VIRGINIA VELEZ, JAIME CAVELIER AND BEATRIZ DEVIA

Figure 6. Relationships between age of leaves (mo) expanded during the wet (P) and dry seasons (p) and
(a) cumulative herbivory, (b) mean monthly herbivory (± SE, n = 10) and (c) the concentration of total
glycosides of flavonoids per leaf dry weight (± SE, n = 3), in Polylepis quadrijuga in the paramo of Chingaza,
Colombia.

suggesting that both temperature and water supply determine the rates of leaf
expansion. Seasonal variation in leaf production have been reported in other
paramo vegetation species. For instance, the giant rosettes of the genus Espele-
tia, show a lower leaf production during the dry season and this was attributed
to low water availability (Smith 1981, Smith & Young 1987) or a combined
effect of low water supply and low temperatures (Cavelier et al. 1992). Irriga-
tion experiments with Espeletia spp. in the Andes of Venezuela, showed that
leaf production can increase with increasing water supply (Orozco 1986) sup-
porting the hypothesis that peaks in leaf production are controlled by water

http://journals.cambridge.org Downloaded: 29 Apr 2016 IP address: 129.81.226.78

 The neotropical treeline species Polylepis quadrijuga 781

Figure 7. Relationship between (a) monthly rainfall and the concentration of total glycosides of flavonoids
(Y = 0.00042X + 0.0582; r = 0.80, df = 9, P < 0.01) and (b) mean monthly minimum temperatures and and
the concentration of total glycosides of flavonoids (Y = 0.074X + 0.03; r = 0.74, df = 9, P < 0.01) in leaves of
Polylepis quadrijuga in the paramo of Chingaza, Colombia.

availability (Alvim & Alvim 1978, Lieberman & Lieberman 1984). The slight
decrease in leaf production when monthly rainfall was higher than 200 mm
(Figure 3b), could be explained in terms of a combined effect of very high soil
water content and low radiation levels due to high cloud cover. Under saturated
soils, nitrogen availability can be reduced (Marrs et al. 1988) limiting the rates
of leaf production, and low radiation levels would result in reduced photosyn-
thetic rates, limiting the available carbohydrates for the formation and expan-
sion of new leaves.
While flowering in P. quadrijuga occurs during the wet season, fruiting and
seed dispersal occur in the transition between the wet and the dry season.
Seasonal patterns of flowering and fruiting have also been measured in Polylepis
besseri in Bolivia (Hensen 1994). It seems unusual that a wind-pollinated spe-
cies, such as P. quadrijuga (Simpson 1979), flowers during the wettest time of
the year, unless this species is self-pollinated. Dry season conditions favour

http://journals.cambridge.org Downloaded: 29 Apr 2016 IP address: 129.81.226.78

 782 VIRGINIA VELEZ, JAIME CAVELIER AND BEATRIZ DEVIA

dispersal of small, wind-dispersed seeds (Van Schaik et al. 1993), since wind
speed increases during this time of year (Sarmiento 1986). It is likely that the
small seeds of P. quadrijuga remain in the seed bank during the dry season
(January-March) and germinate at the beginning of the wet season
(March-April). Such a pattern was shown for seeds of Espeletia timotensis in
Venezuelan paramos (Guariguata & Azocar 1988).

