Plant Ecology & Diversity

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Plant functional diversity in tropical Andean

páramos

Fermin Rada, Aura Azócar & Carlos García-Núñez

To cite this article: Fermin Rada, Aura Azócar & Carlos García-Núñez (2019): Plant
functional diversity in tropical Andean páramos, Plant Ecology & Diversity, DOI:
10.1080/17550874.2019.1674396

To link to this article: https://doi.org/10.1080/17550874.2019.1674396

Published online: 17 Oct 2019.

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PLANT ECOLOGY & DIVERSITY
https://doi.org/10.1080/17550874.2019.1674396

REVIEW

Plant functional diversity in tropical Andean páramos

Fermin Rada, Aura Azócar and Carlos García-Núñez
Instituto de Ciencias Ambientales y Ecológicas, Facultad de Ciencias, Universidad de Los Andes, Mérida, Venezuela

ABSTRACT ARTICLE HISTORY

Background: Tropical high mountains present extreme daily temperature variations, frequent Received 21 December 2017
high air evaporative demands and seasonal differences in soil water availability. Plants have Accepted 26 September 2019
adapted to these conditions through different avoidance-tolerance mechanisms. This review KEYWORDS
focuses on plant-growth forms and their adaptive strategies. Climate change; freezing
Aims: This integrated review of páramo plant traits aims at contributing to understanding the resistance; gas exchange;
functioning of plant-growth forms and their significance on ecosystem properties under giant rosettes; páramo; plant
environmental climate and land-use changes. growth-forms; plant water
Methods: Plant responses are presented along avoidance-tolerance gradients considering relations; tropical Andes
three main aspects: freezing resistance, water relations and gas exchange characteristics.
Results from 45 herbaceous and 42 woody species along elevational gradients in the
Venezuelan high Andes were analysed.
Results: Leaf supercooling is the common avoidance response of woody plants to night-time
freezing temperatures, while herbaceous plants tolerate frost. Trees and caulescent rosettes
maintain more positive leaf water potentials under water deficit conditions compared to more
tolerant herbaceous species. All plant growth-forms showed strong stomatal control under dry-
season conditions.
Conclusions: Páramo plant growth-forms may be separated according to an avoidance-
tolerance gradient in response to water deficit and low temperature resistance. Woody growth-
forms tend to avoid both freezing and water stress, while herbaceous forms tolerate frost and
resist an unfavourable water status. Grasses and cushion plants are at the tolerant extreme of
the gradient and coincide in that both reach the highest elevations in the páramo. Andean
giant rosettes are freezing avoidant, particularly susceptible to water deficit and the most
vulnerable, of all growth-forms, to changing environmental conditions.

Introduction The páramos, a collective term for the alpine eco-

systems of the humid tropical Andes, occur above the
Tropical high mountains offer environmental condi-
treeline, composed of predominantly low-stature
tions that result in unique ecosystems where plants
vegetation, dominated by different plant growth-
present numerous strategies of adaptation. Although
forms (Figure 1) such as giant rosettes, sclerophyllous
these environments are defined as cold, both low and
shrubs, grasses and forbs; at the highest elevations
high temperatures play a key role in shaping plant
acaulescent rosettes and cushion plants usually
responses. Freezing temperatures may occur any
increase their relative abundance. Páramos occur
night of the year with a higher frequency at higher
between 11° N and 8° S along Ecuador, Colombia
elevations and towards the dry season, while high
and Venezuela, with smaller regions to the north of
incoming radiation during clear sky conditions lead
Peru and into Central America in Panama and Costa
to high temperatures on bare soil and plant surfaces.
Rica (Monasterio 1980; Luteyn 1992). The páramos
Hedberg (1964) has defined high tropical mountains as
hold the highest floristic diversity and the largest
environments where ‘summer’ occurs during
number of endemic species of alpine ecosystems
every day and ‘winter’ at every night. In terms of
worldwide (Luteyn 1999; Sklenář et al. 2014). In
water conditions, all tropical high mountain regions,
Venezuela, páramos are found between the natural
in varying degrees, show some seasonality in precipita-
boundaries of continuous forest at around 3000 m to
tion. In addition, at higher elevations, water may be
maximum elevations near 4900 m a.s.l.
frozen during early morning hours, limiting its absorp-
Ample ecological research has been carried out for
tion by roots. Added to these water conditions, low
decades in the Venezuelan páramos (Llambí and
relative humidity and high soil surface temperature on
Rada 2019). These investigations have included
clear days generate extremely high evaporative
plant adaptive responses to the particular conditions
demands (Ramírez et al. 2015).

CONTACT Fermin Rada frada@ula.ve

© 2019 Botanical Society of Scotland and Taylor & Francis
2 F. RADA ET AL.

Figure 1. Representative species of different plant growth-forms of the Venezuelan páramo from the Páramo de Piedras Blancas at
4200 m. A. Giant rosette-shrub association with Coespeletia spicata and Hypericum laricifolium, respectively. B. The forb Senecio
formosus. C. Cushion plants Azorella julliani and Aciachne pulvinata. D. Acaulescent rosette Acaena cylindristachya. Photographic
credits: A, C, D by F Rada; B by M Araujo.

the páramo presents for organisms and has involved Temperature and water availability along
the study of cold temperature and/or freezing resis- elevational gradients
tance, water relations and gas exchange in a vast
One of the peculiarities of tropical high mountain
number of plant species of different plant-growth
climates is their relatively constant seasonal mean air
forms (Azócar and Rada 2006; Rada 2016).
temperature while daily variations are extreme.
However, an integrated approach to the study of
Differences between the warmest and coldest months
these plant traits has not been made so far.
are below 2 K at the lower limit of the páramos
Therefore, in this review we present an overview of
(3000–3600 m) and reach 2.7 K at higher elevations
the functional diversity of páramo plants from
(4200 m) (Azócar and Rada 2006). On a daily basis,
a plant-growth form perspective. This analysis aids
differences between minimum and maximum air tem-
in our efforts to understand how the functional diver-
peratures may vary from 10 K during the wet to more
sity of páramo plants may influence on ecosystem
than 20 K in the dry season, being larger at higher
properties under environmental change, principally
elevations (Figure 2). However, when absolute mini-
related to climate and/or land-use. First, we briefly
mum and maximum temperatures are compared these
describe two of the most important environmental
differences may exceed 30 K (Table 1). Mean air tem-
drivers, temperature and water availability, along
perature along the gradient from Los Plantíos (2600 m)
elevational gradients in the páramo. Second, we
to Piedras Blancas (4300 m) within the largest páramo
review the available studies on cold temperature
complex in Venezuela (Cordillera de Mérida, period
and freezing resistance, followed by leaf water poten-
2015–2016) decreases at a rate of ca. 5 K km−1.
tial studies and stomatal responses and gas exchange
Minimum temperatures of ca. −10°C have been
characteristics of páramo plants. Finally, we briefly
recorded at the higher elevations (Table 1).
examine the implications climate change may have
Additionally, the occurrence of freezing temperatures
on the functional diversity of páramo plant growth
at higher elevations coincides with the ecological limit
forms and eventually on ecosystem properties.
for the distribution of trees. It is at this boundary, ca.
 PLANT ECOLOGY & DIVERSITY 3

