The need for a canopy perspective to understand the importance of phenotypic plasticity for promoting species coexistence and light-use complementarity in forest ecosystems
- 2.1k Downloads
Because of their overwhelming size over other organisms, trees define the structural and energetic properties of forest ecosystems. From grasslands to forests, leaf area index, which determines the amount of light energy intercepted for photosynthesis, increases with increasing canopy height across the various terrestrial ecosystems of the world. In vertically well-developed forests, niche differentiation along the vertical gradient of light availability may promote species coexistence. In addition, spatial and temporal differentiation of photosynthetic traits among the coexisting tree species (functional diversity) may promote complementary use of light energy, resulting in higher biomass and productivity in multi-species forests. Trees have evolved retaining high phenotypic plasticity because the spatial/temporal distribution of resources in forest ecosystems is highly heterogeneous and trees modify their own environment as they increase nearly 1,000 times in size through ontogeny. High phenotypic plasticity may enable coexistence of tree species through divergence in resource-rich environments, as well as through convergence in resource-limited environments. We propose that the breadth of individual-level phenotypic plasticity, expressed at the metamer level (leaves and shoots), is an important factor that promotes species coexistence and resource-use complementarity in forest ecosystems. A cross-biome comparison of the link between plasticity of photosynthesis-related traits and stand productivity will provide a functional explanation for the relationship between species assemblages and productivity of forest ecosystems.
KeywordsComplementarity theory Diversity–productivity theory Forest architecture theory Niche differentiation Species coexistence
Trees are the largest organisms on Earth, and forests hold the greatest biomass among terrestrial ecosystems of the world. Trees are the primary producers that generate, through photosynthesis, the energy that flows through the food and detritus chains (Scheu 2005). Because of their overwhelming size over other organisms, trees are also the “engineers” (Jones et al. 1994) that build the structure of forest ecosystems and define its environmental and chemical properties, as well as the “habitat template” on which other organisms establish (Southwood and Kennedy 1983; Takeda and Abe 2001).
Trees are remarkable because they start out as tiny seedlings and grow to nearly 1,000 times in size during ontogeny. In a mature forest, individuals of various sizes coexist. Some species can acclimate to a wide range of resource availabilities and exist in multiple generations comprising understory seedlings to mature canopy trees. Within the same geographic region, natural forests that are well-developed vertically tend to hold greater diversity of tree species and maintain higher primary productivity than low statured forests (Franklin et al. 1989; Ishii et al. 2004). In this paper, we will review theories related to the structural development of forest ecosystems and how it may promote species coexistence. We will explore how spatial and temporal differentiation in resource use, especially light, among coexisting tree species may provide a functional explanation for why stand productivity increases with increasing species diversity. Finally, we discuss the importance of considering trait plasticity within individuals when assessing the functional diversity of forest ecosystems.
Vertical development, ecosystem productivity, and species diversity
From grasslands to forests, annual net primary production increases with increasing leaf area index (LAI) across the various terrestrial ecosystems of the world (LAI, leaf area per unit ground area, Asner et al. 2003). This is because the amount of light energy intercepted for photosynthesis by a plant canopy increases with increasing LAI, i.e., the greater the leaf area that is packed into a unit of ground area, the greater the ecosystem productivity. In forest ecosystems, LAI tends to increase with increasing canopy height, because biomass density (kg m−3) is relatively constant across various forest types (Kira and Shidei 1967) and thus more leaf area can be stacked vertically in a tall forest. Forests with the largest LAI and greatest biomass in the world are found in the cool-temperate region of the pacific northwest coast of North America (Franklin et al. 2002; Fujimori et al. 1976; Sillett and Van Pelt 2007). In these forests, the canopy reaches 70–100 m in height and comprises the world’s tallest trees. The dominant, evergreen conifer species include some of the tallest tree species in the world: Sequoia sempervirens (D. Don.) Endl., Pseudotsuga menziesii (Mirb.) Franco. var. menziesii, and Picea sitchensis (Bong.). Carr. These trees are not only tall, but extremely long-lived and stand age may reach 800–1,000 years in some areas (Franklin and Dyrness 1973). As a result, great amounts of carbon are stored both above and below ground (Harmon et al. 2004; Winner et al. 2004).
