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Ecology |
2Department of Botany, University of Cape Town, Private Bag, 7701 Rondebosch, South Africa; 3Institute of Systematic Botany, Zollikerstrasse 107, CH 8008 Zurich, Switzerland; 4Centre for Ecosystem Management, Edith Cowan University, Joondalup 6027, Western Australia
Received for publication November 26, 2003. Accepted for publication April 23, 2004.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: adaptive radiation • allocation • annual • phylogeny • relative growth rate • specific leaf area
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, 2000
). Consequently, adaptively radiated lineages typically have high functional and morphological diversity (Erwin, 1992
; Losos and Miles, 2002
). While phylogenetic data have frequently been used to demonstrate the historical occurrence of radiations (Baldwin and Sanderson, 1998
; Jackman et al., 1999
; Malcomber, 2002
), evidence for the phenotype–environment relationship that is a central aspect of adaptive radiation has been less commonly reported. Classic studies in which such relationships have been quantified include those describing bill shape divergence in Geospiza finches (Schluter and Grant, 1984
) and locomotory divergence in Anolis lizards (Williams, 1972
; Losos, 1990
). In plants, studies relating divergence in floral form to pollination syndrome (Hodges and Arnold, 1995
; Johnson and Steiner, 1997
; Johnson et al., 1998
; Fulton and Hodges, 1999
) have perhaps been most effective in exploring the link between phenotypic divergence and the selective environment.
Although modest in size (23 species), the monophyletic African grass genus Ehrharta Thunb. (excluding E. avenacea) displays greater taxonomic and growth form diversity than do the two lineages to which it is most closely related (Verboom et al., 2003
). Despite being of equal or greater age than Ehrharta, the Australasian-centered two- and four-staminate ehrharteoid lineages contain just five and seven species, respectively. Moreover, while these clades contain only suffrutescent and caespitose perennials, Ehrharta additionally includes bulbous and cormous geophytes, as well as annual species. Recently, we presented data showing that the comparatively high taxonomic diversity of Ehrharta in the Cape region of South Africa is the product of rapid speciation in the summer-arid environment established there during the late Miocene (Verboom et al., 2003
). Our reconstructions indicate that Ehrharta radiated in the arid succulent karoo biome of the Cape winter rainfall zone, with most molecular clock calibrations placing the start of radiation in the range 11.3–4.5 million years ago. In this paper, we investigate whether radiation was adaptive, with divergence in plant form and life history being dictated by adaptation to an environment whose physical (topographic, climatic, and edaphic) diversity has long been considered an important driver of plant speciation (Linder, 1985
; Cowling et al., 1992
).
Growth analysis can provide valuable insights into plant form and function (Lambers and Poorter, 1992
; Lambers et al., 1998
) and is the focus of our work on growth form evolution in Ehrharta. When measured under conditions of non-limiting resources, plant growth provides a measure of a species' inherent growth potential, a parameter that may be central to the strategy it employs to survive and reproduce. Variation in the inherent relative growth rates (RGR) of plants has previously been shown to be tied to several key plant attributes, including resource allocation (Poorter, 1989
; Poorter and Remkes, 1990
; Villar et al., 1998
), leaf architecture (Poorter, 1989
; Poorter and Remkes, 1990
; Garnier, 1992
; Atkin et al., 1996
; Grotkopp et al., 2002
), and reserve storage (Mooney and Chiariello, 1984
; Pate et al., 1990
). Moreover, given the evidence that most plant species flower only when they attain a minimum size (Weiner, 1988
; Schmid et al., 1995
), RGR may influence the age of reproductive maturation. In Pinus, for example, minimum generation time is negatively related to RGR (Grotkopp et al., 2002
). Various workers have also noted a correlation between plant RGR and habitat fertility (Grime and Hunt, 1975
; Poorter, 1989
), suggesting that fast- and slow-growth strategies (or their correlates) are optimally suited to more and less fertile environments, respectively.
