'One Physical System': Tansley's Ecosystem As Earth's Critical Zone

Review

Tansley review ‘One physical system’: Tansley’s ecosystem as Earth’s critical zone

Author for correspondence: Daniel deB. Richter1 and Sharon A. Billings2 Daniel deB. Richter 1 2 Tel: +01 919 475 7939 Nicholas School of the Environment, Duke University, Durham, NC 27708, USA; Department of Ecology and Evolutionary Biology Email: [email protected] and Kansas Biological Survey, University of Kansas, Lawrence, KS 66047, USA Received: 29 October 2014 Accepted: 8 January 2015

Contents

Summary 900 V. The metabolism of ecosystems and critical zones 905

I. Introduction 900 VI. Towards a more active biogeoscience 908

II. Tansley’s ecosystem as ‘one physical system’ 901 Acknowledgements 909

III. Earth’s critical zone 901 References 909

IV. Historic developments in ecosystem science 902

Summary

New Phytologist (2015) 206: 900–912 Integrative concepts of the biosphere, ecosystem, biogeocenosis and, recently, Earth’s critical doi: 10.1111/nph.13338 zone embrace scientific disciplines that link matter, energy and organisms in a systems-level understanding of our remarkable planet. Here, we assert the congruence of Tansley’s (1935) Key words: biogeochemistry, biogeosciences, venerable ecosystem concept of ‘one physical system’ with Earth science’s critical zone. ecohydrology, ecosystem ecology, ecosystem Ecosystems and critical zones are congruent across spatial–temporal scales from vegetation-clad metabolism, soil respiration, weathering weathering profiles and hillslopes, small catchments, landscapes, river basins, continents, to profile. Earth’s whole terrestrial surface. What may be less obvious is congruence in the vertical dimension. We use ecosystem metabolism to argue that full accounting of photosynthetically

ﬁxed carbon includes respiratory CO2 and carbonic acid that propagate to the base of the critical

zone itself. Although a small fraction of respiration, the downward diffusion of CO2 helps determine rates of soil formation and, ultimately, ecosystem evolution and resilience. Because life in the upper portions of terrestrial ecosystems signiﬁcantly affects biogeochemistry throughout weathering proﬁles, the lower boundaries of most terrestrial ecosystems have been demarcated at depths too shallow to permit a complete understanding of ecosystem structure and function. Opportunities abound to explore connections between upper and lower components of critical-zone ecosystems, between soils and streams in watersheds, and between

plant-derived CO2 and deep microbial communities and mineral weathering.

the perspectives of Tansley (1935), Lindeman (1942) and Hutch- I. Introduction inson (1948), who deﬁned ecosystems ‘in the sense of physics’ A remarkable congruence now exists in the core concepts of two (quoting Tansley) as involving the study of ‘the living matter of the scientiﬁc disciplines: ecology’s ecosystem and Earth science’s whole earth ...a unit of higher order than the biome’ (Hutchinson, critical zone. This congruence becomes evident when we examine 1940). Here, we observe how these early ideas of the ecosystem

