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AOBPreview originally published online on November 12, 2007
Annals of Botany 2008 101(3):353-360; doi:10.1093/aob/mcm289
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© The Author 2007. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Reproductive Modes in Leiothrix (Eriocaulaceae) in South-eastern Brazil: The Role of Microenvironmental Heterogeneity

Flávia F. Coelho*, Christina Capelo, Leonardo C. Ribeiro and José Eugênio C. Figueira

Departamento de Biologia Geral, Universidade Federal de Minas Gerais, ICB, Caixa Postal 486, cep 30161-970, Belo Horizonte, MG, Brazil

* For correspondence. E-mail flaviafcoelho{at}yahoo.com.br

Received: 10 July 2007    Returned for revision: 3 September 2007    Accepted: 4 October 2007    Published electronically: 12 November 2007


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 

Background and Aims: The genus Leiothrix (Eriocaulaceae) is restricted to South America and contains 37 taxa. The genus is most species-rich in the mountains of Minas Gerais, where 25 species occur, 19 of them in the Serra do Cipó. Leiothrix taxa that inhabit different microhabitats exhibit a number of reproductive modes. Rhizomatous taxa produce seeds plentifully; therefore, this group were defined as rhizomatous seed-producing. The pseudoviviparous reproductive mode was divided into canopy-forming and rooted. In the first, ramets remain attached to a parental rosette suspended by scapes, whereas in the second, ramets take root and may or may not remain attached to a parental rosette. In this study, it is proposed that microenvironmental heterogeneity is an important factor generating and maintaining reproductive modes in Leiothrix.

Methods: Soil analyses and vegetation cover estimates were performed for five Leiothrix taxa occurring in 19 areas along the Serra do Cipó. In these 19 points of the Serra do Cipó, soil data were collected from 27 populations of each species, and vegetation cover data were collected from 20 populations, due to fire that occurred in the region and destroyed most of the vegetation. For each population, three replicates were made. A discriminant function analysis was performed, in an attempt to test the effect of microhabitat features in the differentiation of the reproductive modes.

Key Results: Discriminant function analyses separated the three groups of reproductive modes based mainly on percentage vegetation cover. The pseudoviviparous canopy-forming group occurs under densely crowded conditions, while the pseudoviviparous rooted and rhizomatous seed-producing groups occur in areas with sparse vegetation cover. However, the group pseudoviviparous rooted occurs in soils constituted of exposed sand, while the rhizomatous seed-producing group occurs, frequently, on mat-forming mosses.

Conclusions: Microenvironmental heterogeneity, specifically heterogeneity in percentage cover of vegetation, appears to have influenced the generation and maintenance of reproductive modes in Leiothrix. Reproductive variation within Leiothrix taxa occupying different microenvironments results from a response to fine-scale habitat variation. Therefore, it is proposed that ecological speciation is an important process in adaptive radiation in this genus.

Key words: Clonal growth, environmental heterogeneity, Leiothrix, life history, morphological variation, pseudovivipary, reproductive modes, rupestrian grasslands


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 
Divergent natural selection associated with different habitats or ecological niches is increasingly viewed as the primary cause of speciation in plants (Lexer et al., 2003). For most flowering plant lineages, changes in the ecological attributes of populations, especially involving habitat and resource utilization, are an important component of speciation (Schluter, 2001; Levin, 2003). In continental floras, ecological speciation, i.e. the evolution of new species as a result of divergent selection on traits among populations in contrasting environments, is most apparent in regions with large numbers of endemics (Levin, 2003, 2004). Ecological speciation can generate evolutionary radiation in response to ecological opportunities (e.g. new microenvironments) (Ellis et al., 2006; Friar et al., 2006). Adaptive radiations are generally characterized by the accumulation of substantial morphological and ecological diversity within rapidly speciating lineages (Schluter, 1996). Such radiations appear to have played a central role in the proliferation of ‘stone plants’ in the genus Argyroderma (Aizoaceae) in the Cape Floristic Province in South Africa (Ellis et al., 2006). The role of microhabitat differences, especially substrate types such as sandstone and granite (Verboom et al., 2004) and quartz gravel soil (Ellis et al., 2006), on life history divergence and evolutionary radiation was investigated for Ehrharta (Poaceae) and Argyroderma, respectively, in the Cape region of South Africa. These studies show a direct effect of varied edaphic microhabitat on the adaptive radiation in these genera. Ellis and Weis (2006) suggested that the co-existence of Argyroderma species is facilitated by the response to fine-scale habitat variation. It has been shown that seedling distribution may correlate with microspatial variation in leaf cover and that species respond differently to the components of small-scale environmental heterogeneity in grassland habitat (Silvertown and Dickie, 1980; Silvertown and Wilkin, 1983). At small spatial scales (centimetres), rupestrian grasslands exhibit high heterogeneity in environmental factors such as vegetation cover conditions and soil factors.