In grassland ecosystems, it has been shown experimentally that productivity increases with increasing species diversity (Hector et al. 1999; Tilman et al. 2001). Although stand productivity tends to be higher for more species-rich forest communities (e.g., Harmon et al. 1990; Ishii et al. 2004; Vila et al. 2003, but see Firn et al. 2007), it is difficult to obtain direct evidence supporting the diversity-productivity theory that pertains to forest ecosystems because, in natural forests, the various factors determining community assembly and ecosystem productivity are often confounded (Vila et al. 2005) and field experiments take several years to execute (Hector et al. 2011; Pretzsch 2005; Whittaker et al. 2001). The best test of the diversity–productivity relationship in forest ecosystems that we are aware of is that of Hiura (2001), who showed that species richness, LAI and total carbon are correlated positively with each other across 38 forest plots having different disturbance histories (Table 3 in Hiura 2001), all of which established on relatively flat topography after a volcanic eruption rendering uniform initial conditions.
Complementary resources use and functional diversity
A proposed mechanism for increased productivity with increasing species diversity is that it leads to complementary resource use (Hector 1998; Hooper 1998; Naeem et al. 1994). Complementarity is defined as the increase in resource-use efficiency of a mixed species community compared with that of a monoculture as a result of reduced niche overlap and competitive relaxation (Yachi and Loreau 2007). Because plants are the primary producers that define the structural and energetic properties of terrestrial ecosystems, the diversity of traits concerned with light capture and primary production are important determinants of ecosystem productivity. In grassland ecosystems, the presence of contrasting traits among species, such as foliar architecture and shade tolerance, promotes light-use complementarity and contributes to increasing primary productivity (Vojtech et al. 2008; Zhang et al. 2012). Similarly, for woody species, trait divergence reduces niche overlap and relaxes competition, allowing even closely related species to coexist (Beltran et al. 2012). These observations suggest that not only the number of species per se, but their functional diversity (i.e., phenotypic variation) is an important factor underlying the diversity-productivity theory (Loreau 2010).
Photosynthesis is an important physiological function that determines the productivity and shade tolerance of a species (Anten 2005; Poorter and Bongers 2006; Valladares and Niinemets 2008; Werger et al. 2002). Thus we hypothesize that, if divergence of photosynthesis-related traits among species and their differentiation along the vertical gradient of light availability results in complementary resources use, it would lead to increased ecosystem productivity with increasing species diversity. There are several empirical examples that suggest our hypothesis may apply to forest ecosystems. When plantation forests of the same planting density are compared, productivity tends to be at least as high, or higher for mixed than monoculture stands (Garber and Maguire 2004; Kelty et al. 1992; Piotto 2008). In some mixtures, the increase in productivity was attributed to light-use complementarity between species (Amoroso and Turnblom 2006; Forrester et al. 2005). In natural, mixed forests of Japan and New Zealand, where conifers and broadleaved trees coexist, the basal area of conifers is additive, meaning that stand biomass is higher in mixed forests than in forests comprising only broadleaved trees (Aiba et al. 2007; Midgley et al. 2002). In the mixed conifer-broadleaved forest on Yakushima Island in southern Japan, coexistence of conifers and broadleaved trees is realized through stratification along the vertical gradient of light availability (Inoue and Yoshida 2001; Ishii et al. 2010). Increased productivity and additive basal area of mixed forests may be the result of species differences in above-ground traits (height growth pattern, crown form, leaf morphology, shade tolerance, etc.) that determine photosynthetic gain, as well as below-ground traits (root growth, morphology, etc.) that determine uptake of water and nutrients. Functional differentiation among species may lead to competitive relaxation in mixed stands, whereas competition may be more intense in monocultures and less species-rich forests (Ewel and Mazzarino 2008; Jones et al. 2005; Kelty 2006). A critical physiological function that underlies all of the above characteristics is photosynthetic production and allocation of photosynthate within individual trees (Poorter et al. 2006; Selaya et al. 2007).
The importance of individual-level phenotypic plasticity in trees
Greater functional diversity among coexisting plant species may allow access to more of the total available resources, leading to increased productivity (Cadotte et al. 2009). For example, divergence of species across the spectrum of leaf functions, such as photosynthesis, longevity, herbivore defense, etc. (Onoda et al. 2011; Poorter and Bongers 2006; Wright et al. 2004), may promote species coexistence (Diaz and Cabido 2001; Kraft et al. 2008; Selaya and Anten 2010). Most studies comparing functional traits among coexisting species assign a mean trait to each species, when in reality there is a broad range of phenotypic plasticity both within and across individuals, especially for tall trees, and this range is highly variable among species. Because phenotypic plasticity is expressed at the metamer level in plants (DeKroon et al. 2005), such studies fail to address the importance of phenotypic plasticity and its contribution to species coexistence and ecosystem function.
