AOBPreview originally published online on October 7, 2006
Annals of Botany 2006 98(6):1189-1195; doi:10.1093/aob/mcl214
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Seasonal Timing of Pseudoviviparous Reproduction of Leiothrix (Eriocaulaceae) Rupestrian Species in South-eastern Brazil
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: 9 July 2006 Returned for revision: 9 August 2006 Accepted: 31 August 2006 Published electronically: 7 October 2006
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
|---|
• Background and Aims Pseudovivipary is an asexual reproductive strategy. Leiothrix spiralis and L. vivipara (Eriocaulaceae) are pseudoviviparous and occur in rupestrian grasslands, a habitat that has a predominance of sandy and shallow soil, with low water retention. This study aims to investigate the seasonal variation effect of moisture availability on L. spiralis and L. vivipara pseudoviviparous reproduction, and to compare their life history attributes, on rupestrian grasslands in Southeastern Brazil.
• Methods A field study was conducted, including observations concerning pseudoviviparous reproduction and measurement of demographic variables in both L. spiralis and L. vivipara. Soil moisture measurements were also performed to study its effect on the pseudoviviparous reproduction of L. spiralis and L. vivipara.
• Key Results Flower head and plantlet production in L. spiralis were highly correlated with soil moisture. All scapes split off in the drier period, indicating that this is a splitter ramet species. Plantlet mortality was positively correlated with scapes splitting off. The L. vivipara phenophases were not synchronized to the variation in soil moisture, since flower heads and plantlets were produced throughout the year. Moreover, the splitting off of scapes was not observed. In addition, plantlets were formed early, as soon as the flower heads appeared, and remained suspended. Therefore, this species was called ‘canopy forming’.
• Conclusions Seasonal timing of pseudoviviparous reproduction can be a vital component of the successful establishment of plantlets in L. spiralis, considering that in this species the plantlets are formed only after the flower head touches the ground. In contrast, in L. vivipara, the plantlets are formed early, without touching the ground. Moreover, L. spiralis is a splitter ramet species, while L. vivipara is a canopy-forming species. The pseudoviviparous canopy-forming strategy appears to be more advantageous than the splitter ramet strategy, because even under similar soil moisture conditions, the survival of L. vivipara plantlets was greater than that of L. spiralis.
Key words: Leiothrix spiralis, Leiothrix vivipara, pseudovivipary, reproductive strategies, rupestrian grasslands, Serra do Cipó, water scarcity
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
|---|
Pseudovivipary is an asexual reproductive strategy, in which plantlets are produced instead of a sexual reproductive structure (Elmqvist and Cox, 1996). On the other hand, vivipary is a sexual reproduction process in which seeds germinate within the fruit with subsequent embryo development before the seeds are dispersed from the parent plant (Elmqvist and Cox, 1996).
Several authors have argued that pseudovivipary has evolved in response to a short growing season, enabling plants to complete their cycle of offspring production and establishment during the brief periods favourable to growth and reproduction in markedly seasonal environments (Lee and Harmer, 1980; Elmqvist and Cox, 1996; Sarapult'sev, 2001). In such environments, patches that permit growth and survival of a particular species may be sparsely distributed, in both time and space. Under these circumstances, there may be little chance that a seed, through dispersal, will find better growing conditions in a different patch than its parent, reducing the advantages of seed dormancy or seed dispersal (Elmqvist and Cox, 1996). Moreover, the much greater weight of plantlets than seeds bestows a larger nutrient capital on the plantlet (Lee and Harmer, 1980). The success of pseudovivipary in these environments relies on the parental care provided by the parental plant to the offspring until their establishment. Pseudovivipary differs from other forms of clonal growth in that it often replaces sexual seed production and the produced plantlets become independent of the parent plant very rapidly (Bliss, 1971; Elmqvist and Cox, 1996). The rupestrian grasslands of the Serra do Cipó show a marked seasonality and coarse-grained environment, creating an ideal ecological ‘scenario’ for the evolution of pseudovivipary in Leiothrix. Thus, this work shows a diversification on pseudoviviparous reproduction in two Leiothrix species. Rupestrian grassland is a habitat formed by sandy/rocky, nutrient-poor soils in the rocky grasslands, a substrate very harsh for seed germination and seedling establishment. In these habitats formed by rocky outcrops, the production of pseudoviviparous plantlets may compensate for seedling recruitment failures, as occurs in artic-alpine (Sarapult'sev, 2001) and semi-arid climates areas (Salisbury, 1942).