Figure 2. Mean maximum (■) and minimum (▲) air temperatures along an elevational gradient (Santo Domingo 2600 m, Los
Plantios 3100 m, Mucubají 3550 m, Trasandina 3900 m, Piedras Blancas 4300 m). Data obtained from April-December 2015 for wet
(left) and January-March for dry (right) seasons. Corresponding regressions for the wet, Tmax = −0.0034x+26.731 (r2 = 0.73) and
Tmin = −0,0061x+25,349 (r2 = 0.97), and dry, Tmax = −0.0024x+26.983 (r2 = 0.88) and Tmin = −0,0061x+18.797 (r2 = 0.90), seasons.
Bars correspond to one standard error of the mean.

3000 m in the Venezuelan Andes, where the typical
formations of the páramo (grasses, caulescent rosette-
sclerophyllous shrub associations) replace montane
forests (Sarmiento 1986). Frequency and duration of
nights with below zero temperatures increases with
elevation to 80% of the days at elevations above
4000 m (Table 1). Marked seasonal differences in the
occurrence of below zero night-time temperatures are
observed at the elevation limit of ca. 3100 m. At this
elevation, freezing air temperatures do not occur in the
wet season, while they begin to occur during the dry
season. At higher elevations (3500 m), freezing is
observed during both seasons, and occurs every night
of the year during the dry season (Table 1, Sarmiento
1986).
Absolute maximum air temperatures for the entire
gradient from Los Plantíos (2600 m) to Piedras Blancas
(4300 m) range between 20 and 25°C (Table 1). In
contrast to maximum air temperatures, which do not
seem to have a stressful effect on plant life per se, the
high incoming solar radiation during the day, espe-
cially on clear days, causes high temperatures at the
surface of plants and soils. A steep thermal gradient
between the ground and the air is generated during
daytime hours. At 4200 m, soil temperatures may be
above 50°C while air temperatures (1 m above ground)
are close to 20°C (Ramírez et al. 2015). These thermal
differences lead to differences in plant physiological
functioning when growth-forms that grow close to the
ground (e.g. acaulescent rosettes, cushion plants) are
compared with taller erect growth forms (e.g. shrubs,
giant rosettes). Tropical alpine plants require adapta-
tion to night-time freezing temperatures and high day-
time soil and plant surface temperatures throughout
the year.
In the Venezuelan Andes, there is a marked dry
season between December and March, and in some
cases a less intense dry period between June and
July. The driest páramos in the country have an
average annual rainfall of 650 mm, while the most
humid reach 1800 mm (Sarmiento 1986). Unlike
temperature, which shows a clear decreasing trend
with increasing elevation across the globe, precipi-
tation patterns vary according to different factors
(e.g. latitude, macroslope orientation). In the case of
the gradient from Los Plantios to Piedras Blancas
(Table 1), there is a clear decrease in precipitation
with increasing elevation (this is common in many
other areas along the northern tropical Andes)
(Sarmiento 1986; Leuschner 2000). Additionally,
low relative air humidity occurring mainly during
the dry season, determine high water evaporative

Table 1. Mean air (Tmean), absolute minimum (Tminabs) and absolute maximum (Tmaxabs) temperatures (ºC) measured at 50 cm
above soil level, along an elevational gradient in the Venezuelan páramo for the wet (April-December 2015) and dry (January-
March 2016) seasons. Number of days per year with temperatures below 0°C (D < 0ºC), % days below 0°C, mean night frost
duration (NF) during wet (WS) and dry (DS) seasons and precipitation (P, mm).
Elevation % NF
(m a.s.l.) Tmean Tminabs Tmaxabs D < 0ºC WS/DS WS/DS P
Santo Domingo 2600 11.8 1.6 25.4 0 0/0 0/0 1360
Los Plantios 3100 9.7 −5.5 24.6 65 0/60 0/2h25’ 1005
Mucubají 3550 6.7 −7.7 23.0 130 7/100 1h25'/4h35’ 970
Trasandina 3900 5.5 −9.5 22.4 185 30/100 2h15'/8h15’
Piedras Blancas 4300 3.9 −9.2 21.2 270 60/100 2h55'/8h45’ 760
4 F. RADA ET AL.

Figure 3. Main abiotic environmental factors which determine daily and seasonal plant responses in the Andean tropical high
mountains. Upper and lower portions of the figure correspond to wet and dry seasons, respectively. Left- and right-hand sides
correspond to temperature and water availability, respectively. Seasonal differences in cloud formation determine contrasting
incoming/outgoing radiation levels which have a direct effect on daytime/night-time temperatures. Seasonal differences in water
availability and daily differences in air evaporative demand influence ambient/plant water status. Plants are constantly subjected
to night-time low and daytime high temperatures; and to low water availability and high air evaporative demand during the dry
season which result in continuous temperature and water stresses (→). During the wet season, night-time freezing temperature
stress is important only at higher elevations, while in the day both high temperature and water stresses are important under rare
days with clear skies (-->).