The winter rainfall region of the South African Cape comprises a mosaic of edaphic habitats of variable fertility, suggesting considerable scope for the evolution of divergent growth strategies. Sandstones of the Cape Fold Mountain belt (Table Mountain Group) are readily leached and weather to yield sandy, low-pH soils that are deficient in plant nutrients, particularly phosphorus (Lambrechts, 1979
; Specht and Moll, 1983
; Stock and Allsopp, 1992
). In contrast, the shales, mudstones (Malmesbury, Bokkeveld, and Nama Groups), and granites (Cape Granite Suite and Namaqualand Complex) that dominate the coastal platform and intermontane valleys of the southwest, as well as the entire Namaqualand region, weather to produce soils that generally have a much higher pH and are more fertile than those derived from sandstones (Lambrechts, 1979
; Specht and Moll, 1983
). The powerful influence of these differences on vegetation patterns in the region is well documented (e.g., Cowling et al., 1992
).
This paper reports RGR data for eight species of Ehrharta that differ in life history strategy and habitat. These data are used to investigate four questions that bear on the adaptive nature of the radiation of Ehrharta. (1) What is the range of interspecific RGR variation in Ehrharta? (2) Is RGR variation correlated with specific plant traits, such that variation in the latter describes alternative growth strategies? (3) Is interspecific variation in growth strategy related to differences in substrate preference? (4) Is high RGR essential for rapid reproductive maturation such that its evolution represents a key step in the evolution of an ephemeral (annual) life history?
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) and left in a growth room with the following conditions: day—14 h, 25°C, 400–500 µmol · m–2 · s–1 photosynthetic photon flux density (PPFD; sodium, metal halide, and incandescent lamps), 50% relative humidity; night—10 h, 19°C, 50% relative humidity. Seedlings were allowed to adjust to growth room conditions, and an initial harvest (N = 12 seedlings per species, except for E. melicoides where N = 4) was conducted when seedlings had reached the two-leaf stage, this corresponding to a dry mass of about 50 mg. Subsequent harvests were performed 28 d and 56 d after the initial harvest. Harvested seedlings were carefully dried and divided into root, stem (including culms, rhizomes, and leaf sheaths), leaf (lamina only), and, if present, inflorescence (including spikelets and inflorescence branches) fractions. The total leaf area of each plant was measured using a LI-COR Li-3000/3050 portable leaf area meter (LI-COR, Lincoln, Nebraska, USA), and the dry mass of each fraction was determined on a balance precise to 1 mg, after oven-drying at 90°C (about 48 h).
Data analysis
Seedling relative growth and net assimilation rates (NAR) were calculated on an interval basis over the full 56-d experimental period, using the method of Venus and Causton (1979)
to estimate means and standard errors. In addition, RGR was separately calculated for the first 28 d. Because allocation patterns varied considerably between species and during the experiment, leaf (LMR), stem (SMR), and root (RMR) mass ratios were determined for plants sampled at each harvest (harvest time hereafter indicated by a numerical subscript: e.g., LMR56 = leaf mass ratio at 56 d). For plants sampled at day 56, the natural log of inflorescence dry mass (FDM56) and the inflorescence mass ratio (FMR56) were also determined. Specific leaf area (SLA) was determined for plants sampled at each harvest.
Relationships of seedling RGR to other traits were tested by linear regression–correlation analysis using both raw species values (TIPs) and phylogenetically independent contrasts (PICs: Felsenstein, 1985
). We report both sets of values because, while PIC comparisons have been developed to account for phylogenetic trait covariance, TIP comparisons may be more appropriate in studies of adaptive radiation (Harvey and Rambaut, 2000
). Contrasts were calculated with the comparative analysis package Compare 4.5 (Martins, 2003
) using a pared-down version of our recent Ehrharta phylogeny (Verboom et al., 2003
) and assuming branch length uniformity. Because some nodes in this phylogeny were poorly supported (<50%), the effect of alternative resolutions at these points (N = 105 possible topologies) on trait correlations was examined using Cactus 1.13 (Schwilk, 2001
; Schwilk and Ackerly, 2001
). The TIP correlations were evaluated using Statistica 6.0 (Statsoft, Tulsa, Oklahoma, USA).