900 New Phytologist (2015) 206: 900–912 Ó 2015 The Authors www.newphytologist.com New Phytologist Ó 2015 New Phytologist Trust New Phytologist Tansley review Review 901 compare with Earth’s critical zone, defined by Jordan et al. (2001) the intimacy of interactions among ecosystem components. as the integrated and life-supporting systems of Earth’s surficial Hutchinson’s student Ray Lindeman (1942), in his brilliant essay terrestrial processes. We critique the historical subdivision of on the ecosystem’s trophic energetics, explicitly emphasized how terrestrial ecosystem science into above- and belowground ecosystems were more than biological constructs. In Lindeman’s branches, and argue that ecosystem metabolism can only be (1942) words, resolved by accounting for the full propagation of respiratory CO 2 the discrimination between living organisms as parts of the ‘biotic and carbonic-acid weathering down through geologic substrata to community’ and dead organisms and inorganic nutritives as part of the the very base of the critical zone itself. ‘environment’ seems arbitrary and unnatural. The difficulty in drawing We assert that this larger perspective of the belowground clear-cut lines between the living community and the non-living ecosystem can help bridge above- and belowground ecology, and environment is illustrated by the difficulty in determining the status of a better connect the hydrology and biogeochemistry of the slowing dying pondweed covered with periphytes, some of which are also aboveground ecosystem and its soils with groundwater, streams, continually dying... (M)uch of the non-living nascent ooze is rapidly lakes and rivers. Given the congruence of the two concepts, reincorporated through “dissolved nutrients” back into the living “biotic scientists can reap major breakthroughs from coordinated community.” This constant organic–inorganic cycle of nutritive sub- investigations that engage the disciplines of hydrology, climatol- stance is so completely integrated that to consider such a unit as a lake ogy, microbiology, geochemistry and biogeochemistry, pedology, primarily as a biotic community appears to force a “biological” emphasis ecology and geophysics. Such co-investigations will lead to more upon a more basic functional organization. quantitative assessments of the evolution and resilience of critical- zone ecosystems (Chorover et al., 2011). In so doing, investiga- It is important to understand that Lindeman could have tors will satisfy the concerns and scope of Tansley’s ecosystem substituted a terrestrial system into his text about lakes: for and the recently conceived critical zone of Jordan et al. (2001). example, ‘to consider such a unit as a forest, a grassland, or a wetland primarily as a biotic community appears to force a ‘biological’ emphasis upon a more basic functional organization.’ It is also II. Tansley’s ecosystem as ‘one physical system’ notable that, in these early aquatic ecosystem studies, lake For decades, the term ‘ecosystem’ has enjoyed active use in the sediments were deeply cored sometimes to > 10 m and deep scientific and management literature. Although the term is used in a sediment samples were central to analyses that explored ecosystem variety of ways, we promote the concept’s original scope set by its evolution back through the millennia (Deevey, 1939; Hutchinson framer, Arthur Tansley (1935), who briefly but substantively & Wollack, 1940; Livingstone & Boykin, 1962). defined the ecosystem to be the integrated biotic–abiotic complex: Many of Tansley’s insights remain on target even though the science of ecosystems has grown in many directions and weathered a the whole system (in the sense of physics), including not only the swirl of ideas about ecosystem stability, strategy, resilience and organism-complex, but also the whole complex of physical factors capacity for repair. The ecosystem concept is growing still forming what we call the environment of the biome – the habitat factors in (Table 1), with ecosystems today emphasized to be open, complex, the widest sense. non-linear, adaptive, unpredictable in temporal trajectory (O’Ne- Significantly, as if to emphasize what he meant by ‘the whole ill, 2001; Jørgensen & Svirezhev, 2004; Currie, 2011; Likens, system’, Tansley (1935) added: 2013) and potentially operating far from equilibrium (Scheffer et al., 2001; Filotas et al., 2014). Although the soil component of Though (as biologists) the organisms may claim our primary interest, ecosystems is widely recognized to be polygenetic (Richter & when we are trying to think fundamentally we cannot separate them from Yaalon, 2012), so too are ecosystems at large, that is, ecosystems are their special environment, with which they form one physical system (italics archival, time-dependent products derived from high-order inter- ours). actions of external forcings and internal developments that ebb and Tansley (1935) took pains to frame the ecosystem concept, as is flow over evolutionary and geologic time (Clark & Royall, 1996; evident from his paper’s curious title, ‘The use and abuse of Shugart, 1998). Although the scope and core of the concept can still vegetational concepts and terms’, and from a number of historical be recognized in Tansley (1935), the science is advancing by many details of the paper’s writing (Willis, 1997). But what is lasting measures. about Tansley’s ecosystem concept is that he used ‘physics’ in the tradition of Aristotle, he opened the door to the ecosystem for III. Earth’s critical zone scientists of many disciplines, and he calibrated the ecosystem to cross scales (Evans, 1956; Jenny, 1958). Although Tansley In 2001, Earth scientists outlined a new systems science of surficial described ecosystems to fundamentally ‘overlap, interlock and geological processes writ large, an integrative, interdisciplinary interact with one another’ over space and time, he was a practical study of terrestrial systems, a science of Earth’s ‘Critical Zone’. scientist and foresaw that ecosystems, although overlapped and Critical zones (CZs) are energized by the sun that heats the Earth, interlocking, could be studied as if in isolation. powers plant photosynthesis and drives the planet’s great hydro- G. E. Hutchinson (1940, 1948), enthused by Vernadsky’s logic and biogeochemical cycles. Led by Thomas Jordan and Gail (1929, 1998) biosphere and by Tansley’s fusion of the biotic– Ashley (Jordan et al., 2001), the team marshaled the disciplines of abiotic complex, used metaphors of ‘circles’ and ‘cycles’ to describe hydrology, geomorphology, geology, geochemistry, geophysics,