Though pseudovivipary was known in plants belonging to many families (Alliaceae, Liliaceae, Agavaceae, Poaceae, Saxifragaceae and Polygonaceae) (see Elmqvist and Cox, 1996), only Eriocaulaceae was cited in Coelho et al. (2005) and in Figueira and Del Sarto (2006). This family is typical of the Brazilian rupestrian grassland vegetation, and it is especially notable in the mountains of the Espinhaço mountain chain (Giulietti and Hensold, 1990). A particularly large number of species are found in this region and it probably represents the principal centre of genetic diversity for Eriocaulaceae (Giulietti and Hensold, 1990). Both L. spiralis and L. vivipara are pseudoviviparous, although L. spiralis is also rhizomatous. Rhizomes are structures capable of storage of resources (carbohydrates, mineral nutrients and even water), and may serve as a means of avoiding drought and burning (Grace, 1993). Therefore, this mode of clonal growth is important for the maintenance of L. spiralis populations, which are exposed to stressful conditions (drought, fire and lack of nutrients). In spite of their importance, ramets originating from rhizomes are about half the number of those originating from flower heads (Coelho, 2005). The formation of a pseudoviviparous propagule in L. vivipara is early, occurring just after flower head formation (Fig. 1A), and most of the propagules are kept suspended by the scapes (Fig. 1B). However, in L. spiralis, propagule formation is late, occurring when flower heads are mature and only when they touch the soil (Fig. 1C). Thus, L. vivipara and L. spiralis allocate resources for growth while attached to a parental rosette, and for reproduction when these connections are split off and the ramets become independent. Therefore, as in any other clonal life form, pseudoviviparous ramets can become physiologically independent through splitting of the connections. We call these ramets ‘splitters’ (after Eriksson and Jerling, 1990). Others ramets remain physiologically connected, and keep transporting resources among them. These ramets can be called ‘integrators’ (Eriksson and Jerling, 1990).
|
Pseudovivipary in the Eriocaulaceae has not received attention, and this is the first work that compares the pseudoviviparous reproduction in two Leiothrix species. Leiothrix spiralis and L. vivipara are sympatric species that occur in rupestrian grasslands. A comparison of the life history characteristics of closely related species that live in the same, similar or different habitats may yield valuable information regarding the evolutionary history of the group. Moreover, comparing life history traits of closely related species may also provide insights into their ecological diversification (Ackerly and Nyffeler, 2004). In spite of its importance, there are few studies that compare life history traits of congeneric sympatric species (Madeira and Fernandes, 1999). Although sympatric species are exposed to similar selective pressures, the rupestrian grasslands show peculiar characteristics of soil and topography which provide wide environmental heterogeneity and create a large variety of microhabitats. Each microhabitat can exert different kinds of selective pressure, probably favouring a diversification of reproductive modes (Verboom et al., 2004; Winkworth et al., 2005).