Rupestrian grasslands show peculiar characteristics of soil and topography that provide wide environmental heterogeneity and promote a variety of microhabitats. These microhabitats favoured the diversification and endemism of many flowering plant families (Giulietti et al., 2000). Among flowering plants of rupestrian grasslands in Brazil that show a high level of endemism and richness, the Eriocaulaceae stand out (Ramos et al., 2005). The Eriocaulaceae comprises approx. 1200 species in ten genera. They have pantropical distribution, although the majority of the species occur in the mountainous regions of Venezuela and Brazil (Giulietti and Hensold, 1990). In these regions, they grow on sandy soils and rocky outcrops of quartzite and sandstone (Giulietti and Hensold, 1990). On these soils there is great variation in the vegetation cover, suggesting considerable scope for the diversification of reproductive modes in Leiothrix.

The genus Leiothrix is restricted to South America and contains 37 taxa (Giulietti and Hensold, 1990). Leiothrix flavescens occurs in Brazil, Venezuela, Guyana and Peru, L. celiae is exclusive to Venezuela, and the remaining taxa are endemic to small mountainous areas in the Brazilian states of Minas Gerais and Bahia (Giulietti et al., 1995). The highest species richness of Leiothrix is concentrated in the mountains of Minas Gerais, where 25 taxa occur, 19 of them in the Serra do Cipó (Giulietti and Hensold, 1990).

Recently, data were presented showing a diversification on pseudoviviparous reproduction in two Leiothrix species (Coelho et al., 2006). Of the 19 Leiothrix taxa that occur at the Serra do Cipó, five have widespread spatial distribution. These five Leiothrix taxa: L. curvifolia ‘lanuginosa’, L. curvifolia ‘mucronata’, L. crassifolia, L. spiralis, L. vivipara and L. sinuosa were selected. Moreover, these five taxa exhibit all possible reproductive modes found in the genus. Based on the observation that rupestrian sympatric species of Leiothrix often differ in vegetation cover and edaphic conditions, the species were expected to show differences in microenvironment-related reproductive modes. Thus, in the present study, the microenvironmental heterogeneity is proposed to be an important reproductive mode-generating factor in Leiothrix.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 
Study area
The Serra do Cipó is located in the southern portion of the Espinhaço mountain range in the state of Minas Gerais, Brazil, between 19°12'–19°20'S and 40°30'–43°40'W and altitudes varying from 1000 to >1100 m. The climate is considered mesothermic, with mild summers and a rainy period during the summer, and the temperatures vary from 17 to 20 °C. The annual precipitation in the region is nearly 1500 mm; there is a dry period during the winter, which lasts 6–7 months, and a moist period which lasts 5–6 months. The rupestrian grasslands of the Serra do Cipó comprise a mosaic of edaphic habitats formed at one extreme by quartz gravel-derived soils, and at the other extreme by sandstone-derived soils. Rupestrian grassland has a predominance of shallow and sandy soils with low fertility and low water-holding capacity (Ribeiro and Fernandes, 2000). In these rock outcrop habitats, clonal growth, specifically pseudovivipary, is important in the maintenance of L. spiralis and L. vivipara populations (Coelho et al., 2006).

The vegetation of the Serra do Cipó is diverse, comprising mainly rupestrian grasslands. It has a continuous herbaceous layer with sparse shrubs. The rosette shape is a morphological convergence occurring in various families of herbaceous plants (Menezes and Giulietti, 1986). Poaceae, Cyperaceae, Velloziaceae, Xyridaceae and Eriocaulaceae are quite common in the region (Giulietti et al., 1987). Species from the genus Leiothrix are well represented in these areas and some are even endemic to the mountains of Minas Gerais (Giulietti et al., 1995).

Study species
Leiothrix individuals are morphologically characterized by their habit of growing in a rosette from which scapes with flower head-type inflorescences appear (Giulietti, 1978). Among the six studied taxa, L. curvifolia ‘lanuginosa’ (Bong.) Ruhland, L. curvifolia ‘mucronata’ (Bong.) Ruhland and L. crassifolia (Bong.) Ruhland were classified as rhizomatous seed-producing (RS) species, L. spiralis (Bong.) Ruhland as a pseudoviviparous rooted (PR) species and L. vivipara (Bong.) Ruhland and L. sinuosa Giulietti as pseudoviviparous canopy-forming (PCF) species (Fig. 1). RS species usually produce seeds plentifully. Ramets of the PCF species remain attached to the parental rosette suspended by the scapes (Coelho et al., 2006), while the ramets of the PR species take root and may or not remain attached by the scapes to the parental rosette (Coelho et al., 2007).


