Plant functional types and ecosystem function in relation to ... - DPI/Inpe

Journal of Vegetation Science 8: 463-474, 1997 © IAVS; Opulus Press Uppsala. Printed in Sweden

- Plant functional types and ecosystem function -

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Plant functional types and ecosystem function in relation to global change Díaz, Sandra & Cabido, Marcelo Instituto Multidisciplinario de Biología Vegetal, CONICET - Universidad Nacional de Córdoba, Casilla de Correo 495, 5000 Córdoba, Argentina; Fax +54 51 244092; E-mail [email protected]

Abstract. Plant functional types (PFTs) bridge the gap between plant physiology and community and ecosystem processes, thus providing a powerful tool in climate change research. We aimed at identifying PFTs within the flora of central-western Argentina, and to explore their possible consequences for ecosystem function. We analyzed 24 vegetative and regenerative traits of the 100 most abundant species along a steep climatic gradient. Based on plant traits and standard multivariate techniques, we identified eight PFTs. Our results confirmed, over a wide range of climatic conditions, the occurrence of broad recurrent patterns of association among plant traits reported for other floras; namely trade-offs between high investment in photosynthesis and growth on the one hand, and preferential allocation to storage and defence on the other. Regenerative traits were only partially coupled with vegetative traits. Using easily-measured plant traits and individual species cover in 63 sites, we predicted main community-ecosystem processes along the regional gradient. We hypothesized likely impacts of global climatic change on PFTs and ecosystems in situ, and analysed their probabilities of migrating in response to changing climatic conditions. Finally, we discuss the advantages and limitations of this kind of approach in predicting changes in plant distribution and in ecosystem processes over the next century. Keywords: Argentina; Climate change; Plant functional trait; Regional gradient. Nomenclature: Cabrera (1963-1970); Correa (1969-1984). Abbreviations: PFT = Plant functional type; RGR = Relative growth rate; SLA = Specific leaf area.

Introduction Plant functional types (hereafter PFTs) can be defined as sets of plants exhibiting similar responses to environmental conditions and having similar effects on the dominant ecosystem processes (Walker 1992; Noble & Gitay 1996). Although introduced long ago (Raunkiaer 1934; Grime 1977; Noble & Slatyer 1980; Box 1981, 1996), the concept of plant PFTs has received new attention as one possible framework for predicting ecosystem response to human-induced changes at a global scale. Sample copy Journal of Vegetation Science

Identification of these types is an essential step in global change research initiatives (Smith et al. 1996), and has been given priority in international research agendas (Steffen et al. 1992; Woodward & Cramer 1996). This is because of two reasons. First, in modelling vegetation under changing climatic conditions there is a widely recognized need to move away from single-leaf to wholeplant approaches (Bazzaz 1993; Körner 1993). Second, in doing so, the enormous complexity of individual species and populations needs to be summarized into a relatively small number of general recurrent patterns (Walker 1992; Grime et al. 1996). Recently, some research groups have advocated protocols involving the measurement of traits in large numbers of species, the construction of standardized data bases, the exploration of trait-trait and trait-environment associations, and the empirical testing of hypotheses (Keddy 1992; Leishman & Westoby 1992; Grime et al. 1996). Consistent patterns of association between plant traits have been found in local floras (Boutin & Keddy 1993; Fernández-Alés et al. 1993; Golluscio & Sala 1993; Grime et al. 1988; McIntyre et al. 1995). The relationship between these patterns and ecosystem function has become a topic of growing interest (Schulze & Mooney 1993). Different PFTs are expected to play different roles in terms of matter and energy processes in ecosystems. Therefore, their identification and the estimation of their abundance is highly relevant to the assessment of ecosystem function. Although there has been some progress with respect to the first point, very little has been published explicitly addressing the second (Schulze & Mooney 1993). In this article, we aim at identifying recurrent patterns of association among plant traits within a local flora, and to explore the possible consequences for ecosystem function under contrasting environmental conditions. We develop a protocol based on easily-measured plant traits, which allows the consideration of a large number of species, and the detection of patterns at the individual to ecosystem levels, with minimum time and technological investment. Finally, we assess the possibility that this approach could produce meaningful predictions about

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the responses of native vegetation to the changing climatic conditions expected in the next century.

Methods

Table 1. Climatic conditions at different sites along a regional gradient in central-western Argentina. Sites 59-63 (not shown) correspond to saline lowlands under different semi-arid to arid climatic conditions. See text and Fig. 3 for further description of sites. Meteorological data from the Argentine Meteorological Services and Argentine Railways.

Approach and data sets Steep gradients, in which large changes occur over short distances, are particularly appropriate for the study of the relationships between natural vegetation and present or future climatic conditions. We selected a regional climatic gradient in the centre-west of Argentina (ca. 31° 25' - 32° S, 64° 10' - 68° 37' W), spanning > 400 km between the subhumid high plateaus of the Córdoba mountains and the western semiarid-arid plains. There is a difference in annual rainfall of > 800 mm, and a difference in altitude of > 1500 m between the extreme points (Table 1). Dry and relatively cold winters and rainfall heavily concentrated to the warm season are characteristic to the whole region. The dominant vegetation types range between montane grasslands (highest and wettest extreme), woodlands (intermediate points) and open xerophytic shrublands (driest extreme). Open halophytic shrublands on lowlands with saline soils are scattered along the drier and lower portion of the gradient. We analyzed published vegetation analyses along the gradient (Cabido et al. 1989-1994) in which the abundance of all vascular species had been previously estimated according to the Braun-Blanquet scale. We considered 63 sites and characterized them in terms of climatic variables, with the exception of five sites in saline lowlands, where edaphic conditions take precedence over climatic variables as predominant limiting factors (Cabido et al. 1994). At each site, we selected the five analyses (three in one case) referring to the least disturbed vegetation. We discarded all the species which were present in less than 10 % of all the relevés available. We then selected 100 species with the highest cover values to be analysed in terms of functional traits. In choosing key traits, we aimed at plant processes closely related to ecosystem functions most likely to be modified by climate change (e.g. nutrient cycling, water retention, productivity, carbon storage). We selected 24 traits measurable at the individual plant level (App. 1), according to the following criteria: (1) they should be related to plant responses to resource availability and environmental constraints in situ; (2) they should express a capacity to colonize new areas and to re-establish in situ following disturbance; (3) they should provide information on plant relationships with herbivores, pollinators and dispersers; and (4) they should be easy to measure in the field or with very basic laboratory facilities. Sample copy Journal of Vegetation Science

