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Introduction

  1. Top of page
  2. Introduction
  3. Seedling growth rates
  4. Components of growth rate
  5. Plant hydraulic conductance and architecture
  6. The evolutionary ghost of past atmospheres
  7. Refugia from competition
  8. Plant–soil associations
  9. Disturbance, climate change and biogeographic patterns
  10. Conclusions and future research directions
  11. Acknowledgements
  12. References

What features of angiosperms have enabled them to dominate the biomass of much temperate and tropical vegetation despite the high productivity of many adult gymnosperms, especially conifers? Bond (1989) argued that slow-growing gymnosperm juveniles are poor competitors with angiosperms regenerating in forest gaps and other well lit, well watered habitats. Consequently, gymnosperms are restricted to areas where growth of angiosperm competitors is reduced, for example by cold or nutrient shortages. A historical implication of Bond's hypothesis is that angiosperms overran gymnosperms during the Cretaceous and Tertiary by invading their regeneration niche.

Bond's (1989)‘slow seedling’ hypothesis has considerable appeal because it seeks to explain major phytogeographical patterns and evolutionary trends in terms of observable vegetative traits. Data suitable for testing Bond's plausible arguments were then quite limited, and what was proposed as hypothesis has often been cited as fact in recent reviews of conifer biology (Enright & Hill 1995; Richardson 1998; Smith & Hinckley 1995). Studies of large-scale trends may be exploratory (generating hypotheses) or sceptical (testing hypotheses); both modes of inquiry are essential and indeed complementary (McShea 1998). This review emphasizes the sceptical mode, and aims to test some of the main premises and generalizations of Bond's (1989) slow seedling hypothesis. Although Bond's arguments embraced the polyphyletic gymnosperms, relevant data are mostly limited to the monophyletic conifers, also constraining this review.

A key element of Bond's (1989) hypothesis is that conifer seedlings cannot match the fastest growth rates of angiosperms. This is supported here for early-succession angiosperms, but not for late-succession, north-temperate trees. Few comparative data are available from regions where both angiosperms and conifers have long-lived leaves, a trait that is correlated with reduced seedling growth rate (Reich 1998). Whether Bond's hypothesis can explain the rarity of conifers and gymnosperms in lowland tropical forests therefore remains uncertain.

Bond (1989) attributed the slow growth of juvenile conifers to an inefficient transport system and a low maximum leaf photosynthetic rate, which together prevent conifers from achieving high productivity until sufficient leaf area accumulates. Here a review of hydraulic conductances of temperate and tropical trees suggests that conifers and angiosperms have similarly adequate transport capabilities at the whole-plant level, despite the simple leaf venation and narrow xylem conduits of conifers. Data for temperate trees show that both deciduous and evergreen angiosperms have higher maximum photosynthetic rates (mass basis) than conifers. This difference disappears after accounting for leaf longevity, suggesting that conifers and angiosperms do not differ in their biochemical efficiency of energy conversion, and leaving uncertain the relative photosynthetic capacities of long-lived, tropical angiosperm and gymnosperm leaves.

An oft-repeated generalization is that conifer-dominated vegetation is mainly restricted to nutrient-poor or wet soils, or cold areas, which Bond (1989) interpreted as the outcome of the competitive inferiority of gymnosperms in the regeneration niche. It is useful to distinguish between situations where a species is dominant because of traits for tolerating the environment as opposed to traits for suppressing neighbours; the former type of dominance could occur in the absence of competition (Keddy 1989). The tendency of conifers to dominate at high altitudes and latitudes has numerous exceptions (Sprugel 1989) and could be explained by tracheids being more resistant than vessels to freezing-induced embolization (Sperry & Sullivan 1992; Wang, Ives & Lechowicz 1992). Occupation of wet soils by trees is strongly linked to tolerance of anoxia (Kramer & Boyer 1995). A comprehensive understanding of the biogeography of angiosperms and gymnosperms will need to consider their entire distributions. In the absence of experiments to separate the effects of tolerance and competition, however, this review is restricted to biogeographical patterns on uplands at moderate elevations and latitudes where Bond's (1989) arguments are most likely to apply.

The supposed association of conifers with poor (sandy) soils is shown to be an oversimplification, in at least one case, by quantitative analysis of presettlement forests and soil fertility in a northern cold-temperate region. Although the impression of angiosperm dominance on productive sites still requires confirmation, it is likely that there is a probability gradient of angiosperm dominance paralleling gradients of site productivity.

Seedling growth rates

  1. Top of page
  2. Introduction
  3. Seedling growth rates
  4. Components of growth rate
  5. Plant hydraulic conductance and architecture
  6. The evolutionary ghost of past atmospheres
  7. Refugia from competition
  8. Plant–soil associations
  9. Disturbance, climate change and biogeographic patterns
  10. Conclusions and future research directions
  11. Acknowledgements
  12. References

Bond (1989) emphasized that the angiosperm innovation of the herbaceous habit enabled more effective exploitation of ephemeral habitats, including regeneration gaps in forests, than the woody habit which all gymnosperms possess. Being short-lived, such habitats account for only a small proportion of extant vegetation. In all studies, tree seedlings have slower net assimilation rates and relative growth rates (RGR) than non-woody species (Grime & Hunt 1975; Hunt & Cornelissen 1997a; Poorter 1989). With time, however, perennials become more effective competitors as they accumulate reserves and a deeper root system (Poorter 1989; Schulze 1982). If disturbance does not eliminate competition from trees, whether angiosperms or conifers, their longevity and height enable them to shade and eventually kill herbs and shrubs (Bazzaz 1996; Scholes & Archer 1997; Schulze 1982). Plants with more access to light also construct more roots and are better able to forage for nutrients, so simple traits such as height and crown diameter substantially account for measured competitive ability (Keddy 1989). For these ecological reasons, and because it is uncertain whether the absence of gymnosperm herbs represents a chance failure to evolve or constraints imposed by the gymnosperm bauplan, comparison of growth rates between conifers and angiosperms is here restricted to shared life forms.