Figure 1
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  		FIG. 1. Schematic illustration of the three groups of reproductive modes. (A) RS group (rhizomatous seed-producing group): L. curvifolia ‘lanuginosa’. L. curvifolia ‘mucronata’ and L.crassifolia. (B) PR group (pseudoviviparous rooted group): L. spiralis. (C) PCF group (pseudoviviparous canopy-forming group): L. vivipara, forming more than one ramet per scape. (D) PCF group: L. sinuosa, forming one ramet per scape.

 
In L. curvifolia and L. crassifolia the scapes are shorter than those of pseudoviviparous species (Coelho et al., 2007). Flower head production is intense in those species: on average 15 flower heads are produced per ramet in clones of L. curvifolia, and nine flower heads per ramet in clones of L. crassifolia (Coelho et al., 2007). The flower heads generally touch the ground when the scapes become curved at the end of the reproductive season (Coelho et al., 2008). Seeds fall in the proximity of the mother rosettes (Coelho et al., 2008). The ramets form compact clones originating from rhizomes (Fig. 1A) (Coelho et al., 2007). The growth of those clones is centrifugal, thus the ramets at the centre age earlier than the more peripheral ones. When they die, the clones form rings of densely aggregate ramets (Coelho et al., 2007). Rosettes of L. spiralis are morphologically very similar to the rosettes of L. crassifolia. In contrast to L. crassifolia, in L. spiralis the establishment of ramets by way of rhizomes is rare. The formation of a pseudoviviparous propagule in L. spiralis is late; it occurs when flower heads are mature and only when they touch the soil (Fig. 1B). However, in L. vivipara, propagule formation is early, and occurs just after the flower head formation, and most of them are kept suspended by the scapes (Fig. 1C). The flower heads of the suspended plantlets also proliferate, giving rise to new plantlets. This process may repeat itself several times (Giulietti, 1978). In L. sinuosa, pseudoviviparous ramets do not proliferate (Fig. 1D), but, the parental rosette, as is the case in L. vivipara, produces many scapes, and the majority of the ramets also remain suspended by them.

Leiothrix taxa that inhabit different microhabitats exhibit a number of reproductive modes. Some species reproduce sexually and give rise to numerous ramets originating from rhizomes, forming compact clones (e.g. L. curvifolia ‘lanuginosa’, L. curvifolia ‘mucronata’ and L. crassifolia). Populations of L. crassifolia are easily encountered in the Serra do Cipó. Leiothrix curvifolia ‘lanuginosa’, apart from being abundant in other locations where it occurs, has a low regional frequency (Giulietti, 1978). One taxon, L. spiralis, produces few ramets from rhizomes, but produces pseudoviviparous ramets attached to the parental plant. At the other extreme, some taxa do not produce ramets from rhizomes, but produce numerous pseudoviviparous ramets suspended or rooted, forming more dispersed clones (e.g. L. vivipara and L. sinuosa).

Soil sampling
Soil samples were collected using a borer of 5 cm diameter and 10 cm depth from five populations each of L. spiralis, L. curvifolia ‘mucronata’ and L. crassifolia. For L. curvifolia ‘lanuginosa’, L. vivipara and L. sinuosa, soil samples were collected from four populations each. The roots of these taxa are small and fine, thus rooting depth corresponds to the soil sampling depth. In each of the areas, three replicates were employed and a total of 81 soil samples were obtained in 19 areas of occurrence of Leiothrix species (Fig. 2). Analyses of the chemistry, texture and content of organic matter were conducted for each soil sample. The pH was determined potentiometrically in water, CaCl2 and KCl solution (1 : 2·5). The concentration of hydrogen and aluminium ions was determined by titration with NaOH, and extraction was with Ca(OAc)2 (0·5 mol L–1, pH 7·0).


Figure 2
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  		FIG. 2. Sampling points in 19 areas of occurrence of Leiothrix spp. in the Serra do Cipó, located in the southernmost portion of the Espinhaço Mountains, Brazil. Sampled points included areas outside the National Park of the Serra do Cipó, inside the park and in the Environment Protection Area, Morro da Pedreira.