Production
Annual fine litterfall in P. quadrijuga forest, calculated as the difference
between leaf production (5.0 t ha−1 y−1) and herbivory (1.05 t ha−1 y−1), is
3.9 t ha−1 y−1. If allowance is made for the withdrawal of dry weight before leaf
fall, this production value would be somewhat lower. Assuming a withdrawal
of 17 % of dry weight before leaf fall, estimated from five montane tree species
with similar specific leaf areas (57.0 cm2 g−1; Vera & Cavelier 1994) to that of
P. quadrijuga (57.4 cm2 g−1), annual fine litterfall would be 3.2 t ha−1 y−1. This
value is high when compared with paramo vegetation (1.8 t ha−1 y−1; Cavelier et
al. 1992), the nearby upper montane rain forests (3100 m) of Reserva Carpanta
(1.29 t ha−1 y−1, Rodriguez & Rosas 1993) and other upper montane rain forests
(Proctor 1984)
High production of the P. quadrijuga forest, can be the result of high leaf
nitrogen concentration and high rates of nitrogen retranslocation. Indeed, leaf
nitrogen concentration is very high (3.35 %) even when compared to lowland
rain forests (2.52 %) growing on moderately fertile soils (Vitousek & Sanford
1986). High leaf nitrogen concentrations are probably related to high photosyn-
thetic capacity as measured in the Venezuelan Polylepis sericea (9 µmol m−2 s−1;
Goldstein et al. 1994). Leaf nitrogen retranslocation in P. quadrijuga is higher
(80 %), than values previously reported for tropical montane rain forest trees,
including Sphenostemom papuantum (44 %) in New Guinea (Edwards 1977), and
Myrcianthes sp.(48 %) in an upper montane rain forest of the Central Andes of
Colombia (Vera & Cavelier 1994).
Another life-history trait of P. quadrijuga that may be related to high produc-
tivity is leaf longevity. The average leaf life-span of P. quadrijuga is 8.4 mo,
lower than in trees of tropical lowlands (12–14 mo), lower- (14–16 mo) and
upper-montane rain forests (14–18 mo; Grubb 1977). Low leaf longevity is asso-
ciated in P. quadrijuga, as in other species, with high nitrogen concentration
and low leaf specific weight (Mooney & Gulmon 1982). High leaf nitrogen is
very uncommon in high altitude tropical environments where soil nitrogen
availability is low (Grubb 1971, 1977). It is possible that once nitrogen is incorp-
orated into the biomass of P. quadrijuga, it is used and internally recycled very
efficiently, returning a relatively small fraction to the soil via litterfall where
it may be immobilized in the soil due to high soil water content (Marrs et al.
1988). Furthermore, this Polylepis-forest is highly efficient in the use of nitrogen
sensu Vitousek (1984), since it has the lowest nitrogen circulation in fine lit-
terfall (27.3 kg N ha−1 y−1) reported so far for a tropical forest and high values

http://journals.cambridge.org Downloaded: 29 Apr 2016 IP address: 129.81.226.78

 The neotropical treeline species Polylepis quadrijuga 783

of dry mass/N in fine litterfall (143) when compared to other tropical montane
forests (80–180; Vitousek 1984).

Herbivory: seasonality and leaf age

In spite of a rather small sample size per tree (n = 3) and number of trees
(n = 10) used in the herbivory measurements, some significant seasonal and
leaf-age related results were found that warrant discussion.
Herbivory was 1 % for leaves expanded during the dry season and 20 %
during the wet season. The latter is in the range of values (2–40 %) reported
for lowland rain forest trees in Australia (Lowman 1984, 1992) and understorey
shrubs in Panama (Aide 1988, 1992). Higher herbivory during the wet season
may be the result of higher humidity and relatively high air temperatures
required for the development of the larvae (Uvarov 1931). Higher insect
abundance during the wet season have also been reported for lowland tropical
ecosystems in Africa (Denlinger 1980) and Central America (Smythe 1982;
Wolda 1978, 1980, 1982). Higher larvae abundance is also correlated with high
leaf production. For the plants, higher herbivory during the wet season may be
less detrimental than during the dry season, because productivity is high
enough to satiate the herbivores (Aide 1988, 1992; Coley 1982, Feeny 1976)
preventing them from completely defoliating the canopy.
Higher herbivory in 3-mo-old leaves expanded during the wet season, is
probably the result of an increase in larval abundance during this time of year
(August). Furthermore, cohorts of unmarked 1- and 2-mo-old leaves expanding
at the same time, also showed high herbivory, suggesting that ‘preference’ for
3-mo-old leaves is related to insect abundance rather than to leaf age. Higher
herbivory in young leaves is correlated with high N concentration (3.36–3.45 %
in leaves 1–3 mo old), high water content (43–48 %) and lower specific leaf
weight (160–180 g m−2) as reported for other species (Coley 1983, Feeny 1970,
Hatcher 1990, Mattson 1980, Mattson & Scriber 1987, Mooney & Gulmon 1982,
Rausher 1981).