The largest suitable data set (Cornelissen, Castro Diez & Hunt 1996) showed that RGRs of seedlings of four conifer genera (and some angiosperms) were less than the lower regression confidence limit estimated for 16 angiosperm tree genera (Fig. 1). Correction for initial seed mass by regression analysis is justified by its inverse relationship to RGR (Grubb 1998; Reich et al. 1998b), but the outcome of competitive interactions will be determined by the RGRs of the actual contestants, regardless of their seed size. There was no significant difference between angiosperms and conifers in a straightforward comparison of their RGRs (pooled variance t = 1·41, P = 0·18).

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Figure 1. Relationship between mean relative growth rate (sensu stricto) of temperate angiosperm (○) and conifer (▴) tree seedlings and (ln-transformed) mean seed dry mass. Both variables were averaged by genus when more than one species was measured. A least-squares, linear regression (solid line) and 95% confidence interval (dashed lines) were fitted to the angiosperm data only. Most angiosperm species were deciduous and most conifers were evergreen. The slowest-growing angiosperms (RGR < 0·1 day−1) were mid- and late-succession species (Andrew Cameron, personal communication). Data from Appendix 1 of Cornelissen et al. (1996).

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Consistent with Bond's (1989) generalizations, only angiosperms achieved the fastest RGRs (Fig. 1). However, all seven trees (Fraxinus excelsior, Malus sylvestris, Alnus glutinosa, Sorbus aucuparia, Ulnus glabra, Betula pendula and Salix caprea) that exceeded the maximum RGR of conifers are species of early succession (Andrew Cameron, personal communication). If these results are representative, then Bond's (1989) arguments could explain the dominance of angiosperms in early-succession vegetation. For example, Shainsky & Radosevich (1992) demonstrated experimentally that the initial height advantage of the early succession species Alnus rubra (Red Alder), sustained by its faster height growth rate, was probably the most important factor determining its competitive superiority to Pseudotsuga menziesii (Douglas Fir). However, Bond's arguments might be less relevant to late-succession stages, even on productive sites, where canopy species of both angiosperms and conifers have slower seedling RGRs (Fig. 1).

Bond's (1989) arguments comparing the competitive abilities and ecophysiological characteristics of conifers and angiosperms parallel those developed previously for deciduous and evergreen angiosperms (Goldberg 1982 and references therein). He would contend that deciduousness is difficult for gymnosperms to evolve and maintain because of their poor transport capacity (Bond 1989 and personal communication). The ecophysiological and morphological traits that affect RGR are strongly associated with leaf life span, which in turn is partly controlled by the length of the growing season (Eamus 1999; Kikuzawa 1995; Reich 1998). Incorporation of seasonal effects into a cost–benefit model of leaf longevity predicted a bimodal geographical (latitude and altitude) distribution of evergreenness (Kikuzawa 1995). This matches the distribution of conifers, except at low latitude where evergreen angiosperms strongly dominate (Reich et al. 1995) – a biogeographical pattern which it is important to explain.

Deciduous woody species grow more quickly than evergreen ones (Cornelissen et al. 1996; Reich 1998), but the effect of leaf habit could not be tested with the data in Fig. 1 because nearly all angiosperms were deciduous and nearly all conifers were evergreen. This partly indicates sampling bias, but is more a reflection of real phenological differences between conifers and angiosperms in cold-temperate regions. After accounting for differences in leaf life span by regression analysis, height-growth rates of temperate conifer and angiosperm saplings were similar (Reich et al. 1995). The RGRs of temperate conifer seedlings tended to be greater than those of tropical evergreen angiosperms (Reich 1998). In a comparison of evergreen seedlings of the main canopy species of a Tasmanian cool-temperate rain forest, the three gymnosperms had slower RGRs than the three angiosperms (Read 1985). Existing data do not permit generalization about growth-rate differences between gymnosperm and angiosperm seedlings in the tropics, where both taxa are evergreen.

Components of growth rate

  1. Top of page
  2. Introduction
  3. Seedling growth rates
  4. Components of growth rate
  5. Plant hydraulic conductance and architecture
  6. The evolutionary ghost of past atmospheres
  7. Refugia from competition
  8. Plant–soil associations
  9. Disturbance, climate change and biogeographic patterns
  10. Conclusions and future research directions
  11. Acknowledgements
  12. References

RGR is the product of a physiological component, net assimilation rate, and a morphological component, leaf area ratio (LAR = total leaf area/total plant mass). Various studies have indicated that allocation is substantially more important than physiology in explaining variation in growth rate on an area basis, but this was reversed in mass-based growth analyses (Hunt & Cornelissen 1997b; Reich 1998; Reich et al. 1998c). Specific leaf area (SLA = total leaf area/total leaf dry mass) was implicated as the principal means for adaptive changes in RGR (Hunt & Cornelissen 1997b). The trade-off for increasing RGR by increasing SLA is reduced leaf longevity and increased leaf palatability, which may be tolerable only in productive environments. Leaf life span tends to be longer and to control seedling RGR more strongly in unproductive habitats (Aerts 1995; Reich 1998). The RGRs of seedlings of deciduous angiosperms were significantly greater than those of conifers, even at comparable LAR or its component, SLA, both of which tended to be smaller in conifers (Reich 1998).

