New insights into the functional ecology of paramo plants: what
growth forms can tell us about plant functional types
Marisol Cruz1*and Eloisa Lasso 1,2
1 Grupo de Ecología y Fisiología Vegetal, Departamento
de Ciencias Biológicas, Universidad de Los Andes, Bogotá, Colombia.
2 Smithsonian Tropical Research Institute, Panamá,
Republica de Panamá.
* Correspondence: m.cruz11@uniandes.edu.co
Abstract: Paramos are a unique type of tropical alpine
ecosystem. To understand how biodiversity, ecosystem services and
community resilience in the paramo will be affected by ongoing
environmental change we need to start identifying groups of species with
shared characteristics (i.e. functional types or PFTs). This task is
particularly challenging as paramos host the highest plant diversity of
alpine ecosystems. We measured 22 traits on 42 species belonging to
different growth forms in the Colombian Andes. Hierarchical Clustering
on Principal Components performed in a Factor analysis of mixed data was
used to identify species with similar functional traits and the number
of PFTs present. We identified three PFTs; one composed of forbs and
shrubs with tender leaves, one composed of only rosettes, and a third
group composed by shrubs with tough leaves. If PFTs represent a group of
plants that play similar roles in the ecosystem, and have similar
responses to perturbation, our results imply that paramos might have
limited physiological response and may be highly vulnerable to
environmental changes. On the other hand, the presence of multiple
species sharing functional traits could provide some resilience, if one
species disappears, others may fill the same role and maintain the
functionality of the paramo.
Keywords: Andes; functional traits; high elevation grassland;
PFT; SLA; tropical alpine ecosystem.
INTRODUCTION
In
the tropical Andes, at elevations above 3,200m, there is a unique type
of tropical alpine ecosystem, locally known as paramo. In the paramo,
vegetation has evolved under stressful conditions such as low
atmospheric pressure, low temperatures including freezing temperatures,
large daily fluctuation in temperatures, intense UV radiation and windy
conditions. These conditions, in combination with repeated isolation
events throughout geological times and their island-like nature
(mountain tops separated by lowlands), have promoted a high rate of
speciation (Sklenář and Ramsay, 2001; Madriñán, Cortés and Richardson,
2013; Flantua et al. , 2019), and have resulted in exceptionally
high endemism. As result, paramos host an estimated of 3,595 species of
vascular plants, 60% of which are endemic (Luteyn, 1999) including 14
genera that are endemic to the northern Andes (Sklenář and Balslev,
2005). Understanding which of these almost four thousand species could
be the most affected by the warming and drying trends expected by the
end of this century for the Andes (Urrutia and Vuille, 2009; Buytaert,
Cuesta and Tobon, 2011), is an overwhelming challenge. One approach to
simplify this challenge is to classify groups of species with shared
characteristics or functional traits into plant functional types (PFTs).
The concept of plant functional types proposes that species can be
grouped according to common responses to the environment and/or common
effects on ecosystem processes. For example, traits like leaf area,
foliar nitrogen, and height are related to the species ability to
acquire resources and maximize photosynthetic capacity, which is also
linked to the capacity to sequester carbon. Traits like water use
efficiency and leaf dry matter content (LDCM) and midday leaf water
potential are related to the ability to deal with water deficit
(Markesteijn et al. , 2011; Martínez-Garza, Bongers and Poorter,
2013), and traits like seed mass, and seed dispersal syndromes are
related to reproductive investment, migratory capabilities and
establishment success. Some of these traits may affect biogeochemical
cycles, invasion resistance, stability in the face of disturbance, net
primary productivity (NPP) and therefore can also be linked to species
roles in the ecosystem (Dormann, 2002; Lavorel and Garnier, 2002).
Functional classification is also thought to be a fundamental tool to
reduce the complexity of the floristic composition of plant ecosystems
around the globe, to feed global vegetation models (Woodward and Cramer,
1996), to decide what species to use for restoration based on their
traits and their roles in the ecosystem (Ostertag et al. , 2015),
and for monitoring the effects of global change on vegetation
distribution and ecosystem processes (Lavorel and Garnier, 2002). If we
can determine the trait profile of species, their putative role in the
ecosystem, and how many species share similar roles (the number of PFTs
in an ecosystem) we will be closer to understanding how changes in
temperature and water availability can modify species composition, and
how these changes translate into modifications of ecosystem functioning
(i.e. productivity, nutrient cycling, carbon assimilation) through
changes in species traits (leaf C/N content, photosynthesis) present in
the new altered community (Chapin et al. , 2000).