 
The sum of exchangeable bases (SB = {Sigma} K + Ca2+ + Mg2+ cmolc dm–3), base saturation [V = {Sigma} bases x 100/CEC (capacity for cationic exchange) cmolc dm–3], P (mg dm–3) and aluminium saturation (m = 100 x Al3+/CEC) were determined. The content of organic matter was expressed as a percentage (OM = %C x 1·72). The vegetation cover was also expressed as a percentage (see below, ‘Vegetation cover sampling’). The percentages of coarse sand, thin sand, silt and clay were combined in a single variable denominated ‘texture’ = (silt % + clay %)/(coarse sand % + thin sand %). This variable expresses the relative water-holding and nutrient capacities. This measurement seems to be more appropriate in sandy or gravel and shallow soils, since the percentage moisture can provide a seasonal measure related to the rainy or dry season.

Vegetation cover sampling
Vegetation biomass was collected in the same areas as used for soil sampling. However, a natural fire occurred in the region close to one of the populations of L. curvifolia ‘mucronata’ and L. crassifolia and two populations of L. vivipara, and destroyed most of the vegetation. The 72 remaining populations were collected: 15 (5 populations x 3 samples) of L. spiralis, 12 (4 populations x 3 samples) of L. curvifolia ‘mucronata’, L. crassifolia, L. curvifolia ‘lanuginosa’ and L. sinuosa, and nine (3 populations x 3 samples) of L. vivipara. A quadrat of 50 cm2 was used. Within each quadrat, the percentage vegetation cover was categorized. The categories were recorded by estimating the percentage of the quadrat covered by vegetation: low density of vegetation cover – open area <30 %; intermediate density of vegetation cover – sparse area >30 % and <60 %; high density of vegetation cover – densely crowded area >60 %. The vegetation in each area represented cushion and mat plants (mosses), graminoid tussocks, rosette plants and sclerophyllous shrubs belonging mainly to Poaceae, Cyperaceae, Velloziaceae and Xyridaceae. All plant materials were dried for 72 h at 60 °C in a forced draft oven, and then weighed.

Data analyses
A discriminant analysis (Kleka, 1980) was performed to test the effect of the microhabitats (soil type and percentage vegetation cover) on the reproductive mode. The classification matrix was jackknifed to correct for the overestimate of classification success caused by using the data set for both generating discriminant functions and classifying cases. The following edaphic and vegetation cover variables were included in the analysis as continuous variables, and were described above (see ‘Soil sampling’ above).

The total amount of nitrogen in soil samples was also measured using Kjeldahls method. The soil nitrogen content, however, was not a good predictor of microhabitat separation. Factorial analsyses of variance (ANOVAs) were conducted to compare group means (PCF, PR and RS) for each chemical variable.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 
The areas of occurrence of the three reproductive modes showed significant differences for the following variables: H + Al, V, OM, biomass and texture (Table 1). The groups of reproductive modes were distinct among soil variables and vegetation cover, as shown by the discriminant analysis (Table 2 and Fig. 3). The F-statistic, as well as the P-value, was based on Wilks' lambda, generated by discriminant analysis. The high canonical correlations associated with the first two functions (0·954 and 0·513) indicate that they are appropriate for discriminating among groups of reproductive modes. The first function (Factor I) explained 96 % of the total variability of the data and separated soils with larger indexes of aluminium saturation (m) that are more toxic, but present larger vegetation cover (dry biomass). The second function (Factor II) explained only 4 % of the total variability of the data and combined fertility (K + Ca2+ + Mg2+ or SB) with potential acidity (H + Al), i.e. the amount of exchangeable hydrogen ion that can be made free or active in the soil solution by cation exchange, and texture. The low values of SB indicate that all soils sampled are dystrophic or nutrient poor: (1 > SB > 0 cmol charge dm–3). Soil with a clay texture usually can hold a larger amount of water and nutrients.


Figure 3
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  		FIG. 3. Discriminant function analyses of nine environmental variables among three groups of the reproductive modes found in L. vivipara and L. sinuosa (PCF); L. spiralis (PR); and L. curvifolia ‘lanuginosa’, L. curvifolia ‘mucronata’ and L. crassifolia (RS), in soils with different edaphic properties and densities of vegetation cover. ‘m’ represents aluminium saturation. Confidence ellipses (95 %) are drawn around the centroids of each group defined by the discriminant analysis.

