The controversy over traits conferring shade-tolerance in trees: ontogenetic changes revisited



    1. Department of Plant Physiology, University of Tartu, Riia 23, 51011 Tartu, Estonia, and Centro di Ecologia Alpina, I-38040 Viote del Monte Bondone, Trento, Italy
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Ülo Niinemets (fax 372 7 366021; e-mail


  • 1 Successional replacement of intolerant species by shade tolerators along gap-understorey gradients is commonly associated with increasingly higher low-light carbon acquisition capacities of more tolerant species. This doctrine has recently been challenged because of evidence demonstrating larger leaf dry mass per unit area (MA), lower photosynthetic capacities and inferior whole plant relative growth rates (RGR) in both high and low irradiance in seedlings of shade-tolerators. However, as the individuals of shade-tolerant species often need to endure canopy shade for many years before gap formation, testing of the carbon gain hypothesis of shade tolerance requires examination of species carbon gain potentials during the entire plant ontogeny.
  • 2 Light vs. MA relationships throughout ontogeny demonstrate that saplings and canopy individuals of shade tolerators do have lower MA than intolerant species, and moderately higher photosynthetic capacities in low light, resulting in greater whole plant carbon gain capacities at lower light. The apparent discrepancy between results from studies on seedlings vs. saplings/trees is due to MA increasing at a faster rate in shade intolerators during ontogeny. A strong positive linkage between seed size and species shade tolerance further implies that shade tolerators have larger initial size, absolute growth rate and survivorship in low light despite their lower RGR.
  • 3 The evidence reviewed collectively suggests that the carbon balance concept of species’ successional position is valid for both seedlings and saplings, and that the apparent discrepancies in species rankings on the basis of structural and physiological characteristics are driven by variations in initial size and rate of ontogeny. Analyses of species shade tolerance potentials should therefore consider how any suite of adaptive traits varies with ontogeny.

How do foliar characteristics vary among species of contrasting shade tolerance?

Species’ inherent differences in light requirement underlie the major changes in vegetation composition during succession (Sack & Grubb 2001; Valladares 2003). Because light availability in established plant communities is often very low, in the order of 0.5–2% of above-canopy light, shade tolerance has traditionally been thought to depend on traits that enhance light harvesting efficiency (Bazzaz 1979; Givnish 1988). In particular, any foliage and canopy adjustments that alter quantum interception efficiency of incident light will influence the minimum light requirement for plant survival.

Leaf dry mass per unit area (MA) is a measure of biomass requirement for the construction of unit foliar surface area, and it has been hypothesized that more tolerant species will have lower MA, and a more extensive foliar display, than less tolerant species (Horn 1971; Givnish 1988). Some observations do show a lower MA in shade tolerators (Niinemets 1997; Beaudet & Messier 1998; Niinemets 1998; King 2003), consistent with the hypothesis, but other studies have observed a lower MA in intolerant species (Kitajima 1994; Walters & Reich 1996; Poorter 1999; Walters & Reich 2000; Reich et al. 2003).

It has further been suggested that, under low irradiance, leaf carbon assimilation potential per unit dry mass is higher in shade-tolerant than in intolerant species (Givnish 1988), which provides an explanation for the superior performance of shade tolerators in dense forest shade (Bazzaz 1979; Givnish 1988). Again, some studies agree with this expectation (Givnish 1988; Niinemets et al. 1999; Kazda et al. 2000), while others are inconsistent (Kitajima 1994; Reich et al. 2003), underscoring the overall inconsistency of species rankings according to structural and physiological traits.