Water availability is critical to the timing of reproduction in several herbaceous species in rupestrian grasslands that have a predominance of sandy and shallow soil, with low water retention (Madeira and Fernandes, 1999). In general, habitats formed by rock outcrops are highly stressful for plants (Medina et al., 2006); therefore, drought is a threat to their survival. Some plants avoid drought stress by completing the production of offspring during a period of soil moisture availability, a behaviour often referred to as phenological escape (Rajakaruna et al., 2003). Moreover, under such conditions, sexual reproduction can be reduced or even be replaced by pseudovivipary (Bliss, 1971), since the low water content in the soil can hinder the establishment of seedlings (Pendleton and Meyer, 2004). Vegetative propagules, relative to seedlings, have a greater capacity to survive due to the substantial subsidy of stored carbohydrate reserves from parents (Abrahamson, 1980) and can remain linked to the parental plant through the connections (Harper, 1985).
In the present study, the effect of soil moisture availability on pseudoviviparous reproduction in L. spiralis and L. vivipara was investigated. Based on the premise that water is the main limiting resource in arid and semi-arid ecosystems (Pendleton and Meyer, 2004), as well as in rupestrian grasslands (Madeira and Fernandes, 1999), it was hypothesized that the flowering phenology events, production and establishment of vegetative offspring would occur in the periods of higher soil water availability, for both L. spiralis and L. vivipara, In addition, the following life history attributes were compared between L. spiralis and L. vivipara: plantlet production, scape splitting, plantlet survival and the number of flower heads producing plantlets.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
|---|
Study area and species
This study was conducted in areas of rupestrian grasslands in two locations at Serra do Cipó National Park. The climate is considered mesothermic, with mild summers and a rainy period during the summer, when 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. Rupestrian grasslands occur on quartzite and sandstone outcrops, which form sandy and shallow soils. In this habitat, the diversification of many flowering plant families was possible (Giulietti and Hensold, 1990). Among flowering plants that show a high level of endemism and richness, the Eriocaulaceae stand out (Ramos et al., 2005). Leothrix spiralis individuals were located at 19°15'33''S and 43°31'42''W; and L. vivipara at 19°17'12''S and 43°35'13''W.
Leiothrix individuals are morphologically characterized by their habit of growing in a rosette from which scapes with flower head-type inflorescences appear (Giulietti, 1978). The scapes in pseudoviviparous species function like stolons when the flower heads of rosettes proliferate, giving rise to plantlets (Coelho et al., 2005). Most of the species show both sexual reproduction and clonal growth. However, in L. spiralis and L. vivipara, seed production is rare (Giulietti, 1978). Especially in L. vivipara there is a reduction in the number of flowers per flower head; the greater central portion of the flower head is occupied by leaves (Giulietti, 1978). In L. spiralis, field observations have been unable to detect seedlings of sexual origin and it is thought that population regeneration occurs mainly through clonal propagation (Coelho, 2005). Low seedling recruitment in pseudoviviparous taxa is common in habitats with unfavourable conditions for seed germination and establishment (Lee and Harmer, 1980; Bauert, 1993; Miao et al., 1998). Leiothrix vivipara occurs in dry, sandy soil, sometimes densely covered by a herbaceous layer. The majority of the plantlets formed remain supported by the scapes or are intertwined with herbaceous leaves. Coelho et al. (2005) recorded only one attached plantlet for every 100 supported plantlets, in sites where there was crowding of herbaceous plants. 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. spiralis, the plantlets are formed late, only after the flower heads touch the ground. A few rosettes grow amongst herbaceous plants, even if these are sparse. In addition, practically all the plantlets formed are attached to the ground (Coelho et al., 2005).
Measurement of demographic variables
It is common to find rosettes of L. vivipara in densely crowded conditions (Fig. 1A), which is often an obstacle to obtaining demographic data. Therefore, for this species, 50 rosettes were sampled in a 1·2 m2 plot. For L. spiralis, 100 rosettes were sampled. However, due to their rosette dispersion, it was necessary to establish two 1 m2 plots, containing 50 rosettes each. All rosettes were marked with numbered aluminium tags, so they could be followed monthly during the two rainy seasons from December 2003 to December 2004.
