Tolerance to Shade, Drought, and Waterlogging of Temperate Northern Hemisphere Trees and Shrubs. Niinemets, Ü. & Valladares, F. 76(4):521–547.
Tolerance to Shade, Drought, and Waterlogging of Temperate Northern Hemisphere Trees and Shrubs [link]Paper  doi  abstract   bibtex   
Lack of information on ecological characteristics of species across different continents hinders development of general world-scale quantitative vegetation dynamic models. We constructed common scales of shade, drought, and waterlogging tolerance for 806 North American, European/West Asian, and East Asian temperate shrubs and trees representing about 40\,% of the extant natural Northern Hemisphere species pool. These scales were used to test the hypotheses that shade tolerance is negatively related to drought and waterlogging tolerances, and that these correlations vary among continents and plant functional types. We observed significant negative correlations among shade and drought tolerance rankings for all data pooled, and separately for every continent and plant functional type, except for evergreen angiosperms. Another significant trade-off was found for drought and waterlogging tolerance for all continents, and for evergreen and deciduous angiosperms, but not for gymnosperms. For all data pooled, for Europe and East Asia, and for evergreen and deciduous angiosperms, shade tolerance was also negatively associated with waterlogging tolerance. Quantile regressions revealed that the negative relationship between shade and drought tolerance was significant for species growing in deep to moderate shade and that the negative relationship between shade and waterlogging tolerance was significant for species growing in moderate shade to high light, explaining why all relationships between different tolerances were negative according to general regression analyses. Phylogenetic signal in the tolerance to any one of the three environmental factors studied was significant but low, with only 21-24\,% of cladogram nodes exhibiting significant conservatism. The inverse relationships between different tolerances were significant in phylogenetically independent analyses both for the overall pool of species and for two multispecies genera (Pinus and Quercus) for which reliable molecular phylogenies were available. Only 2.6-10.3\,% of the species were relatively tolerant to two environmental stresses simultaneously (tolerance value $>$3), and only three species were tolerant to all three stresses, supporting the existence of functional trade-offs in adjusting to multiple environmental limitations. These trade-offs represent a constraint for niche differentiation, reducing the diversity of plant responses to the many combinations of irradiance and water supply that are found in natural ecosystems. [Excerpt: Discussion] [::Plant shade tolerance rankings] Any stress factor that decreases the ability of plants to use available light will increase the minimum daily light dose that the plant requires to survive under given conditions. Therefore, there is no single minimum light level that an individual of a particular species tolerates; "shade tolerance" is not an absolute but rather a relative term (Spurr and Barnes 1980). Nutrient and water availabilities, and air and soil temperature are poten tially capable of affecting shade tolerance (Tilman 1993, Bazzaz and Wayne 1994), and they vary in gradients of irradiance across gap-understory continuum. Thus, species' dispersal across light gradients is determined by a complex interplay of various edaphic and climatic factors. Due to this interplay of species' minimum light requirements with other environmental factors, reliable relative rankings of species' shade tolerance potentials are invaluable in trying to understand forest develop ment and diversity. [] [...] [::Plant waterlogging and drought tolerance rankings] Significant negative correlation exists between air humidity and the distance from streams and wetlands (Chen et al. 1999), implying that the way the species respond to gradual changes from excess to limiting water availabilities may significantly modify forest succession along these gradients, and in interaction with shade tolerance determine the forest chronosequence in any specific site with given water availability. Therefore, extended forest gap models also use estimates of species' drought and waterlogging tolerance to predict forest succession (Bugmann and Cramer 1998). Reliable estimates of species' drought and waterlogging tolerance have been noted as primary limitations to further development of these models (Bugmann and Solomon 1995, Bugmann and Cramer 1998). Species' potentials to cope with drought and waterlogging stress are often characterized in succession models using a coarse scale of tolerant/intolerant or by adding the gradation intermediate (Prentice and Helmisaari 1991). Such coarse scale assessments may be adequate for under standing the performance of species assemblages during moderate stress events. More refined species rankings may be needed to predict species' survival during extreme stress periods that occur only infrequently, but that greatly influence community composition. [] [...] [::Inverse correlations between species' ecological potentials] An inverse correlation between species' shade and drought tolerance has been hypothesized in several studies (Smith and Huston 1989, Abrams 1994, Kubiske et al. 1996), but tests of this hypothesis are conflicting. Kubiske et al. (1996) investigated gas-exchange physiol ogy in six species of varying shade and drought tolerance and found a stronger effect of drought on leaf physiology in shade tolerant than in intolerant species. In contrast, Sack (2004) found a similar effect - of drought on growth in 12 species of varying shade and drought tolerance. We observed an inverse correlation between species' shade and drought tolerance for 806 species covering the major dominants in North American, European/West Asian, and East Asian temperate woody ecosystems [...], as well as separately for every continent [...], and plant functional type [...], except for the evergreen angiosperms [...] [] [...] [::Simultaneous tolerance to shade and drought] Certain species appeared to be tolerant of both drought and shade (Appendix A), a simultaneous tolerance that is difficult to understand given the conflicting requirements for efficient light capture (large leaf area, enhanced biomass investment aboveground) and drought avoidance (low leaf area, enhanced biomass investment in roots). However, none of the species tolerant of both shade and drought were very