Plant responses to heterogeneous environments: scaling from shoot modules and whole-plant functions to ecosystem processes

Plant individuals are characterized by modular architecture, consisting of hierarchically positioned similar basic semi-autonomous units termed “modules” that have species- and plant functional-type-specific morphological and physiological characteristics (White 1979; Harper 1985; Silvertown and Gordon 1989; Prusinkiewicz 2000; Kawamura 2010). The basic units underlying the modular organization can be buds, metamers, shoots, branches, or ramets depending on plant functional type (Barthélémy and Caraglio 2007; Kawamura 2010). The plants exhibit a characteristic acclimation “behavior” by changing the size, shape, number, and within-plant arrangement of such modular units in response to variation in local distribution and availability of resources required. Although the degree of plastic changes of the module attributes is genetically and mechanically restricted, module-level plasticity plays a key role in whole-plant acclimation to local resource heterogeneity (White 1979; Silvertown and Gordon 1989; Leverenz and Hinckley 1990; Karban 2008).

Most terrestrial vascular plants are sessile organisms bound to accomplish their life cycle in one single location, and their growth and survival are therefore inevitably affected by environmental conditions prevailing in their habitat (Karban 2008). As environmental conditions strongly fluctuate in time and can change in a predetermined manner, for instance during growth and development of surrounding vegetation, acclimation to habitat environmental conditions is the key for survival of plants in changing environments. The capacity to change morphological and/or physiological characteristics at various organizational levels, phenotypic plasticity, is inherent to all plant species and leads to the enhancement of plants’ efficiency of resource capture and use (e.g., Valladares et al. 2007; Niinemets 2010).

Extensive studies in a variety of taxonomically, phylogenetically, and ecologically different plant species have been conducted to determine phenotypic plasticity to optimize resource harvesting in changing environments in different species and plant functional types (e.g., Valladares et al. 2007 for a review). As a result, a vast body of information has been accumulated on plant plastic responses at scales of organization ranging from leaf to whole-plant (e.g., Barthélémy and Caraglio 2007). Studies demonstrate that leaf-, shoot-, branch-, crown-, and/or ramet-level variations in structural characteristics all contribute to maximization of resource capture of plants in resource-limited environments (Niinemets 2010). Modular responses to local heterogeneity, such as variable placement of foliage units in response to light availability, is one of the most significant drivers in generating the phenotypic plasticity of plants (e.g., Valladares and Niinemets 2007; Mori and Hasegawa 2007; Mori et al. 2008; Niinemets 2010). Nevertheless, there is still limited knowledge on how the module-level responses to within-crown and within-stand microenvironment affect whole-plant function under intrinsic multiple environmental and intrinsic biomechanical constraints. It is thus highly relevant to synthesize the current knowledge on diverse structural controls at various hierarchical scales to understand the resultant effects on plant performance (Kawamura 2010; Kennedy 2010; Niinemets 2010).

Recent studies have shown that species-specific plasticity to spatial and temporal changes in resource availability within the crown results in functional diversification or convergence of key plant traits among coexisting species. Functional diversification has been proven by studies on morphological and physiological plant characteristics determining species-specific strategies for light interception and carbon gain, which contribute to some degree of niche partitioning among species and their resultant coexistence (e.g., Mori and Takeda 2004). Then, recent research has provided evidence of functional convergence, which means phenomena that apparently different key plant characteristics can realize similar levels of ecophysiological function among coexisting species (e.g., Valldares et al. 2002; Ishii et al. 2009; Ishii and Asano 2010). This evidence further emphasizes the importance of plant phenotypic plasticity in affecting the community- and ecosystem-level processes. The determining role of plastic alterations in whole-plant productivity can be further inferred from strong positive relationships between ecosystem-level canopy productivity and the amount of intercepted light (Lagergren et al. 2004; Duursma and Mäkelä 2007). Because shoot growth, leaf arrangement, and development of crown architecture finally all serve to enhance carbon gain at the whole-plant level (e.g., Mori et al. 2008), ecosystem productivity as a composite of carbon gains of coexisting plant individuals is driven by the factors altering individual plant productivity, i.e., plant communities inherently operate as collections of individuals rather than as a canopy with integrated functional attributes (Anten 2002; Anten and Hirose 2001). Thus, dynamic modifications in module-based plant behavior play a key role in stand development and productivity in highly heterogeneous natural environments.

In this issue, we aim to discuss the various aspects of plant variability in response to heterogeneous environments. Kawamura (2010) overviews the module-based plant responses to local heterogeneity, which is of paramount importance for sessile plants to maximize resource capture and utilization. Kennedy (2010) demonstrates how foliage units affect whole-plant functions. These studies emphasize the fundamental importance of shoot-level responses in determining plant performances. Ishii and Asano (2010) discuss the importance of the spatiotemporal differentiation in shoot/leaf- and crown-level morphological responses to capture resources among coexisting species. Ishii and Asano (2010) further suggest that such complementary use of resources among species may contribute to increasing stand productivity. This coincides with the viewpoint of Niinemets (2010), which notes that resource harvesting at various scales from a foliage unit to whole-crown within-plant individuals is one of the significant components in stand dynamics and productivity. Based on the above factors, we conclude that understanding the ecological interactions among morphological and physiological traits at various scales of organization is highly relevant for process-based scaling of resource harvesting and productivity from individual plants to ecosystems.