demands which affect both soil and leaf surfaces.
These two factors, a marked dry season and high air
evaporative demands, may induce water deficit in
plants. The responses of different plant growth
forms to these two major factors (cold tempera-
tures; and water conditions, through limitations in
the soil due to precipitation seasonality or to high
air evaporative demands, Figure 3) that constrain
plant growth are discussed in the following sections.
Plant responses to cold temperatures and
freezing
Freezing temperatures have been described as
a determinant factor that influences fitness and
distribution of plants along elevation gradients (Sakai
and Larcher 1987; Woodward 1990). The formation of
ice crystals inside the cells lead to injury through the
rupture of the cell membranes. Plants may survive
freezing temperatures by (1) avoiding tissue freezing
through having insulating structures or by a process
called supercooling, whereby ice nucleation is pre-
vented, or by (2) tolerating frost by forming ice crystals
in the intercellular spaces (Levitt 1980; Sakai and
Larcher 1987). In the first case, since plants are poiki-
lothermic organisms, insulating structures are only
important in a limited number of plant species.
Supercooling refers to the ability of plant tissues to
maintain water in a liquid state at temperatures
below the freezing point. Secondly, freezing-tolerant

plants resist the formation of ice crystals in their inter-
cellular spaces. The formation of ice nuclei in the
intercellular spaces immediately creates a gradient in
which intracellular water is displaced outwards where
it freezes and thereby prevents the rupture of mem-
branes and organelles by ice crystals inside the cell.
This loss of water into the intercellular spaces causes
the cell to undergo a significant dehydration.
Therefore, a freezing tolerant plant must necessarily
be tolerant to water deficits (Sakai and Larcher 1987;
Larcher 2003; Azócar and Rada 2006).
Early studies on plant freezing resistance mechan-
isms in the páramo were carried out on giant rosettes
of the genera Coespeletia and Espeletia, species with
pubescent leaves on a single stem with marcescent
leaves (Figure 1). These giant rosettes provide
a typical example of the role of insulating structures
in the resistance to freezing temperatures. Hedberg
(1964) first referred to nyctinastic leaf movements in
afroalpine giant rosettes, while Smith (1974) described
these movements for Espeletia schultzii in the
Venezuelan páramos. At night, adult rosette leaves
bend inward, thus protecting the apical bud and slow-
ing down heat loss to the surrounding air. Rada et al.
(1985a) have reported apical bud temperatures above
0°C for Coespeletia timotensis and C. spicata with
surrounding air temperatures of −4 °C. Likewise, the
marcescent leaves around the stem produce the same
effect on the stem pith protecting it from low night-
time temperatures (Smith 1979; Goldstein and
Meinzer 1983; Rada et al. 1985a). Larcher (1975) and
Larcher and Wagner (1976) described supercooling as
an avoidance mechanism in tropical high mountain
plants for the first time in Espeletia semiglobulata
leaves, reporting an ice nucleation temperature of
−12°C. Rada et al. (1985a) have recorded nucleation
temperatures between −14 and −16°C for leaves of
Coespeletia timotensis and C. spicata; Goldstein et al.
(1985), studying 11 different species of giant rosettes
along an elevational gradient, have found that all spe-
cies avoided freezing of leaves by different degrees of
supercooling. These authors and Rada et al. (1987)
have reported a direct relationship between supercool-
ing and temperature with increasing elevation, with
a greater capacity to supercool (lower nucleation tem-
peratures) at higher elevations. A relationship between
leaf supercooling and leaf water status has also been
described (Goldstein et al. 1985; Rada et al. 1987).
Supercooling capacity increases as leaf water potentials
decrease, a condition that accentuates during the dry
season, when minimum night-time temperatures are
recorded in the páramo. In summary, all giant rosettes
of the Venezuelan Andes studied to date rely solely on
PLANT ECOLOGY & DIVERSITY 5
avoidance mechanisms, through protection by insulat-
ing structures (stem pith and apical bud) and super-
cooling in leaf cells. In all cases, ice nucleation
corresponded to injury temperatures meaning that
ice formation produced damage. Mean leaf supercool-
ing capacity for giant rosettes studied along a gradient
between 3100 m and 4200 m is ca. −9°C, with a low
supercooling capacity at lower elevations (−6°C at
3100 m) and higher at 4200 m (−14°C). Minimum
recorded air temperatures at this latter elevation in the
Páramo de Piedras Blancas, where the species of
Coespeletia and Espeletia schultzii cohabit, seldom
drop below −5°C (Rada et al. 1985a). Unlike these
giant rosettes of the Andes, afroalpine rosettes tolerate
freezing of their leaves (Beck et al. 1982). Although
these studies in Africa were carried out at a similar
elevation as those of the páramos, minimum recorded
air temperatures frequently fell below −10°C. Under
these more unfavourable temperature conditions, the
idea that in less extreme environments avoidance
mechanisms prevail, while in more extreme condi-
tions plant survival is attained mainly through freezing
tolerance is supported (Sakai and Larcher 1987;
Azócar et al. 1988; Squeo et al. 1991; Rada 2016).
Considering other plant growth-forms, some
respond to night-time freezing conditions through
avoidance by supercooling while others are freezing
tolerant (Figure 4). The tree Polylepis sericea occurs
well above the continuous forest line (ca. 3100 m) in
the Venezuelan Andes (Llambí 2015), up to 4200 m
elevation and closely associated to rock outcrops
which act as thermal refuges (see Goldstein et al.
1994 for a further description of the biology of this
species). This species has a moderate supercooling
capacity to ca. −9°C (Rada et al. 1985b). In a further
study, Dulhoste (2010) has shown freezing resis-
tance of 20 tree species growing in an elevational
gradient from the cloud forest to the páramo at
3500 m, through supercooling. Similar supercooling
capacities have been reported by Rehm and Feeley
(2015a) for the Peruvian tropical Andes. Shrubs
generally avoid freezing (Squeo et al. 1991), but
two species, Valeriana parviflora and Monticalia
sclerosa, have been found to be tolerant to freezing
(Azócar 2006). On the other hand, forbs, acaules-
cent rosettes, cushion plants (Azócar et al. 1988;
Squeo et al. 1991) and herbaceous grasses are freez-
ing tolerant. Márquez et al. (2006) have reported
that all studied grasses along a 2500–4200 m eleva-
tional gradient were freezing tolerant with injury
temperatures down to −18°C. On the contrary,
woody grasses (bamboos) in the páramos have
been shown to be frost avoidant (Ely et al. 2014,
6 F. RADA ET AL.
Figure 4. Temperature (IT, ■) that causes 50% leaf tissue injury
and ice nucleation temperature (INT, □) for all studied plant
growth-forms of the páramos. CP, cushion plants (4 species);
Gr, grasses (9); AR, acaulescent rosettes (4); F, forbs (8); Sh tl,
frost-tolerant shrubs (2); WG, woody grasses (5); Sh av, frost-
avoiding shrubs (5); CR, caulescent rosettes (10); and Tr, trees
(17). Significant differences between mean IT and INT for the
first five growth-forms listed (CP to Sh tl) can survive ice
formation in leaf tissues, i.e. freezing tolerant. No significant
differences for the remaining four growth-forms indicate that
ice formation causes leaf tissue injury and are frost avoidant.
Bars correspond to one standard error of the mean. Different
small letters indicate significant differences in IT among plant
growth-forms (One-way Permanova (Pseudo F = 8.54,
P < 0.01). Sources: CP (Squeo et al. 1991; F Rada, E Márquez,
R Dulhoste unpublished data); Gr (Márquez et al. 2006); AR
(Squeo et al. 1991; Alvizu 2004; F Rada, E Márquez, R Dulhoste,
P Alvizú unpublished data); F (Azócar et al. 1988; Squeo et al.
1991; Azócar 2006; Rada et al. 2008); Sh tl (Azócar 2006); WG
(Ely et al. 2014); Sh av (Squeo et al. 1991; Alvizu 2004; Azócar
2006); CR (Goldstein et al. 1985; Rada et al. 1985a, 1987); Tr
(Rada et al. 1985b; Cavieres et al. 2000; Dulhoste 2010).
2019). In general, with a few exceptions, woody
plants tend to be avoiders, while herbaceous plants
are freezing tolerant. Moreover, injury temperatures
are lower in herbs, with cushion plants and grasses
being the most resistant, contributing to explain
why these groups reach the highest elevations
under natural conditions (Cuesta et al. 2019;
Figure 4). These results agree with the hypothesis
by Sakai and Larcher (1987) whereby plants under
less extreme temperature conditions, i.e. lower ele-
vations, rely on avoidance mechanisms, while plants
subjected to more extreme conditions tolerate freez-
ing. Regardless of the mechanism, avoidance or
tolerance, there is an increase in resistance with
increasing elevation (Figure 5). More importantly,
injury temperatures are always below the minimum
recorded temperatures at the different elevations in
the Venezuelan páramo.
Few studies have been carried out on the freezing
resistance of páramo plants in their establishment
phases (seedlings or juveniles). As mentioned in the
previous section, the more extreme temperature con-
ditions occur at the soil surface. Therefore, plants are
Figure 5. The relationship between injury temperature and
elevation for all plants (n = 64) studied from different growth-
forms for the Venezuelan páramos (Tinjury = 2*10−6x2 – 0,0175x
+ 28,046; r2 = 0,38, P = 0.12). Dotted line represents absolute
minimum temperature -elevation relation (Tmin = −0.0061x
+18.797, r2 = 0.90) along a páramo elevational gradient.
Sources: see list in Figure 4.
subjected to lower absolute minimum temperatures
during establishment. García-Varela and Rada (2003)
have studied freezing resistance mechanisms in juve-
niles of Coespeletia timotensis and C. spicata, while
Rada et al. (2011) have described freezing resistance
in Polylepis sericea saplings and ramets. Both studies
have reported similar avoidance responses as their
adult counterparts, but survival of saplings was asso-
ciated to more favourable microsites for establishment,
i.e. rocks or ‘nurse’ plants (see Llambí et al. 2013 for
other upper treeline species). Rehm and Feeley (2015a)
have reported that juvenile tree species maintained
freezing resistance similar to that of their adults at
a tropical treeline and that rare extreme temperature
events might limit the advance of these species into the
open páramo. However, these authors have also
pointed out that another species, Weinmannia fagar-
oides, has the ability to withstand lower freezing tem-
peratures, suggesting that extreme low temperatures
are not limiting its upper elevational limit.
In general, research in the Venezuelan páramos
suggest that even though for some species, their
upper distribution limit may be determined by their
inability to withstand freezing temperatures, there are
many others which do not seem to be affected. In the
particular case of trees, there are many species
(Dulhoste 2010; Rehm and Feeley 2015a) which clearly
have the capability to survive freezing night-time tem-
peratures but currently occur at lower elevations than
the potential temperature limits, e.g. the evident con-
tinuous forest line in the cloud forest-páramo ecotone.
This suggests that there must be other limiting factors
(see below), determining the distribution of trees
along elevational gradients in the páramo. Studies
have suggested that treelines, on a global scale, are