These observations of higher photosynthetic rates and lower MA in shade-intolerant species in both high and low light have led to radical suggestions that species’ shade tolerance is not associated with a suite of traits enhancing growth in shade, but with the dependence of survival on resistance to herbivory, pathogen attack and mechanical damage (Kitajima 1994) and on conservation of carbon by reducing dark respiration (Reich et al. 2003). Although plants growing in shade with extremely limited carbon reserves may be especially vulnerable to biotic and abiotic damage, a possible trade-off between growth and survival traits does not explain why the physiological and morphological rankings of species with varying shade tolerance vary from study to study. In fact, of the above studies, all those reporting a lower MA and higher photosynthetic capacity in intolerant species at a common light level have investigated seedlings, while reports of lower MA in shade-tolerant species are restricted to studies of saplings or mature trees, suggesting that the rate of ontogenetic development may provide an explanation.

Time-dependent modification of light vs. leaf structure and physiology relationships: ontogeny matters

Most of the detailed work on the carbon balance of species shade tolerance has been conducted with first-year seedlings (Walters & Reich 1999), because this stage is thought to control species establishment in the understorey (Reich et al. 2003). However, in deeply shaded understories, saplings only 0.2–1 m in height are commonly 7–20 years old (Niinemets 1998; King 2003), implying that scaling from first-year seedling responses to species establishment potential in mid- and late-successional forest stands is bound to have inherent limitations. Limited temporal duration is particularly relevant given that there is a significant time-dependent increase of MA with tree age (Rijkers et al. 2000).

Because shade-intolerant species often have smaller seeds than tolerators (Grubb & Metcalfe 1996; Körner 2005), but greater biomass accumulation rates (Kitajima 1994), ontogeny may be of special significance in understanding the divergent patterns in MA. Differences in the rate of ontogenetic development imply that MA can increase faster in shade intolerators due to lower initial plant mass (Sack & Grubb 2001, 2003), explaining the lower MA in seedlings and higher MA in saplings and canopy trees of shade-intolerant species.

As a further complication, MA depends strongly on the average light environment, which may change as the trees gain in size, but data on the dependence of MA on light in various-sized plants are scant. To test quantitatively the hypothesis of ontogenetic changes in MA rankings among species differing in shade tolerance, I constructed MA vs. light relationships (Fig. 1) for different-sized and -aged individuals of four species of European temperate deciduous trees of contrasting shade tolerance (tolerance of Betula pendula < Populus tremula < Corylus avellana < Fagus sylvatica). From these data, I calculated the values of MA corresponding to a low (3 mol m−2 d−1) and high irradiance (40 mol m−2 d−1). Typical average irradiances experienced by plants in understories of deciduous temperate forests from the start of foliage formation until full maturation are in the order of 2–5 mol m−2 d−1, while the high value corresponds to completely open locations (Niinemets et al. 1999).

Figure 1.

Ontogenetic modification of the dependencies of leaf dry mass per unit area (MA) on average integrated daily quantum flux density in two shade-intolerant (Betula pendula and Populus tremula) and tolerant species (Fagus sylvatica and Corylus avellana). All data were re-fitted by non-linear regressions in the form of y = a +blog(x), and all relationships are significant at P < 0.001. r2 is the explained variance, and h the average tree height. Species shade tolerance increases as B. pendula (light requirement index of Ellenberg (Ellenberg 1991; Hill et al. 1999); LF = 7) < P. tremula (LF = 6) < C. avellana (LF = 4) < F. sylvatica (LF = 3). Data sources were: for B. pendula, □ = Öquist et al. 1982 (average plant age, A = 0.3 years.); ▪ = Nygren & Kellomäki 1983 (A = 2.3 years.), ○ = Kull & Niinemets 1993 (A = 4.5 years.), • = Niinemets et al. 1999 (A = 40 years.); for P. tremula, □ = Tselniker et al. 1983 (A = 0.3 years.); ○ = Niinemets 1997 (A = 5 years.), • = Niinemets & Kull 1998 (A = 27 years.); for F. sylvatica, □ = Gansert & Sprick 1998 (A = 0.6 years.); ▪ = Gansert & Sprick 1998, Kriebitzsch et al. 1999 (A = 1.5 years.), ○ = Niinemets 1995 (A = 23 years.), • = Fleck et al. 2003 (A = 50 years.); and for C. avellana, ○ = Kull & Niinemets 1993 (A = 4 years.), • = Niinemets & Kull 1998 (A = 26 years.).