The maximum leaf photosynthetic rate of temperate conifers was less than that of angiosperms on an area and a mass basis for deciduous species, and on a mass basis for evergreen species (Fig. 2). Generally, the ranking of mass-based net photosynthesis among functional groups was consistent for seedlings and mature plants in the field (Reich 1998), so this large database for saplings and adults may be indicative of trends for seedlings. Greenhouse-grown seedlings of temperate deciduous angiosperms (three species) had higher photosynthetic rates than evergreen conifers (five species) on a mass basis, but not on an area basis (Reich et al. 1998c). Glasshouse seedlings of four angiosperms had mass-based, maximum photosynthetic rates double those of three codominant gymnosperms from Tasmanian temperate rain forest (Read & Busby 1990). There is a consistently stronger relationship between RGR and maximum photosynthetic rate on a mass basis than on an area basis (Reich et al. 1998c), suggesting that mass-based gas-exchange rates are more relevant to the competitive ability of seedlings in the context of Bond's (1989) arguments.

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Figure 2. Maximum net photosynthetic rate of temperate angiosperms and conifers on projected leaf-area and leaf-mass bases for deciduous (leaf life span < 1 year) and evergreen (leaf life span ≥ 1 year) trees. Fully expanded, young- to medium-aged ‘sun’ leaves growing on juvenile and adult plants (2–15 m tall) were measured. The number of species in each sample is indicated below the lower axes. Box plots show median (central horizontal line), interquartile range (box) and range (whiskers) with outlying values depicted as asterisks. Probability values are for separate variance t-tests of ln-transformed photosynthetic rates. Data from Reich et al. (1998a) and Peter Reich (personal communication), averaged when measurements were made on the same species at different sites.

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The age classes in Fig. 2 are probably still too coarse to fully account for effects of leaf longevity because (i) so many temperate angiosperms have very short leaf life spans and so many conifers have very long leaf life spans; and (ii) maximum photosynthetic rate declines with leaf life span (data not shown), partly because long-lived leaves tend to have smaller SLA and percentage N (Reich et al. 1999). For the range of leaf life spans (15–30 months) having a similar and substantial number (10) of both conifer and angiosperm species, there was no significant difference (pooled variance t-tests, P > 0·85) between taxa in maximum photosynthetic rate on either area or mass bases (Reich, Ellsworth & Walters 1998a, data not shown). This suggests that conifer and angiosperm leaves of similar longevity do not differ in their biochemical efficiency of energy conversion. As in the case of RGR, available data do not permit extrapolation to tropical systems, where both angiosperms and gymnosperms have long-lived leaves.

Plant hydraulic conductance and architecture

  1. Top of page
  2. Introduction
  3. Seedling growth rates
  4. Components of growth rate
  5. Plant hydraulic conductance and architecture
  6. The evolutionary ghost of past atmospheres
  7. Refugia from competition
  8. Plant–soil associations
  9. Disturbance, climate change and biogeographic patterns
  10. Conclusions and future research directions
  11. Acknowledgements
  12. References

Bond (1989) argued that anastamosing vein systems enable faster solute transport and thus more rapid expansion of angiosperm leaves compared with gymnosperm leaves which have open venation. Hydraulic conductance is the ratio of water-flow rate to the pressure differential causing flow, and is a measure of transport sufficiency (when normalized by leaf area). Computer simulations have estimated lower overall conductance in leaves with open, dichotomous venation compared with those having closed, anastamosing venation but an identical volume ratio of parenchyma and xylem (Anita Roth-Nebelsick, Dieter Uhl & Volker Mosbrugger, unpublished results). However, there is no empirical evidence that the hydraulic conductance of leaves depends on the complexity of venation, including the presence of tertiary venation (Becker, Tyree & Tsuda 1999a; Tyree et al. 1999). In ferns, reticulate venation is generally viewed as a strengthening trait because it is not correlated with the transpiration demands of different habitats (Wagner 1979).

Specialized transfusion tissue in conifer needles, and large flow resistances in the finest veins and non-vascular tissue of angiosperm leaves, may tend to equalize leaf hydraulic conductances in these taxa (Becker et al. 1999a). Furthermore, reduced sap-flow rates do not necessarily imply an insufficient supply of nutrients to the leaves because so-called ‘futile’ nutrient cycles, such as those involving N and Mg, deliver nutrients at rates far in excess of the demands for plant growth (Stitt & Schulze 1994). Finally, closed networks require more vascular tissue than open networks to adequately supply equivalent volumes of leaf parenchyma (Kull & Herbig 1994; Roth et al. 1995), and this extra energetic expense could negatively affect leaf expansion rates.