For each individual plant of both species, the following life history components were measured monthly: (a) the number of flower heads per parental rosette; (b) the number of propagules (plantlets) originating from flower heads per parental rosette; and (c) the number of splitter plantlets. For each plot, the following data were recorded: (a) the number of episodes of production of flower heads (the frequency of flowering in 13 months); (b) the number of episodes of plantlet production (the frequency of plantlet production in 13 months); and (c) the number of surviving plantlets.
Measurement of soil moisture
At monthly intervals, from December 2003 to December 2004, soil samples were collected at three random points in the vicinity of the L. spiralis plots. The same procedure was employed for L. vivipara from December 2003 to October 2004. Soil samples were collected monthly until October, since in November a natural fire occurred in the region close to the L. vivipara population, and destroyed most of the rosettes. The samples were obtained with the help of a steel cylindrical object of 2·0 cm diameter and 5·0 cm depth. Both L. spiralis and L. vivipara roots are small and fine, thus the rooting depth corresponds to the soil sampling depth. In the laboratory, samples were weighed prior to drying them, and were then dried at 60 °C for at least 48 h, and weighed again. The amount of water in the soil was determined using the following equation: [soil fresh weight (FW) – soil dry weight (DW) = gwater in the soil]. Data are presented as percentage water content: (FW – DW/FW x 100).
Data analysis
To test the prediction about the synchronization of the plants' phenological events to water availability in the soil, Spearman correlations for soil moisture in relation to the number of flower heads, the number of plantlets produced, plantlet fixation in the soil, the number of dead plantlets and the scapes splitting off were used. In addition, the effect of scapes splitting off on plantlet mortality was also tested using Spearman correlation.
The frequency of plantlet production, the scapes splitting off and the plantlet survival in L. spiralis and L. vivipara were compared using the 
2 test. It was not necessary to apply any statistical test to verify differences in the proportion of plantlets rooted vs. plantlets suspended between L. spiralis and L. vivipara, because no suspended plantlets were found in L. spiralis. Likewise, no splitter plantlets were found in L. vivipara. Mean values for soil water content (gwater) in the L. spiralis and L. vivipara plots were compared applying the Mann–Whitney U-test (Sokal and Rohlf, 1981).
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
|---|
Flower head production in L. spiralis was highly correlated with soil moisture (r = 0·85; P < 0·001; n = 349; Fig. 2A). The plantlet formation from flower heads started in February, in the rainy period, and ended in April, at the beginning of the dry season, when the soil was still moist (11·5 %) (Fig. 2A). Plantlet fixation occurs until the end of the rainy season, when the soil is still moist. From the 349 flower heads formed, 183 produced plantlets and, of these, 67 survived until November (Fig. 2B). In contrast, in L. vivipara, flower heads and plantlet production occurred during the whole year (Fig. 3A). In addition, plantlets are formed early, as soon as the flower heads appear. From December to March and from August to October (Fig. 3B), most of the flower heads had already produced plantlets in the sampling period. In December, January and February, rain was heavy and a shallow pool of water formed inside the L. vivipara plot. However, in March, the percentage of water decreased to 14·7% and increased to 20% in May (Fig. 3). The variation in water availability in the soil in the L. vivipara plot was higher than in the L. spiralis plot. However, the mean values of the soil water content (g) did not differ statistically between the plots (U = 61; P = 0·9). In this species, most of the plantlets were suspended (74 %; n = 333) and the remainder (26 %; n = 333) were fixed in the soil (Fig. 3B). Plantlet fixation in this species occurred during the whole year.
|
|
The results show that L. spiralis presents scapes splitting off. The splitting off of their scapes started in June, which coincided with a small decrease in the amounts of water in the soil (Fig. 4). In September, the soil contained only 0·7 % water and, due to this marked decrease in moisture, practically all scapes split off (r = –0·73; P = 0·01; Fig. 4). Plantlet mortality was positively correlated with scapes splitting off (r = 0·82; P = 0·001; Fig. 4). Plantlets of L. spiralis are linked to the parental plant for about 4 months. A month after the beginning of the dry season, 50 % of the scapes had been fragmented, and splitting off was 100 % in the drier period (Fig. 4). In contrast to L. spiralis, L. vivipara did not present splitter plantlets (Table 1), and plantlet mortality was not associated with the percentage of water in the soil, both for fixed (r = –0·07; P = 0·8) and for suspended plantlets (r = –0·34; P = 0·3) (Fig. 5).