For first-year seedlings of shade-intolerant species, low-light MA values were predicted to be 14.1 and 16.5 g m−2, and high-light values to be 31.8 g m−2 and 53.0 g m−2 for B. pendula and P. tremula, respectively (Fig. 1). The corresponding values of MA for the shade-tolerant species F. sylvatica were 41.4 g m−2 in low light and 57.2 g m−2 in high light (Fig. 1). In seedlings of North American temperate deciduous species, comparable low-light (1.5–5% of above-canopy light) MA values are 11–17 g m−2 for intolerant Betula alleghaniensis, B. papyrifera and P. tremuloides (Reich et al. 1998; Walters & Reich 2000), and 30–49.5 g m−2 in shade-tolerant Acer saccharum and Quercus rubra (Walters & Reich 1996, 2000), further supporting the lower MA in seedlings of intolerant species.

Values of MA in saplings and trees are three- to fourfold larger than in seedlings at both low and high light in the shade-intolerant species (B. pendula and P. tremula), but low-light values do not vary during ontogeny in the shade-tolerant species (C. avellana and F. sylvatica), and in high light, MA values increase only moderately with increasing height (Fig. 1). Low-light MA values of tolerant and intolerant species are therefore expected to equalize about 3–5 years after germination, when the plants are c. 1 m tall, as observed by DeLucia et al. (1998). After this ontogenetic stage, MA of intolerant species exceeds that of shade-tolerant species in both low and high light (Fig. 1).

Although these data strongly support the hypothesis of ontogenetic effects on species MA rankings, the extensive amount of data needed made this analysis possible for only four species. As a further test, I re-analysed the data of Yevstigneyev (1990) and Niinemets (1998) on MA changes between seedlings and saplings of 11 species of varying shade tolerance that were grown in full light. MA in seedlings decreased as the minimum irradiance for species survival (Imin) increased (Fig. 2a), but MA increased with increasing Imin in saplings (Fig. 2b). MA in seedlings and saplings was not correlated (inset in Fig. 2b). The relative change in MA between seedlings and saplings (Fig. 2c), as well as the absolute change (r2 = 0.72, P < 0.001), increased with increasing Imin. These data collectively demonstrate a larger ontogenetic change in MA in species with lower shade tolerance, leading to reversal of MA rankings from juvenile to mature phases. Although species minimum light requirement increased with plant age, the species ranking was independent of ontogenetic age (Fig. 2c inset).

Figure 2.

Relationships between species minimum irradiance for survival (Imin) and whole-plant MA in (a) open-grown seedlings and (b) saplings, and between Imin and (c) the relative change in MA[(MA,saplingMA,seedling)/MA,seedling] in 11 species with contrasting light requirement (data of Niinemets 1998; Yevstigneyev 1990). The inset in (b) demonstrates the lack of correlation between MA in seedlings and saplings, and the inset in (c), the relationship between the minimum relative irradiances for seedlings and saplings. Data were fitted by linear regressions. Imin for every species was experimentally determined as the relative irradiance at which the species survival is zero. The values of Imin increase with increasing plant age due to ontogenetic changes in plant light requirement. The following species were included: Acer campestre, A. platanoides, Acer tataricum, Betula pendula, Carpinus betulus, Fraxinus excelsior, Populus tremula, Quercus robur, Salix caprea, Tilia cordata and Ulmus glabra. Values of Imin are strongly associated with observational estimates of species shade tolerance (r = − 0.83 for the correlation between Imin and LF defined in Fig. 1).