Bond (1989) also supposed that the conducting system of conifers was less efficient than that of angiosperms due to the greater resistance of tracheids compared with vessels. This was supported by measurements on stem segments (Becker et al. 1999a; Wang et al. 1992), which unfortunately are not a surrogate for whole-plant measurements. Leaf-area normalized, whole-plant hydraulic conductances of conifers and angiosperms were statistically indistinguishable (Becker et al. 1999a) for both tropical sapling-sized plants and temperate adult trees (Fig. 3). Differences in xylem anatomy between conifers and angiosperms manifested at the branch level are apparently compensated to equalize the sufficiency of water supply to leaves. This is consistent with the observation that the maximum leaf diffusive conductances of temperate conifers and deciduous angiosperm trees did not differ significantly when compared on the same leaf-area basis (Becker et al. 1999a). Despite having the lowest vein density, the gymnosperm Gingko biloba had the second fastest maximum transpiration rate (leaf-area basis) compared with 11 deciduous angiosperms (Kull & Herbig 1994).

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Figure 3. Whole-plant hydraulic conductance (dots depict species means) of angiosperms and conifers, normalized by leaf area for (a) tropical sapling-sized plants growing on N-poor white sand and (b) temperate adult trees. The three largest values in (a) for evergreen angiosperm saplings correspond to colonizer species that did not compete with the broad-leaved conifers. Values in (a) were measured with a high-pressure flow meter; those in (b) were estimated from the relationship between transpiration rate and xylem water potential. Box plots as in Fig. 2. Data from Tables 3 and 4 (excluding the suspiciously large value for Betula alba) of Becker et al. (1999a).

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One obvious compensatory mechanism, incorporated in the formal plant hydraulic model of Whitehead, Edwards & Jarvis (1984), is to adjust the area ratio of leaf : sapwood cross-section. This was significantly larger in first-year shoots of deciduous temperate plants than in those of evergreens, but ratios of evergreen angiosperms and conifers were statistically indistinguishable (Fig. 4). The latter result strongly suggests that differences in water-transport efficiency do not entirely account for the differences in leaf : twig area ratios. Compared with deciduous leaves, evergreen leaves require more mechanical support because of their higher mass density, and greater redundancy of transport tissue to compensate embolism-induced loss of conductance capacity during their longer lifetimes. Both of these requirements could lead to increased wood cross-sectional area (Brouat et al. 1998).

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Figure 4. Leaf : twig area ratios for first-year shoots of temperate trees and shrubs from open, mesic habitats in the Great Smokey Mountains of Tennessee, USA, to compare deciduous and evergreen angiosperms and evergreen conifers. Twig cross-sectional area was measured over bark but otherwise represented mostly sapwood. Leaf area per shoot was estimated as the product of average leaf area and number of leaves per shoot. Plot conventions as in Fig. 2. Leaf : twig area ratios of evergreen species did not differ significantly between seven angiosperms and four conifers (Mann–Whitney U = 16, P = 0·71) but were significantly smaller (U = 209, P = 0·00001) than those of 19 deciduous angiosperm species. Data from White (1983a,b).

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Allometric analysis of Sitka Spruce (Picea sitchensis) branches suggested that their diameters were more related to the requirements for mechanical load than to hydraulic transport (Farnsworth & Van Gardingen 1995), but such relationships may be size-dependent (Bertram 1989). Additional allocation to sapwood by evergreens could reduce their potential growth rate, depending on the degree of C limitation. Quantitative studies are necessary to resolve this issue, but clearly a whole-plant perspective is essential (Becker et al. 1999a).

The evolutionary ghost of past atmospheres

  1. Top of page
  2. Introduction
  3. Seedling growth rates
  4. Components of growth rate
  5. Plant hydraulic conductance and architecture
  6. The evolutionary ghost of past atmospheres
  7. Refugia from competition
  8. Plant–soil associations
  9. Disturbance, climate change and biogeographic patterns
  10. Conclusions and future research directions
  11. Acknowledgements
  12. References

The hypothesized inferior competitive ability of gymnosperms (Bond 1989) may have been exacerbated by atmospheric changes in geological time. A large decline in atmospheric CO2 concentration, [CO2], was probably a consequence of enhanced silicate-weathering rates associated with the evolution of land plants, with faster weathering assumed after the appearance of angiosperms (Berner 1994). Evidence is accumulating that gymnosperms (and other primitive plant groups) are now operating under photosynthetically suboptimal conditions owing to their retention of stomatal properties (low density and poor control) that evolved when atmospheric CO2 was more concentrated than at present (Beerling & Woodward 1996, 1997). Robinson (1994) argued that faster-evolving angiosperms (Lidgard & Crane 1988; Tallis 1991) were better able than gymnosperms to adjust stomatal structure and physiology to the stress of declining [CO2], and that this is reflected in the higher water-use efficiencies (photosynthetic gain per water loss) of modern angiosperms.

[CO2] declined throughout most of the Cretaceous (Beerling & Woodward 1996), as the number of angiosperm genera increased, but the number of coniferous genera remained relatively constant during this period (Lidgard & Crane 1988). Thus the floristic evidence is ambiguous regarding a possible competitive disadvantage of conifers. However, Bond (1989) rightly cautioned that diversity is not synonymous with ecological importance. Consistent with prediction, coniferous forests occupied less land area, and herbaceous vegetation more, during the Last Glacial Maximum (18 000 years ago) and the Younger Dryas Stadial (11 000 years ago) when [CO2] was 30% lower than during the present interglacial before anthropogenic forcing began (Adams et al. 1990; Robinson 1994; Willis 1996). A recent meta-analysis of CO2 effects on net CO2 assimilation and biomass increment showed no significant difference between conifers and angiosperms, but the statistical power of these tests was low, and taxonomic effects may have been confounded with pot-size effects (Curtis & Wang 1998).