tolerant to either of these limitations, which indicates that this trade-off inevitably shaped the observed patterns to at least some degree. Interestingly, essentially all of the species tolerant of both shade and drought were those colonizing relatively warm habitats (minimum winter T $>$ -15 °C) extending from the temperate deciduous forests to warm temperate forests at the transition to Mediterranean habitats (see Plate 1). This suggests that the species tolerant of both shade and drought may require extended growing periods to construct a canopy that can support high leaf area, even though this leaf area may be drought stressed during a significant part of the year. [] [...] [::Poly tolerance: rarity and possible implications] Several species that were moderately tolerant (toler ance value $>$3.0) simultaneously to several environ mental factors such as Acer negundo (shade/drought), Lonicera xylosteum (shade/drought), Prunus padus (shade/waterlogging), Rhododendron ponticum (shade/ drought), and Tamarix ramosissima (waterlogging/ drought), have been reported as invasive outside their natural areas (Randall and Marinelli 1996, Mooney and Hobbs 2000). However, the three plant species in our study that were simultaneously tolerant to all three environmental limitations (Amelanchier laevis, Rhododendron periclymenoides, and Rhododendron viscosum, with tolerance value for all characteristics $>$3.0) are species with very limited invasive potential, suggesting that polytolerance is not associated with invasiveness. Besides, the mean tolerance value was 3.0-3.5 for these species suggesting that polytolerant plants were not very tolerant to any of these environmental limitations. Being simultaneously tolerant to several environmental limi tations could imply a lack of full adaptation to each particular limitation. [Conclusions] Limited and often biased information on species' ecological potentials and scarcity of comparative in formation on species' ecological potentials on different continents has hampered the development of general world-scale vegetation dynamic models. All temperate forests in the Northern Hemisphere are physiognomi cally similar, often sharing species from the same genera at various stages of succession (Alnus, Betula, Pinus, and Populus in early-successional forests and Abies, Acer, Fagus, and Picea in late-successional forests), suggesting similar performance of temperate forests on different continents and possibilities for common general patterns at broad geographical scales. [] With a few exceptions, the negative correlations among shade, drought, and waterlogging tolerance were significant for our global data set as well as within each functional or phylogenetic group considered. These negative correlations indicate that the number of possible combinations of ecological potentials in a species is limited by trade-offs between tolerance to differing environmental limitations. In fact, and as the data demonstrate, few species are characterized by simultaneous tolerance to two environmental factors, and even fewer are moderately tolerant to three environmental factors. Although most species com monly cope with multiple environmental limitations, polytolerance has not been frequently achieved during the evolution of trees and shrubs of the Northern Hemisphere. The trade-offs among the tolerances to different limiting factors found here represent a con straint for niche differentiation of coexisting species since they reduce the diversity of plant responses to the many combinations of irradiance and water supply that are found in natural ecosystems. [] [...]
@article{niinemetsToleranceShadeDrought2006,
  title = {Tolerance to Shade, Drought, and Waterlogging of Temperate Northern Hemisphere Trees and Shrubs},
  author = {Niinemets, Ülo and Valladares, Fernando},
  date = {2006-11},
  journaltitle = {Ecological Monographs},
  volume = {76},
  pages = {521--547},
  issn = {0012-9615},
  doi = {10.1890/0012-9615(2006)076[0521:TTSDAW]2.0.CO;2},
  url = {https://doi.org/10.1890/0012-9615(2006)076[0521:TTSDAW]2.0.CO;2},
  abstract = {Lack of information on ecological characteristics of species across different continents hinders development of general world-scale quantitative vegetation dynamic models. We constructed common scales of shade, drought, and waterlogging tolerance for 806 North American, European/West Asian, and East Asian temperate shrubs and trees representing about 40\,\% of the extant natural Northern Hemisphere species pool. These scales were used to test the hypotheses that shade tolerance is negatively related to drought and waterlogging tolerances, and that these correlations vary among continents and plant functional types. We observed significant negative correlations among shade and drought tolerance rankings for all data pooled, and separately for every continent and plant functional type, except for evergreen angiosperms. Another significant trade-off was found for drought and waterlogging tolerance for all continents, and for evergreen and deciduous angiosperms, but not for gymnosperms. For all data pooled, for Europe and East Asia, and for evergreen and deciduous angiosperms, shade tolerance was also negatively associated with waterlogging tolerance. Quantile regressions revealed that the negative relationship between shade and drought tolerance was significant for species growing in deep to moderate shade and that the negative relationship between shade and waterlogging tolerance was significant for species growing in moderate shade to high light, explaining why all relationships between different tolerances were negative according to general regression analyses. Phylogenetic signal in the tolerance to any one of the three environmental factors studied was significant but low, with only 21-24\,\% of cladogram nodes exhibiting significant conservatism. The inverse relationships between different tolerances were significant in phylogenetically independent analyses both for the overall pool of species and for two multispecies genera (Pinus and Quercus) for which reliable molecular phylogenies were available. Only 2.6-10.3\,\% of the species were relatively tolerant to two environmental stresses simultaneously (tolerance value {$>$}3), and only three species were tolerant to all three stresses, supporting the existence of functional trade-offs in adjusting to multiple environmental limitations. These trade-offs represent a constraint for niche differentiation, reducing the diversity of plant responses to the many combinations of irradiance and water supply that are found in natural ecosystems.