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Table 1 The literature of ecosystem science is relevant to ecosystem and that tie together the driving processes of the atmosphere, canopy- critical zone scientists alike boundary layers, biota, soil and full weathering profiles that include deep aquifers. At a time when a Working Group of the Topics Citations International Commission on Stratigraphy is evaluating ‘the Histories of ecosystem Hagen (1992); Golley (1993); Willis (1997) Anthropocene’ as a new, contemporary unit of geological time science (Zalasiewicz et al., 2011, 2015; Haff, 2014; Waters et al., 2014; Origins of ecosystem Forbes (1887); Thienemann (1918); Edgeworth et al., 2015), how better to promote an understanding concept before Elton (1927); Vernadsky (1929, 1998); Tansley (1935) Major (1969) of the human forcings of the planet than by accelerating Energy flow and Lindeman (1942); Odum (1956, 1968); interdisciplinarity across the Earth sciences (Richter & Mobley, metabolism Megonigal et al. (2004) 2009)? Indeed, CZ science may become the science of the Biogeochemistry Hutchinson (1948); Schlesinger & Anthropocene (Latour, 2014) and recent CZ literature demon- Bernhardt (2013) strates the great potential for collaborations among the disciplines Nutrient cycling and Chadwick et al. (1999); Richter & soil formation over Markewitz (2001); Vitousek (2004) that CZ science calls together (Table 2). Nevertheless, ambitious time interdisciplinarity is not the only hallmark of CZ science; CZ Spatial scales Evans (1956); Currie (2011) science is notable for its congruence with the scope of ecosystem Landscape Sukachev & Dylis (1968); Urban et al. (1987) science conceived decades ago by Arthur Tansley (1935). Microbial influence Firestone & Davidson (1989); on nutrient cycling Billings & Tiemann (2014) Reaction kinetics Lehmeier et al. (2013); Min et al. (2014) IV. Historic developments in ecosystem science Systems analysis O’Neill (1986, 2001) Cybernetics Engelberg & Boyarsky (1979); Patten & Odum (1981) 1. Above- and belowground Complexity Filotas et al. (2014) Lindeman (1942) argued firmly that it was ‘arbitrary and Propagation of Reiners & Dreise (2004) ecosystem effects unnatural’ to isolate plant producers from heterotrophic decom- Thermodynamics and Jørgensen & Svirezhev (2004) posers. Ecosystem science was, after all, about the system and the conservation integration of its components and processes. As ecosystem science Succession Odum (1969); Christensen (2014) developed, however, many terrestrial ecologists divided into two Resource management Pickett et al. (1992); Christensen (2005) camps: those who studied aboveground plant dynamics and those Watershed ecosystem Bormann et al. (1969); Likens (2013) Critical zone ecosystem This paper who focused on belowground processes. Literature and journals were created that rarely reference the other’s papers. Each developed terminologies and organized professional meetings. Given Lindeman’s (1942) powerful statement about the integral pedology and ecology to explicitly frame an Earth systems science nature of production and decomposition (quoted above), it is that included all activities of plants, microbes and animals, tempting to envision him opposing such a rift between above- and including human beings, as integral to and dependent on the belowground terrestrial ecology. How ironic that ecosystem science planet’s diverse and numerous CZs. Over the long term, the that was launched to integrate auto- and heterotrophic organisms functioning of CZs is supported by a richness in diversity, not only and their environment would develop scientists who would display of biological organisms, but of soils, sediments and regoliths, such guild-like behavior with regard to their expertise and interests dynamic and deep aquifers, biogeochemical weathering reactions with the above- or belowground ecosystem! and by geophysical preconditioning of the crustal substrates Such a critique of terrestrial ecosystem science is not new, and themselves. CZs were called ‘critical’ because of the fundamental was in fact Wardle’s in writing his tour de force, Communities and dependence of life on CZ structures and functions, and on the Ecosystems (2002) that linked activities of aboveground plant gravity with which human activities are transforming most of producers with belowground heterotrophic decomposers. Binkley Earth’s CZs (Vitousek et al., 1997). As a result, Jordan et al. (2001) (2006) also critiqued the division between above- and belowground emphasized the need for new integrative studies to coordinate scientists and the lack of interaction between what he called measurements and modeling of CZs across space and time, all to ‘ecologists’ and ‘soil scientists.’ Binkley’s (2006) essay, entitled accelerate an understanding of CZ change and management across ‘Soils in ecology and ecology in soils’, attributed much of the human to geologic time scales. problem to the disciplinary formation of ecology and soil science Within a decade of the framing of CZs by Jordan et al. (2001), during the 20th century. Binkley (2006) characterized 19th century international scientists and research managers, led by Drs Susan concepts of terrestrial science held by the likes of Darwin, Brantley and Enriqueta Barrera, have helped launch an interdis- Dokuchaev and Pasteur to be well-integrated, whole-system ciplinary network of Critical Zone Observatories (CZOs) in the representations of the natural world, and he spiced his essay with USA, UK, Germany, France, China and other nations (Fig. 1). CZ a quote from Hans Jenny (Stewart, 1984), the noted pedologist and scientists and research funders, affectionately called ‘critical zonists’ ecosystem scientist, who provocatively commented ‘Many ecolo- by Latour (2014), are ambitious to grow this new science of gists glibly designate soil as the abiotic environment of plants, a coordinated observation, experimentation and modeling based at phrase that gives me the creeps.’ Although Wardle (2002), Binkley observatories world-wide, each wirelessly streaming real-time data (2006) and Jenny (1980) laid bare the historic divisions within

