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Commentary Ecosystems in four dimensions The ecosystem concept is perhaps the most important concept in ecology for scientists (Cherrett, 1989) and the public at large. Eighty years ago, Arthur Tansley (1935) noted that the method of science entailed separating parts of the universe for intensive study. These isolated parts, or systems, are included in larger systems that overlap, interlock, and interact with one another. The isolation of the parts is artificial in many ways, but necessary for advancing understanding. Sixty years later, Reiners (1986) asserted that ecosystems were dimensionless, ranging in scale and scope from a single decaying acorn to the entire planet’s biosphere. But if an ecosystem can be anything from an acorn to a planet, how useful can this concept be for scientific inquiry? The power of the idea depends on how the boundaries of ecosystems are defined and addressed. The spatial extent of ecosystems has often been delimited by abrupt structural changes, such as the boundaries of a lake, and the border of a forest and a meadow. Ecosystems are also demarcated within a single type of vegetation, such as the boundary between forests of different ages, or different dominant plant species. The classical importance of defining spatial boundaries became less critical with the development of geographical information systems and mathematical approaches for dealing with gradients of change without requiring sharp boundaries or covarying changes in ecological factors. Modern conceptualization of ecosystems may embrace the sorts of overlapping, interlocking, and interacting factors noted by Tansley, allowing a more diffuse consideration of the areal bounds of any system of interest. Whether the defined boundaries of an ecosystem are sharp or diffuse, it is important that the boundaries do not leave out important processes and components. A forest ecosystem that was defined to contain only the aboveground portions of trees would not be a viable object of study for hydrology, physiology or biogeochemistry. In this issue of New Phytologist, Richter & Billings (pp. 900–912) discuss the critical need to include depth and timescale of ecological processes below the soil surface, and demonstrate the value of extending classic thinking about ecosystems to include the full ‘critical zone’ concept from Earth science.
Beyond two dimensions The two-dimensional (areal) extent of ecosystems has received much more attention than the next two dimensions: the depth of an ecosystem beneath the surface of the ground, and the changes in ecosystems over time. The depth of an ecosystem has often been the Ó 2015 The Authors New Phytologist Ó 2015 New Phytologist Trust
focus of soil scientists rather than ecologists (Binkley, 2006). Indeed, soils are often almost absent from summaries of the history of ecology (e.g. Real & Brown, 1991; Golley, 1993). Soils do appear in many ecological studies, of course, but most of these include the surficial organic horizon (for forests) and the uppermost mineral horizons. In a similar way, ecological investigations often cover relatively short spans of time, owing to the short-term nature of science funding and the challenge of characterizing time frames that exceed the span of scientific careers and the longevity of the major plants. These other two dimensions of ecosystems – depth and time – connect in very substantial ways that may be more important than the shallower, more-rapid frames of many ecosystem studies.
‘But if an ecosystem can be anything from an acorn to a planet, how useful can this concept be for scientific inquiry?’