Ontogenetic changes in MA have further important implications for modifications in species photosynthetic ranking. For leaves sampled from similar light environments, the strong negative relationship between MA and leaf photosynthetic capacity per unit dry mass (Reich et al. 2003; Wright et al. 2004) provides an explanation for a strong decline in photosynthetic capacity with increasing tree age and size. As with MA, time- and size-dependent changes in foliar photosynthetic capacities appear to occur faster in intolerant trees. Although leaf photosynthetic capacity per unit dry mass of shade-intolerant species may initially be larger in seedlings (Kitajima 1994; Reich et al. 2003), assimilation rates in low light of saplings and mature canopy trees of shade tolerators can exceed those of shade-intolerant species (Niinemets et al. 1999; Kazda et al. 2000). These data jointly indicate that shade tolerant species do not have inherently lower photosynthetic capacities, but the initial low rates in seedlings are associated with their larger MA values.

Complex interactions between seed size and relative vs. absolute growth rates

Studies investigating the physiological basis of species differences in shade tolerance have tried to correlate plant performance with relative plant growth rate (RGR, plant biomass production per unit existing biomass and per unit time, Kitajima 1994; Reich et al. 2003). RGR is the product of leaf area ratio (LAR, total leaf area per unit total plant dry mass), and net assimilation rate (NAR, total plant carbon gain per unit of leaf area and time). LAR, in turn, is equal to the fraction of total plant biomass present in leaves divided by MA. Thus, larger MA and lower NAR lead to seedling RGRs that are two- to fourfold lower in shade-tolerant A. saccharum and Q. rubra than in shade-intolerant B. alleghaniensis, B. papyrifera and P. tremuloides (Walters & Reich 1996).

Surprisingly, these strong differences in growth rate are not associated with species-specific survivorship values in low light (Kitajima 1994; Walters & Reich 1996, 1999, 2000), leading to the conclusion that the survival of shade-tolerant species in low light is associated with traits that improve species resistance to abiotic and biotic stresses, and that plant survival is not directly associated with whole plant carbon gain (Kitajima 1994; Reich et al. 2003). This hypothesis rests on the assumption of greater plant vulnerability to abiotic damage, and to pests and herbivory, in plants with tighter carbon budget.

Because larger relative growth rate is not always compatible with greater competitive potential, it has been hypothesized that differences in plant fitness are associated with the components of RGR (NAR and LAR) and with biomass partitioning (Lambers & Poorter 1992). Despite this, the overall utility of RGR in determining species competitive ability in low light is not disputed in studies of the mechanism of seedling shade tolerance. The concept of RGR should be reassessed, given the positive correlation between seed size and shade tolerance (Grubb & Metcalfe 1996; Körner 2005) that results in greater size and larger carbon reserves in shade tolerators. Larger seeds enable shade-tolerant species to ‘buy time’ before carbon starvation in the understorey (Reich et al. 2003). In addition, if accidental damage, herbivory and/or pest attacks are the primary factors limiting seedling establishment, larger size and greater below-ground carbon reserves should confer an advantage and thus result in a greater survivorship. Cornelissen (1999) demonstrated for 58 woody species of contrasting seed size that 1000-fold differences in seed size still correspond to 1000-fold differences in total plant dry mass even 3 weeks after germination. Although small-seeded species have larger RGRs (Cornelissen et al. 1996; Körner 2005), absolute plant masses and absolute growth rates are lower for a long period after seed germination. In moderately low light (8% of above-canopy irradiance) the seedlings of the shade-intolerant species B. alleghaniensis and B. papyrifera required two growing seasons with fourfold differences in RGR to overcome initial size differences due to 1000-fold lower seed size than the shade tolerant Q. rubra (Walters & Reich 1996). At lower irradiance (2%), RGR values were again significantly larger in shade-intolerant species but they never caught up with the shade tolerators due to low rates of survival (Walters & Reich 1996). In fact, a re-analysis of the data of Walters & Reich (1996, 2000) demonstrates that survivorship across the species is strongly related to absolute plant dry mass (Fig. 3a). The correlation between RGR and survivorship was not significant for all data pooled (Fig. 3b; Walters & Reich 1996, 2000) and was even negative for species means (inset in Fig. 3b; see also Kitajima 1994). The relationship between plant size and survival levels off at a plant size of c. 1000 mg (Fig. 3), possibly because of a certain basal level mortality (1–5%) that is independent of plant size.