Mean temperature (°C) Sites

1- 5 6 - 10 11 - 15 16 - 20 21 - 23 24 - 28 29 - 33 34 - 38 39 - 43 44 - 48 49 - 53 54 - 58

Altitude (m a.s.l.)

Annual

Min.

Max.

2155 1850 1450 1000 900 750 600 350 368 652 500 641

8.1 8.9 11.4 13.1 13.1 15.6 17.5 19.6 19.6 18.3 18.2 18.0

3.9 5.2 6.8 8.8 9.4 9.2 10.7 12.2 12.4 12.4 12.5 10.4

12.9 15.8 18.5 21.6 21.9 23.8 24.5 26.8 25.2 25.2 25.5 25.7

No. Annual frost-free rainfall months (mm) 0 0 2 4 5 5 6 8 8 7 6 6

911.5 840.4 887.3 996.0 996.0 826.4 662.0 520.0 520.0 381.0 260.0 85.0

In some cases, traits were surrogates for other, more quantitative labour or technology-demanding attributes. Specific leaf area (SLA) was used as an indicator of relative growth rate (RGR). Although not experimentally tested on our data set, a strong correlation between these two variables has been found repeatedly, especially when a wide spectrum of life histories is considered (Lambers & Poorter 1993; Reich et al. 1992). Seed size and shape were used as possible indicators of seed persistence in the soil, though more cautiously, since there is still no information of how widespread the relationship is demonstrated by Thompson et al. (1993) for British species. Data analysis To construct functional types on the basis of these traits, we used a non-hierarchical multivariate approach, following Díaz et al. (1992) (Fig. 1a). The scales of measurement of plant traits were originally continuous, categorical or binary, but they were all transformed into categorical or binary scales for analysis (App. 1). We subjected the 24 attributes × 100 species matrix to standard multivariate ordination and classification techniques (DCA and TWINSPAN; see, e.g. Gauch 1981). In order to identify the predominant plant traits along the climatic gradients, we built a 100 species × 63 sites matrix (obtained from the vegetation surveys mentioned above) and multiplied it by the attributes × species matrix. The result was a 24 attributes × 63 sites matrix

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Fig. 1. Main steps involved in the research protocol. Dashed lines separate different scales of analysis. Only results corresponding to scales a and b are reported in this paper.

(Fig. 1b), which was subjected to DCA. All the original matrices are available on request.

Plant functional types We distinguished eight functional types on the basis of a TWINSPAN classification of the attributes × species matrix (Fig. 2, Table 2). The main trend of variation as reflected by DCA-axis I in Fig. 2 separated plants with traits generally associated with high investment in photosynthesis and fast growth (high LWR and SLA, short plant and leaf life span, small investment in support and storage organs, shoot expansion concentrated to the most favourable season, low protection against herbivores, and C3 and C4 photosynthesis) and plants with traits generally associated with slow growth and high persistence in time and preferential allocation to storage and defence (low LWR and SLA, high longevity, high investment in support and storage organs, evergreen or semi-deciduous, strongly protected against drought and herbivory, and with C3 and CAM photosynthesis). These trade-offs have been documented repeatedly for other floras over narrower spectra of environmental conditions (Grime 1977; Chapin 1980; Grime et al. 1988). Regeneration traits showed less clear trends. Partial decoupling between regenerative and vegetative traits has often been reported (Grime et al. 1988; Leishman & Westoby 1992; McIntyre et al. 1995). In this case, there were significant correlations between vegetative traits defining DCA-axes I and II and pollination mode, seed size and seed number (Table 3). Specialized pollination Sample copy Journal of Vegetation Science

syndromes predominated in PFTs 4 - 6 and 8, wind pollination syndromes predominated in PFTs 1 and 2. PFTs 3 and 7 were heterogeneous in this sense. Absolute seed numbers per individual were maximum in PFTs 5 and 6 (which included the largest plants), decreasing toward both extremes of the first ordination axis. However, this trend needs further confirmation, since seed output in many of these species is highly variable between years and local conditions. No clear-cut pattern in dispersal mode or seed shape appeared among PFTs, although irregularly-shaped and/or vertebrate-dispersed seeds were more common in PFTs 4 - 6 and 8. Seed size tends to be associated with adult size and longevity when wider ranges of growth forms are analysed (see Westoby et al. 1992 for a review). Dispersal mode tends to be related with the distance a seed is likely to reach, with seeds dispersed by wind, or by highly mobile animals such as bats, birds, and ungulates, being more likely to reach longer distances (Hughes et al. 1994). In the case of British species, seed shape and size are strongly correlated with the probability of a seed becoming buried and incorporated into a persistent seed bank (Thompson et al. 1993). However, that association could not be found for the Australian flora which includes species with large, hard-coated seeds which germinate after fire (M. Leishman pers. comm.). Taxonomic considerations Our PFT classification was not independent of taxonomic affiliation. Some of the PFTs identified were strongly or absolutely dominated by one plant family

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Fig. 2. Detrended Correspondence Analysis of the attributes × species matrix. Functional types defined by TWINSPAN and described in Table 2. Characters most consistently associated with different areas on the ordination plane (Table 3) displayed in boxes.