Phytochemistry
The concentration of total flavonoids in P. quadrijuga was higher for leaves
expanded during the wet than during the dry season (Figure 6c), and there
was no relationship with leaf age as it has been shown for other species (Coley
1983, Crawley 1983, Feeny 1976, Hatcher 1990, Rhoades & Cates 1976,
Scriber & Slansky 1981). Furthermore, there is a significant positive relation-
ship between monthly rainfall and flavonoid concentration (Figure 7a). Higher
flavonoid concentration with increasing rainfall, may be the result of increased
production of carbon-based compounds due to lower nitrogen availability
(Barz & Koster 1981, Chew & Rodman 1979, Gershenzon 1984, Mattson 1980,
Mattson & Scriber 1987, Stafford 1990) in saturated soils (Marrs et al. 1988).
The correlation of flavonoid concentration and average monthly minimum tem-
peratures may be the result of an effect of low temperatures on plant metabol-
ism, particularly during the dry season when water availability is low.

http://journals.cambridge.org Downloaded: 29 Apr 2016 IP address: 129.81.226.78

 784 VIRGINIA VELEZ, JAIME CAVELIER AND BEATRIZ DEVIA

The two flavonoid compounds identified in P. quadrijuga were a flavone and

a catechin, compounds know as UV-B protectors (Caldwell et al. 1983,
Rhoades & Cates 1976, Stafford 1990) and potential herbivore deterrents
(Harborne 1988, 1992). The flavone could have a potential positive effect in
the paramo environment since it has been shown that UV-B radiation increases
with increasing altitude in tropical mountains (Caldwell 1971, Caldwell et al.
1980, Robberecht et al. 1980). Indeed, UV-B induces the accumulation of
greater amounts of flavonoid pigments such as flavones (Caldwell et al. 1983,
Hrazdina & Parsons 1982, Murali & Teramura 1986, Teramura 1983). The
catechin is a tannin precursor, a compound able to bind proteins and con-
sequently lower the nutritional value of the leaf tissue (Feeny 1970, Harborne
1992, Rhoades & Cates 1976). Flavonoids have also been isolated from Polylepis
incana (Catalano et al. 1995) and used as keys in the systematics of the genus.
Of the above ecological traits of P. quadrijuga, high production values may
be the key factor in understanding the occurrence of this tree species in an
ecosystem otherwise dominated by grasses and giant rosettes of the genus Espe-
letia. High production, that results from, high leaf nitrogen concentration, very
high foliar nitrogen retranslocation and short leaf longevity, should allow this
woody species to compete successfully with other growth forms (i.e. grasses),
where most of their biomass is photosynthetically active. Traits like high foliar
concentration of flavonoids and seasonal phenology and herbivory, could also
play an important role in the adaptation of this species to the harsh paramo
environment, with high levels of UV-B radiation and marked seasonal variation
in rainfall, temperatures and insect abundance.

A C K N O W L E D G E M E N TS

We thank the personnel at Parque Nacional Natural Chingaza for their support
while carrying out the field work at ‘Sietecuerales’, particularly A. Repizzo, G.
Didier and Mr. Beltran. We also thank Orlando Martinez for advice on statist-
ics and Ruben Restrepo (ICN) for insect identification.

L I T E R A T U RE C I T E D
AIDE, T. M. 1988. Herbivory as a selective agent on the timing of leaf production in a tropical
understorey community. Nature 336:574–575.
AIDE, T. M. 1992. Dry season leaf production: an escape from herbivory. Biotropica 24:532–537.
AIDE, T. M. 1993. Patterns of leaf development and herbivory in a tropical understory community.
Ecology 74:455–466.
ALVIM, P. OF T. & ALVIM, R. 1978. Relation of climate to growth periodicity in tropical trees. Pp. 445–
464 in Tomlinson, P. B. & Zimmerman, M. H. (eds). Tropical trees as living systems. Cambridge
University Press, Cambridge.
ARNAL, H. 1983. Estudio ecológico del bosque alti-andino de Polylepis sericea Webb en la Cordillera de Mérida.
Universidad Central de Venezuela, Caracas, Venezuela. 270 pp.
BARZ, W. & KOSTER, J. 1981. Turnover and degradation of secondary (natural) products. Pp. 35–73 in
Conn, E. E. (ed.). The biochemistry of plants. Secondary plant products. Volume 7. Academic Press, New
York.
BORCHERT, R. 1983. Phenology and control flowering in tropical trees. Biotropica 15:81–89.