associated with a mean root-zone temperature of 6.7°
C, and near 5°C for tropical treelines (Körner and
Paulsen 2004). While seedling or sapling stages may
be critical in the establishment of trees (Hoch and
Körner 2005; Rada et al. 2011), and certain studies
have suggested a temperature related limitation in
carbon investment towards growth instead of
a constraint in the photosynthesis process per se
(Hoch and Körner 2005; Körner 2012); the physiolo-
gical mechanisms that limit the upper tree distribution
is still under debate. Further ecophysiological studies
on the genus Polylepis may lead us to the answers, and
as Körner (2012) has very accurately suggested, the
‘treeline will be understood once we find the func-
tional differences between trees and alpine shrubs’.
Leaf water potentials in páramo plants
The water status of a plant is determined by the
balance between water uptake by the roots and water
loss through transpiration from the leaves. The former
depends on the availability of water in the soil and the
latter on air evaporative demand and stomatal control.
The ability of a plant to respond to environmental
water deficit may be determined through its capacity
to survive under low leaf water potentials (ΨL) condi-
tions. Those species that manage to maintain higher
(less negative) ΨL and therefore a more favourable
water status under limiting water conditions rely on
avoidance mechanisms, while those which survive
these adverse conditions reaching lower (more nega-
tive) ΨL are more tolerant to water deficit. Woody
plants tend to be less tolerant than herbaceous plants
when comparing responses of different plant growth-
forms along this avoidance-tolerance gradient
(Figure 6). Under wet season conditions no differences
in minimum leaf water potentials (ΨLmin) were found
between growth-forms, all showing values between
−0.9 and −1.3 MPa. This is expected as soil water is
available and air evaporative demand is relatively low
in the wet season, and therefore, water deficit does not
seem to represent a major constraint. Conversely,
during the dry season, under limiting soil water avail-
ability and high temperature and air evaporative
demand, ΨLmin are lower (−1.4 to −2.7 MPa). During
this season, trees and giant rosettes show the highest
ΨLmin, while grasses show the lowest.
Most giant rosettes have stems with a well-
developed pith that allows them to have a high water-
capacitance, i.e. high capacity to store water (Rada
2016). This pith permits giant rosettes to maintain
a favourable water balance even when conditions of
water availability in the soil or high evaporative
PLANT ECOLOGY & DIVERSITY 7
Figure 6. Mean minimum leaf water potentials (ΨLmin) during
wet (■) and dry (□) seasons for the different páramo plant
growth-forms studied. Tr, trees (13 species); CR, caulescent
rosettes (5); Sh, shrubs (6); F, forbs (12); excluded growth-forms,
AR, acaulescent rosettes (5); CP, cushion plants (3); Gr, herbaceous
grasses (9). Number of species studied for each plant life-form in
parenthesis. Bars correspond to one standard error of the mean.
Different lower case letters indicate significant differences in dry
season ΨLmin between plant growth-forms (One-way Permanova
(Pseudo F = 6.64, P < 0.01). Sources: Tr (Rada et al. 1996; Cavieres
et al. 2000; Dulhoste 2010; F Rada, L Ramírez unpublished data);
CR (Goldstein et al. 1989; Rada et al. 1998, 2012); Sh (Rada 1993;
Llambí et al. 2003; Pirela 2006); F (Briceño 1992; Llambí et al.
2003; García-Varela 2008); AR (Rada 1993; Pirela 2006;
García-Varela 2008); CP (Cáceres 2011; Ramírez et al. 2015;
P Alvizú, F Rada unpublished data); Gr (García-Varela 2008;
F Rada, E Márquez, R Dulhoste unpublished data).
demand are adverse. Giant rosettes with the highest
capacitance are found at the highest elevations in the
driest páramos (Goldstein et al. 1984; Rada 2016).
For example, Coespeletia timotensis, the species with
the highest capacitance, grows from 4200 m to
4600 m in the subnival páramo of Piedras Blancas.
Its high capacitance allows it to maintain constantly
positive leaf ΨL compared to other giant rosettes,
even in the dry season (Meinzer and Goldstein
1985). In contrast, Coespeletia moritziana is the
giant rosette most tolerant to water deficit (Rada
et al. 2012). This species grows on poorly developed
soils and fractured rocks, which are associated with
low soil water retention. For C. moritziana, ΨLmin
during the dry season can reach −1.8 MPa compared
to the minimum water potentials of other rosettes
which do not fall below −1.5 MPa (Goldstein et al.
1984; Rada et al. 1998). Additionally, unlike other
high elevation giant rosettes, C. moritziana shows
the ability to osmotically adjust from wet to dry
season, allowing lower water potentials without tur-
gor loss (Rada et al. 2012). With respect to establish-
ing giant rosette seedlings and juveniles, in which
pith capacitance does not play an important role in
maintaining a favourable water status, different
authors have found that the effect of adverse envir-
onmental conditions at ground level are the main
8 F. RADA ET AL.
cause for their high mortality rates (Smith 1981;
Goldstein et al. 1985; Estrada and Monasterio 1988;
Guariguata and Azócar 1988) and attributed it to
a low physiological capacity to tolerate drought.
Additionally, García-Varela (2000) and Mora et al.
(2019) have reported that juveniles of Coespeletia
timotensis and C. spicata were associated with favour-
able microsites such as those near to adult rosettes or
rocks.
There are other giant rosettes (e.g. Ruilopezia atro-
purpurea) that differ from those described above by
their morphological characteristics, including the
absence of leaf pubescence and lack of a well-
developed stem pith. For R. atropurpurea minimum
leaf water potentials of −1.5 MPa have been described
(Baruch and Smith 1979; Rosquete 2004; Navarro
2013), a value comparable to those for Coespeletias.
Navarro (2013) has described osmotic adjustments for
adult individuals of this species, which allows them to
withstand water stress during the dry season without
relying on a well-developed stem pith. All these
authors have agreed in that this species does not have
the necessary adaptations to grow in more extreme
environments, being restricted to higher precipitation,
moderate temperatures and relatively nutrient-rich
soils found in low elevation páramos near the contin-
uous forest line (Monasterio and Vuillemuier 1986).
Trees have been considered as avoiders of water
deficit (Leuschner 2000; Cabrera 2002; Dulhoste
2010) through different anatomical and functional
characteristics. Dulhoste (2010) has reported mini-
mum water potentials of ca. −1.5 MPa for forest –
páramo ecotone trees, with a minimum of −2.0 MPa
for Diplostephium venezuelense, a small tree able to
colonise páramos above the continuous forest line
(Llambí et al. 2013). Rada et al. (1985b) have reported
minimum water potentials of −2.0 MPa for Polylepis
sericea, distributed between 4200 and 4600 m in the
Venezuelan Andes, growing higher than any other
tree. Important osmotic adjustments have been
described for both tree species, allowing them to main-
tain turgor during periods of water deficit (Rada et al.
1985a; Dulhoste 2010). For shrubs, Hypericum larici-
folium is the most representative and abundant species
growing along a wide elevation range between 2600 m
and 4300 m. This species reaches minimum water
potentials of ca. −1.8 MPa during periods of water
deficit in the dry season (Rada 1993; Llambí et al.
2003; Pirela 2006). At the other extreme, grasses exhi-
bit the lowest leaf ΨLmin with a mean of −2.8 MPa and
values as low as −4.0 MPa for Nassella mexicana or
Cortaderia hapalotricha (Pirela 2006; García-Varela
2008; Ramírez et al. 2015).
For leaves to remain physiologically active, it is
necessary that their cells be turgid. The capacity to
maintain turgor in plants can be determined by com-
paring ΨLmin during periods of water deficit with
osmotic potentials at the turgor loss point (ΨLtlp).
None of the studied growth-forms in the páramo has
shown significant differences between these two
potentials (Figure 7). These results suggest that in
general, even during periods of peak water deficit,
most plant species maintain turgor. However, at least
two of the studied species within each growth-form
present ΨLmin below ΨLtlp during the dry season, e.g.
the cushion plant Aciachne pulvinata (ΨLmin = −2.6
and ΨLtlp = −2.2 MPa), the grass Vulpia myuros (−3.7
and −2.2 MPa), the hemiparasite forb Castilleja fissifo-
lia (−2.8 and −2.2 MPa), the acaulescent rosette
Calandrinia acaulis (−2.7 and −2.4 MPa) and the
shrub Monticalia sclerosa (−1.9 and −1.6 MPa) while
ΨLmin were always above ΨLtlp in all trees and caules-
cent rosettes (data not presented). Trees and caulescent
rosettes always present more positive ΨLmin and ΨLtlp.
For trees, this may be explained by their root systems
that allow them to obtain water from deeper soil layers
and for caulescent rosettes by the high capacitance of
their stem piths. As with herbaceous growth-forms, it
has been reported that when water deficit becomes
extreme during severe dry seasons, aerial biomass is
lost, remaining in a dormant state until the following
wet season when new leaves are produced (Rada 1993).
Figure 7. Leaf water potentials (ΨL), minimum ( ) and at the
turgor loss point ( ), for the different páramo plant growth-forms
during the dry season. Tr, Trees (13 species); CR, Caulescent
rosettes (7); Sh, Shrubs (4); F, Forbs (6); excluded life-forms: AR,
Acaulescent rosettes (3); CP, Cushion plants (3); Gr, Grasses (3).
Bars correspond to one standard error of the mean. Different
lower case letters indicate significant differences in ΨL at the
turgor loss point between plant growth-forms (One-way
Permanova (Pseudo F = 7.80, P < 0.01). Source: Tr (Rada et al.
1985b,1996 ; Dulhoste 2010; R Dulhoste, F Rada, unpublished
data); CR (Rada et al. 2012; Navarro 2013; F Rada unpublished
data); Sh (Alvizu 2004); F (Briceño 1992; Rada 1993; Alvizu2004);
AR (Alvizu 2004); CP (Alvizu 2004); Gr (Alvizu 2004).
 PLANT ECOLOGY & DIVERSITY 9