Refugia from competition

  1. Top of page
  2. Introduction
  3. Seedling growth rates
  4. Components of growth rate
  5. Plant hydraulic conductance and architecture
  6. The evolutionary ghost of past atmospheres
  7. Refugia from competition
  8. Plant–soil associations
  9. Disturbance, climate change and biogeographic patterns
  10. Conclusions and future research directions
  11. Acknowledgements
  12. References

Bond (1989) suggested that conifers were restricted to less-productive sites, or successional stages that he assumed to have less intense competition in the regeneration niche. Various theoretical models predict that competition intensity increases with productivity, remains constant as productivity changes, or is dependent on the ratio of resource supply to demand, which may be unrelated to productivity (Twolan-Strutt & Keddy 1996 and references therein). Competition intensity refers to the effects of all neighbours upon the ability of a population or an individual to acquire a resource of limited availability (Keddy 1989). Empirical studies, mostly of non-woody plants, do not yet permit generalizations about the relationship of total (above- and below-ground) competition intensity to productivity (Twolan-Strutt & Keddy 1996). Measurements of the intensity of competition in woody vegetation along productivity gradients are needed to determine if competition controls species dominance on unproductive sites, and whether survival or growth is then the more important response to measure (Goldberg & Novoplansky 1997; Grace 1990; Grubb 1998; Miller 1996).

The traits that confer competitive superiority differ along environmental gradients, and conifers prevail not so much where growth rates are slow as where they are less important in determining the outcome of competition (Aerts & van der Peijl 1993; Berendse & Elberse 1990; Lambers & Poorter 1992; van der Werf et al. 1993). Chapin, Autumn & Pugnaire (1993) assumed that species typical of resource-poor environments had faster growth rates at low resource supply than species from resource-rich environments. However, fast-growing species from resource-rich environments actually outgrow species from resource-poor environments at both high and low resource levels (Berendse & Elberse 1990; Huante, Rincón & Acosta 1995; Lambers & Poorter 1992; Reich, Walters & Ellsworth 1992; van der Werf et al. 1993; but cf. Walters & Reich 1996).

In theoretical models where nutrients limited growth rate, nutrient-conserving species achieved greater equilibrium biomass and competitively replaced species with faster nutrient loss (Aerts 1995; Aerts & van der Peijl 1993; Berendse 1994). These models assumed a trade-off between plant traits associated with nutrient conservation and productivity (per ground area or population N content, depending on the model). Nutrient conservation is characteristic of evergreens with long-lived leaves having low nutrient concentrations and inflexible gas-exchange rates when resource shortage is relieved. However, Grubb (1998) noted that plants that strongly reduce their respiration rate when resources are in short supply might show some opposite characteristics. Incorporating nutrient conservation into empirical studies of competition requires explicit consideration of nutrient-loss rates. This will be complicated by the likely inverse relationship between the cost of loss and the actual loss-rate gradient (Keddy 1989).

Bond (1989) speculated that heavy shade would offer a refuge to conifers by reducing the growth-rate advantage of angiosperms in the same fashion as nutrient shortage. Absolute differences in RGR do decrease with decreasing insolation (Boot 1996). Across both temperate and tropical species, there is an inverse correlation between growth rate of well illuminated seedlings and their survivorship in shade (Kitajima 1996; Kobe et al. 1995). Bond (1989) predicted that shade-tolerant conifers would persist against angiosperm competitors in forests where gaps are small and saplings are shaded. In the Cape forests of South Africa, however, gap size was unimportant to plant species composition because critical interactions occurred among juveniles in deep shade long before a gap occurred (Midgley et al. 1990). From studies in the temperate rain forest of Chile, Lusk (1996) concluded that heavily shaded understories do not appear to be a major evolutionary refuge for conifers, because few species maintain large seedling banks under closed forest canopies. Bond (personal communication) now considers that to be a fair generalization and attributes it to the drought sensitivity of broad-leaved conifers in shady places, as demonstrated for southern Australian species (Brodribb & Hill 1998, 1999). It remains to be seen whether shade-tolerant conifers are generally drought-intolerant, as presumed by Smith & Huston (1989).

Plant–soil associations

  1. Top of page
  2. Introduction
  3. Seedling growth rates
  4. Components of growth rate
  5. Plant hydraulic conductance and architecture
  6. The evolutionary ghost of past atmospheres
  7. Refugia from competition
  8. Plant–soil associations
  9. Disturbance, climate change and biogeographic patterns
  10. Conclusions and future research directions
  11. Acknowledgements
  12. References

There was no systematic, quantitative survey to support Bond's (1989) generalization that, outside boreal and montane regions, conifers occur on nutrient-poor sites, especially sandy, acidic or waterlogged soils. Anecdotal counter-examples can readily be cited. Thus conifers sometimes dominate or codominate with angiosperms on mesic, fertile soils in Europe (Barbéro et al. 1998; Eyre 1968) and the USA (Abrams, Orwig & Demeo 1995; Allen & Peet 1990; Keddy & MacLellan 1990; Loehle 1988), and as long-lived seral stages in the southern hemisphere (Neal Enright, personal communication). Such exceptions to a general hypothesis are to be expected in probabilistic systems (Midgley & Bond 1989) so their frequency must be quantitatively assessed.