(e.g. 72 % Poaceae in PFT 1, 100 % Bromeliaceae in PFT 4, 100 % Cactaceae in PFT 8), whereas the representation of different families was much more even in other cases (e.g. PFTs 3 and 6). A considerable imprint of phylogeny has also been noted by most of the authors who constructed PFTs on the basis of several plant traits (Grime et al. 1988; Leishman & Westoby 1992). Presentday plant-trait covariation sometimes coincide with, and sometimes is quite independent of, that produced by phylogenetic evolution (Ackerly & Donoghue 1995). Since phylogenetic differentiation and current fitness are not mutually exclusive processes, the ecological relevance of PFTs should not be dismissed because of their association with phylogeny (Ackerly & Donoghue 1995; Westoby et al. 1995).

lishment in situ following disturbance. On the other hand, species react individualistically to environmental factors (Huntley 1991) and our results indicate the presence of different capacities for dispersal in time and space within each PFT. This suggests that no PFT will be eliminated by climate change simply because of dispersal limitations. If there were consistent differences in migration ability among PFTs, we would not be able to predict vegetation response to rapid changes in climate from our observations of plant distribution under current environmental conditions (Chapin et al. 1996).

Responsiveness of PFTs to climate change Evidence from the literature

Implications The relevant time scale for the expected global climate change is of decades and centuries, rather than millennia. Therefore, vegetation responses are likely to involve local extinction and differential colonization by, rather than directional selection on, existing taxa (Huntley 1991). The lack of a clear trend among PFTs with respect to regeneration traits complicates predictions about their differential capacity of colonization of new areas or re-estabSample copy Journal of Vegetation Science

There is growing evidence that physiological traits measured during short periods at the leaf level are insufficient for reliable predictions of the effects of climate change on multi-species assemblages. Characteristics largely irrelevant at the physiological level (such as phenology, life history and canopy display) are crucial to responses in mixed stands (Bazzaz 1993; Körner 1993; Díaz 1995). The identification of PFTs bearing distinctive key traits seems a promising way forward. For

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Table 2. Summary of characteristics of the main plant functional types (PFTs) produced by TWINSPAN and DCA on a set of the 100 most abundant species along a climatic gradient in central-western Argentina (no. of species in each PFT indicated in brackets). Attributes listed when found in > 50 % species within each PFT. See Table 1 for further explanation of traits and definition of scales of measurement. List of species and families within each PFT available upon request. PFTs

Growth form

Vegetative traits

Regenerative traits

FT 1 (29)

Short graminoids (≤ 50 cm)

C4 and C3 pathway; High LA, SLA, and LWR; Short-lived (some annuals); Very low carbohydrate storage; Very low to nil C-immobilization in xylem; Low resistance to drought; Highly palatable for ungulates; Shoot biomass peak: spring - early autumn

Various seed sizes and shapes; Seed number low to intermediate (< 1000); Various dispersal agents; Wind pollination; Reproductive peak: spring - early autumn

FT 2 (12)

Tussock grasses and large-leaved forbs (≤ 100 cm)

C3 pathway; High LA, SLA, and LWR;Various lifespans; Moderate carbohydrate storage; Short-term C-immobilization in standing dead matter; Moderate resistance to drought; Moderately palatable; Clonal expansion Shoot biomass peak: summer

Various seed sizes and shapes;dispersal agents; Various seed numbers (< 100 to > 1000);Various dispersal agents; Wind pollination; Reproductive peak: summer

FT 3 (23)

Short (≤ 50 cm) herbaceous and semi-woody erect, creeping, or rosette-like dicots

C3 pathway; High LA and LWR, intermediate SLA; Lifespan short to moderate; Moderate carbohydrate storage; Very low C-immobilization in xylem; Moderate resistance to drought; Various levels of palatability; Shoot biomass peak: highly variable, uncommon in mid summer

Various seed sizes and shapes; Seed number low to intermediate (< 1000); Various dispersal agents; Animal unspecialized and specialized pollination; Reproductive peak: highly variable, uncommon in mid-summer

FT 4 (4)

Saxicolous or epiphytic rosettes (≤ 100 cm)

CAM pathway; High LA and LWR, very low SLA; Lifespan moderate, evergreen; Moderate carbohydrate storage; Some short-term C-immobilization in standing dead biomass; High resistance to drought; Low to nil palatability; Clonal expansion; Shoot biomass constant along the annual cycle or with peak in early spring

Seed size intermediate to large (2-10 mm); Irregular seed shape; Moderate seed number (100 - 1000); Animal and wind-assisted dispersal; Animal-specialized pollination; Reproductive peak: spring

FT 5 (11)

Trees (> 300 cm)

C3 pathway; High to moderate LA, and SLA, low LWR; Very long-lived, deciduous or semi-deciduous; Very high carbohydrate storage; Very high C-immobilization in xylem and bark; Very low ramification at ground level; Drought avoidance; Various levels of palatability (herbivory often deterred by thorns); Leaf biomass peak: late spring - early summer

Large seed size (4 - 10 mm); Flattened seeds; Very high seed number (several thousands); Various dispersal agents (vertebrate dispersal common); Animal specialized pollination; Reproductive peak: early spring - early autumn

FT 6 (12)

Evergreen shrubs and small trees (≤ 300 cm)

C3 pathway; Low LA, SLA, and LWR; Very long-lived, evergreen; High carbohydrate storage; High C-immobilization in xylem and bark; Ramified at ground level; High resistance to drought; Unpalatable; Leaf biomass constant or small peak in spring

Large seed size (4 - 10 cm); Various seed shapes; High seed number (a few thousands); Various dispersal agents; Animal-specialized pollination; Reproductive peak: spring- early autumn