In addition to pairwise trait comparisons, principal components analysis (PCA) was used to examine whether covariance among the seedling traits (excluding RGR) identifies species groupings that correspond to divergent strategies for seedling growth. The association of such groupings with differences in RGR was tested subsequently by regressing species' PC1 scores against their measured RGRs (PIC and TIP data). Two such analyses were done, one with PCA based on all seedling traits examined (excluding RGR) and a second using only LMR0, LMR56, SMR0, SMR56, SLA28, and FDM56. The latter trait set describes temporal variation in biomass allocation, leaf architecture midway through the experiment, and reproductive maturation and differs from the first two analyses in better ensuring variable independence. The PCA and regression analyses were performed with Statistica 6.0.
To test whether species associated with different soil types differ with respect to growth rate, we compared seedling RGRs of species natively occurring on highly leached sandstone-derived and the more fertile shale-derived soils. Because none of the species included here occupy both shale- and sandstone-derived soils, these categories are distinct; however, several species in each category also occur on granitic soils that typically have intermediate nutrient status. Ehrharta barbinodis, which is exclusive to granites, was omitted from this comparison as it does not fit into either category. A Student t test, as implemented in Statistica 6.0, was used to evaluate the significance of any mean difference.
Historical shifts in substrate preference and seedling RGR were reconstructed using the same phylogeny as that used to calculate PICs. In the case of RGR, this tree was pared down to include only the eight species included in this study, but for substrate, the full set of African species was included. Substrate preferences were reconstructed using Fitch parsimony (all possible reconstructions) as implemented in MacClade 4.0 (Maddison and Maddison, 2000
), while RGR was reconstructed using squared-change parsimony (Huey and Bennett, 1987
; Maddison, 1991
) also as implemented in MacClade 4.0.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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= 0.1 level the relationships of RGR with LMR56, SMR56, and FDM56 remain significant under most (98, 92, and 86%, respectively) alternative arrangements (Table 2).
Principal components analysis of seedling traits
The PCA based on all seedling traits listed in Table 2 (excluding RGR and seed mass) resolves three principal species groups that differ markedly in terms of RGR (Fig. 2). The first of these comprises the two geophytic species (56–80 mg · g–1 · d–1), the second E. melicoides and the branched perennials E. barbinodis and E. thunbergii (84–108 mg · g–1 · d–1), and the third the annual E. longiflora plus the tufted perennials E. erecta and E. calycina (121–130 mg · g–1 · d–1). Based on this analysis, species' PC1 scores are significantly correlated with RGR on the evidence of both TIP- (r = –0.876, df = 6, P < 0.005) and PIC-based comparisons (r = –0.811, df = 6, P < 0.02). This relationship is also evident when PCA is based only on LMR0, LMR56, SMR0, SMR56, SLA28, and FDM56 (TIP: r = –0.824, df = 6, P < 0.02; PIC: r = –0.731, df = 6, P < 0.05). These PIC-based correlations are largely robust to alternative resolution of unsupported nodes. When PC1 scores are based on all seedling traits, 93% of all alternative topologies indicate significant (P < 0.05) correlations with RGR, this decreasing to 83% when PC1 scores are based on LMR0, LMR56, SMR0, SMR56, SLA28, and FDM56 alone.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) generated a diversity of growth forms, a pattern that we investigated by means of a comparative growth experiment. Our data indicate a 2.3-fold range in seedling RGR variation (56–130 mg · g–1 · d–1) among eight Ehrharta species and show that this variation is linked to differences in adult morphology, life history strategy, and habitat.
While the majority of plant growth studies have relied exclusively on single trait comparisons to explore the significance of RGR variation, we followed Grotkopp et al. (2002)
in using multivariate methods to identify growth strategies defined by multiple traits. Many of the single trait correlations that we report are weak, either due to small sample size or because RGR variation is determined by differences in several traits. For example, our data show RGR to be positively associated with SLA in Ehrharta, but this relationship is weaker than has generally been reported (Poorter, 1989
; Poorter and Remkes, 1990
; Garnier, 1992
; Atkin et al., 1996
; Grotkopp et al., 2002
). Nonetheless, our data (Table 2) generally corroborate the widespread observation (e.g., Poorter, 1989
) that variation in plant RGR is more closely tied to differences in leaf architecture and mass allocation than it is to leaf physiology. In Ehrharta, RGR appears to be unrelated to NAR. Also, in contrast to some earlier studies (Grime and Hunt, 1975
; Marañon and Grubb, 1993
; Wright and Westoby, 1999
), we do not detect a correlation between RGR and seed mass.