A classic example of the importance of the critical zone issues of depth and time on ecosystems was described by the soil scientist, Hans Jenny, for a sequence of forests on the coast of California (Jenny et al., 1969). The ‘ecological stairstep’ consists of a consistent parent material for soil development, with varying lengths of time for ecological processes to develop (Fig. 1). Terraces raised above the ocean for 100 000 years are dominated by grasslike vegetation, with a strongly humified upper mineral soil. After another 100 000 years of ecological processes, the terraces are dominated by redwood and Douglas-fir trees; the upper soils have begun to loose iron and other elements, leaving quartz crystals behind. Soils and vegetation continue to change over millennia, with shifting dominance toward tall Bishop pine trees as the soils continue to weather and soil horizons deepen. The terrace locations closer to the terrace edge have better drainage of water during wet winters. Well-drained locations have had the mobilized iron moved farther down the soil profile. The more poorly drained locations to the rear of the terraces have accumulated a dense layer of clay- and iron-enriched soil at 0.5–1.0 m depth that allows water to saturate the upper soil during wet winters. The differences in soil depth leads to huge differences in the forests, with tree heights dropping from 30 m on the deep soils to c. 3 m on the shallow soils. The climate is the same across terraces, but slow changes in the depth of the ecosystems (with concomitant changes in soil fertility) led to differences in vegetation and soils that are as profound as those encountered across a very large climate gradient. The critical zone (see Richter & Billings) for understanding the ecological factors that distinguish these ecosystems extends to variable depths in the
New Phytologist (2015) 206: 883–885 883 www.newphytologist.com
884 Forum
Commentary
New Phytologist
Fig. 1 The difference that depth makes. The ecological staircase along the coast of northern California consists of a series of terraces lifted above sea level over a period of 500 000 years (Jenny et al., 1969). The soils and ecosystems developed on these terraces developed from the same original geologic material (greywacke sandstone), but soil development differs substantially over time because of differences in the water regime. Locations closer to the edge of the terraces drain water well, with byproducts of mineral weathering transported deep into the soil (lower left). The rearward portion of the terraces drain more poorly, and iron released from mineral weathering precipitates to further restrict water drainage (lower right). The well-drained portions of older terraces support large, productive forests of redwood and Douglas-fir (upper left) on deep, fertile soils. Farther back on each terrace, the restricted soil depth supports only short, low-productivity vegetation of dwarf Bishop pine, Bolander pine, and Mendocino cypress (upper right). The ecological staircase provides an excellent example of the value of extending classic thinking about ecosystems to include the full ‘critical zone’ concept from Earth science, as discussed by Richter & Billings in this issue of New Phytologist (pp. 900–912). Photos: pygmy vegetation courtesy of Sarah Bisbing, others courtesy of Ron Amundson.
soils, as well as to linkages across the landscape over very long periods of time. How deeply do most ecosystems extend into the soil? Depending on physical and chemical aspects of soils, trees roots are commonly found at 3–6 m depth, with some cases reporting over 20 m depth (Stone & Kalisz, 1991; Schenk & Jackson, 2002). A plantation of Eucalyptus trees in Brazil reached 25 m in height in 5 years, while roots grew to a depth of 18 m, and more than half the length of fine roots in these Eucalyptus forests occur below 1 m (Laclau et al., 2013). These deep roots provide substantial water uptake (especially in the dry season) and high uptake capacities for calcium and potassium (da Silva et al., 2011). Deep soils are quite important at the other end of the environmental gradient as well; one study of arid and semi-arid ecosystems found that roots deeper than 1 m in the soil dominated the uptake of calcium, potassium, and phosphorus (McCulley et al., 2004). The important dimension of depth of an ecosystem can also depend on the local vegetation New Phytologist (2015) 206: 883–885 www.newphytologist.com