FT 7 (4)

Aphyllous or scale-leaved shrubs (≤ 200 cm)

C3 pathway; Extremely low to nil LA and LWR (scale-like leaves or aphyllous, succulent); Long-lived, evergreen; High carbohydrate storage; Some C-immobilization in xylem and bark; Highly ramified at the ground level; High resistance to drought and salinity; Palatability low to nil; Green biomass constant

Small (≤ 2 mm) and spheroidal seeds; Seed number high to very high (a few to several thousands); Various dispersal agents; Various pollination agents; Reproductive peak: spring-early autumn

FT 8 (5)

Globular, cylindrical, and columnar branched stemsucculents of various sizes

CAM pathway; Aphyllous, with green succulent stem; Long to very long-lived, evergreen; Moderate carbohydrate storage; Some C-immobilization in xylem; Very low ramification at ground level; Drought avoidance; Unpalatable (herbivory deterred by thorns); Green biomass constant

Small- to intermediate-sized, isodiametric seeds (≤ 2 - 4 mm); High seed number (a few thousands); Dispersed by highly mobile animals; Animal-specialized pollination; Reproductive peak: spring-early autumn

example, plant growth stimulation by elevated CO2 seems positively associated not only with C3 photosynthesis and RGR, but also with the presence of storage organs, indeterminate growth, deciduous habit, and moderate nutritional demands (Hunt et al. 1991, 1993; Poorter 1993). Protected meristems, reduced leaf area, waxy or hairy coats, taproots and reserve organs should enhance survival under severe and/or untimely drought and frost events (Schulze 1982). The capacity to migrate over the landscape, tracking climatic conditions is associated with high dispersal ability, rapid establishment and maturation (Grime et al. 1988). Sample copy Journal of Vegetation Science

Predictions on the basis of PFTs On the basis of our results (Table 2 and Fig. 2), we expect maximum growth stimulation in situ by changing atmospheric conditions for plants at intermediate positions on the ordination plane in Fig. 2, namely members of PFT 3, PFT 6 and especially PFT 5, which combine high sink strength for carbon, C3 photosynthesis, moderate nutritional demands and resistance to drought and frost. A lower degree of growth enhancement by climate change should be expected towards both extremes of DCA I in Fig. 2 (PFTs 1 - 4 and PFTs 7 and 8). We

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Table 3. Spearman’s Rank Correlation Coefficient (Norusis 1992) between the two first DCA axes and 24 plant traits in the dataset. Correlation coefficients between all pairs of traits are available on request. NS = p > 0.10; * = p ≤ 0.10; ** = p ≤ 0.05; *** = p ≤ 0.001. DCA I DCA II

DCA II

– 0.12 NS

Vegetative traits LWR SLA Lifespan Drought–avoidance Carbon immobilization Vegetative phenology Size Thorniness Palatability Waxiness/Hairiness Leaf succulence Ramification Deciduousness Carbohydrate storage LA C-pathway Height/width Vegetative spread

– 0.76 *** – 0.70 *** 0.67 ** – 0.66 *** 0.64 *** – 0.64 *** 0.62 *** 0.56 *** – 0.56 *** 0.51 *** 0.44 *** 0.42 *** 0.38 *** 0.34 ** – 0.33 *** – 0.27** 0.13 NS – 0.12 NS

0.36 *** 0.06 NS – 0.47*** – 0.02 NS – 0.46 *** 0.12 NS – 0.65 *** 0.07 NS – 0.31 ** 0.31 ** 0.30 ** – 0.41 *** – 0.37 *** – 0.03 NS – 0.13 NS – 0.27 ** – 0.57 *** 0.20 *

0.59 *** 0.56 *** 0.30 ** 0.25 NS 0.10 NS 0.07 NS

0.31 *** – 0.49 *** – 0.01 NS – 0.03 NS 0.03 NS 0.10 NS

Regeneration traits Pollination mode Seed number Seed size Seed dispersal Reproductive phenology Seed shape

found no strong correlation between PFTs and dispersal ability, and at least some members of each PFT are expected to disperse across the two regional gradients (through wind or highly mobile vertebrates). The rate of establishment in new sites should be maximum for PFTs 1 - 3 (short-lived, presumably fast-growing, grasses, sedges and forbs with high SLA), decreasing towards the right extreme of DCA-axis I (long-lived, presumably slow-growing, plants which usually take many years to reach maturity).

From PFTs to ecosystem function Community structure influences ecosystem function strongly (Schulze & Mooney 1993), and the role of particular species in ecosystems depends largely on their density and individual size (Chapin 1993). Following this rationale, we analyzed the vegetation at different sites along the climatic gradient in terms of the key plant traits exhibited by their dominant species (Fig. 3). The ordination graph strongly resembled that of PFTs Sample copy Journal of Vegetation Science