http://journals.cambridge.org Downloaded: 29 Apr 2016 IP address: 129.81.226.78

 The neotropical treeline species Polylepis quadrijuga 785

CALDWELL, M. M. 1971. Solar U.V. irradiation and the growth and development of higher plants.
Pp. 131–268 in Giese, A. C. (ed.). Photophysiology. Volume VI. Academic Press, New York.
CALDWELL, M. M., ROBBERECHT, R. & BILLINGS, W. D. 1980. A steep latitudinal gradient of solar
ultraviolet-B radiation in the arctic-alpine zone. Ecology 61:600–611.
CALDWELL, M. M., ROBBERECHT, R. & FLINT, S. D. 1983. Internal filters: prospects for
UV-acclimation in higher plants. Physiologia Plantarum 58:445–450.
CATALANO, S., CIONI, P. L., MARTINOZZI, M., DE FEO, V. & MORELLI, I. 1995. Chemical
investigation of Polylepis incana (Rosaceae). Biochemical Systematics and Ecology 23:105–107.
CAVELIER, J. 1996. Environmental factors and ecophysiological process along altitudinal gradients in
wet tropical mountains. Pp. 399–439 in Mulkey, S.S., Chazdon, R. L. & Smith, A.P. (eds). Tropical
forest plant ecophysiology. Chapman & Hall, New York.
CAVELIER, J., MACHADO, J. L., VALENCIA, D., MONTOYA, J., LAIGNELET, A., HURTADO, A.,
VARELA, A. & MEJIA, C. 1992. Leaf demography and growth rates of Espeletia barclayana Cuatrec.
(Compositae), a caulescent rosette in a Colombian paramo. Biotropica 24:52–63.
COLEY, P. D. 1980. Effects of leaf age and plant life history patterns on herbivory. Nature 284:545–546.
COLEY, P. D. 1982. Rates of herbivory in different tropical trees. Pp. 123–132 in Leigh, Jr. E. G., Rand,
A. S. & Windsor, D. M. (eds). The ecology of a tropical forest: seasonal rhythms and long-term changes.
Smithsonian Institution Press, Washington.
COLEY, P. D. 1983. Herbivory and defensive characteristics of tree species in a lowland tropical forest.
Ecological Monographs 53:209–233.
CRAWLEY, M. J. 1983. Herbivory, the dynamics of animal-plant interactions. Studies in ecology. Volume 10.
University of California Press, Berkeley. 437 pp.
CHEW, F. S. & RODMAN, J. E. 1979. Plant resources for chemical defenses. Pp. 271–281 in Rosenthal,
G. A. & Janzen, D. H. (eds). Herbivores: their interaction with secondary plant metabolites. Academic Press,
New York.
DEL ARCO, J. M., ESCUDERO, A. & VEGA, M. 1991. Effects of site characteristics on nitrogen
retranslocation from senescing leaves. Ecology 72:701–708.
DENLINGER, D. L. 1980. Seasonal and annual variation of insect abundance in the Nairobi National
Park, Kenya. Biotropica 12:100–106.
DOMINGUEZ, X. A. 1973. Métodos de investigación fitoquı́mica. Editorial Limusa, México. 281 pp.
DUGAND G. A. 1978. El paisaje vegetal y sus mudanzas en el tiempo. Cespedesia 7:9–23.
EDWARDS, P. J. 1977. Aspects of mineral cycling in a New Guinean montane forest. II. The production
and disappearance of litter. Journal of Ecology 65: 971–992
ELLENBERG, H. 1958. Wald oder Steppe? Die natürliche Pflanzendecke der Anden Perus. Umschau
1958: 645–681.
FEENY, P. 1970. Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by
winter moth caterpillars. Ecology 51:565–581.
FEENY, P. 1976. Plant apparency and chemical defense. Pp.1–40 in Wallace, J. & Mansell, R. L. (eds).
Biochemical interaction between plants and insects. Recent Advances in Phytochemistry. Volume 10. Plenum
Press, New York, NY.
FLÜCK, H. 1963. Intrinsic and extrinsic factors affecting the production of secondary plant products.
Pp. 167–185 in Swain, T. (ed.). Chemical plant taxonomy. Academic Press, London.
GEISSMAN, T. A. (ed.) 1962. The chemistry of flavonoid compounds. Pergamon Press, Oxford. 666 pp.
GERSHENZON, J. 1984. Changes in the levels of plant secondary metabolites under water and nutrient
stress. Pp. 273–321 in Timmermann, B. N., Steelink, C. & Loewns, S. A. (eds). Phytochemical adaptations
to stress. Recent advances in phytochemistry. Volume 18. Plenum Press, New York.
GOLDSTEIN, G., MEINZER, F. C. & RADA, F. 1994. Environmental biology of a tropical treeline
species, Polylepis sericea. Pp. 129–149 in Rundel, P. W., Meinzer, F. C. & Smith, A. P. (eds). Tropical
alpine environments: plant form and function. Cambridge University Press, Cambridge.
GRUBB, P. J. 1971. Interpretation of the ‘Massenerhebung’ effect on tropical mountains. Nature
229:44–45.
GRUBB, P. J. 1977. Control of forest growth and distribution on wet tropical mountains: with special
reference to mineral nutrition. Annual Review of Ecology and Systematics 8:83–107.
GUARIGUATA, M. R. & AZOCAR, A. 1988. Seed bank dynamics and germination ecology in Espeletia
timotensis (Compositae), an Andean giant rosette. Biotropica 20:54–59.
HARBORNE, J. B. 1973. Phytochemical methods. Chapman & Hall, London. 278 pp.
HARBORNE, J. B. 1988. Introduction to ecological biochemistry. (3rd edition.) Academic Press, New York.
HARBORNE, J. B. 1992. Flavonoid pigments. Pp. 389–429 in Rosenthal, G. A. & Berenbaum, M. R.
(eds). Herbivores, their interaction with secondary plant metabolites. Vol I. The chemical participants. Academic
Press, New York.
HATCHER, P. E. 1990. Seasonal and age-related variation in the needle quality of five conifer species.
Oecologia 85:200–212.