type. The rooting depth of an ecosystem dominated by grasses or herbs may deepen by several meters if woody plants become established (Jackson et al., 2000). The relationship between plants and soils is reciprocal, and plants can alter soils (and subsoils) even more deeply than the extent of roots. The physical and chemical environment deep belowground shows the influence of plant-mediated changes in hydrology and chemistry. Plants strongly influence the water regime deep below the soil surface; the presence of water directly affects chemical reactions and activities of microorganisms, and indirectly influences gas permeability and the oxidation/reduction status. Biological activity within soils generates large amounts of CO2. Upper soils often have CO2 concentrations of 1%, increasing by several fold with depth below the soil surface (Richter & Markewitz, 1995). The combination of CO2 and water yields carbonic acid, a major driver of long-term weathering of minerals. Mineral weathering in turn generates alkalinity that can be Ó 2015 The Authors New Phytologist Ó 2015 New Phytologist Trust
New Phytologist
Commentary
transported to streams and lakes, further extending the depth of the influence of biological processes. The spatial extent of ecological processes and interactions is incomplete, and perhaps insufficient, unless the depth extends through the critical zone. How far do ecosystems extend in time? This dimension of the critical zone (see Richter & Billings) may be more problematic than the issues of ecosystem depth. Highly dynamic processes often receive more attention than very slow processes. For example, thousands of studies have examined the rate of mass loss of plant litter from mesh bags, typically finding that half of the mass is lost within one to several years (Berg & McClaugherty, 2014). Shortterm decomposition may have implications for the rates of nutrient supply to microbes and plants within a single year. However, decomposition rates may provide little if any insight on the processes that influence the long-term accumulation of organic matter in soils (Schmidt et al., 2011). Most soils contain organic matter that formed over a period of hundreds or thousands of years, yet these soils may have high flow-through of carbon atoms that cycle from plant detritus to the atmosphere with an average residence time of a few years or decades. The stabilization of very small proportions of the carbon added to soils each year accounts for long-term patterns of soil carbon accumulation, and these changes are essentially invisible in short-term studies. Similarly, the long-term processes of soil weathering and horizon development in the ecological staircase in California would have been overlooked in any short-term rate of change, but were fundamental to the current ecological characteristics of the sites.
Critical zones of ecosystems include four dimensions Richter & Billings tackle these issues and stress the opportunities offered by integrating the classical concept of ecosystems with the Earth science concept of critical zones. The critical zone idea harks back to Tansley’s advocacy for viewing ecological processes and interactions comprising ‘one physical system’ that encompasses sufficient area, depth, and time to embrace all the important dynamics of an ecosystem. Richter & Billings note that many environmental monitoring programs invest heavily in measuring shallow and rapid processes. Without an adequate conceptualization of ecosystems extending through critical zones, these programs miss the deep and slow processes that can shape long-term dynamics. Our world has largely been shaped by deep, slow, and long-lasting processes and interactions. This is a good time to dig deeper into Tansley’s ecosystem concept and extend it to embrace full critical zones. Dan Binkley1,2 1
Forum 885
2
Department of Forest Ecology and Management, Swedish University of Agricultural Sciences, 901 83 Ume a, Sweden (tel +1 970 491 6519; email [email protected])
References Berg B, McClaugherty C. 2014. Plant litter: decomposition, humus formation, carbon sequestration, 3rd edn. New York, USA: Springer. Binkley D. 2006. Soils in ecology and ecology in soils. In: Warkentin BP, ed. Footprints in the soil. Amsterdam, the Netherlands: Elsevier, 259–278. Cherrett JM. 1989. Key concepts: the results of a survey of our members’ opinions. In: Cherret JM, ed. The contribution of ecology to an understanding of the natural world. Oxford, UK: Blackwell Scientific Publications, 1–16. Golley FB. 1993. A history of the ecosystem concept in ecology: more than the sum of the parts. New Haven, CT, USA: Yale University Press. Jackson RB, Schenk HJ, Jobba gy EG, Canadell J, Clello GD, Dickinson RE, Field CB, Friedlingstein P, Heimann M, Hibbard K et al. 2000. Belowground consequences of vegetation change and their treatment in models. Ecological Applications 