|
|
|
These results indicate that L. spiralis and L. vivipara differ in their reproductive strategies. Leiothrix spiralis is a species with splitter strategy, in which plantlets do not remain attached to the parental rosette. Leiothrix vivipara, on the other hand, is a species with a ‘canopy-forming’ strategy, in which the majority of the formed plantlets remain suspended without touching the ground and are always attached to the parental rosette. The frequency of rooted plantlets was higher in L. spiralis than in L. vivipara (Table 1). However, the total number of plantlets produced (rooted plantlets + suspended plantlets) was higher in L. vivipara (Table 1). The percentage of flower heads producing plantlets is also higher in L. vivipara; about 100 % of the flower heads produced plantlets, in contrast to the percentage in L. spiralis, in which about half of them produced plantlets (Table 1;
= 250; P < 0·0001). Moreover, the proportion of plantlets established was significantly higher in L. vivipara than in L. spiralis. Of the 86 plantlets recruited in L. vivipara, 55 (63·9 %) survived, while of the 183 plantlets recruited in L. spiralis, 67 (36·6 %) survived ( = 18·9; P < 0·001). The results suggest that the differential survival between plantlets of L. vivipara and L. spiralis may be due to the maintenance of the connections in the L. vivipara plantlets, since there was no difference in the soil water content between L. vivipara and L. spiralis plots. |
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
|---|
Both reproduction and survival of plants are directly affected by water availability in the soil where they grow (Crawford, 1990). In the rupestrian grasslands of Serra do Cipó, water is available only during a part of the year (Madeira and Fernandes, 1999), influencing the phenology of species that grow there.
The seasonal timing of plantlet production can be a vital component of successful plantlet establishment, considering that in L. spiralis the plantlets are formed only after the flower head touches the ground. This species appears to use the strategy referred to as phenologial escape, by completing its life cycle avoiding water scarcity. The water shortage leaves the soil more compact, making the penetration of the fine roots of young plantlets more difficult. The fact that plantlets were produced at the end of the rainy season facilitated their fixation in the soil, which was still moist. This guaranteed their establishment since, after the end of the rains, when the soil becomes more compact, fixation is more difficult. The fact that none of the plantlets died while connected to the parental plant suggests a physiological integration between plantlets and parental rosettes, and that the scapes function as stolons. During the dry season, the scapes become very fragile and can easily split off, especially because of the desiccation (ACO Neves, UFMG, Brazil, unpubl. res.). In the rainy season, on the other hand, the scapes are flexible and hardly split (F. F. Coelho, UFMG, Brazil, pers. comm.). Leiothrix spiralis then can be called a ramet splitter species, because each plantlet becomes independent after establishment. The ‘bottleneck’ of survival in L. spiralis seems to be located during the transition from the scapes splitting off and the beginning of the rainy season. Integration among ramets may be advantageous to allow the photoassimilates to flow from the parental ramet to the daughters (Marshall, 1990). However, according to Pitelka and Ashmun (1985), integration among ramets becomes unfavourable if the environment is very stressful, because it reduces the tendency of the parental rosette to support sinks in integrated ramet systems. In such environments, the metabolic cost of maintaining plantlets can be high for the parental rosette (Pitelka and Ashmun, 1985). If the probability of a ramet dying is dependent on the fate of other ramets in the same genet, the splitting of the connection will minimize the risk of genet extinction (Cook, 1979; Oborny and Kun, 2002).
