DISCUSSION
In this study, after evaluating 42 species and 20 functional traits in
one paramo site on the eastern range of the Northern Andes in Colombia,
we found that many of the species studied shared similar attributes or
functional traits, and they were clustered in three groups or plant
functional types (PFTs). Traits that were powerful functional
descriptors of PFTs in the paramo were traits related to the leaf
nutrient status (C, N and P), leaf toughness, thickness and leaf dry
matter content (LDMC), seed dispersal syndromes and physiological traits
related to water use efficiency and tolerance to water deficit like
Ψnoon, WUE and transpiration rate. Cuticular conductance
did not differ among species, among growth forms or among PFTs, and
given how time consuming this trait is to measure it could be omitted
for future functional classification in the paramo.
We did find some evidence that growth forms correspond to PFTs and could
be used to define groups with similar ecological and physiological
traits, as was found for the Venezuelan paramos (Rada, Azócar and
García-Núñez, 2019) and the tundra (Chapin et al. , 1996).
However, for shrubs the story is complex; some species shared traits
with the forbs while others form their own group. The classification of
upright and prostrate shrub appears to be impractical since both forms
were clustered together, and according to our data it would make more
sense to classify them into tough and tender leaved shrubs. Where shrubs
with tough leaves present a series of traits that suggest higher
tolerance to water deficit.
One limitation of our study is that we did not include grasses or
cushion plants in our analysis and these groups could potentially
increase the number of PFTs. However, the increase of functional types
is likely to be small if grasses belong to just one PFT as in the
Venezuelan paramo where all nine species of grasses studied shared
similar water and temperature resistant strategies (Rada, Azócar and
García-Núñez, 2019). Similarly, in Chingaza, a different Colombian
paramo, Cárdenas-Arévalo and Vargas-Ríos (2008) identified only three
PFTs after analyzing 70 species, including rosettes, shrubs, forbs,
grasses and cushion plants. Although all these findings from different
paramos might suggest that paramos have reduced functional responses, we
should keep in mind that mountains have complex environmental gradients
and various microclimates (Scherrer and Körner, 2011; Sklenář et
al. , 2016; Körner and Hiltbrunner, 2018) and that many species show
significant variation in functional traits across elevation gradients
(Baruch and Smith, 1979; Baruch, 1984; Meinzer, Goldstein and Rundel,
1985; Rada et al. , 1998; Wang et al. , 2016), which
suggests a wide acclimation capacity for many species which was not
explored here. Our study presents a picture of the functional diversity
at a single elevation, but is possible that many of these species can
acclimate and modify their traits; understanding species plasticity is
key to fully evaluate if the few PFTs identified in paramos imply a
limited capacity to respond to changes in the environment.
The paramo hosts the highest plant diversity of alpine ecosystems
worldwide (Sklenář, Hedberg and Cleef, 2014), which has hindered our
ability to understand the ecology and physiology of most of their
species and the ecosystem services they provide. Paramos are entirely
different from alpine temperate ecosystems so we cannot assume a priori
that the same functional responses that we know from alpine areas apply
to the paramo and here we provide some insights into the functional
ecology of the paramo. To understand the adaptations and traits of
paramo plants we have to take into account that in this tropical alpine
ecosystem, temperature variation is not seasonal but diurnal; in a
single day differences between absolute minimum and absolute maximum
temperatures may exceed 20 to 30K (Sklenář et al. , 2016;
Leon-Garcia and Lasso, 2019; Rada, Azócar and García-Núñez, 2019),
including freezing temperatures. These species need to withstand great
daily temperature changes and freezing temperatures. From studies on the
plant response to freezing tolerance in the Venezuelan paramo (Llambí
and Rada, 2019), we know that the strategy to deal with freezing
temperatures varies among growth forms (Rada, Azócar and García-Núñez,
2019). Rosettes avoid freezing with insulating structure and
supercooling, whereas forbs, cushion plants and grasses are freeze
tolerant (Azocar, Rada and Goldstein, 1988; Squeo et al. , 1991).
However, as we show in our study, shrubs are hard to place in a single
strategy; some species avoid freezing (Squeo et al. , 1991), while
others tolerate freezing (Azócar, 2006). Less is known about species’
tolerance to high temperature, which is the new challenge for plants in
a warming world, but from a screening on heat tolerance in 21 paramo
species we know that all species can tolerate high temperatures; and
irreversible damages to the photosynthetic apparatus occurs when the
leaves reaches 45oC, in some species, or in other
species this happens at temperatures as high as 53.9oC, and rosettes seems to be especially tolerant
(Leon-Garcia and Lasso, 2019). Again, growth forms appear to be
associated with the strategies to deal with high temperatures, as well
as with freezing temperature.
Besides temperature, water availability is also considered one of the
most important environmental drivers in the paramo (Rada, Azócar and
García-Núñez, 2019). The sudden daily changes in
temperatures typical of the paramos also influence water availability.