Figure 3.

Survivorship of seedlings exposed to different environmental conditions in relation to total plant dry mass (a) and relative growth rate (b) in species of contrasting shade tolerance. Data are from Walters & Reich (2000) for shade-tolerant species Acer saccharum (•) and shade-intolerant species B. alleghaniensis (▪), B. papyrifera (□) and P. tremuloides (▵) grown for 50–64 days, and from Walters & Reich (1996) for shade-intolerant species Betula alleghaniensis and B. papyrifera, intermediate species Ostrya virginiana and tolerant species Acer saccharum and Quercus rubra grown for 90 days (○). Species were grown at four different light treatments (0.6%, 1.5%, 2.8% and 7.3% of incident irradiance) and at three different nutrient treatments (very low/low/high) in the study of Walters & Reich (2000), and at two light levels (2% and 8%) in the study of Walters & Reich (1996). The inset in (a) shows the correlation between species average RGR and total dry mass, and the inset in (b), the correlation between species-specific average survivorship and average RGR. For the entire set of data, the species average survivorship was positively correlated with species average log(dry mass) (r2 = 0.87, P < 0.001). Plant total dry mass determined at the end of the growing season includes leaves, roots and stems, while the values of RGR were calculated using the initial seedling dry mass before the treatments and the final dry mass. The initial dry mass included still existing seed reserves.

Contrary to what has been suggested on the basis of RGR, these data indicate that the growth potential is not particularly limited in shade-tolerant species in low light. Total mass, rather than RGR, seems to determine the initial species success in colonizing understorey habitats. Total mass during seedling establishment in low light is, in turn, determined by seed size rather than by RGR.

What happens to plant growth rates after seedling establishment in low light? Do the differences in RGR mean that shade-intolerant species finally catch up? This would happen, provided survivorship does not differ between tolerant and intolerant species, and RGR remains higher in shade-intolerant species during their entire ontogeny. However, survivorship varies with initial plant size (Fig. 3a) and RGR decreases with increasing tree size (Sack & Grubb 2001, 2003). Because MA changes faster in shade-intolerant species, RGR is also likely to change faster, leading to RGR rank changes among woody species of contrasting shade tolerance (Sack & Grubb 2001, 2003). Few studies have investigated the growth rates of established saplings (Pacala et al. 1994; DeLucia et al. 1998; Niinemets 1998; Lin et al. 2002), and even fewer studies have investigated both the above- and below-ground plant biomass pools (DeLucia et al. 1998; Niinemets 1998; Claveau et al. 2005). Nevertheless, the growth rate vs. long-term irradiance response curves developed simultaneously for seven to ten species of contrasting shade tolerance, demonstrate an overall positive correlation between plant growth potential in low light and species shade tolerance rank with only a few exceptions (Pacala et al. 1994; Lin et al. 2002).


This analysis emphasizes the importance of understanding temporal changes in foliar structure, leaf assimilation and plant growth potentials beyond the seedling stage. Because saplings often grow in deeply shaded understories for extended time periods before gap formation, long-term studies that capture ontogenetic changes are needed if we are to understand species growth potential in the understorey.

The current analysis further suggests that the usefulness of the concept of relative growth rate should be reassessed for comparisons among species that differ greatly in seed size. Even several-fold differences in initial RGR may be poorly reflected in differences in plant survival, because compensation for initial size differences in the shade may take a long time, even if not prevented by enhanced mortality of smaller plants and time-dependent modifications in foliage functioning and growth potentials. Overall, the carbon gain hypothesis of plant shade tolerance is still valid, provided an appropriate estimator of species growth potential is used.


The author's work on species shade tolerance has been supported by the Estonian Science Foundation (grant 5702) and the Estonian Ministry of Education and Science (grant 0182468As03). Thoughtful comments from the anonymous reviewers and essential suggestions from Dr Lindsay Haddon are greatly appreciated.