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