Systematic survey indicates that the typical impression of pines predominating on sandy, north-temperate sites (Finley 1976; Schmidt, Spencer & Bertsch 1997) is an oversimplification, especially when mixed forests containing conifers are also considered. Angiosperm (mostly oak) forest and savanna occupied 40% of sandy upland soils of Wisconsin, USA before ‘European’ settlement, while 40% of coniferous upland forest occurred off (but typically bordering) sandy soils (Fig. 5). Fire and climatic change were probably responsible for blurring this association between vegetation and soils (Cottam, Loucks & Curtis 1965; Delcourt & Delcourt 1996; Finley 1976; Radeloff et al. 1999; Szeicz & MacDonald 1991).

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Figure 5. Occurrence of (a) non-boreal, coniferous forest (black) off sandy, upland soils (areas outlined by solid lines) and (b) angiosperm forest and savanna (black) on sandy, upland soils in Wisconsin, USA prior to ‘European’ settlement. Mixed mesic forest with angiosperms and Hemlock (Tsuga canadensis) covering most of the northern half of the state's non-sandy soils is not shown, nor are vegetation distributions in two north-eastern areas (outlined by dotted lines) of mixed soils which included some unmapped sandy areas. For clarity, areas of water and wetland within sandy blocks are not shown. The scale bars (100 km) are oriented west–east. After Cottam et al. (1965) and Madison & Grundlach (1993).

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In north-eastern Hungary's early postglacial period, deciduous trees replaced conifers on podsolic soils in about 100 years, thereby triggering the development of brown-earth soils over the subsequent 1000 years (Willis et al. 1997). If vegetation change generally occurs so much more quickly than the soil change it triggers, considerable noise in plant–soil associations may be expected. Thus large areas of pine forest are not underlain by nutrient-poor podsols despite the common presumption of their tight association (Scholes & Nowicki 1998).

The chemical fertility of soils occupied by conifers should be measured, rather than presumed to be low. In upper Michigan, USA, either of the shade-tolerant species Tsuga canadensis (Hemlock) or Acer saccharum (Sugar Maple) dominated stands on fragipans while mixed Hemlock–hardwood stands were associated with sandier soils (Pastor & Broschart 1990). The supposedly nutrient-poor conditions under Hemlock were considered a consequence of the poor-quality litter (Davis et al. 1994) that is characteristic of evergreen conifer forests (Gower, Isebrands & Sheriff 1995). Yet a comparison of 24 Hemlock-dominated and 40 Maple-dominated upland stands in this region showed no statistical distinction between them for exchangable K+, Mg2+ and Ca2+ or total N (0–0·1 m soil depth), based on 95% confidence intervals calculated for data (weighted by sample size) in Table 2 of Spies & Barnes (1985). Davis et al. (1998 and references therein) also found no significant differences in abiotic factors between upland Hemlock and Maple patches (3–30 ha). Although tropical (Bornean) white-sand soils may be dominated by conifers and are often characterized as extremely infertile, there is as yet no evidence that tree growth rates on them are slower than those on more typical, but also infertile, lowland soils (Becker et al. 1999b). A caveat is that growth rates of seedlings are expected to be more responsive than those of larger trees to differences in soil fertility (Reich 1998).

Failure to detect differences in soil fertility between angiosperm- and conifer-dominated stands on moderately poor soils qualifies the presumption that conifers prevail on less-productive sites, but does not discredit Bond's (1989) hypothesis that angiosperms outcompete conifers on more productive sites. Just as conifers cannot match the fastest RGRs and photosynthetic rates of angiosperms but overlap at the lower end of the range, so they may be excluded from productive sites while ‘sharing’ less-productive sites with angiosperms. This implies a probability gradient of angiosperm dominance paralleling gradients of site productivity.

The true nature of gymnosperm distributions with respect to soil type and fertility will be better characterized by complete, quantitative regional surveys of presettlement patterns than by a tabulation of anecdotal generalizations and inferences. Even then, there are two complicating factors – disturbance and climate change.

Disturbance, climate change and biogeographic patterns

  1. Top of page
  2. Introduction
  3. Seedling growth rates
  4. Components of growth rate
  5. Plant hydraulic conductance and architecture
  6. The evolutionary ghost of past atmospheres
  7. Refugia from competition
  8. Plant–soil associations
  9. Disturbance, climate change and biogeographic patterns
  10. Conclusions and future research directions
  11. Acknowledgements
  12. References

Modern plant distributions have been grossly altered by human disturbance in ways that appear to particularly distort conifer distributions. Low- and mid-elevation populations of northern and southern temperate and tropical conifers have been eliminated by logging or fire in preparation for agriculture (Enright & Ogden 1995; Eyre 1968; Kershaw & McGlone 1995; Richardson & Rundel 1998; Runkle 1985; Whitmore 1984). The occurrence of pine throughout the world is dependent on maintenance of the natural fire regimes to which it is adapted, and it is in the role of aggressive postdisturbance colonizers that pines are most clearly differentiated from other conifers and angiosperm trees (Agee 1998; Richardson & Rundel 1998). With suppression of fire or other large-scale disturbance, the conifer component of some forests may decline (Batek et al. 1999; Bond & Midgley 1995; Enright & Ogden 1995; Radeloff et al. 1999). Alternatively, fire-sensitive conifers may suffer if climatic change favours fire-promoting vegetation (Kershaw & McGlone 1995).