10: 470–483. Jenny H, Arkley RJ, Schultz AM. 1969. The pygmy forest-podsol ecosystem and its dune associates of the Mendocino coast. Mardro~ no 20: 60–74. Laclau JP, Silva EA, Lambais GR, Bernoux M, Le Maire G, Stape JL, Bouillet J-P, De Moraes Goncßalves JL, Jourdan C, Nouvellon Y. 2013. Dynamics of soil exploration by fine roots down to a depth of 10 m in Eucalyptus grandis plantations. Frontiers in Plant Science 4: 1–12. McCulley RJ, Jobba gy EG, Pockman WT, Jackson RB. 2004. Nutrient uptake as a contributing explanation for deep rooting in arid and semi-arid ecosystems. Oecologia 141: 620–628. Real LA, Brown JH. 1991. Foundations of ecology: classic papers with commentaries. Chicago, IL, USA: University of Chicago. Reiners WA. 1986. Complementary models for ecosystems. The American Naturalist 127: 59–73. Richter DdeB, Billings SA. 2015. ‘One physical system’: Tansley’s ecosystem as Earth’s critical zone. New Phytologist 206: 900–912. Richter DD, Markewitz D. 1995. How deep is soil? BioScience 45: 600–609. Schenk HJ, Jackson RB. 2002. Rooting depths, lateral root spreads and belowground/above-ground allometries of plants in water-limited ecosystems. Journal of Ecology 90: 480–494. Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, K€ogel-Knabner I, Lehmann J, Manning DAC et al. 2011. Persistence of soil organic matter as an ecosystem property. Nature 478: 49–56. da Silva EV, Bouillet J-P, Goncßalves JLdM, Jr AbreuCH, Trivelin PCO, Hinsinger P, Jourdan C, Nouvellon Y, Stape JL, Laclau J-P. 2011. Functional specialization of Eucalyptus fine roots: contrasting potential uptake rates for nitrogen, potassium and calcium tracers at varying soil depths. Functional Ecology 25: 996–1006. Stone EL, Kalisz PJ. 1991. On the maximum extent of tree roots. Forest Ecology and Management 46: 59–102. Tansley AG. 1935. The use and abuse of vegetational concepts and terms. Ecology 16: 284–307. Key words: areal extent of ecosystems, boundaries, changes in ecosystems with time, depth of an ecosystem, Earth’s critical zone, ecological stairstep, ecology, Tansley’s ecosystem concept.
Department of Ecosystem Science and Sustainability, Colorado State University, Fort Collins, CO 80523, USA;
Ó 2015 The Authors New Phytologist Ó 2015 New Phytologist Trust
New Phytologist (2015) 206: 883–885 www.newphytologist.com
Commentary Ecosystems in four dimensions The ecosystem concept is perhaps the most important concept in ecology for scientists (Cherrett, 1989) and the public at large. Eighty years ago, Arthur Tansley (1935) noted that the method of science entailed separating parts of the universe for intensive study. These isolated parts, or systems, are included in larger systems that overlap, interlock, and interact with one another. The isolation of the parts is artificial in many ways, but necessary for advancing understanding. Sixty years later, Reiners (1986) asserted that ecosystems were dimensionless, ranging in scale and scope from a single decaying acorn to the entire planet’s biosphere. But if an ecosystem can be anything from an acorn to a planet, how useful can this concept be for scientific inquiry? The power of the idea depends on how the boundaries of ecosystems are defined and addressed. The spatial extent of ecosystems has often been delimited by abrupt structural changes, such as the boundaries of a lake, and the border of a forest and a meadow. Ecosystems are also demarcated within a single type of vegetation, such as the boundary between forests of different ages, or different dominant plant species. The classical importance of defining spatial boundaries became less critical with the development of geographical information systems and mathematical approaches for dealing with gradients of change without requiring sharp boundaries or covarying changes in ecological factors. Modern conceptualization of ecosystems may embrace the sorts of overlapping, interlocking, and interacting factors noted by Tansley, allowing a more diffuse consideration of the areal bounds of any system of interest. Whether the defined boundaries of an ecosystem are sharp or diffuse, it is important that the boundaries do not leave out important processes and components. A forest ecosystem that was defined to contain only the aboveground portions of trees would not be a viable object of study for hydrology, physiology or biogeochemistry. In this issue of New Phytologist, Richter & Billings (pp. 900–912) discuss the critical need to include depth and timescale of ecological processes below the soil surface, and demonstrate the value of extending classic thinking about ecosystems to include the full ‘critical zone’ concept from Earth science.