 


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  		TABLE 1. Soil and vegetation cover variables (pH, H + Al, SB, V, P, m, OM, vegetation biomass and texture) measured in populations of the three groups of reproductive modes

 


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  		TABLE 2. Canonical discriminant functions – standardized coefficients

 
The jackknife classification matrix results (Table 3) indicated 100 % separation of the PCF group, 56 % separation of the PR group and 72 % of separation of the RS group from the other groups. The total of correctly classified samples was 77 %. The PCF group, that includes L. vivipara and L. sinuosa, occurs in densely crowded areas, usually with vegetation cover of >60 % and <80 % for L. vivipara and of >80 % and <100 % for L. sinuosa. The PR group, represented by a single species (L. spiralis), occurs preferentially in areas with sparse vegetation of >30 % and <60 %, and in sandy soils and more nutrient-poor soils than the RS group. This latter group (L. curvifolia ‘mucronata’, L.crassifolia and L. curvifolia ‘lanuginosa’) also occurs in areas with sparse vegetation of >30 % and <60 %, but in clay and more fertile soils than the PR group. It is common to find, in particular, L. curvifolia ‘lanuginosa’ growing on mat plants (mosses). In these areas, therefore, the soils have more organic matter than the soils where L. spiralis occurs. This is the main factor that separates RS from PR, as shown on the second two axes of the discriminant analysis (Fig. 3).


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  		TABLE 3. Jackknifed classification matrix of the groups of reproductive modes generated from two discriminant functions and percentage of correct classifications for each group

 


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
ACKNOWLEDGEMENTS
 LITERATURE CITED
 
Vegetation cover was the primary determinant in the distribution of Leiothrix taxa with the varying reproductive modes. Some outcrops in the rupestrian grasslands at the Serra do Cipó are constituted just of exposed sand, without any vegetation cover. However, on contiguous outcrops, a dense vegetation cover can be found, dominated by herbaceous vegetation. Thus, the heterogeneity among close or even contiguous microhabitats can indicate the origin of the different reproductive modes within Leiothrix.

The PCF group was separated from the other groups by being found preferentially under densely crowded conditions. The majority of the ramets formed remain supported by the scapes or intertwined with herbaceous leaves (Coelho et al., 2006). Coelho et al. (2005) recorded only one attached plantlet for every 100 supported plantlets, in sites crowded by herbaceous plants. Soils with dense vegetation cover should hold a larger amount of water, and therefore the rosette mothers of L. vivipara attached to the soil can invest in the formation of ramets. The herbaceous vegetation promotes intense shading and greater soil moisture. Ramets of pseudoviviparous plants are photosynthetically active (Lee and Harmer, 1980; Pierce et al., 2003); therefore, each suspended ramet is a photosynthetic unit of a dispersed ‘canopy’ where the light incidence is more intense. To remain suspended by the scapes reaching the top of the herbaceous cover, the ramets can acquire necessary photosynthates and translocate them to the rosettes attached to the soil through their scapes. The development of a canopy-forming strategy in this species was possible because: (a) the formation of pseudoviviparous ramets is early, occurring just after flower head formation; (b) the flower heads of the suspended ramets also proliferate, giving rise to new ramets; and (c) it is difficult for the ramets to touch the ground in sites where there is crowding of herbaceous plants.

The PR reproductive mode occurs preferentially in microhabitats with sparse vegetation. Few pseudoviviparous ramets of L. spiralis grow amongst herbaceous vegetation, which would impede contact of those ramets with the soil. The PR reproductive mode seems to be an efficient strategy for reproduction and ramet spreading, enhancing their chances of survival (Coelho et al., 2006). This guerilla-type expansion strategy, as occurs in L. spiralis, is associated with fast habitat occupancy, spatial exploration (Harper, 1985; Fahrig et al., 1994) and low resource supply (de Kroon and Hutchings, 1995; Ye et al., 2006). A higher spatial spread favoured by the guerilla growth form can be advantageous, if it allows escape of L. spiralis ramets from uncrowded conditions. Therefore, it is likely that vegetation cover exerts selection pressure on the clonal growth form of this plant. As in L. spiralis, the ramets are formed only after the flower head touches the ground; few pseudoviviparous ramets of this species grow amongst herbaceous vegetation, which would be impede contact of those plantlets with the soil (Coelho et al., 2006).

The RS group, comprising L. curvifolia ‘lanuginosa’, L. curvifolia ‘mucronata’ and L. crassifolia, also prevailed in soils with sparse herbaceous vegetation. These species form compact clones (phalanx-type) originating from rhizomes and they produce numerous seedlings originating from seeds (Coelho et al., 2008). Although the rupestrian grassland soils are inherently nutrient poor, rhizomes are usually thought to store buds and resources in order to be able to regenerate in more favourable conditions (Grace 1993; Dong and de Kroon, 1994). Moreover, among ramets of the clone, a continuous flow of mineral nutrients stored in the rhizomes and photosynthates acquired from the ramets can occur. This can ensure the survival and the growth of the ramets and clones in nutrient-poor areas (Humphrey and Pike, 1998). Sackville Hamilton et al. (1987) suggested that sexual reproduction may be more important for clonal plants with a phalanx growth form than for those with a guerrilla growth form, because phalanx plants depend more on seeds for colonization of available microhabitats than guerrilla plants do, which would be in accordance with the present findings, that the seedling recruitment is more important than the clonal recruitment in the RS species studied. Mainly because the rupestrian grasslands soils are inherently nutrient poor, specific microhabitats might have acted as strong selective pressure toward the rhizomatous seed-producing strategy.