(Fig. 2), showing clear differences in the predominant attributes of vegetation under different environments along the gradient. Having identified which plant traits are most common under specific sets of climatic conditions (Fig. 3, Table 1), and assuming that those traits influence ecosystem processes, we predicted the relative magnitudes of major ecosystem processes at contrasting points of the gradient (Fig. 3, bottom). The information and predictions of community and ecosystem processes produced by this kind of multivariate analysis can be spatially referenced, provided topographic and vegetation maps are available (Fig. 1c). This may be a useful tool for management and modelling at the regional scale. Montane grasslands Towards the left extreme of DCA-axis I (Fig. 3), high investment in photosynthesis (high LWR), presumably fast growth (high SLA) and short leaf life span are dominant traits in montane grasslands, where the most important environmental constraint is probably low temperature (Table 1). We thus predicted, at the ecosystem level (Fig. 3, bottom left), maximum biomass turnover, productivity, and nutrient cycling, and only moderate capacity for C-sequestration in biomass and water uptake by the rhizosphere. These systems should also exhibit maximum carrying capacity for ungulates, due to their high leaf:support tissue ratio and presumably high nutritional quality (SLA is associated positively with N-concentration in plant tissue and negatively with concentration of defensive compounds, Lambers & Poorter 1992; Reich et al. 1992). The presence of comparatively high densities of large herbivores (S. Díaz unpubl.) should also enhance nutrient cycling (Chapin & McNaughton 1989). These communities show much less structural complexity (spatial arrangement of plant structures) than woodlands and shrublands (Díaz et al. 1992; Gardner et al. 1995). This should influence the diversity of higher trophic levels (Lawton 1983). Woodlands and woodland-shrubland communities Woodland and woodland-shrubland communities at the centre of the ordination plane (Fig. 3) were dominated by large, long-lived, deep-rooted woody plants which coexist with smaller, shorter leaved, shallowrooted grasses, forbs and epiphytes. Therefore, biomass accumulation, carbon sequestration and soil water retention should be highest in those ecosystems, as compared with high-altitude grasslands, and xerophytic and halophytic vegetation (right extreme of DCA I, Fig. 3). Woodlands and woodland-shrublands also exhibit maximum structural complexity, which is given both by the

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Fig. 3. DCA ordination of the attributes × sites matrix. See Table 1 for climatic conditions at different sites. ■ = montane grasslands; from left to right sites 1 - 10 and 11 - 20, predominant PFTs: 1 (44 % of total vegetation cover), 2 (31 %), 3 (13 %); ✻ = montane woodlands, sites 21 - 33; predominant PFTs: 5 (72 %), 6 (9 %), 4 (7 %); ● = Xerophytic woodlands and woodland-shrubland communities, sites 34 - 48, predominant PFTs: 3 (31 %), 5 (31 %), 1 (15 %); ▲ = open xerophytic shrublands, sites 49 - 58, predominant PFTs: 6 (65 %), 5 (15 %), 1 (11 %); ◆ = halophytic vegetation on poorly drained soils, sites 59 - 63, predominant PFTs: 7 (83 %), 6 (16 %). Plant traits and expected community-ecosystem processes associated with different sectors of the ordination plane are displayed in boxes, and at the bottom, respectively.

convergence of several PFTs and by the architecture of most trees and shrubs, and is positively related with local insect diversity (Gardner et al. 1995). Open shrublands At the right extreme of DCA I (Fig. 3), low SLA, CAM photosynthesis, low to nil investment in leaves, evergreenness, high degree of ramification at the ground level (less risk of cavitation, as compared with a single thick trunk) and the presence of succulent above-ground organs, strongly protected by waxy, pubescent and/or spiny coats, are the predominant traits in open, short xerophytic and halophytic shrublands. All these traits probably represent an advantage under the prevailing water limitations and temperature fluctuations but should lead, at the ecosysSample copy Journal of Vegetation Science

tem level, to minimum biomass accumulation, biomass turnover, productivity, nutrient cycling, C-sequestration and carrying capacity for ungulates (Fig. 3, bottom right). The dominant PFTs have various root architectures, but the overall root web is less developed than those predominating in woodlands and woodland-shrublands. This, together with the low vegetation cover (< 60 %, as compared to 90 100 % in woodlands and grasslands; Cabido et al. 1989, 1993), should lead to a comparatively low water uptake by vegetation. Structural complexity is higher than in grasslands (predominance of woody plants), but lower than in woodlands and woodland-shrublands (smaller plants, lower diversity of PFTs). These predictions seem to be supported by recent results from Aguiar et al. (1996) for the transition between grasslands and shrublands in the Patagonian steppe.

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Persistence and regeneration: Trends of variation at the community and PFT levels The resemblance between the main trends of variation among PFTs and communities (DCA axis I in Figs. 2 and 3) is not surprising, since the distinct functional types which locally represent most of the biomass determine the major plant traits at any site along the environmental gradients. However, some patterns arose at the community level (Fig. 3) that were not well defined at the level of individual PFTs (Fig. 2, Tables 2 and 3). This is because communities represent particular combinations of various PFTs. Notably, seed dispersal mode and seed shape were poor discriminators between PFTs (Tables 2 and 3). However, endozoochory was rather common in woodlands and woodlands-shrublands (Fig. 3), becoming rarer toward the transitions to other vegetation types. This was due to the combination of PFTs 4 6 and 8 and some vertebrate-dispersed members of PFTs 3 and 7 at these sites. These patterns, together with the strong predominance of specialized animal pollination, suggest that specialized plant-animal interactions may play a more important role (or at least may be more common) in woodlands and woodland-shrublands than in other communities (Fig. 3, bottom). Similarly, large flattened seeds predominated in woodlands and woodland-shrublands (Fig. 3), whereas in montane grasslands and open halophytic shrublands small spheroidal seeds were common (with the exception of some Poaceae and Asteraceae with elongated seeds). According to Thompson et al. (1993), this kind of seed is more likely to persist in the soil than large irregularly-shaped ones. Although further studies of the actual persistence of seeds in soil banks are clearly needed, this suggests higher probabilities of regeneration in situ following disturbances, such as untimely or unusually severe drought or frost events, in montane grasslands and halophytic vegetation. On the other hand, maximum persistence of established vegetation, once environmental conditions have become unsuitable for regeneration, should be expected for woodlands, woodlands-shrublands, and short open shrublands. This is because the dominant PFTs are likely to survive as adults for very long periods under climatic conditions unfavourable for regeneration (Valiente-Banuet 1994). Grasslands should show a very low persistence in situ under unfavourable conditions, as a direct consequence of their dominant PFTs (short life span, low resistance to drought, modest reserve organs) but very fast expansion rates, mainly due to the faster establishment and development of their constituent PFTs.