If temperatures descend below zero, water freezes and becomes
unavailable, and when temperatures increase on clear days, evaporative
demand increases (Ramirez, Rada and Llambí, 2014). Therefore, even in
relatively wet paramos, water deficit can occasionally occur, especially
in the dry season. The strategies of paramo plants to deal with water
deficit also seem to be somewhat related to the growth form (Rada,
Azócar and García-Núñez, 2019). In the Venezuelan drier paramos, many
species of grasses and shrubs can reach quite low water potentials at
noon which suggests they are tolerant of water deficit, while rosettes
maintain higher (less negative) water potentials during the day, even in
the dry season, which indicates they rely on avoidance mechanisms (Rada,
Azócar and García-Núñez, 2019). In fact, many of these stem rosettes are
known to store water in their stem pith allowing them to sustain higher
water potentials thorough the day (Goldstein, Meinzer and Monasterio,
1984; Meinzer, Goldstein and Rundel, 1985).
In our study site, a relatively wet paramo, we found that all growth
forms analyzed seem to behave more like avoiders with relatively high
values (less negative) of noon water potential. However, one of the
functional groups identified, the PFT-3, consisting of shrubs with tough
leaves, had the lowest water potential at noon, slightly higher values
of WUE and higher LDMC (Figure 3; Table A1 ). A higher LDMC is
also associated with having leaves with higher modulus of elasticity
(Niinemets, 2001) and more rigid lignified cell walls (Niinemets and
Kull, 1998), which could allow them to support lower leaf water
potentials and maintain leaf turgor even in periods of lower water
availability. High LDMC has also been found to be associated with higher
cavitation resistance against drought (Markesteijn et al. , 2011)
and is a typical trait associated with higher survival in drier
conditions (Martínez-Garza, Bongers and Poorter, 2013) suggesting that
this group may be more tolerant of water deficit than the other two
groups. In a future drier world paramo species in PFT-3 may have a
higher probability of surviving than species in the other PFTs,
especially those in the groups of rosettes. On the other hand, based on
the Dim. 2 that separates species according to their seed dispersal
strategy, shrubs in the PFT-3 are mainly dispersed by endo-zoochory and
could migrate longer distances perhaps being more successful in
following their climate niche as environmental conditions change, while
forbs and rosettes in PFT-1 and 2 whose seeds are dispersed mainly by
wind, gravity or water might be too slow to migrate upward.
High mountain regions are warming faster than the lowlands and could be
more sensitive to climate change than other ecosystems at the same
latitudes (Diaz and Bradley, 1997; Liu and Chen, 2000; Rangwala, Sinsky
and Miller, 2013; Ning and Bradley, 2014). Therefore, predicting the
responses to climate change of mountain ecosystems has become a major
priority. For the tropical high Andes, projections suggest a 3.0 ± 1.5°C
rise in the next century (Buytaert, Cuesta and Tobon, 2011), and a
decreasing precipitation trend in Northern Colombia and Venezuela, but a
small increase in precipitation for Ecuador and Southern Colombia in the
next hundred years (Urrutia and Vuille, 2009; Buytaert, Cuesta and
Tobon, 2011). While most paramo plants can deal with somewhat higher
temperatures (Rada et al. , 1992; Körner, 2003; Rada, Briceño and
Azocar, 2008; Leon-Garcia and Lasso, 2019), their response to water
deficit could differ greatly among groups and future changes in water
availability could change the plant community. The combination of lower
precipitation, as projected for the Northern Andes, and higher
temperatures, which may increase air evaporative demands and reduce soil
water content, could greatly affect plant water relations and gas
exchange. For the drier Venezuelan paramo, where many grasses and shrubs
are more tolerant of water deficit, the shrub-herbaceous plant community
is likely to show some degree of resilience (Llambí and Rada, 2019;
Rada, Azócar and García-Núñez, 2019). However, the iconic giant
rosettes, common in many of the paramos of the Northern Andes, could
suffer in a drier world given their low capacity to tolerate water
deficit (Azócar, Rada and García-Núñez, 2000). These giant rosettes are
nurse plants with strong facilitation effects and are considered key
species in the maintenance of paramo plant diversity (Mora, Llambí and
Ramírez, 2019). Additionally, their rosette-like arrangement of heavily
pubescent leaves, sometimes forming a basket, facilitates water
interception from rain and fog which is then slowly released to the
soil, helping in one of the key ecosystem services of the paramo,
regulation and provision of water. A paramo without the PFT-2 made by
rosettes would definitively lose some of its functionality.
In a future drier paramo the species of shrubs belonging to PFT-3 are
the species with a highest chance of withstanding the drier conditions
given their higher tolerance to water deficit, and high LDMC values.