In contrast to L. spiralis, L. vivipara ramets did not split off and the parental rosettes did not produce flower heads and plantlets only during the rainy season; instead, this occurred during the 11 months of this study. During the dry season, the rosettes lose most outlying leaves, and only the centre ones remain (Coelho, 2005). Thus, the resource allocation for growth is not necessary, and all available resources can be allocated for reproduction. Vegetative propagules were produced throughout the year and most of them remained suspended by the scapes. In densely crowded conditions, the scapes remain interwined with herbaceous leaves (Coelho et al. 2005), and the numerous plantlets produced gain support to reach the top of the herbaceous cover. Because of this growth form, in which vegetative propagules remain attached to the parental rosette suspended by the scapes, L. vivipara was described as a pseudoviviparous canopy-forming species (Coelho, 2005). Plantlets of pseudoviviparous plants are photosynthetically active (Lee and Harmer, 1980; Pierce et al., 2003), therefore each suspended plantlet 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 plantlets can acquire the necessary photosynthates and translocate them to the rosettes attached to the soil through their scapes. Thus, the suspended plantlets function as photosynthesizing leaves, the principal source of photoassimilates (in the source–sink transport system) (Marshall, 1990). Then, even under similar environmental conditions to those of L. spiralis, L. vivipara did not sever their connections, probably due to the low maintenance cost. Integration is suggested to occur when resource-sharing benefits outweigh the cost for the ramet to stay interconnected (Pitelka and Ashmun, 1985).
This diversification of the pseudoviviparous strategy might have resulted from specific characteristics of their microhabitats, especially of the herbaceous vegetation cover. Some outcrops in the rupestrian grasslands at the Serra do Cipó are just constituted of exposed sand, without any vegetation cover. However, on contiguous outcrops, a dense vegetation cover can be found, dominated by herbaceous plants. Thus, the heterogeneity among close or even contiguous microhabitats can indicate the origin of the different pseudoviviparous modes in L. spiralis and L. vivipara. The canopy-forming species occurs preferentially in densely crowded conditions, while the species producing rooted plantlets occurs preferentially under low herbaceous density. Few pseudoviviparous plantlets of L. spiralis grow amongst herbaceous vegetation, which would be an impediment for the contact of those plantlets with the soil (Coelho et al. 2005).
In addition, no seedlings from either species were found during the study period. Pseudovivipary seemed to represent the mechanism that leads to the survival and maintenance of the study populations, which grow in soils poor in nutrients and water. In areas formed by dry and sandy soils, sexual reproduction becomes unfavourable, because the substrate is very harsh for seed germination and seedling establishment (Scarano, 2002; Sampaio et al., 2005). Although the ability for seed dispersal is extremely important in plant demography (Harper and White, 1974), the probability of seedling establishment is normally low and frequently restricted to windows of opportunity in space and time (Cook, 1985). In contrast, vegetative propagules have the advantage of staying connected to the parental plant at least during the first stages of their lives. This increases their survival probability in environments with extreme conditions (Harper, 1985). Moreover, vegetative propagules have a much greater biomass than seedlings and become adults much faster, a fact that allows establishment rates higher than those of seedlings (Pan and Price, 2002).
In conclusion, L. spiralis presented synchrony in phenological events as a function of the percentage of soil moisture, which influenced the measured life history traits. Moreover, it corresponds to a splitter ramet strategy, because each plantlet became independent after establishment. In contrast, L. vivipara presented neither synchrony of phenological events nor splitting of connections. Instead, it presented as a pseudoviviparous canopy-forming species, because each suspended plantlet can act as the leaves in a canopy tree. This strategy appears to be more advantageous than the splitter ramet strategy because, even under similar soil moisture conditions, the survival of L. vivipara plantlets was greater than that of L. spiralis. Moreover, when the two species are found in the same microhabitat, the population of L. vivipara is usually greater than that of L. spiralis. Thus, the pseudoviviparous canopy-forming strategy seems to minimize the impact of the scarcity of water in the soil on the measured life history traits in L. vivipara.