Stomatal control and gas exchange
The degree of stomatal opening or closure at the leaf-
air interphase is a key factor which determines both
the amount of water vapour losses from the leaf
lamina to the air (transpiration), and of CO2 from
the air entering the substomatal cavities of the leaf
and determine the CO2 assimilation rate. Through
stomatal control, plants must optimise the relation-
ship between CO2 assimilation and leaf conductance,
known as intrinsic water use efficiency (IWUE). An
unfavourable water status in páramo plants occurs
mostly during the dry season, when a reduction in
precipitation leads to reduced soil water availability
and there is a high air evaporative demand produced
by high incident radiation, high temperature and low
relative humidity. Such high air evaporative demand
effect can also occur during the wet season, but due to
the occurrence of fewer days with clear skies, it plays
a less important role. The effect of climatic season-
ality on water availability is evident when stomatal
responses of all growth-forms between seasons is
compared (Table 2). A reduction of 50–60% in sto-
matal conductance (gs) in all growth forms occurs
between seasons; only bamboos differ, showing
a smaller reduction (22%). This may be explained
by the humid environments with which the bamboos
have been associated (Ely 2009; Ely et al. 2019).
Seasonal stomatal closure is concomitant with
a reduction in CO2 assimilation in the different
plant growth-forms of the páramo. The reductions
in CO2 assimilation rates range from 30–45% for
most growth-forms and up to 65–75% in grasses
and forbs. Many of the species belonging to these
two latter groups usually enter a semi-dormancy
stage, losing above-ground biomass as the dry sea-
son progresses. Regarding IWUE, most growth-
forms show an increase towards the dry season
when water becomes a limiting resource (e.g.
Llambí et al. 2003). The three growth-forms which
show no significant seasonal differences in IWUE
are: the giant rosettes, which partly compensate by
mobilising water from their large water storage in
the pith; herbaceous grasses which, as indicated
above, lose part of all of their aerial biomass during
the dry season and bamboos which generally live in
constantly humid environments.
Páramo plants and climate change
The specific environmental conditions at high ele-
vations have given rise to the unique alpine eco-
systems of the tropical Andes. Variability in
climate, topographic, geomorphologic and soil
characteristics lead to strong spatial heterogeneity
over very short distances and along elevational
gradients. This close relationship between climate
and environment in continuously occurring tran-
sitional zones reveal important differences in the
structure of vegetation communities (Fariñas and
Monasterio 1980; Ramírez et al. 2009; Llambí
2015). Páramos maintain high rates of endemism
due to an ′island′ effect which, through isolation,
favour speciation (Pouchon et al. 2018). These
biologically diverse ecosystems (Beniston 2003)
are considered important biodiversity hotspots
(Myers et al. 2000) and have been described as
highly exposed and sensitive to climate change
(Gosling and Bunting 2007; Buytaeart et al. 2010;
Cuesta et al. 2017).
Plants may respond in three different ways to
changes in climate: adaptation, migration or local
extinction (Thuiller et al. 2008). Mountain vegeta-
tion should migrate upward in response to climate
change; however, Walther et al. (2005) have sug-
gested that vegetation will not move as a ´front´ and
shifts would occur according to individualistic