Beyond two dimensions The two-dimensional (areal) extent of ecosystems has received much more attention than the next two dimensions: the depth of an ecosystem beneath the surface of the ground, and the changes in ecosystems over time. The depth of an ecosystem has often been the Ó 2015 The Authors New Phytologist Ó 2015 New Phytologist Trust
focus of soil scientists rather than ecologists (Binkley, 2006). Indeed, soils are often almost absent from summaries of the history of ecology (e.g. Real & Brown, 1991; Golley, 1993). Soils do appear in many ecological studies, of course, but most of these include the surficial organic horizon (for forests) and the uppermost mineral horizons. In a similar way, ecological investigations often cover relatively short spans of time, owing to the short-term nature of science funding and the challenge of characterizing time frames that exceed the span of scientific careers and the longevity of the major plants. These other two dimensions of ecosystems – depth and time – connect in very substantial ways that may be more important than the shallower, more-rapid frames of many ecosystem studies.
‘But if an ecosystem can be anything from an acorn to a planet, how useful can this concept be for scientific inquiry?’
A classic example of the importance of the critical zone issues of depth and time on ecosystems was described by the soil scientist, Hans Jenny, for a sequence of forests on the coast of California (Jenny et al., 1969). The ‘ecological stairstep’ consists of a consistent parent material for soil development, with varying lengths of time for ecological processes to develop (Fig. 1). Terraces raised above the ocean for 100 000 years are dominated by grasslike vegetation, with a strongly humified upper mineral soil. After another 100 000 years of ecological processes, the terraces are dominated by redwood and Douglas-fir trees; the upper soils have begun to loose iron and other elements, leaving quartz crystals behind. Soils and vegetation continue to change over millennia, with shifting dominance toward tall Bishop pine trees as the soils continue to weather and soil horizons deepen. The terrace locations closer to the terrace edge have better drainage of water during wet winters. Well-drained locations have had the mobilized iron moved farther down the soil profile. The more poorly drained locations to the rear of the terraces have accumulated a dense layer of clay- and iron-enriched soil at 0.5–1.0 m depth that allows water to saturate the upper soil during wet winters. The differences in soil depth leads to huge differences in the forests, with tree heights dropping from 30 m on the deep soils to c. 3 m on the shallow soils. The climate is the same across terraces, but slow changes in the depth of the ecosystems (with concomitant changes in soil fertility) led to differences in vegetation and soils that are as profound as those encountered across a very large climate gradient. The critical zone (see Richter & Billings) for understanding the ecological factors that distinguish these ecosystems extends to variable depths in the
New Phytologist (2015) 206: 883–885 883 www.newphytologist.com
884 Forum
Commentary
New Phytologist
Fig. 1 The difference that depth makes. The ecological staircase along the coast of northern California consists of a series of terraces lifted above sea level over a period of 500 000 years (Jenny et al., 1969). The soils and ecosystems developed on these terraces developed from the same original geologic material (greywacke sandstone), but soil development differs substantially over time because of differences in the water regime. Locations closer to the edge of the terraces drain water well, with byproducts of mineral weathering transported deep into the soil (lower left). The rearward portion of the terraces drain more poorly, and iron released from mineral weathering precipitates to further restrict water drainage (lower right). The well-drained portions of older terraces support large, productive forests of redwood and Douglas-fir (upper left) on deep, fertile soils. Farther back on each terrace, the restricted soil depth supports only short, low-productivity vegetation of dwarf Bishop pine, Bolander pine, and Mendocino cypress (upper right). The ecological staircase provides an excellent example of the value of extending classic thinking about ecosystems to include the full ‘critical zone’ concept from Earth science, as discussed by Richter & Billings in this issue of New Phytologist (pp. 900–912). Photos: pygmy vegetation courtesy of Sarah Bisbing, others courtesy of Ron Amundson.