|
ACKNOWLEDGEMENTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
|---|
We thank Fábio R. Scarano, Kátia T. Ribeiro and Frederico S. Lopes for their helpful comments on an earlier version of the manuscript, two anonymous referees for reviewing this manuscript, Leonardo C. Ribeiro for field assistance, and Célia Goodwin for revision of the English. We also thank the IBAMA for permission to work at the Serra do Cipó National Park, and for providing us with accommodation. This investigation was supported by Brasilian CAPES and a grant from CNPq (479929/2001-7), whose assistance we gratefully acknowledge.
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
|---|
-
Abrahamson WG. (1980) Demography and vegetative reproduction. In Solbrig OT (Ed.). Demography and evolution in plant population(University of California Press, Los Angeles) pp. 90–106.
Ackerly DD and Nyffeler R. (2004) Evolutionary diversification of continuous traits: phylogenetic tests and application to seed size in the California flora. Evolutionary Ecology 18:249–272.[CrossRef]
Bauert MR. (1993) Vivipary in Polygonum viviparum: an adaptation to cold climate? Nordic Journal of Botany 13:473–480.
Bliss LC. (1971) Artic and alpine life cycles. Annual Review of Ecology and Systematics 2:405–438.
Coelho FF. (2005) Variação nas histórias de vida de Leiothrix na Serra do Cipó. (Universidade Federal de Minas Gerais, Brazil) MG, PhD Thesis.
Coelho FF, Neves ANO, Capelo C, Figueira JEC. (2005) Pseudovivipary in two rupestrian endemic species (Leiothrix spiralis and Leiothrix vivipara). Current Science 88:1225–1226.
Cook RE. (1979) Asexual reproduction: a further consideration. American Naturalist 113:769–772.[CrossRef]
Cook RE. (1985) Growth and development in clonal plant population. In Jackson JBC, Buss LW, Cook RE (Eds.). Population biology and evolution of clonal organisms(Yale University Press, New Haven) pp. 259–296.
Crawford RMM. (1990) Studies in plant survival: ecological case histories of adaptation to adversity(Blackwell Scientific Publications, Oxford).
Elmqvist T and Cox PA. (1996) The evolution of vivipary in flowering plants. Oikos 77:3–9.
Eriksson O and Jerling L. (1990) Hierarchical selection and risk spreading in clonal plants. In van Groenendael J and de Kroon H (Eds.). Clonal growth in plants: regulation and function(SPC Academic Publishing, The Hague) pp. 79–94.
Figueira JEC and Del Sarto ML. (2006) Clonal growth and dispersal potential of Leiothrix flagellaris (Eriocaulaceae) in the rocky grassland of Southeastern Brazil. Revista Brasileira de Botânica in press.
Giulietti AM. (1978) Os gêneros Eriocaulon L. e Leiothrix Ruhl. (Eriocaulaceae) na Serra do Cipó Minas Gerais, Brasil(Universidade de São Paulo, São Paulo, Brazil) PhD Thesis.
Giulietti AM and Hensold N. (1990) Padrões de distribuição geográfica dos gêneros de Eriocaulaceae. Acta Botânica Brasilica 4:133–158.
Grace JB. (1993) The adaptive significance of clonal reproduction in angiosperms: an aquatic perspective. Aquatic Botany 44:159–180.
Harper JL. (1985) Module, branches, and the capture of resources. In Jackson JBC, Buss LW, Cook RE (Eds.). Population biology and evolution of clonal organisms(Yale University Press, New Haven) pp. 1–33.
Harper JL and White J. (1974) The demography of plants. Annual Review of Ecology and Systematics 5:419–463.
Lee JA and Harmer R. (1980) Vivipary, a reproductive strategy in response to environmental strees? Oikos 35:254–265.