Table 2. Mean maximum stomatal conductance (gsmax, mmol m−2s−1), CO2 assimilation (Amax, μmol m−2s−1) and
intrinsic water use efficiency (Amax/gsmax x10−2) during wet (WS) and dry (DS) seasons, for the different plant growth-
forms of the Venezuelan Andean páramo (number of species studied in parenthesis). Tr – Trees, CR – Caulescent
rosettes, Sh – shrubs, AR – Acaulescent rosettes, F – forbs, excluding those herbs categorised in other growth-forms,
Gr – grasses, WG – Woody grasses.
gsmax Amax Amax/gsmax
Growth-form WS DS WS DS WS ES
Tr (7)1 199 ± 54 87 ± 24 9.1 ± 1.9 6.3 ± 0.5 5.5 ± 0.8 7.6 ± 0.9
CR (6)2 115 ± 27 55 ± 6 5.7 ± 1.4 3.7 ± 1.0 5.3 ± 1.2 6.5 ± 1.4
Sh (7)3 120 ± 10 51 ± 7 8.7 ± 1.2 4.9 ± 0.6 4.1 ± 0.6 12.6 ± 2.2
AR (6)4 165 ± 18 68 ± 19 7.4 ± 1.3 4.6 ± 0.7 4.7 ± 1.2 7.3 ± 0.9
F (15)5 156 ± 19 57 ± 15 10.2 ± 1.3 3.5 ± 0.7 5.2 ± 0.6 8.2 ± 2.0
Gr (10)6 139 ± 33 61 ± 8 8.2 ± 0.6 2.3 ± 0.8 7.0 ± 1.5 5.6 ± 2.4
WG (3)7 89 ± 22 69 ± 9 6.3 ± 1.1 4.8 ± 0.8 7.3 ± 0.8 7.1 ± 1.1
Source: 1 Rada et al. (1996), Cavieres et al. (2000), Dulhoste (2010); 2 Goldstein et al. (1989), Rada et al. (1998, 2012), Navarro (2013), F Rada,
R Dulhoste unpublished data; 3 Rada (1993), Pirela (2006), Cáceres, Llambí et al. (2003); 4 Rada (1993), Cabrera et al. (2000), Pirela (2006),
Cáceres and Rada (2011); 5 Cabrera et al. (2000), Pirela (2006), García-Varela (2008), Llambí et al. (2003); 6 Pirela (2006), García-Varela (2008),
F Rada, E Márquez, R Dulhoste unpublished data; 7 Ely (2009).
10 F. RADA ET AL.
responses by species and the disaggregation and
emergence of other species associations under
environmental change (Williams and Jackson
2007). On the other hand, Körner (2003) has sug-
gested that projections that assume that vegetation
will move up along isotherms overestimate this
shift, while the effect on single species may be
underestimated. Unless micro-habitat conditions
are considered, climate warming projections may
be misleading (Scherrer et al. 2011). Additionally,
Scherrer and Körner (2011) have suggested that,
due to the thermal heterogeneity at a micro-
habitat scale in alpine habitats there may be more
suitable sites available than have been assumed
under climatic change scenarios. Evidence for
migration has been described for mountain envir-
onments and supported through an increase in spe-
cies richness at mountain summits as an effect of
global warming (Grabherr et al. 1994; Pauli et al.
1996, 2012). Pauli et al. (1996) and Rehm and Feeley
(2015b) have reported that migration of vascular
plants has occurred at a lower rate when compared
to temperature changes, an evidence of a time lag
between temperature increases and vegetation
responses. In the particular case of the cloud forest-
páramo ecotone in the Andes, Rehm and Feeley
(2015b) have described a dsiplacement upslope of
cloud forest trees three times slower than expected
from concurrent warming. Other factors, e.g.
decreasing water availability, high incoming radia-
tion, competition with low strata vegetation of the
open páramo, which may be responsible for this
fairly stable forest treeline need to be studied.
Therefore, how plants will respond in terms of
adaptation or extinction will depend largely on their
physiological and ecological characteristics. How phy-
siological responses change via plasticity or evolution
are determinant in the projections of the effects of
climate change on vegetation distribution. Cuesta
and Becerra (2012) and Cuesta et al. (2017) have
suggested that for tropical Andean plant communities,
species with restricted ranges and/or at higher eleva-
tions will show a large reduction in their habitats and
many of them may be driven towards extinction (see
also Mavárez et al. 2019).
The tropical high Andes stands out as a region of
high projection uncertainty, limiting the reliability of
future predictions. Projections suggest a 3 ± 1.5°C
rise for the Andes in the next century (Buytaeart et al.
2011) while Vuille et al. (2003) have reported a rise of
0.34°C per decade in the last 30 years for the northern
Andes. With respect to precipitation, Buytaeart et al.
(2010) have described large errors in simulations
when models are compared to observational data.
Different reports suggest a 300 mm/year increase in
the next hundred years for Ecuador and Southern
Colombia, while Northern Colombia and Venezuela
show a decreasing precipitation trend (Urrutia and
Vuille 2009; Buytaeart et al. 2011).
There is no clear evidence of the direct effect of
daytime higher temperatures on photosynthetic
processes of páramo plants. Different authors have
shown that alpine plants present a particularly wide
range of temperatures in which photosynthesis
remains at or near optimum, suggesting that CO2
assimilation would not be affected by an increase in
temperature per se (Rada et al. 1992; Rada et al.
2008; Körner 2012). However, higher temperatures
will have an effect on air evaporative demands and
soil water availability. Higher evaporative demands,
lower soil water content and projected decreases in
precipitation for the páramos suggest an accentu-
ated effect on plant water relations and gas
exchange. Considering all plant growth-forms stu-
died, shrubs and herbaceous growth-forms tend to
be more tolerant to water deficit (i.e. include species
which present the lowest ΨLmin) than trees (forest –
páramo ecotone species and Polylepis sericea) and
caulescent rosettes. In addition, shrubs and herbac-
eous growth-forms seem to have a greater capacity
to respond to a broader range of water availability
conditions (larger standard errors within these
growth-forms, Figure 6). For example, the shrub
genus Hypericum presents extremely avoidant spe-
cies, H. juniperinum, restricted to very humid habi-
tats; and H. laricifolium, a shrub which largely
dominates the páramos along a wide elevational
gradient (2200–4500 m) including humid and
desert páramos (Fariñas et al. 2008; Cáceres et al.
2015). Therefore, these patterns suggest that even
though some species within these growth-forms
may disappear, others may functionally replace
them, giving this ecosystem a certain degree of
resilience with regard to shrub-herbaceous plant
communities.
Trees, with the exception of Polylepis sericea, are
restricted to lower elevations and transition zones
between upper cloud forests and low páramo
(Ramírez et al. 2009; Arzac et al. 2011, 2019).
Considering that all tree species studied to date along
forest – páramo gradients have shown avoidance
responses to water deficit (higher ΨLmin, Figure 6),
under expected scenarios of greater water stress, only
those species tolerating lower leaf water potentials
would be fit to colonise páramos at higher elevations.
Dulhoste (2010) has described Diplostephium