Several studies show that the microenvironmental heterogeneity can generate differentiation in the growth form and reproductive modes, and may generate adaptive radiation (Harper et al., 1961; Monasterio and Sarmiento, 1991; Bengtsson et al., 1994; Rauscher, 2002; Verboom et al., 2004; Ellis et al., 2006; Friar et al., 2006). Verboom et al. (2004) showed an association between life history strategy and habitat (native substrate) for eight Ehrharta, a group of grasses that radiated in arid environments of the Cape region of South Africa. Ellis et al. (2006) were studying evolutionary radiation of ‘stone plants’ in Argyroderma, and found four groups of strategies for the plants occupying different edaphic microenvironments. Ecologists have considered that at smaller spatial scales, related species that co-occur in local communities usually exhibit spatial or temporal differentiation in microhabitat (Ackerly et al., 2006). It is at this local scale that the ecological differentiation influences the co-existence of closely related species (Ackerly et al., 2006). Habitat divergence plays a crucial role in sympatric or parapatric speciation, because the evolution of reproductive barriers must somehow take place in the presence of gene flow (Welch and Rieseberg, 2002; Rajakaruna, 2004). Since ecological speciation involves niche shifting in an environmental mosaic (Levin, 2005), microhabitat specialization may thus be an important mechanism maintaining the reproductive modes within Leiothrix. According to Levin (2005), ecological speciation is a more likely venue for major changes within genera. The large number of endemic species within Leiothrix in Serra do Cipó therefore supports the ecological speciation hypothesis. This view is in accord with the proposition of Levin (2003, 2004, 2005). Although speciation by polyploidy is considered more common in plants than in animals, it accounts for only 2–4 % of plant speciation events (Schluter, 2001). Thus, even in plants, most speciation events can be due to divergent natural selection influenced by abiotic or biotic environmental forces (Schluter, 2001; Levin, 2003).

The present results suggest that reproductive mode diversification within Leiothrix occupying different microenvironments probably results from response to fine-scale habitat variation. Moreover, the results suggest a possible role for microhabitat specialization in reproductive mode diversification of Leiothrix and perhaps in its broader radiation in Serra do Cipó. Clonal propagules from rosettes of Leiothrix have extremely local dispersal capabilities, and even seed-producing taxa do not possess mechanisms especially adapted to long-distance dispersal, which is essential to facilitate local adaptation in fine-scale habitat mosaics.

In conclusion, the findings of the present study corroborate the hypothesis that microenvironmental heterogeneity has acted on the reproductive mode variation of Leiothrix, and that habitat mosaics of the rupestrian grasslands have played an important role in the broader radiation of Leiothrix in Serra do Cipó. In addition, it is proposed that ecological speciation, driven by divergent natural selection on reproductive traits and resulting from features of the environment, is an important process in adaptive radiation in this genus, since none of the Leiothrix taxa studied seems able to grow in all available habitats. Such an inability can cause diversification of reproductive strategies in space and may enhance the possibilities for sympatric speciation (Tuomisto, 2006). Finally, this study provides the first speculations about the processes underlying the phenomenal radiation of Leiothrix in the rupestrian grasslands in Brazil, and provides support for the hypothesis of Levin (2003) that changes in the ecological attributes of populations, especially involving habitat and resource utilization, are an important component of speciation in flowering plant lineages.


   ACKNOWLEDGEMENTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGEMENTS
LITERATURE CITED
 
The authors are grateful to Rogério P. Martins, Kátia T. Ribeiro and Adriana T. Salomão for helpful comments on earlier versions of the manuscript; Fábio Scarano and one anonymous reviewer for providing valuable and insightful comments on the manuscript; Goran Neshich for providing valuable comments on the language; and Ana Carolina O. Neves and Flávio Fonseca for their assistance and pleasant company during fieldwork. We also thank the Ibama for permission to work and collect at the Serra do Cipó National Park, and for providing us with accommodation. This investigation was supported by Brazilian Capes and a grant from CNPq (479929/2001-7), whose assistance we gratefully acknowledge.