Madeira JA and Fernandes GW. (1999) Reproductive phenology of sympatric taxa of Chamaecrista (Leguminosae) in Serra do Cipó, Brazil. Journal of Tropical Ecology 15:463–479.[CrossRef]
Marshall C. (1990) Source–sink relations of interconnected ramets. In van Groenendael J and de Kroon H (Eds.). Clonal growth in plants: regulation and function(SPC Academic Publishing, The Hague) pp. 23–42.
Medina BMO, Ribeiro KT, Scarano FR. (2006) Plant–plant and plant–topography interactions on a rock outcrop high in Southeastern Brazil. Biotropica 38:27–34.
Miao SL, Kong L, Lorenzen B, Johnson RR. (1998) Versatile modes of propagation in Cladium jamaicense in the Florida Everglades. Annals of Botany 82:285–290.
Oborny B and Kun A. (2002) Fragmentation of clones: how does it influence dispersal and competitive ability? Evolutionary Ecology 15:319–346.[CrossRef][Medline]
Pan JJ and Price JS. (2002) Fitness and evolution in clonal plants: the impact of clonal growth. Evolutionary Ecology 15:583–600.[CrossRef][Medline]
Pendleton BK and Meyer SE. (2004) Habitat-correlated variation in blackbrush (Coleogyne ramosissima: Rosaceae) seed germination response. Journal of Arid Environments 59:229–243.[CrossRef]
Pierce S, Stirling CM, Baxter R. (2003) Pseudoviviparous reproduction of Poa alpina var. vivipara L. (Poaceae) during long-term exposure to elevated atmospheric CO2. Annals of Botany 91:613–622.
Pitelka LF and Ashmun JW. (1985) Physiology and integration of ramets in clonal plants. In Jackson JBC, Buss LW, Cook RE (Eds.). Population biology and evolution of clonal organisms(Yale University Press, New Haven) pp. 399–435.
Rajakaruna N, Bradfield GE, Bohm BA, Whitton J. (2003) Adaptive differentiation in response to water stress by edaphic races of Lasthenia californica (Asteraceae). International Journal of Plant Science 164:371–376.[CrossRef]
Ramos CO, Borba EL, Funch LS. (2005) Pollination in Brazilian Syngonanthus (Eriocaulaceae) species: evidence for entomophily instead of anemophily. Annals of Botany 96:387–397.
Salisbury EJ. (1942) Reproductive capacity of plants(Bell, London).
Sampaio MC, Picó FX, Scarano FR. (2005) Ramet demography of a nurse bromeliad in Brazilian restingas. American Journal of Botany 92:674–681.
Sarapul'tsev IE. (2001) The phenomenon of pseudoviviparity in alpine and arctomontane grasses (Deschampsia Beauv, Festuca L, and Poa L.). Russian Journal of Ecology 32:188–196.
Scarano FR. (2002) Structure, function and floristic relationship of plant communities in stressful habitats marginal to the Brazilian Atlantic rainforest. Annals of Botany 90:517–524.
Sokal RR and Rohlf FJ. (1981) Biometry(Freeman, San Francisco).
Verboom GA, Linder HP, Stock WD. (2004) Testing the adaptive nature of radiation: growth form and life history divergence in the African grass genus Ehrharta (Poaceae: Ehrhartoideae). American Journal of Botany 91:1364–1370.
Winkworth RC, Wagstaff SJ, Glenny D, Lockhart PJ. (2005) Evolution of the New Zealand mountain flora: origins, diversification and dispersion. Organisms Diversity and Evolution 5:237–247.[CrossRef]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  F. F. Coelho, C. Capelo, L. C. Ribeiro, and J. E. C. Figueira Reproductive Modes in Leiothrix (Eriocaulaceae) in South-eastern Brazil: The Role of Microenvironmental Heterogeneity Ann. Bot., February 1, 2008; 101(3): 353 - 360. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Flowering Newsletter bibliography for 2006 J. Exp. Bot., April 20, 2007; (2007) erm028v2. [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||