venezuelense as the woody species which presents the
most similar water relations to those of P. sericea,
which grows in small patches under sheltered condi-
tions above the continuous forest line. Coincidently,
D. venezuelense was found to be the dominant species
in continuous forest borders in the forest – páramo
ecotone, and the only tall woody species present in the
adjacent open páramo (Ramírez et al. 2009; Llambí
et al. 2013). However, other factors such as the high
radiation loads characteristic of páramos outside the
continuous forest canopy need to be considered. Bader
et al. (2007) have reported that excess solar radiation
limits tree establishment above the continuous forest
line, with Diplostephium species showing the highest
survival when plant cover was experimentally
removed from saplings growing in páramos adjacent
to the continuous forest line.
The giant rosettes may be considered the most
dominant growth-form of the páramo. Nevertheless,
most studied species of this group, with the exception
of Coespeletia moritziana, maintain relatively high ΨL
(> −1.5 MPa) in order to survive. Presently, in order to
maintain high ΨL, giant rosettes maintain nearly closed
stomates during water deficit periods which, in turn,
limit processes such as CO2 assimilation. Under
a scenario of severe lack of water, giant rosettes
would not have the capacity to control stomates
further which will affect survival. Consequently, this
growth-form seems to be the most susceptible to chan-
ging environmental conditions. Azócar et al. (2000)
have suggested that giant rosettes in high elevation
ecosystems may display low resilience and a fragile
functional stability. Additionally, habitat loss due to
climate change in giant rosettes is expected to be more
severe on species living at higher elevations and found
in restricted habitats (Mavárez et al. 2019), i.e. endemic
species such as Coespeletia timotensis or C. moritziana.
Conclusions
Based on the gathered evidence on plant functional
traits for the Venezuelan páramos, we suggest that
due to the functional diversity of species and exist-
ing redundancy within plant-growth forms, the per-
petuation of most existing plant-growth forms and
the stability in terms of the general ecosystem prop-
erties would seem to be guaranteed. However, one
of the main components of this ecosystem, the giant
rosettes, would be affected under projected limiting
water availability conditions for the Northern
Andes and would place them under a vulnerable
status.
PLANT ECOLOGY & DIVERSITY 11
On a tolerance gradient and on a plant growth-
form basis; caulescent rosettes, trees and woody
grasses are less resistant to water deficit, while the
two former growth-forms are less resistant to freezing
temperatures (Figure 8). In general, even though direct
effects of night-time freezing temperatures are
a determinant factor in the survival and distribution
of specific páramo plant species, they seem to play
a less important role in the composition and vegeta-
tion dynamics, at a plant growth-form level, towards
higher elevations. Additionally, all climate change sce-
narios indicate increasing temperatures and an
ascending frost line towards higher elevations (Vuille
et al. 2003; Braun and Bezada 2013; IPCC 2013;
Rabatel et al. 2013) which would favour those less
resistant species. However, it should be kept in mind
that even though mean temperatures are on the rise,
extreme temperature events, including lower mini-
mum freezing temperatures are occurring (Inouye
2008; Sierra-Almeida and Cavieres 2010). High day-
time temperatures seem to be more important in the
case of plants growing at ground level, i.e. acaulescent
rosettes, prostrate herbs, cushion plants or establishing
seedlings, where extremely high temperatures fre-
quently occur. However, indirect high temperature
effects may be determining survival and distribution
of plant growth-forms in the páramos (Figure 8).
These effects are mainly related to higher ambient
water evaporative demands, which would have
a direct effect on plant gas exchange and water rela-
tions, e.g. limiting stomatal opening and affecting CO2
assimilation rates. On a species-specific basis, some
plants may be restricted by other factors, such as
high radiation inputs including UV radiation, nutrient
relations, plant-plant and plant-pollinator interac-
tions, seed dispersal mechanisms, which have an effect
on current status of plant communities in the páramo
and which will undoubtedly have an influence on
future vegetation patterns (Llambí and Rada 2019).
Finally, there are two research aspects which need to
be further studied in order to have a better under-
standing of plant functioning and responses under
the high elevation extreme conditions and to compre-
hend the effects of future climate change on this eco-
system. First, considering that establishment
represents a filter phase determining the success of
any plant species in the páramo, especially since con-
ditions at the soil surface are more extreme, studies on
factors affecting seedling and juvenile fitness are
required. Second, intra and interspecific relations
between plant species and growth-forms need to be
considered to better understand distribution patterns
12 F. RADA ET AL.