soils, as well as to linkages across the landscape over very long periods of time. How deeply do most ecosystems extend into the soil? Depending on physical and chemical aspects of soils, trees roots are commonly found at 3–6 m depth, with some cases reporting over 20 m depth (Stone & Kalisz, 1991; Schenk & Jackson, 2002). A plantation of Eucalyptus trees in Brazil reached 25 m in height in 5 years, while roots grew to a depth of 18 m, and more than half the length of fine roots in these Eucalyptus forests occur below 1 m (Laclau et al., 2013). These deep roots provide substantial water uptake (especially in the dry season) and high uptake capacities for calcium and potassium (da Silva et al., 2011). Deep soils are quite important at the other end of the environmental gradient as well; one study of arid and semi-arid ecosystems found that roots deeper than 1 m in the soil dominated the uptake of calcium, potassium, and phosphorus (McCulley et al., 2004). The important dimension of depth of an ecosystem can also depend on the local vegetation New Phytologist (2015) 206: 883–885 www.newphytologist.com
type. The rooting depth of an ecosystem dominated by grasses or herbs may deepen by several meters if woody plants become established (Jackson et al., 2000). The relationship between plants and soils is reciprocal, and plants can alter soils (and subsoils) even more deeply than the extent of roots. The physical and chemical environment deep belowground shows the influence of plant-mediated changes in hydrology and chemistry. Plants strongly influence the water regime deep below the soil surface; the presence of water directly affects chemical reactions and activities of microorganisms, and indirectly influences gas permeability and the oxidation/reduction status. Biological activity within soils generates large amounts of CO2. Upper soils often have CO2 concentrations of 1%, increasing by several fold with depth below the soil surface (Richter & Markewitz, 1995). The combination of CO2 and water yields carbonic acid, a major driver of long-term weathering of minerals. Mineral weathering in turn generates alkalinity that can be Ó 2015 The Authors New Phytologist Ó 2015 New Phytologist Trust
New Phytologist
Commentary
transported to streams and lakes, further extending the depth of the influence of biological processes. The spatial extent of ecological processes and interactions is incomplete, and perhaps insufficient, unless the depth extends through the critical zone. How far do ecosystems extend in time? This dimension of the critical zone (see Richter & Billings) may be more problematic than the issues of ecosystem depth. Highly dynamic processes often receive more attention than very slow processes. For example, thousands of studies have examined the rate of mass loss of plant litter from mesh bags, typically finding that half of the mass is lost within one to several years (Berg & McClaugherty, 2014). Shortterm decomposition may have implications for the rates of nutrient supply to microbes and plants within a single year. However, decomposition rates may provide little if any insight on the processes that influence the long-term accumulation of organic matter in soils (Schmidt et al., 2011). Most soils contain organic matter that formed over a period of hundreds or thousands of years, yet these soils may have high flow-through of carbon atoms that cycle from plant detritus to the atmosphere with an average residence time of a few years or decades. The stabilization of very small proportions of the carbon added to soils each year accounts for long-term patterns of soil carbon accumulation, and these changes are essentially invisible in short-term studies. Similarly, the long-term processes of soil weathering and horizon development in the ecological staircase in California would have been overlooked in any short-term rate of change, but were fundamental to the current ecological characteristics of the sites.