Yet, even in this group the leaf water potential values were never too
negative, indicating that all species, even the more tolerant ones, are
probably living on the edge of their safety margin. In previous work in
this same paramo, we found that two shrubs species in the genusHypericum were highly vulnerable to xylem cavitation; they lost
50% of water conductivity at values as high as -1.50 MPa, very close to
the lowest leaf water potential measured in the dry season (Ayarza,
Garzón-López and Lasso, 2018), an indication of a very narrow safety
margin. How changes on CO2 atmospheric concentrations,
which has been steadily rising (IPCC, 2014) will interact with the
expected changes in water availability in the paramo is unclear, but
based on what is known for other ecosystems, an increase in
CO2 is likely to mitigate drought stress if plants can
reduce their stomatal conductance (g s), improve
their water use efficiency and increase photosynthesis (Bazzaz, 1990;
Körner and Diemer, 1994; Long et al. , 2004). More physiological
studies on the vulnerability of water deficit of paramo plants and the
interaction with CO2 are urgently needed given that
water deficit is likely to be one of the threatening environmental
driver in a changing paramo. Using this PFT classification we can also
guide drought experiments to evaluate whether this classification and
set of traits are indeed good indicators of species responses to water
deficit and vulnerability to future changes.
Paramos are well known for their role regulating and provisioning water
to major cities in South America (Carrillo-Rojas et al. , 2016).
They are also important carbon reservoirs in tropical mountains
(Hofstede, 1999). There is a growing consensus that the impact of
species on ecosystem properties is partially mediated by the traits of
their component species (Chapin et al. , 2000; Díaz and Cabido,
2001; Kazakou et al. , 2006) and here we can start discussing how
these paramo species from different taxonomic groups might share similar
roles in ecosystem functionality (Hubbell, 2005). For example, LDMC and
C:N ratios appear to be crucial traits of living leaves that influence
the quality of the litter produced, and therefore their ‘after‐life
effects’ on ecosystem properties (Kazakou et al. , 2006). Species
belonging to PFT-1 with tender leaves with high N and P content and low
LDMC are probably fast-growing species whose dead leaves will decompose
rapidly and help in the rapid turnover of carbon and nutrients. Species
in PFT-3 with high LDMC and species in PFT-2 with thicker and tougher
leaves and higher C:N ratios decompose slowly, decreasing the liberation
of carbon and nutrients to the system, two processes that are important
for the role of paramos as carbon reservoirs. In terms of their
physiological strategies and their putative role in sequestering carbon,
species of forbs and shrubs in PFT-1 show an acquisitive strategy,
presenting the highest leaf nitrogen and phosphorus content and slightly
higher photosynthetic rate (although not statistically significant),
while the rosettes in PFT-2 behave more as conservative species (Reichet al. , 2003; Diaz et al. , 2004; Wright et al. ,
2004). Photosynthesis is the basis for vegetation growth, but several
parameters related to carboxylation efficiency (e.g. Vcmax) at this high
elevation are still unknown and are necessary to accurately simulate
gross primary production (GPP) and the role of the paramo on the carbon
cycle under climate change using Earth System Model predictions. Here we
only measured the light-saturated photosynthetic rate and the Ci/Ca
ratio. However, they both consistently showed no difference among growth
forms or PFTs, supporting the optimization of photosynthetic traits
hypothesis (Wang et al. , 2016) which suggests that the
incorporation of the paramo taxa into global vegetation models (Woodward
and Cramer, 1996) could be relatively simplified despite the immense
species diversity of the paramo.
Although there is a widespread consensus that growth forms are related
to functional adaptations, and that plant traits should reveal the
response of these plants to biotic and abiotic stresses in the ecosystem
(Westoby et al. , 2002; Reich et al. , 2003; Kattge et
al. , 2011), our data suggest some caution in classifying species into
PFTs based only on growth forms, especially in the case of shrubs.
Clearly shrubs are a complex group that varies from paramo to paramo and
even within the same paramo, as our data and those from the Venezuelan
paramo indicate. Shrubs presented the largest variance for many traits,
suggesting a greater capacity to respond to a broader range of
conditions. More growth forms should be analyzed; especially grasses,
and seedlings and seed responses need to be evaluated because they could
differ from their adult counterparts. This data set represents a
baseline to start discussing how species from different taxonomic groups
can perhaps share similar roles in the paramo functionality and how much
they differ in their strategies to acquire resources and withstand
environmental stress. In our study site in the mid paramo, dominated by
grasses, shrubs, forbs, and giant rosettes, we did find that rosettes
and forbs group into their own functional groups, but shrubs belong to
different groups. As in previous screening of functional diversity in
the paramos (Cárdenas-Arévalo and Vargas-Ríos, 2008; Rada, Azócar and
García-Núñez, 2019), we also found high redundancy and apparent limited
physiological response despite the extremely high plant diversity
typical of the paramo.
CONCLUSIONS
Our results add to a series of studies, which suggest that the paramo,
despite being very diverse, has few functional types, and high
redundancy, where many species share physiological strategies and
traits. However, a careful examination of shrub species and other growth
forms such as grasses, sedges and cushion plants is indispensable to
fully understand the diversity of functional strategies in the paramo.
Future studies should expose species from the different PFTs to drier
and warmer conditions to understand the differences among PFTs in terms
of vulnerability to environmental changes. We also need to better relate
PFTs and functional traits to properties and services in the paramo
ecosystem like water supply and carbon storage.