Figure 8. Schematic diagram showing the effects of temperature and water deficit on all studied plant growth-forms of the
Venezuelan Andean páramos. CR, Caulescent rosettes; Tr, Trees; WG, Woody grasses; Sh, Shrubs; AR, Acaulescent rosettes; F, Forbs;
CP, Cushion plants; Gr, Grasses. * Most shrub species studied avoided frost, although there were two which were frost tolerant.
This was the only growth-form which presented both avoidance and tolerance. Under predicted scenarios of increased water
deficit; caulescent rosettes, trees and woody grasses would seem to be most affected. Temperature per se seems to be less
important in determining vegetation dynamics in the páramos (see text for details).

in the páramos, especially at higher elevations. Under
climate change scenarios, biotic pressures, e.g. compe-
tition, surely play an important role in the lower
páramo boundaries, as lower elevation plant species
move up. While at higher elevations, under harsher
conditions, the existence of favourable microhabitats,
through facilitation; could allow associations between
species which will, in the end, determine the occur-
rence of different plant communities (Cáceres et al.
2015; Hupp et al. 2017; Mora et al. 2019).
CRN2-2005]; Institute of International Education (IIE);
CDCHT-ULA.
Notes on contributor
F Rada, A Azócar and C García-Núñez specialise in plant
physiological ecology, focusing on plant responses to differ-
ent stresses, mainly related to temperature and water, in
diverse tropical ecosystems.

Acknowledgements
Financial support by the Consejo de Desarrollo Científico,
Humanístico, Tecnológico y de las Artes (CDCHTA-ULA),
Fondo Nacional de Ciencia, Tecnología e Innovación
(FONACIT) and the Inter-American Institute for Global
Change Research (IAI) throughout the years is gratefully
appreciated. FR wishes to thankfully acknowledge the
Institute of International Education (IIE) and the
Universidad de Los Andes (UniAndes) for their significant
support commencing this year. The authors appreciate help-
ful comments on the manuscript made by the editor-in-
chief and two anonymous reviewers.
Disclosure statement
No potential conflict of interest was reported by the authors.
Funding
This work was supported by the Fondo Nacional de Ciencia
Tecnología e Innovación [P12-0387]; Interamerican
Institute for Global Change Studies (IAI) [CRN-040,
ORCID
Aura Azócar http://orcid.org/0000-0003-4486-2414
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