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 

    Ackerly DD, Schwilk DW, Webb CO. Niche evolution and adaptive radiation: testing the order of trait divergence. Ecology (2006) 87:S50–S61.[Web of Science][Medline]

    Bengtsson J, Fagerström T, Rydin H. Competition and coexistence in plant communities. Trends in Ecology and Evolution (1994) 9:246–250.[CrossRef]

    Coelho FF, Neves ANO, Capelo C, Figueira JEC. Pseudovivipary in two rupestrian endemic species (Leiothrix spiralis and Leiothrix vivipara). Current Science (2005) 88:1225–1226.[Web of Science]

    Coelho FF, Capelo C, Neves ACO, Martins RP, Figueira JEC. Seasonal timing of pseudoviviparous reproduction of Leiothrix (Eriocaulaceae) rupestrian species in Southeastern Brazil. Annals of Botany (2006) 98:1189–1195.[Abstract/Free Full Text]

    Coelho FF, Capelo C, Neves ACO, Figueira JEC. Vegetative propagation strategies of four rupestrian species of Leiothrix (Eriocaulaceae). Revista Brasileira de Botânica (2007) in press.

    Coelho FF, Capelo C, Figueira JEC. Seedlings and ramets recruitment in two rhizomatous species of rupestrian grasslands: Leiothrix curvifolia var. lanuginosa and Leiothrix crassifolia (Eriocaulaceae). Flora (2008) 203. in press.

    Dong M, de Kroon H. Plasticity in morphology and biomass allocation in Cynodon dactylon, a grass species forming stolons and rhizomes. Oikos (1994) 70:99–106.[CrossRef][Web of Science]

    Ellis AG, Weis AE. Coexistence and differentiation of ‘flowering stones’: the role of local adaptation to soil microenviroment. Journal of Ecology (2006) 94:322–335.[CrossRef][Web of Science]

    Ellis AG, Weis AE, Gaut BS. Evolutionary radiation of ‘stone plants’ in the genus Argyroderma (Aizoaceae): unraveling the effects of landscape, habitat, and flowering time. Evolution (2006) 60:39–55.[Web of Science][Medline]

    Fahrig L, Coffin DP, Lauenroth WK, Shugart HH. The advantage of long-distance clonal spreading in highly disturbed habitats. Evolutionary Ecology (1994) 8:172–187.[CrossRef][Web of Science]

    Friar EA, Prince LM, Roalson EH, McGlaughlin ME, Cruse-Sanders JM, De Groot SJ, Porter JM. Ecological speciation in the east maui-endemic Dubautia (Asteraceae) species. Evolution (2006) 60:1777–1792.[Web of Science][Medline]

    Giulietti AM. Os gêneros Eriocaulon L. e Leiothrix Ruhl. (Eriocaulaceae) na Serra do Cipó Minas Gerais, Brasil (1978) São Paulo, Brazil: Universidade de São Paulo. PhD Thesis.

    Giulietti AM, Menezes NL, Pirani JR, Meguro M, Wanderley MGL. Flora de Serra do Cipó, Minas Gerais: caracterização geral e lista de espécies. Boletim Botânico da Universidade de São Paulo (1987) 9:1–151.

    Giulietti AM, Hensold N. Padrões de distribuição geográfica dos gêneros de Eriocaulaceae. Acta Botânica Brasilica (1990) 4:133–158.

    Giulietti AM, Amaral MCE, Bittrich V. Phylogenetic analyses of inter- and infrageneric relationships of Leiotrhix Ruhland (Eriocaulaceae). Kew Bulletin (1995) 50:55–71.[CrossRef]

    Giulietti AM, Harley RM, Queiroz LP, Wanderley MGL, Pirani JR. Caracterização e endemismos nos campos rupestres da Cadeia do Espinhaço. In: Tópicos Atuais em Botânica—TB Cavalcanti, BMT Walter, eds. (2000) Brasília: Embrapa. 311–318.

    Grace JB. The adaptive significance of clonal reproduction in angiosperms: an aquatic perspective. Aquatic Botany (1993) 44:159–180.[CrossRef][Web of Science]

    Harper JL, Clatworthy JN, Mcnaughton IH, Sagar GR. The evolution and ecology of closely related species living in the same area. Evolution (1961) 15:209–227.[CrossRef][Web of Science]

    Harper JL. Module, branches, and the capture of resources. In: Population biology and evolution of clonal organisms—Jackson JBC, Buss LW, Cook RE, eds. (1985) New Haven, CT: Yale University Press. 1–33.

