Why do species of woody seedlings change rank in relative growth rate between low and high irradiance?

It is often assumed that if a plant species has a higher relative growth rate (RGR) than another species in deep shade, it will have a lower RGR at high irradiance (Spurr & Barnes 1980; Thomas & Bazzaz 1999; Walter 1973). In other words, species change rank (crossover) between low and high irradiance. This idea was suggested chiefly by the finding that in deep shade the mass-based net photosynthetic rates of the leaves of shade plants exceed those of sun plants, while at high irradiance the reverse is true (Björkman & Holmgren 1963; Boardman 1977; Givnish 1988). This finding has been assumed to scale up to the level of whole-plant RGR (Shugart 1984). In the past decade, however, a contrary view concerning RGRs has emerged, the idea that if a plant grows faster than another at high irradiance it will also do so in the shade (Kitajima 1994; Poorter 1999). According to this later view, light plays a role in maintaining the mixture of forest species only through the well established trade-off between survival rate in deep shade and RGR in bright light (Kitajima 1994, 1996). Similar experimental studies of RGR responses to irradiance for woody seedlings report surprisingly different results. Here we indicate why such disparate results have been produced. We provide a simple analytical approach to understanding why crossovers should occur among particular species at particular stages of ontogeny. This approach is useful for understanding the maintenance of forest species richness, as well as for interpreting plant specialization in physiology and morphology to contrasting irradiance regimes. We reconsider here seven studies (Table 1) that focused on the dry-mass RGRs of five to 15 species of woody seedlings from temperate or tropical systems, at two or more irradiances (comprising at least understorey shade, i.e. ≈2% daylight, and tree-fall gap irradiance, i.e. 10–25% daylight); in each study the species spanned a wide spectrum of shade tolerance/light demand. The results can be summarized by the correlation coefficients of RGRgap and RGRunderstorey calculated from the final harvests of all species in each study (Kitajima 1994). The extreme opposite results are shown in Fig. 1: an almost complete positive correlation (Kitajima 1994), and a nearly significant negative one (Agyeman, Swaine & Thompson 1999). While most studies show an overall positive correlation, its strength varies (Table 1, iii). Plots of RGRgapvs. RGRunderstorey from two contrasting studies: (a) a study showing a strong positive correlation (data from Kitajima 1994); (b) one showing a negative trend (data from Agyeman et al. 1999). How do such different patterns arise from the same type of experiment? We suggest that a major cause is the different methods used to grow seedlings, and the harvest intervals chosen. For instance, we suppose that harvesting seedlings after a short time will produce rank retentions that would not be found in longer studies, and that do not represent the relative performances of seedlings during longer periods of growth in the wild. For example, while a certain small-seeded, light-demanding species may grow more quickly than a certain large-seeded shade-tolerator, both in deep shade and at high irradiance immediately after emergence, we suggest that the advantage in deep shade may well be temporary. After a year or two (assuming it survives), it may well be outranked in the shade by the shade-tolerator. This is expected from what is known of seedling physiology. The small-seeded seedling will have an initial burst of relative growth consistent with its initially very high specific leaf area (lamina area/lamina dry mass, SLA), which gives it a relatively high leaf area ratio (lamina area/plant dry mass, LAR; Grubb 1998a; Grubb et al. 1996; Marañón & Grubb 1993; Wright & Westoby 1999). As a result, it will have the superior RGR at both gap and understorey irradiances. However as the seedlings grow larger, differences among species' SLAs diminish (Grubb et al. 1996; Veneklaas & Poorter 1998), lose their correlation with seed size (Grubb et al. 1996), and cease to be the chief determinant of RGR (Grubb et al. 1996), a point further explained in the following section. Once other factors influence RGR, the large-seeded shade-tolerator may outrank the small-seeded light-demander at understorey irradiance, although not at gap irradiance (indicated by the trends of RGR over time in Walters, Kruger & Reich 1993). A longer study will therefore produce more rank changes between gap and understorey irradiance than a shorter study. We can test this idea with the data from the seven studies reviewed here. First, however, we need to take a step beyond the correlation analysis described above, and for each study to consider the crossovers of the individual species pairs. For each study, we fitted for each species a line representing dry mass relative growth (in g g−1 week−1) as a logarithmic function of irradiance (% daylight), using ordinary linear regression: where R, the slope of the line, represents responsiveness to irradiance, and L, the y intercept, represents the theoretical dark loss rate, the