http://journals.cambridge.org Downloaded: 29 Apr 2016 IP address: 129.81.226.78

 786 VIRGINIA VELEZ, JAIME CAVELIER AND BEATRIZ DEVIA

HENSEN, I. 1994. Estudios ecológicos y fenológicos sobre Polylepis besseri Hieron en la Cordillera Oriental
Boliviana. Ecologı́a en Bolivia 23:21–32.
HRAZDINA, G. & PARSONS, G. F. 1982. Induction of flavonoid synthesizing enzymes by light in
etiolated Pea (Pisum sativum cv. Midfreezer) seedlings. Plant Physiology 70:506–510.
JANZEN, D. H. 1967. Synchronization of sexual reproduction of trees within the dry season in Central
America. Evolution 21:620–637.
KESSLER, M. 1995. Present and potential distribution of Polylepis (Rosaceae) forests in Bolivia. Pp. 281–
294 in Churchill, S.P., Balslev, H., Forero, E. & Luteyn, J. (eds). Biodiversity and conservation of neotropical
montane forests. New York Botanical Garden, New York.
KOOTSTRA, A. 1994. Protection from UV-B-induced DNA damage by flavonoids. Plant Molecular Biology
26: 771–774.
LAUER, W. 1981. Ecoclimatological conditions of the paramo belt in the tropical high mountains.
Mountain Research and Development 1:209–221.
LIEBERMAN, D. & LIEBERMAN. M. 1984. The causes and consequences of synchronous flushing in a
dry tropical forest. Biotropica 16:193–201.
LOUBRY, D. 1994. La phénologie des arbres caducifoliés en foret guyanaise (5° de latitude nord):
illustration d’un déterminisme a composantes endogene et exogene. Canadian Journal of Botany
72:1843–1857.
LOUDA, S. M. 1984. Herbivore effect on stature, fruiting and leaf dynamics of a native crucifer. Ecology
65:1379–1386.
LOWMAN, M. D. 1984. An assessment of techniques for measuring herbivory: is rainforest defoliation
more intense than we thought? Biotropica 16:264–268.
LOWMAN, M. D. 1992. Leaf growth dynamics and herbivory in five species of Australian rain-forest
canopy trees. Journal of Ecology 80:433–447.
MABRY, T. J. 1969. The ultraviolet and nuclear magnetic resonance analysis of Flavonoids. Pp. 1–31 in
Harborne, J. B. & Swain, T. (eds). Perspectives in phytochemistry. Academic Press, London.
MARQUIS, R. J. 1984. Leaf herbivores decrease fitness of a tropical plant. Science 226:537–539.
MARRS, R. H., PROCTOR, J., HEANEY, A. & MOUNTFORD, M. D. 1988. Changes in soil
nitrogen-mineralization and nitrification along an altitudinal transect in tropical rain forest in Costa
Rica. Journal of Ecology 76:466–482.
MATTSON JR., W. J. 1980. Herbivory in relation to plant nitrogen content. Annual Review of Ecology and
Systematics 11:119–161.
MATTSON, W. J. & SCRIBER, J. M. 1987. Nutritional ecology of insects folivores of woody plants.
