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 Thomas 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 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 (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 Wright Veneklaas 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 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 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 McConnaughay 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 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 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 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