negative RGR in complete darkness. We note that fitting the logarithmic model sometimes results in positive L values; this occurs because in some studies data are scarce for RGRs at very low irradiance, where species respond strongly to irradiance. As L is purely theoretical, and as even positive values can be usefully compared with other species'L values, we have included them in the analysis. Excluding the species with positive L values does not alter the findings of our analysis. All statistics were performed using minitab for Windows Release 12. Very frequently the fit is significant (P < 0·05), even when only three data points are available. We are concerned here only with the range of irradiance over which species show increasing RGRs, and therefore we exclude growth data for photoinhibitory irradiances or limitation, by nitrogen for example (for these studies we excluded data for irradiances above 23% daylight). As data are scarce, methods of less than ideal exactitude must suffice; we fitted the function to only two data points when the absence of other data made this necessary. While the logarithmic function is adequate, other models such as the Michaelis–Menten function may have advantages when more data are available (see sapling studies below). A major advantage of using a two-parameter function such as the logarithmic is that we can easily estimate the irradiance at which the crossover of any two species' RGR functions occurs, the crossover point irradiance (CPI): Equation 2 emphasizes that just as any two non-parallel lines must cross, any two species' RGR functions must cross over. Therefore two species must switch rank at a particular irradiance if their R values differ. When the difference between two species'R values is small, relative to the difference between their L values, the CPI may become wholly theoretical, occurring above 100% or below 0% daylight. Otherwise the CPI is likely to occur between 0 and 100% daylight. The CPI may be calculated for each species pair; it then allows prediction of which of the pair grows more quickly at any irradiance. The estimated R and L values may be used to calculate the difference between the species' RGRs at any irradiance. We emphasize that R and L values are statistical quantities, and are subject to uncertainty – largely due to intraspecific variability in RGR response. For this reason, any study that quotes studies'R and L values, or the derived CPI values, should also provide standard errors or confidence intervals (Sokal & Rohlf 1995). We do not offer here the parameters for prediction for any particular species or species pair. Below, when we refer to a species'R value (or L value), we mean a central value for the species. In the following analysis of CPIs we are chiefly interested in comparing trends across studies; for the statistics we use (median and interquartile range) the standard errors of individual species' values are not needed. Once the CPIs are calculated for each species pair, the percentage occurring between understorey and gap irradiances can be determined (Table 1, iv). When a species pair's CPI falls within this range, a rank-reversal between understorey and gap irradiance results. The percentage of species pairs' CPIs that occurs between understorey and gap irradiance provides a more complete quantification of rank reversals for each study than is possible in a plot of RGRgapvs. RGRunderstorey (of the type shown in Fig. 1), or in considering correlation coefficients. Ultimately the information is the same: >50% indicates the emergence of a negative correlation across species between these irradiances, that is, the plot beginning to slope negatively. This analysis again highlights the disparity among the studies: the percentage of species pairs crossing over between gap and understorey irradiance ranges from 11 to 68%. Just as species' RGR functions change during ontogeny, species pairs' CPIs will change with time. We predict that they will often increase, at least for many of those species pairs comprising a small-seeded light-demander and a large-seeded shade-tolerator. As we suggested earlier, when RGRs are determined primarily by seed size (through SLA), the light-demander will grow more quickly at both gap and understorey irradiances, and so the species pair's CPI will at this stage be very low, well below understorey irradiance. However, as the seed-size effect diminishes, the shade-tolerator will often outperform the light-demander at understorey irradiance; the CPI will hence increase to a value above that irradiance. We can test this hypothesis with the seven studies' data. However, as the studies included different sets of species, we cannot compare their species pairs' CPIs directly; instead we compare their CPI summary statistics. Most useful here are the median and interquartile range of the species pairs' CPIs (Table 1, v). The variability of the studies' medians is apparent. For the two studies showing strongest general rank retention (Grubb et al. 1996; Kitajima 1994), most of the species pairs' crossovers occur at <2% daylight; the other studies show a range of higher median values. The studies used various pretreatments and growth periods (Table 2). Confirming our hypothesis, the