Experiments conducted in grasslands have provided much insight regarding diversity–function relationships in plant communities. We must use caution, however, when applying theories derived from low-statured ecosystems to forest ecosystems (Scherer-Lorenzen et al., 2005). As we have illustrated, elucidation of the underlying physiological mechanisms may provide a functional explanation for the diversity–productivity theory as it applies to forest ecosystems. Among these, we believe that individual-level phenotypic plasticity of photosynthesis-related traits is especially important because the breadth of physiological plasticity is what allows tree species to coexist along the vertical gradient of light availability within the forest canopy, as well as in the light-limited understory. In contrast to the view from the ground, a canopy perspective reveals the breadth of phenotypic plasticity of each species contributing to their coexistence and various ecosystem functions. It may also reveal new relationships between functional diversity and ecosystem functioning previously undiscovered in grassland experiments, where the vertical variation in the light environment and leaf functions is much less than in forest ecosystems. A cross-biome exploration of the link between plasticity of photosynthesis-related traits and stand productivity may provide a functional explanation for the relationship between species assemblages and productivity of forest ecosystems.
H.I. is grateful to Drs. T. Hiura and A. Kume for recommendation to the ESJ Ohshima Award and to Drs. H. Takeda, E.D. Ford, T.M. Hinckley, D.G. Sprugel, and J.F. Franklin for instruction and inspiration in forest ecology over the years. The authors thank the many colleagues and collaborators at University of Washington, Wind River Canopy Crane Research Facility, USDA Forest Service, Humboldt State University, University of California at Berkeley, Oregon State University, FFPRI Hokkaido Research Station, Kobe University, Kyoto University, Hokkaido University, Kyushu University, and Tokyo University of Agricultural Technology for their cooperation and guidance. Special thanks to Dr. Steve Sillett (HSU) for inspiring and training H.I. and A.W. in tall-tree canopy ecology.
- Franklin JF, Dyrness CT (1973) Natural vegetation of Oregon and Washington. Oregon State University Press, CorvallisGoogle Scholar
- Franklin JF, Perry DA, Schowalter ME, Harmon ME, McKee A, Spies TA (1989) Importance of ecological diversity in maintaining long-term site productivity. In: Perry DA, Meurisse R, Thomas B, Miller R, Boyle J, Means J, Perry CR, Powers RF (eds) Maintaining the long-term productivity of Pacific Northwest forest ecosystems. Timber, Portland, pp 82–97Google Scholar
- Franklin JF, Spies TA, VanPelt R, Carey AB, Thornburgh DA, Berg DR, Lindenmayer DB, Harmon ME, Keeton WS, Shaw DC, Bible K, Chen J (2002) Disturbances and structural development of natural forest ecosystems with silvicultural implications, using Douglas-fir forests as an example. Ecol Manag 155:399–423CrossRefGoogle Scholar
- Fujimori T, Kawanabe S, Saito H, Grier CC, Shidei T (1976) Biomass and primary production in forests of three major vegetation zones of the northwestern United States. J Jpn Soc 58:360–373Google Scholar
- Garber SM, Maguire DA (2004) Stand productivity and development in two mixed-species spacing trials in the Central Oregon Cascades. For Sci 50:92–105Google Scholar
- Harmon ME, Bible K, Ryan MG, Shaw DC, Chen H, Klopatek J, Li X (2004) Production, respiration, and overall carbon balance in an old-growth Pseudotsuga/Tsuga forest ecosystem. Ecosystems 7:498–512Google Scholar