Principal components analyses based on individual seedling traits reveal the existence of three distinct seedling classes characterized by marked differences in RGR and reproductive maturation rate. At one extreme, E. longiflora, E. erecta, and E. calycina (fast growers) are characterized by a comparatively high RGR and earlier flowering time. During the course of our experiment, these three species all had a pronounced switch in dry mass investment from leaves to stems, the late investment in stems coinciding with inflorescence stalk (culm) production. These were the only species to flower prior to the final harvest. At the other end of the spectrum, E. capensis and E. dura (slow growers) are comparatively slow growing and had a comparatively low level of investment in stems in the later stages of our experiment. Also, these species did not flower. The remaining species, E. melicoides, E. thunbergii, and E. barbinodis (intermediates), form a group that is intermediate between the fast and slow growers with respect to RGR and flowering behavior. Although none of these species produced measurable quantities of inflorescence material prior to the final harvest, at least two initiated bud development.
The contrasting growth strategies identified here at the seedling level are correlated with differences in adult plant form and life history strategy. For example, both the slow growers are starch-storing geophytes that flower reluctantly, typically only after fire (Linder and Ellis, 1990
; Verboom et al., 2002
). On the other hand, the fast growers include the single annual species plus two tufted perennials, each of which is sister to a clade of annual species (Fig. 3) and produces copious amounts of seed annually (G. A. Verboom, personal observation). Seeding and reserve storage offer alternative means for escaping seasonal adversity (see later), and we believe that in Ehrharta the seasonally arid rainfall regime that dominates much of the western Cape has played a key role in driving the evolution of these life forms. The incidence of high RGR in annuals has been noted previously (e.g., Garnier, 1992
; Garnier and Vancaeyzeele, 1994
) and may be understood in terms of selection for rapid reproductive maturation (cf. Grotkopp et al., 2002
), such that a viable seed bank can be produced within a single growing season (Grime, 1979
; Chapin, 1980
; Poorter, 1989
). On the other hand, investment in reserve storage and perennating underground structures facilitates vegetative persistence by fueling respiration during dormancy (e.g., Meyer and Hellwig, 1997
; Wyka, 1999
) and subsequent regrowth (e.g., Kausch et al., 1981
). Observations of seedlings at the start of our growth experiment suggest that formation of these structures begins early in development and may account for comparatively high SMRs in the slower-growing species. Importantly, because reserve storage typically incurs a cost to growth (Mooney and Chiariello, 1984
; Pate et al., 1990
) and early flowering (Verburg and Grava, 1998
), there is a trade-off between seeding and storage strategies, which explains why our data position them at opposite ends of a RGR spectrum. In terms of Grime's (1974
, 1979)
CSR scheme, these are best characterized, respectively, as "ruderal" and "stress-tolerator" strategies. The importance of high RGR as a determinant of invasive potential (Baruch and Bilbao, 1999
; Grotkopp et al., 2002
) is also supported by our data: of the species included here, only those utilizing a high-RGR, ruderal strategy have become widely naturalized outside their native ranges. Ehrharta calycina, E. erecta, and E. longiflora reportedly occur in both North America and Australasia (e.g., Munz, 1974
; Marchant et al., 1987
), with the first of these species posing a particularly serious invasive threat to the native woodlands of southwestern Australia (Panetta and Hopkins, 1991
; Milberg and Lamont, 1995
).