range of CPI medians reflects the range of seedling growth periods; for the seven studies, median CPI is correlated strongly to experimental duration (Fig. 2; r2 = 0·73; P = 0·014). The longer the study, the greater the irradiance at which its species tend to change rank. The dispersion of the species pairs' CPIs also increases: studies' interquartile ranges increase linearly with seedling age (r2 = 0·92; P < 0·001). Median species pair crossover-point irradiance (CPI) vs. seedling growth period (pretreatment + experimental growth period) for the seven studies in Table 1. We note that the results of two other studies of species' dry mass RGRs across irradiances (Boot 1996; Reich et al. 1998a) are consistent with these trends: including points for these species gives for the first trend r2 = 0·73 (P = 0·002), and for the second trend r2 = 0·90 (P < 0·001). We did not include these studies in the full analysis because they did not match the criteria met by the other seven studies – one covered too few species (Boot 1996), and for the other the lowest irradiance used was 5% daylight (Reich et al. 1998a). The trends described above ensure that short studies of species that vary in seed size produce low CPIs (<2% daylight), with minimal scatter, while longer studies produce crossover points scattering widely, with their medians occurring between gap and understorey irradiances. Most of the studies were long enough to result in >20% of the crossover points occurring between gap and understorey irradiance. This finding illustrates the principle that very short studies do not adequately represent the processes of long-term natural establishment, unless one can competently scale up. The finding that median CPI increases stably with time suggests that scaling up is possible. This analysis is only roughly quantitative; we compare studies of different species, grown in different locations, in different ambient conditions. Further, many of the studies used imperfect methodologies, including problematic calculations of RGRs (e.g. weighing for 'initial biomass' of the ungerminated embryo-cum-endosperm, or weighing young seedlings after removal of cotyledons or still-attached seeds), pretreating species differently, growing species for different lengths of time and/or in differently sized pots, and fertilizing and watering on an ad hoc basis. These are confounding influences, and future experiments will presumably achieve greater rigour. The robust and systematic trends we demonstrate suggest that once such rigour is achieved in several long, multiple-harvest experiments on identical groups of species, quantitative trends may emerge which will allow prediction of rank reversals and rank retentions over different growth periods. Why should so many species pairs' CPIs increase as seedlings mature? We have suggested that seed size is a major factor. Because most researchers select mainly small-seeded light-demanders and large-seeded shade-tolerators, this effect is common. For light-demanders and shade-tolerators of similar seed size, we might expect a smaller CPI shift. The importance of such seed size effects on CPI shifts in nature requires study. While seed size correlates strongly with shade tolerance for certain species sets, for others there is only a weak correlation, or none, as light demand is only one of a host of potentially strong evolutionary influences on seed traits (Grubb 1996; Grubb 1998b; Grubb & Metcalfe 1996). A completely different reason for the CPI shift may be the fact that plants become increasingly pot-bound, chiefly due to increasing nutrient limitation (cf. Ingestad 1982), but perhaps also to space limitation (Cresswell & Causton 1988; McConnaughay & Bazzaz 1992). This issue also requires study. Leaving such questions aside for the moment, we can use the parameters of the species' RGR to further investigate the CPI shift. As described earlier, L and R determine each species pair's CPI by equation 2. We ask to what degree this equation constrains the possible CPI: is there a general relationship between L and R? Classical theory suggests a negative correlation. For leaves, mass-based dark respiration rate is positively correlated across species with light compensation point and maximum mass-based photosynthetic rate (Givnish 1988). If modelled logarithmically, this relation becomes a negative L- vs. R-type correlation (with dark respiration rate analogous to –L, and photosynthetic rate analogous to RGR). For whole plants, a species'R value will be determined not only by photosynthetic responsiveness, but also by morphology; and a species'L value will reflect not only dark respiration rate but also loss of parts. Remarkably, there is a significant whole-plant L vs. R correlation for four of the seven studies at P < 0·05, and for a fifth at P = 0·078 (Table 1, vi; Fig. 3). The slopes of regression for each study vary greatly (Table 1, vii); as expected (Sokal & Rohlf 1995) the two studies with shallowest L vs. R slopes show no correlation. L vs. R plot for the species in a single study (data from Agyeman et al. 1999). The L vs. R trade-off described is a new example of a quantifiable trade-off between resource acquisitiveness and retentiveness (cf. Grime 1974). Mechanistically, the