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Ecosystem function under shifting climatic conditions The results discussed above demonstrate the relationship between plant traits and community structure and suggest consequences for ecosystem function. Under a changing climate, one should expect shifts in the relative abundance of PFTs because of local extinction and migration across the landscape (Huntley 1991) and therefore alterations of the predominant plant traits and ecosystem functions along regional gradients. Although it is widely accepted that species will show individualistic responses as they have done in the past (Huntley 1991), it is reasonable to expect that species that show similarities in essential functional characteristics will behave in relatively similar ways when tracking environmental conditions across the landscape. Present distributions can be used as a model for the future, provided at least one member of each functional type has the capacity to migrate over the landscape fast enough to keep pace with changing environmental conditions (Chapin et al. 1996). This requisite seems to be met by the plants we analysed, since there was no strong correlation between PFTs and dispersal ability. An appropriate mesoscale climatic model for the study area is still unavailable. Although general increases in temperature are likely, there is not enough information on rainfall patterns and frequency of extreme events (N. Fernández & R. Rodríguez pers. comm.). Therefore, and only as an illustration of our approach, we hypothesized an increase in mean monthly temperatures along the whole gradient by the time atmospheric CO2 concentration reaches 700 ppm, and predicted changes in plant distribution across the region on that basis. Under a hypothetical increase in mean monthly temperature, it is reasonable to expect an advance up the mountains of PFTs now typical of lower vegetation belts (montane woodlands, grassland-shrublands, lowmountain grasslands at intermediate positions on DCA axis I, Fig. 3), at the expense of the high-mountain grasslands (left extreme of DCA axis I, Fig. 3). Therefore, we may expect ecosystem processes listed in the left column at the bottom of Fig. 3 to shift towards those in the central column. These changes are likely to be relatively fast. PFTs predominating in high-mountain grasslands show low persistence as adults once environmental conditions have become unfavourable for establishment and the potentially invading PFTs can establish and reach maturity at high to moderate rates. Changes along this portion of the gradient might be evident over decades. As a result of a hypothetical increase in mean monthly temperatures, and provided the annual rainfall does not increase disproportionately with respect to present values, we may expect a progressive advance of PFTs

- Plant functional types and ecosystem function typical of very dry conditions (right extreme of DCA axis I, Fig. 3) over more mesic shrublands-woodlands and woodlands (intermediate positions on DCA axis I, Fig. 3). A direct consequence would be a shift from ecosystem processes listed in the central column at the bottom of Fig. 3 towards those in the right column. The rates of change could be rather low in this case, since the present vegetation is expected to be highly persistent in the established phase once environmental conditions have become unfavourable and the invading PFTs need a long time to establish and reach maturity. These replacements might take place over centuries. Possibilities and limitations of the approach Our approach emphasizes the links between PFTs, community structure, and ecosystem processes. It seems a promising tool in predicting the direction and rate of changes in plant distribution and ecosystem function in the face of climate change. Some limitations should be stressed, however. One is that the precision of our predictions directly depends on the availability of accurate mesoscale climatic models. Another limitation is the still very limited knowledge about how different plant traits (e.g. photosynthetic pathway, sink strength for carbon, frost resistance) and different combinations of environmental factors (e.g. changes in evapotranspiration, nutrient availability, frequency of extreme events) will interact in determining whole-plant responses to a changing climate. A third limitation is the uncertainty about the various feedback processes which are likely to arise at the community and ecosystem levels (e.g. mineralization:immobilization balance, Díaz 1995). More research is needed in these areas. In the meantime, approaches such as the one described in this paper may help us simplify the overwhelming complexity of natural ecosystems into far fewer categories, and in setting up more cost-effective monitorial and experimental projects.

Concluding remarks Our results confirm, over a wider range of climatic conditions, the occurrence of broad patterns of association among plant traits reported for other floras. On the basis of the recurrence of strongly correlated attributes, some authors have suggested the use of a highly reduced set of characters to predict ecosystem function under climate change (e.g. size and growth form, Chapin 1993) or disturbance (e.g. growth form, McIntyre et al. 1995). Nemani & Running (1996) have advocated that only those plant traits which can be detected from remote sensors should be considered if ecologists are to actively contribute to global science. Approaches of this kind are Sample copy Journal of Vegetation Science

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very useful, since simplification is urgently required in these research areas. This is particularly true in the case of global vegetation models. However, several other aspects of plant behaviour have to be included for finerscale enquiries (Box 1996; Noble & Gitay 1996; Thompson et al. 1996). Regeneration attributes are extremely important to understand plant migration over the landscape and responses to disturbance in situ. Partial decoupling between vegetative and regenerative attributes have been documented repeatedly (including this study). This suggests that we may still need multiple character sets to assess responses of vegetation under changing atmospheric conditions, and different sets of plant traits and PFTs according to the purpose and scale of our questions (Noble & Gitay 1996; Thompson et al. 1996). On the basis of easily-measured plant traits and standard vegetation surveys, our approach summarized the complexity of vegetation over a heterogeneous region into a relatively few PFTs and allowed predictions about major community-ecosystem processes. This suggests that the PFT approach is a promising way forward in predicting shifts in plant distribution in the face of global change. The PFT approach is not intended to substitute for monitorial and manipulative tests at the individual to landscape scales, but rather it may contribute to improve their design and their benefit/cost ratio. One advantage of our protocol is its wide applicability to other geographical areas, including those with distinct floras and/or modest technological resources. Two cautionary remarks are worth stressing here, which apply in general to multiscale approaches which strongly rely on the links between plant traits and ecosystem function. Firstly, the consideration of individual attributes that are relevant to higher complexity levels is indispensable to minimise the risks involved in scaling up (Woodward et al. 1991; Körner 1993; Díaz 1995). Secondly, we need more accurate climatic predictions at the mesoscale, and further research on interactions among plant traits and on feedbacks at the community-ecosystem level. These are essential inputs to improve the accuracy of our predictions about the magnitude and rate, as well as direction, of changes in plant distribution under a future climate. Acknowledgements. Comments by F. S. Chapin III and J. P. Grime greatly improved this paper. We are grateful to the UCPE staff, University of Sheffield, and especially to J.P. Grime, for inspiring interaction. We thank S. Carlquist and P. Baas for useful comments, our research team and A. Acosta for support, and D. Abal-Solís for drawing the figures. The research was sponsored by the European Union ISC Programme (CI1*CT94-0028), The British Council - Fundación Antorchas (BNS 992/21) and Universidad Nacional de Córdoba (Res. 263/95).