Critical zones of ecosystems include four dimensions Richter & Billings tackle these issues and stress the opportunities offered by integrating the classical concept of ecosystems with the Earth science concept of critical zones. The critical zone idea harks back to Tansley’s advocacy for viewing ecological processes and interactions comprising ‘one physical system’ that encompasses sufficient area, depth, and time to embrace all the important dynamics of an ecosystem. Richter & Billings note that many environmental monitoring programs invest heavily in measuring shallow and rapid processes. Without an adequate conceptualization of ecosystems extending through critical zones, these programs miss the deep and slow processes that can shape long-term dynamics. Our world has largely been shaped by deep, slow, and long-lasting processes and interactions. This is a good time to dig deeper into Tansley’s ecosystem concept and extend it to embrace full critical zones. Dan Binkley1,2 1
Forum 885
2
Department of Forest Ecology and Management, Swedish University of Agricultural Sciences, 901 83 Ume a, Sweden (tel +1 970 491 6519; email [email protected])
References Berg B, McClaugherty C. 2014. Plant litter: decomposition, humus formation, carbon sequestration, 3rd edn. New York, USA: Springer. Binkley D. 2006. Soils in ecology and ecology in soils. In: Warkentin BP, ed. Footprints in the soil. Amsterdam, the Netherlands: Elsevier, 259–278. Cherrett JM. 1989. Key concepts: the results of a survey of our members’ opinions. In: Cherret JM, ed. The contribution of ecology to an understanding of the natural world. Oxford, UK: Blackwell Scientific Publications, 1–16. Golley FB. 1993. A history of the ecosystem concept in ecology: more than the sum of the parts. New Haven, CT, USA: Yale University Press. Jackson RB, Schenk HJ, Jobba gy EG, Canadell J, Clello GD, Dickinson RE, Field CB, Friedlingstein P, Heimann M, Hibbard K et al. 2000. Belowground consequences of vegetation change and their treatment in models. Ecological Applications 10: 470–483. Jenny H, Arkley RJ, Schultz AM. 1969. The pygmy forest-podsol ecosystem and its dune associates of the Mendocino coast. Mardro~ no 20: 60–74. Laclau JP, Silva EA, Lambais GR, Bernoux M, Le Maire G, Stape JL, Bouillet J-P, De Moraes Goncßalves JL, Jourdan C, Nouvellon Y. 2013. Dynamics of soil exploration by fine roots down to a depth of 10 m in Eucalyptus grandis plantations. Frontiers in Plant Science 4: 1–12. McCulley RJ, Jobba gy EG, Pockman WT, Jackson RB. 2004. Nutrient uptake as a contributing explanation for deep rooting in arid and semi-arid ecosystems. Oecologia 141: 620–628. Real LA, Brown JH. 1991. Foundations of ecology: classic papers with commentaries. Chicago, IL, USA: University of Chicago. Reiners WA. 1986. Complementary models for ecosystems. The American Naturalist 127: 59–73. Richter DdeB, Billings SA. 2015. ‘One physical system’: Tansley’s ecosystem as Earth’s critical zone. New Phytologist 206: 900–912. Richter DD, Markewitz D. 1995. How deep is soil? BioScience 45: 600–609. Schenk HJ, Jackson RB. 2002. Rooting depths, lateral root spreads and belowground/above-ground allometries of plants in water-limited ecosystems. Journal of Ecology 90: 480–494. Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, K€ogel-Knabner I, Lehmann J, Manning DAC et al. 2011. Persistence of soil organic matter as an ecosystem property. Nature 478: 49–56. da Silva EV, Bouillet J-P, Goncßalves JLdM, Jr AbreuCH, Trivelin PCO, Hinsinger P, Jourdan C, Nouvellon Y, Stape JL, Laclau J-P. 2011. Functional specialization of Eucalyptus fine roots: contrasting potential uptake rates for nitrogen, potassium and calcium tracers at varying soil depths. Functional Ecology 25: 996–1006. Stone EL, Kalisz PJ. 1991. On the maximum extent of tree roots. Forest Ecology and Management 46: 59–102. Tansley AG. 1935. The use and abuse of vegetational concepts and terms. Ecology 16: 284–307. Key words: areal extent of ecosystems, boundaries, changes in ecosystems with time, depth of an ecosystem, Earth’s critical zone, ecological stairstep, ecology, Tansley’s ecosystem concept.
Department of Ecosystem Science and Sustainability, Colorado State University, Fort Collins, CO 80523, USA;
Ó 2015 The Authors New Phytologist Ó 2015 New Phytologist Trust
New Phytologist (2015) 206: 883–885 www.newphytologist.com