    Humphrey LD, Pyke DA. Demographic and growth responses of a guerilla and a phalanx perennial grass in competitive mixtures. Journal of Ecology (1998) 86:854–865.[CrossRef][Web of Science]

    Klecka WR. Discriminant analysis. Quantitative applications in the social sciences (1980) Thousand Oaks, CA: Sage Publications.

    de Kroon H, Hutchings MJ. Morphological plasticity in clonal plants: the foraging concept reconsidered. Journal of Ecology (1995) 83:143–152.[CrossRef][Web of Science]

    Lee JA, Harmer R. Vivipary, a reproductive strategy in response to environmental stress? Oikos (1980) 35:254–265.[CrossRef][Web of Science]

    Levin DA. The ecological transition in speciation. New Phytologist (2003) 161:91–96.[Web of Science]

    Levin DA. Ecological speciation: the role of disturbance. Systematic Botany (2004) 29:225–233.[CrossRef][Web of Science]

    Levin DA. Niche shifts: the primary driver of novelty within angiosperm genera. Systematic Botany (2005) 30:9–15.[CrossRef][Web of Science]

    Lexer C, Welch ME, Raymond O, Rieseberg LH. The origin of ecological divergence in Helianthus paradoxus (Asteraceae): selection on trangressive characters in a novel hybrid habitat. Evolution (2003) 57:1989–2000.[CrossRef][Web of Science][Medline]

    Menezes NL, Giulietti AM. Campos rupestres Paraíso botânico na Serra do Cipó. Ciência Hoje (1986) 5:38–44.

    Monasterio M, Sarmiento L. Adaptive radiation of Espeletia in the cold andean tropics. Trends in Ecology and Evolution (1991) 6:387–391.[CrossRef]

    Pierce S, Stirling CM, Baxter R. Pseudoviviparous reproduction of Poa alpina var. vivipara L. (Poaceae) during long-term exposure to elevated atmospheric CO2. Annals of Botany (2003) 91:613–622.[Abstract/Free Full Text]

    Ramos CO, Borba EL, Funch LS. Pollination in Brazilian Syngonanthus (Eriocaulaceae) species: evidence for entomophily instead of anemophily. Annals of Botany (2005) 96:387–397.[Abstract/Free Full Text]

    Rajakaruna N. The edaphic factor in the origin of plant species. International Geology Review (2004) 46:471–478.[Web of Science]

    Rauscher JT. Molecular phylogenetics of the Espeletia complex (Asteraceae): evidence from nrDNA ITS sequences on the closest relatives of an andean adaptive radiation. American Journal of Botany (2002) 89:1074–1084.[Abstract/Free Full Text]

    Ribeiro KT, Fernandes GW. Patterns of abundance of a narrow endemic species in a tropical and infertile montane habitat. Plant Ecology (2000) 147:205–218.[CrossRef][Web of Science]

    Sackville Hamilton NR, Schmid B, Harper JL. Life history concepts and population biology of clonal plants. Proceedings of the Royal Society B: Biological Sciences (1987) 232:35–57.[Abstract/Free Full Text]

    Schluter D. Ecological causes of adaptive radiation. American Naturalist (1996) 148:S40–S64.[CrossRef][Web of Science]

    Schluter D. Ecology and the origin of species. Trends in Ecology and Evolution (2001) 16:372–380.[CrossRef]

    Silvertown JW, Dickie JB. Seedling survivorship in natural populations of nine perennial chalk grassland plants. New Phytologist (1980) 88:555–558.[CrossRef][Web of Science]

    Silvertown JW, Wilkin FR. An experimental test of the role of micro-spatial heterogeneity in the co-existence of congeneric plants. Biological Journal of the Linnean Society (1983) 19:1–8.[Medline]

    Tuomisto H. Edaphic niche differentiation among Polybotrya ferns in western Amazonia: implications for coexistence and speciation. Ecography (2006) 29:273–284.

    Verboom GA, Linder HP, Stock WD. Testing the adaptive nature of radiation: growth form and life history divergence in the african grass genus Ehrharta (Poaceae: Ehrhartoideae). American Journal of Botany (2004) 91:1364–1370.[Abstract/Free Full Text]

    Welch ME, Rieseberg LH. Habitat preference between a homoploid hybrid sunflower species, Helianthus paradoxus (Asteraceae), and its progenitors. American Journal of Botany (2002) 89:472–478.[Abstract/Free Full Text]

    Ye XH, Yu FH, Dong M. A trade-off between guerrilla and phalanx growth forms in Leymus secalinus under different nutrient supplies. Annals of Botany (2006) 98:187–191.[Abstract/Free Full Text]


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