Bond (1989) suggested that disturbance alone, without competition in the regeneration niche, could exclude slow-growing conifers if it is frequent enough to prevent them overtopping angiosperms or reaching reproductive maturity. In the Central Ozarks of Missouri, USA, however, Pinus echinata formed nearly pure stands on acidic bedrock where the fire-return interval was shortest (10 years) and less than this pine's maturation period (Batek et al. 1999). Xerophytic angiosperms predominated where fires were less frequent. In such disturbance-dominated landscapes, life-history traits such as resprouting ability are probably more important than competitive ability based on seedling RGR (Batek et al. 1999). Both angiosperms and conifers possess fire-resistant and fire-sensitive species, and dominance in fire-disturbed systems will depend on which particular species are present.

Whitney (1986) has noted that the relative importance of substrate versus fire disturbance in the maintenance of pine forests in Michigan, USA cannot be definitively assessed because these factors are inseparably linked. In some cases there may even be a synergistic relationship between fire and low soil fertility. Kellman (1984) hypothesized that a slow rate of canopy closure makes the vegetation of unproductive sites more fire-prone than that on productive sites. This effect may be enhanced by the lower mineral content of plant tissues on infertile soils, which produces more flammable fuel.

In seeking to explain phytogeographical patterns, it is important to appreciate how dynamic the distribution of vegetation types and species has been, and how the composition of some forests has changed over time (Davis et al. 1994, 1998; Radeloff et al. 1999). Jack Pine (Pinus banksiana) has dominated the sandy glacial outwash of the Yellow Dog Plains in Upper Michigan, USA for 9000 years – strong presumptive evidence for an ‘edaphic climax’ (Brubaker 1975) – but such stability is exceptional. Pleistocene glaciations may have affected the apparent association between conifers and soils through climatic changes, and by initiating successional processes that are not yet complete or by eliminating species that have not had sufficient time to reinvade. Most modern forest types in North America arose only 3000–6000 years ago, and the most widespread forest type in eastern North America from 12000–9000 years ago was an open woodland comprising spruce and thermophilous hardwoods, which does not exist now (Graumlich & Brubaker 1995). In western North America, lowland and montane forests are dominated by conifers, and this has been attributed to the inability of tall deciduous tree species that survived in eastern North America after the Pleistocene to migrate across the dry heart of the continent and compete with conifers in the west (Eyre 1968). The relative rarity of conifers in the lowland rain forests of Latin America and Africa might be related to the greater degree of Pleistocene and Holocene desiccation of those continents compared with Australasia, where mainland conifers are nevertheless largely confined to azonal or nominally infertile soils (Kershaw & McGlone 1995; Tallis 1991; Whitmore 1984).

The observations in this and the preceding section show that modern plant–soil relations reflect, to varying degrees, human intervention, temporally asymmetrical plant–soil interactions, incomplete dispersal processes, and historical accidents occurring over geological time. Even during ecological time, late-succession species replace each other less predictably than do species of early-succession habitats. Apparently, dispersal patterns and stochastic events can override differences in physiological response to environmental resources (Bazzaz 1996), and these differences may be quite small in shade (Walters & Reich 1996). Biogeographical evidence that is most free of such effects will provide the best tests of the slow seedling hypothesis.

Studies providing such evidence are rare. Richardson & Bond's (1991) conclusion that pine invasions are most prevalent in grasslands, where there is limited competition in the regeneration niche, was contradicted by their observation that grass competes intensely with pine seedlings. Furthermore, their analysis was based on non-experimental studies reporting changes in pine distribution, with all the attendant problems of a non-random sample. Evidence that conifers in South Africa are excluded from some forests by competition with faster-growing angiosperms was equivocal (Midgley & Bond 1989; Midgley, Bond & Geldenhuys 1995). On the other hand, 3000 years ago in northern USA, T. canadensis (Hemlock) invaded stands that were dominated by Pinus strobus (White Pine), but not those where angiosperms were more abundant (Davis et al. 1998).

Conclusions and future research directions

  1. Top of page
  2. Introduction
  3. Seedling growth rates
  4. Components of growth rate
  5. Plant hydraulic conductance and architecture
  6. The evolutionary ghost of past atmospheres
  7. Refugia from competition
  8. Plant–soil associations
  9. Disturbance, climate change and biogeographic patterns
  10. Conclusions and future research directions
  11. Acknowledgements
  12. References

Seedling RGRs of deciduous, early-succession angiosperms exceeded those of evergreen conifers, which supports Bond's (1989) ideas about the competitive inferiority of conifers in productive environments. It is not known if this difference in growth potential extends to evergreen or late-succession angiosperms, so the generality of Bond's arguments remains uncertain. Surprisingly little systematic effort has been made to test the ecophysiological explanations suggested to account for the slow growth rates of conifer seedlings. Whole-plant hydraulic conductances and leaf diffusive conductances of conifers were similar to those of angiosperms, despite the less efficient conduits of conifers and probably because of architectural adjustments. Temperate conifer leaves did not achieve the highest photosynthetic rates measured for angiosperms, but leaves of these taxa with similar longevities had comparable photosynthetic rates. The differences in seedling RGR between conifers and angiosperms are thus attributable to the different allocation (C and N) and phenological strategies of their leaves, rather than to inferior transport capacity or energy-conversion efficiency in conifers. Samples were too small, and taxonomically and geographically restricted, to consider any of these conclusions definite. Both conifers and angiosperms can dominate infertile sites, and disturbance, especially by fire, may determine which taxon prevails.