The assignment of species to PFTs is all but straightforward. Some
classification schemes use quantitative continuous traits that are
assumed to reflect life history trade-offs and involve time-consuming
fieldwork. Another approach is to assign species to functional groups
based on discrete dominant traits such as growth form, leaf habit, or
ability to fix nitrogen, (Ramsay, Kent and Duckworth, 2000; Wrightet al. , 2004; Reich, Wright and Lusk, 2007; Powers and Tiffin,
2010). This second approach represents a fast and relatively easy way to
distinguish and characterize functional types. However, the utility and
ecological meaning of functional type classifications based on these
discrete traits must be evaluated on a case-by-case basis. For example,
in the tropical dry forests of Costa Rica, Powers and Tiffin (2010)
evaluated if morphological and physiological traits of tropical dry
forest tree species varied with leaf habit (i.e. evergreen, deciduous
and semi-deciduous species), but found little value in the functional
type classification based on leaf habit alone. In contrast, Chapinet al . (1996) demonstrated that plant functional types strongly
coincide with growth forms in Artic ecosystems and found strong support
for the utility of using growth forms as predictors of the response of
Artic environments to global change. For the paramo, there is
conflicting evidence about the utility of growth forms as a proxy of
functional types (Azócar, Rada and García-Núñez, 2000; Cárdenas-Arévalo
and Vargas-Ríos, 2008; Rada, Azócar and García-Núñez, 2019), perhaps due
to differences in environmental conditions among paramos, the species
being studied, and the classification of growth forms used by different
authors (see Hedberg and Hedberg, 1979; and Ramsay and Oxley, 1997 for
examples of Paramo´s classification schemes).
From previous attempt to classify PFTs in the paramo it seems that
paramos has few functional groups and that rosettes clearly differ from
other growth forms, but whether all shrubs and forbs share common
responses and traits is still unclear. Cárdenas-Arévalo and Vargas-Ríos
(2008) in a Colombian paramo identified only three PFTs after analyzing
70 species and eleven traits, where grasses and bamboos dispersed by
anemochory were grouped together, forbs and cushion plants formed a
second group and rosettes a third group. Species of shrubs were
distributed across different PFTs. From a series of physiological
studies on plants from the drier Venezuelan paramos we know that
rosettes behave as avoiders, avoiding water deficit and freezing
(Azócar, Rada and Goldstein, 1988; Squeo et al. , 1991) whereas
grasses, cushion plants and forbs behave as freezing and water deficit
tolerators. Shrubs could be either tolerators or avoiders (Rada, Azócar
and García-Núñez, 2019). These previous works point to the potential of
using growth forms as proxies for PFTs, but more work is needed to
understand if the use of growth form is the best approach to classify
the vegetation into PFTs in paramos with different climate and
vegetation characteristics, to identify what traits are useful for this
classification, and to understand whether shrubs can indeed represent
many different physiological and ecological strategies. Understanding
the functional ecology of paramo plants is crucial given the apparently
limited number of physiological strategies identified in those previous
studies.
In this study, we evaluated a series of morphological and physiological
traits related to water relations and gas exchange, nutrient status,
acquisitive strategies and seed dispersal in 42 paramo species belonging
to different growth forms. Our main objectives were: 1) to identify the
number of plant functional types (PFTs) present in our sample; 2) to
determine which traits are crucial for PFT identification; and 3) to
establish if PFTs correspond with species growth forms, that is to
evaluate how useful growth forms are in defining PFTs in the paramos.
The identification of functional types in the paramo could eventually be
used to make predictions on the effect of climatic and anthropogenic
changes in the diversity and ecosystem processes in this unique tropical
ecosystem that covers approximately 36,000 km2,
supplies water to the major cities in South America, and stores large
quantities of organic carbon in its soils (Hofstede, 1999).
MATERIALS AND METHODS