Matching the results of earlier studies (e.g., Grime and Hunt, 1975
; Poorter, 1989
), our data demonstrate a broad correlation between species growth potential and the fertility of the habitats in which they occur. In particular, we found that species native to shale-derived substrates have a significantly higher mean RGR than those native to quartzitic sands, with granitic soils typically accommodating a mix of high- and low- RGR species and having an intermediate mean RGR. Recent attempts to explain the evolution of low growth potentials in plants from nutrient-deficient environments have identified selection for long-lived, low-SLA leaves as being central (Lambers and Poorter, 1992
; Lambers et al., 1998
). In Ehrharta, however, SLA variation alone poorly explains differences in RGR, which suggests that other factors are involved. Instead, we invoke selection on the entire life history to explain the association between RGR and substrate type. In highly seasonal environments such as those found in the western Cape, the success of an annual strategy depends both on an inherent capacity to grow fast and flower early (van Rooyen, 1999
) as well as on nutrient availability being sufficient to ensure that fast growth can be realized. Under nutrient-limited conditions, inherently fast-growing species show RGR depression (e.g., Fichtner and Schulze, 1992
), which may result in delayed flowering. In E. calycina, for example, we have found (G. A. Verboom, unpublished data) substrate type to influence both RGR (50 mg · g–1 · d–1 on sandstone-derived soil vs. 70 mg · g–1 · d–1 on granite-derived soil) and time to flowering (0% plants flowering within 2.5 mo of germination on sandstone-derived soil vs. 90% on granite-derived soil). Thus, we expect an obligate reseeding strategy to fail when soil nutrient status is low and the growing season brief. We therefore reason that the success of such a strategy depends on the availability of suitably fertile substrate. At least in the Cape, annual grasses (including all annual Ehrharta species) tend to be restricted to comparatively fertile habitats, such as those underlain by shale- and granite-derived substrates (Linder and Ellis, 1990
). In nutrient-deficient environments, we expect year-to-year survival to rely more heavily on vegetative persistence structures because rapid seedling development is not fundamental to such a strategy. In this study, all species native to sandstone-based substrates have low RGRs and survive the dry season clonally, apparently by utilizing starch and other reserves stored in their corms (E. capensis), bulbs (E. dura), and buried culm bases (E. thunbergii and E. barbinodis). The role of reserve accumulation and storage in summer drought survival has also been demonstrated in Restionaceae, a family of graminoid plants that dominates the sandy, oligotrophic heathlands of the Cape (Stock et al., 1987
). In Ehrharta, however, a geophytic strategy is not restricted to situations of extreme nutrient deficiency, the arid-land geophyte E. eburnea being endemic to shale- and dolerite-based soils.
Character state reconstruction suggests that low RGR and an association with nutrient-deficient sandstone-derived substrates are ancestral in Ehrharta, the evolution of higher RGRs (>100 mg · g–1 · d–1) coinciding with (or following) a transition to the shale- and granite-derived soils that dominate the Cape coastal platform and the arid Namaqualand region. Within the latter environments, which correspond largely to semi-arid and succulent shrublands (Verboom et al., 2003
), an obligate reseeding (i.e., annual) strategy appears to have arisen twice, both times in lineages characterized by high RGR (Fig. 3). In contrast, low-RGR lineages rely to a greater extent on vegetative survival of underground structures. Based on these patterns, we suggest that the evolution of an annual life history is contingent both upon the availability of suitably fertile substrates, as well as the prior evolution of an inherent capacity to grow and mature rapidly. The role of phylogenetic provenance in determining particular evolutionary outcomes is well documented and is commonly termed phylogenetic constraint (e.g., Price and Carr, 2000
). In Ehrharta, selection for an obligate (i.e., annual) vs. a facultative reseeding strategy (e.g., E. calycina and E. erecta) appears to be driven by moisture availability, with annual clades being able to survive in areas that are drier and that have a shorter wet season (data in Verboom et al., 2003
) than those occupied by their perennial sister species.
The observation that radiation in Ehrharta has been accompanied by the emergence of divergent growth forms suggests that radiation in this genus has been adaptive. This conclusion is reinforced by the observation that growth form variation reflects fundamental differences in the way in which species acquire, invest, and utilize resources and that the evolution of alternative life history strategies depends on features of the extrinsic environments in which they occur (cf. Schluter, 2000
). Here we have argued that substrate heterogeneity played a key role in directing the evolution of alternative strategies for coping with summer drought and so underlies the growth form diversity found in Ehrharta. This underlines our previous assertion (Verboom et al., 2003
) that the onset of a summer-arid climate in the Cape around the end of the Miocene played a central role in stimulating diversification in Ehrharta.
While phylogenetic data are being used increasingly to identify putative adaptive radiations, the selective processes underlying the phenotypic divergence that typically accompanies these events are often poorly explored and remain speculative. In testing the relationship between growth, plant form, and the physical environment within a radiated group, our study addresses this central, yet neglected, aspect of adaptive radiation research. As far as we know, ours is the first explicitly phylogenetic study to investigate plant growth in the context of an adaptive radiation scenario.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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