Possible differences in competitive ability between conifers and angiosperms in the regeneration niche and their biogeographical consequences deserve further study. The dominance of angiosperm trees on productive sites needs to be quantitatively surveyed and interpreted after accounting for effects of climate change and human disturbance. Data from evergreen angiosperms and broad-leaved conifers in warm climates are especially needed to fill the gaps in comparisons of seedling growth rates, photosynthesis and leaf traits in order to determine whether the hypothesized competitive superiority of angiosperm seedlings could explain the widespread dominance of this taxon in the tropics.

Interpretation of seedling-competition studies would be simplified for sites where conifer- and angiosperm-dominated forests occur on soils of different fertility experiencing the same climate. For example, on Blackhawk Island in Wisconsin, USA, conifer-dominated stands occur on sandy soils with slow N mineralization while angiosperms prevail on soils richer in clay and N supply (Pastor et al. 1984). Comparative study of growth rates, C and nutrient budgets (especially as related to biomass allocation), and ecophysiology of potentially competitive angiosperm and conifer seedlings growing on contrasting soil types would provide a basis for refining hypotheses about possible differences in the regeneration niche of these two plant groups. Seedling performance in a range of light environments (understorey, small and large canopy gaps) should be studied. Although Bond (1989) emphasized recruitment in gaps or open areas, even late-succession, shade-tolerant species persist under a wide variety of gap regimes, and dendroecological studies indicate that in old-growth, temperate forests only 15–50% of canopy trees of dominant species originated in gaps (Lorimer, Frelich & Nordheim 1988; Parshall 1995). In the understorey, seedlings may compete more with larger plants than with themselves.

Although intensive studies, such as those by Shainsky & Radosevich (1992) and Putz (1992), are invaluable in elucidating the mechanisms of conifer–angiosperm seedling competition, something less time-consuming would facilitate a broad survey of the growth potential of juvenile conifers and angiosperms under natural conditions. An approach combining leaf-level measurements with simulations at the whole-plant level for a growing season, as in Hollinger (1992), is likely to be efficient and informative. Phytometer experiments (e.g. Twolan-Strutt & Keddy 1996) with species representative of important functional groups (such as seral stage and fire tolerance) could characterize RGRs in the field, while also providing information about the relative importance of root and shoot competition, and about competition intensity along environmental gradients, provided the appropriate parameters are measured (Freckleton & Watkinson 1997). It is essential that the relationship between seedling RGR and dominance of biomass be empirically established for woody species.

It is difficult to assess empirically whether the allocation and phenological strategies of gymnosperm leaves are constrained by their transport capacity because large, thin, deciduous forms do not exist. A solution to this dilemma might be to employ the modelling approach of Roth et al. (1995), parameterized by hydraulic conductance data from extant leaves, to characterize the potential of conifers to produce large, thin, short-lived leaves without anastamosing venation. Although there is a tendency to consider conifers a unique group of evergreen species with long-lived foliage, the leaf life spans of conifers overlap greatly with those of angiosperms (Reich et al. 1995). Furthermore, during the Eocene (50 M years ago) many conifers at high northern latitudes were deciduous (Tallis 1991) so evergreenness is not some evolutionarily conservative trait of this group. If simulations showed that conifer venation could adequately supply water and nutrients to ‘disposable’ leaves, then the competitively advantageous property of fast assimilation rate would follow by analogy with angiosperms (Reich et al. 1995). This would imply that the absence of such leaves in conifers is more probably due to a chance failure of evolution, rather than to physiological constraints.

Acknowledgements

  1. Top of page
  2. Introduction
  3. Seedling growth rates
  4. Components of growth rate
  5. Plant hydraulic conductance and architecture
  6. The evolutionary ghost of past atmospheres
  7. Refugia from competition
  8. Plant–soil associations
  9. Disturbance, climate change and biogeographic patterns
  10. Conclusions and future research directions
  11. Acknowledgements
  12. References

A conference grant from Universiti Brunei Darussalam enabled attendance at an IUFRO Workshop in the Republic of South Africa, where discussions with William Bond and Norman Pammenter proved inspiring. Many colleagues helped by pointing out useful sources of information or facilitating a visit to the superb forests of Yakushima Island, Japan. Jim Becker sent maps, Peter Reich shared photosynthetic data, and Mel Tyree and Makoto Tsuda were valued collaborators in a comparative study of hydraulic conductance. Constructive critical comments from William Bond, Stuart Davies, Neal Enright, Deborah Goldberg, Doyle McKey, Peter Reich, Ian Turner, the editor and reviewers helped to clarify the exposition.

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  3. Seedling growth rates
  4. Components of growth rate
  5. Plant hydraulic conductance and architecture
  6. The evolutionary ghost of past atmospheres
  7. Refugia from competition
  8. Plant–soil associations
  9. Disturbance, climate change and biogeographic patterns
  10. Conclusions and future research directions
  11. Acknowledgements
  12. References
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