Nitrogen, water, fiber, and mineral consideration. Pp. 105–146 in Slansky, Jr. F. & Rodrı́guez, J. G.
(eds). Nutritional ecology of insects, mites, spiders and related invertebrates. J. Wiley & Sons, New York.
MAXWELL-LEFROY, H. 1923. Manual of entomology. E. Arnold & Co., London. 541 pp.
MOONEY, H. A. & GULMON, S. L. 1982. Constraints on leaf structure and function in reference to
herbivory. Bioscience 32:198–206.
MURALI, N. S. & TERAMURA, A. H. 1986. Intraspecific differences in Cucumis sativis sensitivity to
ultraviolet-B radiation. Physiologia Plantarum 58:673–677.
OROZCO, A. 1986. Economı́a hı́drica en rosetas juveniles de Espeletia en el Páramo Desértico. Tesis de Maestrı́a.
Universidad de los Andes, Mérida, Venezuela. 95 pp.
PROCTOR, J. 1984. Tropical forest litterfall. II: The data set. Pp. 83–113 in Sutton, S. L. & Chadwick,
A. C. (eds). Tropical rain forest: the Leeds symposium. Leeds Philosophical and Literary Society, Leeds,
UK.
RADA, F., GOLDSTEIN, G., AZOCAR, A. & MEINZER, F. C. 1985. Daily and seasonal osmotic changes
in a tropical treeline species. Journal of Experimental Botany 36:989–1000.
RAUSHER, M. D. 1981. Host plant selection by Battus philenor butterflies: the roles of predation,
nutrition, and plant chemistry. Ecological Monographs 51:1–20.
REICH, P. B. & BORCHERT, R. 1982. Phenology and ecophysiology of the tropical tree Tabebuia
neochrysantha (Bignoniaceae). Ecology 63:294–299.
REICH, P. B. & BORCHERT, R. 1984. Water stress and tree phenology in a tropical dry forest in the
lowlands of Costa Rica. Journal of Ecology 72:61–74.
REPIZZO, A. 1993. Presentación de la Reserva Biológica de Carpanta. Pp. 17–29 in Andrade, G. I. (ed.).
Carpanta selva nublada y páramo. Fundación Natura, Colombia.
RHOADES, D. F. & CATES, R. G. 1976. Toward a general theory of plant antiherbivore chemistry.
Pp. 168–213 in Wallace, J. W. & Mansell, R. L. (eds). Biochemical interactions between plants and insects.
Recent Advances in Phytochemistry. Volume 10. Plenum Press, New York.
ROBBERECHT, R., CALDWELL, M. M. & BILLINGS, W. D. 1980. Leaf ultraviolet optical properties
along a latitudinal gradient in the arctic-alpine life zone. Ecology 61:612–619.
RODRÍGUEZ, E. & ROSAS, M. L. 1993. Caida de hojarasca en el bosque altoandino de Carpanta.
Pp. 81–95 in Andrade, G. I. (ed.). Carpanta selva nublada y páramo. Fundación Natura, Colombia.

http://journals.cambridge.org Downloaded: 29 Apr 2016 IP address: 129.81.226.78

 The neotropical treeline species Polylepis quadrijuga 787

SANABRIA, A. 1983. Análisis fitoquı́mico preliminar. Universidad Nacional de Colombia, Facultad de