[Excerpt: Discussion]

[::Plant shade tolerance rankings] Any stress factor that decreases the ability of plants to use available light will increase the minimum daily light dose that the plant requires to survive under given conditions. Therefore, there is no single minimum light level that an individual of a particular species tolerates; "shade tolerance" is not an absolute but rather a relative term (Spurr and Barnes 1980). Nutrient and water availabilities, and air and soil temperature are poten tially capable of affecting shade tolerance (Tilman 1993, Bazzaz and Wayne 1994), and they vary in gradients of irradiance across gap-understory continuum. Thus, species' dispersal across light gradients is determined by a complex interplay of various edaphic and climatic factors. Due to this interplay of species' minimum light requirements with other environmental factors, reliable relative rankings of species' shade tolerance potentials are invaluable in trying to understand forest develop ment and diversity. [] [...]

[::Plant waterlogging and drought tolerance rankings] 

Significant negative correlation exists between air humidity and the distance from streams and wetlands (Chen et al. 1999), implying that the way the species respond to gradual changes from excess to limiting water availabilities may significantly modify forest succession along these gradients, and in interaction with shade tolerance determine the forest chronosequence in any specific site with given water availability. Therefore, extended forest gap models also use estimates of species' drought and waterlogging tolerance to predict forest succession (Bugmann and Cramer 1998). Reliable estimates of species' drought and waterlogging tolerance have been noted as primary limitations to further development of these models (Bugmann and Solomon 1995, Bugmann and Cramer 1998). Species' potentials to cope with drought and waterlogging stress are often characterized in succession models using a coarse scale of tolerant/intolerant or by adding the gradation intermediate (Prentice and Helmisaari 1991). Such coarse scale assessments may be adequate for under standing the performance of species assemblages during moderate stress events. More refined species rankings may be needed to predict species' survival during extreme stress periods that occur only infrequently, but that greatly influence community composition.