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- Plant functional types and ecosystem function change, pp. 53-70. Chapman & Hall, New York, NY. Lambers, H. & Poorter, H. 1992. Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences. Adv. Ecol. Res. 23: 187-261. Lawton, J.H. 1983. Plant architecture and the diversity of phytophagous insects. Annu. Rev. Entomol. 28: 23-39. Leishman, M.R. & Westoby, M. 1992. Classifying plants into groups on the basis of associations of individual traits: evidence from Australian semi-arid woodlands. J. Ecol. 80: 417-424. McIntyre, S., Lavorel, S. & Tremont, R.M. 1995. Plant lifehistory attributes: their relationship to disturbance response in herbaceous vegetation. J. Ecol. 83: 31-44. Nemani, R. & Running, S.W. 1996. Implementation of a hierarchical global vegetation classification in ecosystem function models. J. Veg. Sci. 7: 337-346. Noble, I.R. & Gitay, H. 1996. A functional classification for predicting the dynamics of landscapes. J. Veg. Sci. 7: 329336. Noble, I.R. & Slatyer, R.O. 1980. The use of vital attributes to predict successional changes in plant communities subject to recurrent disturbances. Vegetatio 43: 5-21. Norusis, M.J. 1992. SPSS for Windows. SPPS Inc., Chicago, IL. Poorter, H. 1993. Interspecific variation in the growth response of plants to an elevated ambient CO2 concentration. Vegetatio 104/105: 77-97. Poorter, H. & Bergkotte, A. 1992. Chemical composition of 24 wild species differing in relative growth rate. Plant, Cell Environ. 15: 221-229. Raunkiaer, C. 1934. The life forms of plants and statistical plant geography; being the collected papers of C. Raunkiaer. Clarendon Press, Oxford. Reich, P.B., Walters, M.B. & Ellsworth, D.S. 1992. Leaf lifespan in relation to leaf, plant, and stand characteristics among diverse ecosystems. Ecol. Monogr. 62: 365-392. Sánchez, E. & Arriaga, L. 1990. El síndrome Kranz en Poaceae de la flora Argentina. Parodiana 6: 73-102. Schulze, E.-D. 1982. Plant life forms and their carbon, water and nutrient relations. Encycl. Plant Physiol. N.S. 12B: 615-676. Schulze, E.D. & Mooney, H.A. (eds.) 1993. Biodiversity and ecosystem function. Springer-Verlag, Berlin.

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Sipowicz, D., Cabido, M. & Acosta, A. 1986. Producción primaria y aspectos fenológicos en comunidades de pastizal y césped. In: Luti, R. (ed.) Efecto de las actividades humanas sobre los ecosistemas montañosos y de tundra. MaB 6, pp. 371-384. UNEP-UNESCO, Montevideo. Smith, T.M., Shugart, H.H. & Woodward, F.I. (eds.) 1996. Plant functional types. Cambridge University Press, Cambridge. Steffen, W.L., Walker, B.H., Ingram, J.S.I. & Koch, G.W. 1992. Global change and terrestrial ecosystems (IGBP Report No. 21). IGBP-ICSU, Stockholm. Thompson, K., Band, S.R. & Hodgson, J.G. 1993. Seed size and shape predict persistence in soil. Funct. Ecol. 7: 236241. Thompson, K., Hillier, S.H., Grime, J.P., Bossard, C.C. & Band, S.R. 1996. A functional analysis of a limestone grassland community. J. Veg. Sci. 7: 371-380. Valiente-Banuet, A. 1994. Patrones de cambio temporal de la vegetación asociados a la evolución de paisajes desérticos de México. Libro de Resúmenes del VI Congreso Latinoamericano de Botánica (2-8 October, Mar del Plata, Argentina), p.779. van der Pijl, L. 1982. Principles of dispersal in higher plants. Springer-Verlag, Berlin. Walker, B.H. 1992. Biodiversity and ecological redundancy. Conserv. Biol. 6: 18-23. Westoby, M., Jurado, E. & Leishman, M.R. 1992. Comparative evolutionary ecology of seed size. Trends Ecol. Evol. 7: 368-372. Westoby, M., Leishman, M.R. & Lord, J.M. 1995. On misinterpreting the ‘phylogenetic correction’. J. Ecol. 83: 531534. Woodward, F.I. & Cramer, W. 1996. Plant functional types and climatic changes: Introduction. J. Veg. Sci. 7: 306308. Woodward, F.I., Thompson, G.B. & McKee, Y.F. 1991. The effects of elevated concentrations of carbon dioxide on individual plants, populations, communities and ecosystems. Ann. Bot. 67: S23-S38. Received 13 December 1995; Revision received 19 June 1996; Accepted 22 December 1996;

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App. 1. Traits recorded on the 100 most abundant species along two climatic gradients in central-western Argentina. 10 randomly chosen, healthy looking adult individuals were considered for traits measured in the field or in the laboratory. Scales of measurement were originally categorical (cat), continuous (cont) or binary (bin). Trait