species that increase their RGR most when given a larger resource supply often pay a price in high respiration rate (Reich et al. 1998a; Reich et al. 1998b) and/or short-lived parts (Walters & Reich 1999). The trade-off has further relevance as a tool for investigating the physiological and morphological bases for species pairs' crossovers. Firstly, for most studies the tightness of the line's fit (Figure 3) means that we can predict each species'L value from its R value from the regression: where ɛi represents the error, the deviation of species i's L value from that predicted by the line. This equation must constrain the CPI for each species pair, as it correlates L and R, the parameters used for the CPI calculation. The variation among the studies'L vs. R slopes (α;Table 1, vii) indicates that a separate equation holds for each study; therefore, a study's α value can play a major role in determining the CPI values of its species pairs. This is clarified if equation 3 is substituted into equation 2: If there were no scatter about a study's L vs. R regression (and therefore for each species pair ɛspeciesA = ɛspeciesB = 0), all the species' RGR functions would cross over at eα − 1, that is, the steeper the slope of the study's L vs. R line, the higher will be the study's median CPI (studies' median CPIs and α values are positively correlated, r = 0·84, P = 0·018). α should vary with median CPI across the studies is not As we have the studies a range of seedling growth the differences in morphology among a of young seedlings of species from a wide range of seed and the changes in morphology of each species during ontogeny, will the slope of the L vs. R line. of the effects will however, we suggest that initially α values can arise from the of initially high values for small-seeded light-demanders and initially low values for large-seeded shade-tolerators, as described Because of the morphological differences among seedlings, species in L may in R during For instance, suppose that during one species has a more negative L than and therefore a irradiance as a result of its If this species also has smaller than the other it is a small-seeded and so a higher it can have a larger R R is both to L, for physiological and positively to This a L vs. R slope (Fig. The species with the more negative L however, have larger and therefore have the lower initial (for instance, if it is a If this is the the species with the more negative L may also have the smaller a plant will produce scatter about the study's L vs. R line, the slope of the of the slope of the loss rate vs. responsiveness during from (a) to A slope may also result when the shade-tolerators are species their cotyledons in the seed species will take longer than species to the stage of positive RGR (Grubb 1998a). shade-tolerators in the understorey will take a long time to up with small-seeded light-demanders in dry mass and leaf in their will for a longer As a result, R is very This is another by which two species in L can in R (Fig. a given irradiance, the species' become more during growth (Grubb et al. 1996; Veneklaas & Poorter 1998), and across irradiances & Poorter If we consider a of species in seed size, as do the seven studies, we are likely to that over time the effect of the initial of the species' at each irradiance will become by species differences in other traits that the L vs. R relationship and the L vs. R slope will will (Fig. this stage possible major of species in RGR in to and leaf in deep Agyeman et al. 1999; & & Reich net photosynthetic rates & Bazzaz 1996; & Reich but et al. and whole-plant & Grubb 1994; & All these traits influence the leaf rate mass which is the other of RGR = high irradiance the species will be those with and low irradiance the species' and not their values, often determine their relative performances et al. 1999; et al. 1994; & 1988). In at low irradiance may show a weak negative correlation with RGR et al. 1999; & as it is those species with values that tend to have the lowest in the shade, due to high and short leaf (Walters & Reich 1999). These effects indicate the of the by Veneklaas & Poorter that RGR differences at low irradiance, while differences at high irradiance. a does not to very young seedlings, RGR at both low and high irradiance is determined by seed differences in and therefore as found by Kitajima The leaf mass the other of does not RGR in young seedlings of woody species et al. 1999; et al. 1994; Reich et al. 1998a; & Reich 1996). However, among certain sets of species the differences in may and the larger, more differences in (Reich et al. 1998a; Veneklaas & Poorter & Reich 1996). Once seed differences in (and have as we have to play a strong determining This first for plants at high irradiance, and later for plants in deep occur when short studies are used as the of 1999; Veneklaas & Poorter at the of such studies the plants at high irradiance have from the first while those in deep shade have is however, that woody seedlings in deep shade the second in which is the in species RGR differences et al. 1999; et al. 1994; & 1988). Once the seedlings have this second as we have the L vs. R slope and many of the light-demanders that initially outranked shade-tolerators