Ciencias, Departamento de Farmacia, Bogotá. 96 pp.
SARMIENTO, G. 1986. Ecological features of climate in high tropical mountains. Pp. 11–45 in
Willeumier, F. & Monasterio, M. (eds). High altitude tropical biogeography. Oxford University Press, N.Y.
SCRIBER, J. M. & SLANSKY, Jr. F. 1981. The nutritional ecology of immature insects. Annual Review
of Ecology and Systematics 26:183–211.
SIMPSON, B. B. 1979. A revision of the genus Polylepis (Rosaceae: Sanguisorbeae). Smithsonian
Contributions to Botany 43:1–62.
SIMPSON, B. B. 1986. Speciation and specialization of Polylepis in the Andes. Pp. 304–316 in Vuilleumier,
F. & Monasterio, M. (eds). High altitude tropical biogeography. Oxford University Press, N.Y.
SMIT, A. 1978. Pollen morphology of Polylepis boyacensis Cuatrecasas, Acaena cylindristachya Ruiz et Pavon
and Acaena Elongata L. (Rosaceae) and its application to fossil material. Review of Palaeobotany and
Palynology 25:393–398.
SMITH, A. P. 1978. Establishment of seedlings of Polylepis sericea in the paramo (Alpine) zone of the
Venezuelan Andes. Bartonia 45:11–14.
SMITH, A. P. 1981. Growth and population dynamics of Espeletia (Compositae) of the Venezuelan Andes.
Smithsonian Contributions to Botany 48:1–45.
SMITH, A. P. & YOUNG, T. P. 1987. Tropical alpine plant ecology. Annual Review of Ecology and
Systematics 18:137–158.
SMYTHE, N. 1982. The seasonal abundance of night-flying insects in a neotropical forest. Pp. 309–318
in Leigh, Jr., E. G., Rand, A. S. & Windsor, D. M. (eds). The ecology of a tropical forest: seasonal rhythms
and long-term changes. Smithsonian Institution Press, Washington.
STAFFORD, H. A. 1990. Flavonoid metabolism. CRC Press, Florida. 298 pp.
SYSTAT 1992. SYSTAT: Statistics, Version 5.2 Edition. SYSTAT Inc. Evansto, IL. 724 pp.
TANNER, E. V. J. 1977. Four montane rainforest of Jamaica: a quantitative characterization of the
floristics, the soils, and the foliar mineral levels, and a discussion of the interrelations. Journal of
Ecology 65:883–918.
TERAMURA, A. H. 1983. Effects of ultraviolet-B radiation on the growth and yield of crop plants.
Physiologia Plantarum 58:415–427.
UVAROV, B. P. 1931. Insect and climate. Transactions of the Entomological Society of London. Volume
79. 247 pp.
VAN DER HAMMEN, T. 1974. The Pleistocene changes of vegetation and climate in tropical south
America. Journal of Biogeography 1:3–26.
VAN SCHAIK, C. P., TERBORGH, J. W. & WRIGHT, S. J. 1993. The phenology of tropical forests:
adaptive significance and consequences for primary consumers. Annual Review of Ecology and Systematics
24:353–377.
VERA, M. F. & CAVELIER, J. 1994. Tasas de retraslocación de nutrientes foliares en especies arbóreas
del Parque Regional Natural Ucumarı́. Pp. 203–224 in Rangel, J. O. (ed.). Ucumari. Un caso tı́pico de
la diversidad biótica andina. Corporación Autónoma Regional de Risaralda y Universidad Nacional de
Colombia, Bogotá, Colombia.
VITOUSEK, P. M. 1984. Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology
65:285–298.
VITOUSEK, P. M. & SANFORD, Jr. R. L. 1986. Nutrient cycling in moist tropical forest. Annual Review
of Ecology and Systematics 17:137–167.
WALTER, H. & MEDINA, E. 1969. La temperatura del suelo como factor determinante para la
caracterización de los pisos subalpino y alpino en los Andes de Venezuela. Boletı́n de la Sociedad
Venezolana de Ciencias Naturales 28:201–210.
WOLDA, H. 1978. Seasonal fluctuations in rainfall, food and abundance of tropical insects. Journal of
Animal Ecology 47:369–381.
WOLDA, H. 1980. Seasonality of tropical insects. I. Leafhoppers (Homoptera) in Las Cumbres, Panamá.
Journal of Animal Ecology 49:277–290.
WOLDA, H. 1982. Seasonality of homoptera on Barro Colorado Island. Pp. 319–330 in Leigh, Jr. E. G.,
Rand, A. S. & Windsor, D. M. (eds). The ecology of a tropical forest: seasonal rhythms and long-term changes.
Smithsonian Institution Press, Washington.

http://journals.cambridge.org Downloaded: 29 Apr 2016 IP address: 129.81.226.78