- Hector A, Schmid B, Beierkuhnlein C, Caldeira MC, Diemer M, Dimitrakopoulos PG, Finn JA, Freitas H, Giller PS, Good J, Harris R, Hogberg P, Huss-Danell K, Joshi J, Jumpponen A, Korner C, Leadley PW, Loreau M, Minns A, Mulder CPH, O’Donovan G, Otway SJ, Pereira JS, Prinz A, Read DJ, Scherer-Lorenzen M, Schulze E-D, Siamantziouras A-SD, Spehn EM, Terry AC, Troumbis AY, Woodward FI, Yachi S, Lawton JH (1999) Plant diversity and productivity experiments in European grasslands. Science 286:1123–1127PubMedCrossRefGoogle Scholar
- Hector A, Philipson C, Saner P, Chamagne J, Dzulkifli D, O’Brien M, Snaddon JL, Ulok P, Weilenmann M, Reynolds G, Godfray HCJ (2011) The Sabah Biodiversity Experiment: a long-term test of the role of tree diversity in restoring tropical forest structure and functioning. Phil Trans R Soc B 366:3303–3315PubMedCrossRefGoogle Scholar
- Inoue A, Yoshida S (2001) Forest stratification and species diversity of Cryptomeria japonica natural forests on Yakushima. J For Plann 7:1–9Google Scholar
- Ishii H, Tanabe S, Hiura T (2004) Exploring the relationships among canopy structure, stand productivity and biodiversity of temperate forest ecosystems. For Sci 50:342–355Google Scholar
- Ishii H, Takashima A, Makita N, Yoshida S (2010) Vertical stratification and effects of crown damage on maximum tree height in mixed conifer-broadleaf forests of Yakushima Island, southern Japan. Plant Ecol 211:27–36Google Scholar
- Jones HE, McNamara N, Mason WL (2005) Functioning of mixed-species stands: evidence from a long-term forest experiment. In: Scherer-Lorenzen M, Korner, C, Schulze E (eds) Forest diversity and function Temperate and boreal systems. Springer, Berlin, pp 111–130Google Scholar
- Kelty MJ, Larson BC, Oliver CD (eds) (1992) The ecology and silviculture of mixed-species forests. Kluwer, BostonGoogle Scholar
- Kira T, Shidei T (1967) Primary production and turnover of organic matter in different forest ecosystems of the Western Pacific. Jpn J Ecol 17:70–87Google Scholar
- Lowman MD, Rinker HB (2004) Forest canopies, 2nd edn. Academic, San DiegoGoogle Scholar
- Maeno H, Hiura T (2000) The effect of leaf phenology of overstory trees on the reproductive success of an understory shrub, Staphylea bumalda DC. Can J Bot 78:781–785Google Scholar
- Onoda Y, Westoby M, Adler PB, Choong AMF, Clissold FJ, Cornelissen JHC, Diaz S, Dominy NJ, Elgart A, Enrico L, Fine PVA, Howard JJ, Jalili, Kitajima K, Kurokawa H, McArthur C, Lucas PW, Markesteijn L, Pérez- Harguindeguy N, Poorter L, Richards L, Santiago LS, Sosinski Jr. EE, Van Bael SA, Warton DI, Wright IJ, Wright SJ, Yamashita N (2011) Global patterns of leaf mechanical properties. Ecol Lett 14:301–312Google Scholar
- Pretzsch H (2005) Diversity and productivity in forests: evidence from long-term experimental plots. In: Scherer-Lorenzen M, Korner C, Schulze E (eds) Forest diversity and function Temperate and boreal systems. Springer, Berlin, pp 41–64Google Scholar
- Scherer-Lorenzen M, Korner C, Schulze E (2005) The functional significance of forest diversity: a synthesis. In: Scherer-Lorenzen M, Korner C, Schulze E (eds) Forest diversity and function: temperate and boreal systems. Springer, Berlin, pp 377–389Google Scholar
- Scheu S (2005) Linkages between tree diversity, soil fauna and ecosystem processes. In: Scherer-Lorenzen M, Korner C, Schulze E (eds) Forest diversity and function Temperate and boreal systems. Springer, Berlin, pp 211–234Google Scholar
- Vila M, Inchausti P, Vayreda J, Barrantes O, Garcia C, Ibanez JJ, Mata T (2005) Confounding factors in the observed productivity–diversity relationship in forests. In: Scherer-Lorenzen M, Korner C, Schulze E (eds) Forest diversity and function Temperate and boreal systems. Springer, Berlin, pp 65–86Google Scholar
- Vojtech E, Loreau M, Yachi S, Spehn EM, Hector A (2008) Light partitioning in experimental grass communities. Oikos 117:1351–1361Google Scholar
- Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas M-L, Niinemets U, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov PI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827PubMedCrossRefGoogle Scholar