in the shade will be in RGR and then in whole-plant species pairs' CPIs shift from below to between understorey and gap level irradiance. the issue of species differences in seedling RGRs across irradiance to the maintenance of forest species The has in from the in the seven studies, and in 1999; & Reich A result from a very short study, such as that of Kitajima will suggest that in nearly a plant that grows most quickly at low irradiance also grows most quickly at high irradiance, and so the light cannot species through species differences in RGR responses to are other in which light can play a as in the there is for a trade-off between survival rate in deep shade and RGR at high irradiance for seedlings and (Grubb et al. 1996; & Kitajima 1994; et al. 1996; 1999). However, the results of short studies do not reflect long-term processes in the When we consider the five studies of the >20% of the species pairs in each study show rank in RGR between gap and understorey irradiance (Table 1, iv). changes to RGR with resource supply rates can potentially to the maintenance of species 1992). the species pairs into type increases We have used following (and that these are and light-demanding and In for the five studies in which >20% of species pairs' CPIs between 2 and daylight, of species pairs of all of have crossovers between 2 and daylight (Table 3). the median CPI and CPI interquartile range for a of seedlings increase linearly with seedling age over the long as for the short the data to this are analogous studies performed on groups of species at the sapling stage have used different methodologies, results not with those of seedling of have and/or RGR & 1994; Wright et al. for this approach used on seedlings 1999). This approach has the to be but it does not immediately of whole-plant relative as or for a given species are to and not at well & 1999; & Grubb 1994). In the several studies of sapling RGRs above, data were at many irradiances, and a Michaelis–Menten fitted to the increase of RGR with irradiance. The model has been used to test for a trade-off between and where the is as one of the the maximum RGR at high irradiance of the and the is as the second the estimated slope of the growth function at irradiance, which indicates the RGR for very deep shade et al. 1994). These studies have a weak trade-off et al. 1994; Wright et al. 1998), or no relationship et al. between and on the of species findings do not a rank retention of species' RGRs across irradiances. For instance, in a study of the RGRs of species of from a wide range of natural light et al. 1994), of species pairs over between 2 and daylight. The median CPI in this study is daylight – a value any of those for the seedling studies (Table 1, consistent with the finding for seedlings that median CPI for a of species pairs increases as plants Further, it suggests that the of the median CPI by the sapling When an the of the seedling growth period and the initial of seedlings used must be As the median CPI of a study's species and the CPI interquartile range, increase as plants the of species pairs' rank reversals will be greatly In future studies it will be to determine the of time one to model in and to grow species for that of or for a shorter over which time harvests are RGRs calculated from later harvest intervals will represent long-term trends than RGRs calculated from analysis indicates that and/or trends may be and natural processes occurring over longer periods may be This that as species' RGR functions change during ontogeny, the changes are studies will be useful in this The L vs. R trade-off described above allows of the morphological and physiological factors a species pair's rank or rank retention at a given irradiance. study of the slope of this and it to species and of study, may to the prediction of species' relative performances at specific irradiances from physiological and morphological The studies made so the idea that species differences in RGR across irradiance do a for the maintenance of species in This assumed that species' RGRs, as determined from plants in reflect their relative in natural This requires above, but potentially very is variation in to as to the light in all of the studies we have & species cross over in to other The CPI approach in be to determining crossovers in for instance, and supply crossovers may also change with one study that when five species from contrasting were grown on the three species from primarily the two from but only for one – by the second the 1996). The crossovers were to a trade-off between rates and leaf 1996), the same principle that we have is one for crossovers in to irradiance. In nutrient studies the principle has also been in of the and loss rates of than & 1993). If woody species cross over in RGR in to and their crossovers change over the patterns may determine an of forest The final however, is this we a for the and even the of forest systems, of any at least at the with the of this – and of also (for the understanding of seed patterns and the of and – will be a theoretical and for understanding and from the level of species to the of species, to We and Wright for their the and of for

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