[] [...]

[::Inverse correlations between species' ecological potentials] An inverse correlation between species' shade and drought tolerance has been hypothesized in several studies (Smith and Huston 1989, Abrams 1994, Kubiske et al. 1996), but tests of this hypothesis are conflicting. Kubiske et al. (1996) investigated gas-exchange physiol ogy in six species of varying shade and drought tolerance and found a stronger effect of drought on leaf physiology in shade tolerant than in intolerant species. In contrast, Sack (2004) found a similar effect - of drought on growth in 12 species of varying shade and drought tolerance. We observed an inverse correlation between species' shade and drought tolerance for 806 species covering the major dominants in North American, European/West Asian, and East Asian temperate woody ecosystems [...], as well as separately for every continent [...], and plant functional type [...], except for the evergreen angiosperms [...]

[] [...]

[::Simultaneous tolerance to shade and drought]

Certain species appeared to be tolerant of both drought and shade (Appendix A), a simultaneous tolerance that is difficult to understand given the conflicting requirements for efficient light capture (large leaf area, enhanced biomass investment aboveground) and drought avoidance (low leaf area, enhanced biomass investment in roots). However, none of the species tolerant of both shade and drought were very tolerant to either of these limitations, which indicates that this trade-off inevitably shaped the observed patterns to at least some degree. Interestingly, essentially all of the species tolerant of both shade and drought were those colonizing relatively warm habitats (minimum winter T {$>$} -15 °C) extending from the temperate deciduous forests to warm temperate forests at the transition to Mediterranean habitats (see Plate 1). This suggests that the species tolerant of both shade and drought may require extended growing periods to construct a canopy that can support high leaf area, even though this leaf area may be drought stressed during a significant part of the year.

[] [...]

[::Poly tolerance: rarity and possible implications]

Several species that were moderately tolerant (toler ance value {$>$}3.0) simultaneously to several environ mental factors such as Acer negundo (shade/drought), Lonicera xylosteum (shade/drought), Prunus padus (shade/waterlogging), Rhododendron ponticum (shade/ drought), and Tamarix ramosissima (waterlogging/ drought), have been reported as invasive outside their natural areas (Randall and Marinelli 1996, Mooney and Hobbs 2000). However, the three plant species in our study that were simultaneously tolerant to all three environmental limitations (Amelanchier laevis, Rhododendron periclymenoides, and Rhododendron viscosum, with tolerance value for all characteristics {$>$}3.0) are species with very limited invasive potential, suggesting that polytolerance is not associated with invasiveness. Besides, the mean tolerance value was 3.0-3.5 for these species suggesting that polytolerant plants were not very tolerant to any of these environmental limitations. Being simultaneously tolerant to several environmental limi tations could imply a lack of full adaptation to each particular limitation.

[Conclusions]

Limited and often biased information on species' ecological potentials and scarcity of comparative in formation on species' ecological potentials on different continents has hampered the development of general world-scale vegetation dynamic models. All temperate forests in the Northern Hemisphere are physiognomi cally similar, often sharing species from the same genera at various stages of succession (Alnus, Betula, Pinus, and Populus in early-successional forests and Abies, Acer, Fagus, and Picea in late-successional forests), suggesting similar performance of temperate forests on different continents and possibilities for common general patterns at broad geographical scales.

[] With a few exceptions, the negative correlations among shade, drought, and waterlogging tolerance were significant for our global data set as well as within each functional or phylogenetic group considered. These negative correlations indicate that the number of possible combinations of ecological potentials in a species is limited by trade-offs between tolerance to differing environmental limitations. In fact, and as the data demonstrate, few species are characterized by simultaneous tolerance to two environmental factors, and even fewer are moderately tolerant to three environmental factors. Although most species com monly cope with multiple environmental limitations, polytolerance has not been frequently achieved during the evolution of trees and shrubs of the Northern Hemisphere. The trade-offs among the tolerances to different limiting factors found here represent a con straint for niche differentiation of coexisting species since they reduce the diversity of plant responses to the many combinations of irradiance and water supply that are found in natural ecosystems.

[] [...]},
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  number = {4}
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