Description

Description of classes in matrix

Photosynthetic pathway Leaf area (LA)

Photosynthetic metabolism, on the basis of literature1 and leaf anatomy observation cat Leaf area (cm2) based on field and herbarium measurements cont

Specific leaf area (SLA)

cat bin

aphyllous or evergreen = 0; deciduous = 1

Leaf succulence

Estimation of leaf area:leaf dry weight (cm2.g–1), indicates RGR2, 3 based on field and herbarium measurements Leaf weight: non-photosynthetic weight, based on floras4, herbaria, and field observation Leaf shedding in the unfavourable season3, based on floras4 and field observation Based on field observation5

CAM = 1; C4 = 2; C3 = 3 aphyllous = 0; > 0 - 0.1 cm2 = 1; > 0.1 - 1 = 2; > 1 - 9 = 3; > 9 = 4 aphyllous = 0; > 0 - < 10 cm2.gr–1 = 1; 10 - < 100 = 2;100 - ≤ 500 = 3; > 500 = 4 LWR < 1 = 0; LWR ≅ 1 = 1; LWR > 1 = 2

cat

Size

Adult size3 (cm), based on floras4 and field observation

cont

Height:width Lifespan

Total height:total width (h:w) Persistence of an individual in the established phase3, on floras4 and field observation basis Capacity to store carbohydrate that can be broken down and allocated to new growth (thickened roots and stems, bulbs, rhizomes)3 Capacity to invest C in support tissue (xylem and bark), in compounds that cannot be broken down to be used in further biosynthesis3

cat cat

Leaf weight ratio (LWR) Deciduousness

cont

Waxiness/Hairiness Thorniness

Degree of ramification at the ground level, considered an advantage under drought6, based on field observations (only for woody species) Presence of drought-avoiding organs (tap root, thick trunk, succulent stem, ephemeral leaves) Presence of hairs, waxes or cutines Presence of thorns

bin cat

Vegetative spread

Capacity to produce expanding clones3, based on floras4 and field observation

bin

Palatability

Subjectively assessed on the basis of literature4 and field observation

cat

Shoot phenology

Seasonality of maximum production of photosynthetic tissue, based on field observation and literature7

cat

Seed size

cont cont

< 0.15 = 1; 0.15 - >1 = 2; 1 - 5 = 3; > 5 = 4

Seed number

Length (mm) on floras4 and herbarium basis, possibly related to persistent seed banks in the soil8 Variance of seed length, width and depth, possibly related to persistent seed banks in the soil8 Number of seeds per plant

non-succulent = 0; slightly succulent = 1; highly succulent = 2 ≤ 20 cm = 1; 20 - 60 = 2; > 60 - < 100 = 3; 100 - < 300 = 4; > 300 - < 600 = 5, ≥ 600 = 6 h:w > 1 = 0; h:w ≅ 1 = 1; h:w < 1 = 2 annual = 1; biennial = 2; 3 - 10 yr = 3; 11 - 50 yr = 4; ≥ 50 yr = 5 no specialized storage organs = 0; specialized storage organs = 1 herbaceous monocots = 0; herbaceous dicots = 1; semi-woody dicots = 2; woody dicots with trunk and bark = 3 non-woody species = 0; 1 single trunk = 1; 2 - 10 = 2; > 10 = 3 evident drought-avoiding organs present = 0; evident drought-avoiding organs absent = 1 hairs, waxes and/or cutines absent = 0; present = 1 no thorns = 0; slightly thorny = 1; very thorny (e.g. Cactaceae) = 2 no evident clonal expansion = 0; evident clonal patches = 1 unpalatable = 0; low palatability, or palatable only at juvenile stages = 1; moderately palatable = 2; highly palatable = 3 no evident peak = 1; winter, autumn, early spring = 2; late spring, spring, spring- summer, late summerearly autumn = 3; late spring-summer, summer = 4 < 2 = 1; 2 - < 4 = 2; 4 - 10 = 3; > 10 = 4

cont

Seed dispersal in space

Type of dispersal, according to literature9 and seed morphology observation10

cat

Pollination mode

Type of pollination agent, according to literature11, field observation, and floral syndromes12 Seasonality of maximum production of flowers and fruits, based on field observation and literature7

cat

< 100 seeds = 1; 100 - 999 = 2; 1000 - 5000 = 3; > 5000 = 4 no obvious dispersal agent = 0; animals with relatively low mobility (ants, rodents) = 1; highly mobile animals (large mammals, bats, birds) = 2; wind = 3 anemophyllous = 0; unspecialized zoophyllous = 1; specialized zoophyllous = 2 no evident peak = 1; winter, autumn, early spring = 1; late spring, spring, spring-summer, late summerearly autumn = 3; late spring-summer, summer = 4

Carbohydrate storage Carbon immobilization

Ramification Drought avoidance

Seed shape

Reproductive phenology

1Sánchez

bin cat

cat bin

cat

& Arriaga (1990), Hattersley & Watson (1992). & Bergkotte (1992), Reich et al. (1992). 3Positively related with sink strength for carbon (Poorter 1993; Díaz 1995). 4Cabrera (1963-1970), Correa (1969-1984). 5Enhances survival under water stress. 6Narrower stem diameter is associated with decreased vessel diameter, and therefore with reduced cavitation risk under severe water stress (Carlquist 1988). 7Alessandria & Casermeiro (1986); Sipowicz et al. (1986); Morello (1958); Díaz et al. (1994). 8Thompson et al. (1993). 9Howe & Smallwood (1982); van der Pijl (1982). 10Expertise provided by L. Galetto. 11Faegri & van der Pijl (1979). 12Expertise provided by A.A. Coccuci. 2Poorter

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