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Fig. 1 A map of international Critical Zone Observatories (CZOs) and afﬁliated CZ sites (Banwart et al., 2013; reproduced with permission from the University of Shefﬁeld, UK).

Table 2 The new and burgeoning literature of Earth’s critical zone science includes interdisciplinary contributions on a range of advanced topics, many of which overlap with ecosystem science

Topics Citations

Synthetic conceptual works that challenge ways of doing science Brantley et al. (2007); Banwart et al. (2013); Latour (2014); Lin (2014) Energy ﬂows and respiration Oh et al. (2005); Rasmussen et al. (2011b) Biogeochemistry Fimmen et al. (2008); Cenki-Tok et al. (2009); Tishchenko et al. (2014) Eco- and pedo-hydrology Lin (2012); Salve et al. (2012); Band et al. (2014) Microbial, root and chemical responses to redox oscillations Thompson et al. (2006); DeAngelis et al. (2010); Yang et al. (2012); Hall et al. (2013, 2014)

Acclimation and response of vegetation to elevated CO2 and Norby et al. (2004); Jackson et al. (2009); Drewry et al. (2014) geoengineering Biotic effects on topography Dietrich & Perron (2006) Novel isotopes to estimate complex critical zone processes Chabaux et al. (2003); Derry et al. (2006); von Blanckenburg et al. (2012); Bouchez et al. (2013) Tree root and climate control of land surface mobility Schwarz et al. (2010); Anderson et al. (2013) Soil and regolith production Braun et al. (2012); Lebedeva & Brantley (2013) Topographic development of the deep subsurface Rempe & Dietrich (2014); J. St Clair et al. (unpublished) Residence times of weathering profiles Rasmussen et al. (2011a); Bacon et al. (2012); Bazilevskaya et al. (2013); Brantley et al. (2013) Nonlinearity in vegetation, soil and topographic responses to Pelletier et al. (2013) elevation and aspect Weathering rate dependence on hydrologic residence time Maher (2010) Ecological resilience under variability Srinivasan & Kumar (2014) Critical zone services Field et al. (2015) terrestrial ecosystem science, here we emphasize the opportunities are open systems, the fundamental openness of ecosystems from these estrangements create for more fully integrating above- and below is practically unstudied. This is not an insignificant point, for belowground components of terrestrial ecosystems. if we characterize lower boundaries poorly, we may significantly misinterpret the evolution and resilience of terrestrial ecosystems, an idea we expand on below. 2. The superficiality of belowground investigation We present three examples to characterize how the lower Before we can attend to the integration of above- and belowground boundaries of terrestrial ecosystems have been superficially studied. ecology, we must examine the development of belowground Our first example comes from two review papers that address the terrestrial ecology itself. Like it or not, most belowground question of how land use change alters soil organic matter (Post & ecosystem science has been peculiarly superficial in its depth of Kwon, 2000; West & Post, 2002). In the 360 studies of the two exploration (Richter & Markewitz, 1995) and thus is limited in its reviews, the median depth of soil sampling was c. 20 cm. About expansiveness of interpretation. Relatively superficial understand- 90% of the 360 studies sampled the soil to 30 cm or less (Fig. 2). ing of belowground systems has had scientific and societal Although it is difficult to sample the belowground ecosystem, often consequences. Although all may generically agree that ecosystems composed of rocks, roots, and indurated and plastic clays, sampling

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understory plants, and of the forest ﬂoor and mineral soil. Depth of sampling belowground varied among the 36 ecosystems, with the belowground sample generally conceived to represent the root zone. Although the data accumulated in the IBP ecosystems were a landmark in the history of ecosystem science, belowground contents of carbon and nutrients were reported with little to no indication of the depth of sampling. Cole & Rapp (1981) noted:

There are many assumptions, some of them perhaps unacceptable, built into these calculations, but the major difficulty derives from lack of information regarding below-ground processes. Very few studies included any root information, and none had annual elemental increment information for the root system. Consequently it was not possible to include roots in any flux calculations. Thus, even by the 1970s and 1980s, quantitative data describing terrestrial ecosystems continued to be confined largely to above- Fig. 2 Histogram of maximum depth of soil sampling in > 360 research ground components. It was during the IBP project that fine roots studies that estimated changes in soil organic carbon in response to land use were discovered to be highly ephemeral structures and that their change (Post & Kwon, 2000; West & Post, 2002). rapid turnover rivaled the fluxes of carbon and nutrients in the annual turnover of leaf fall (Harris et al., 1980). The continuing difficulties only partly explain the sampling depths revealed in controversy surrounding rates of fine root turnover and their Fig. 2. The surficial sampling reflects the widely held assumption contribution to fluxes of the carbon and nutrients of terrestrial that the most important and dynamic soil layers for gains and losses ecosystems (Gaudinski et al., 2001; Matamala et al., 2003; Preg- of carbon and nutrients are those that are most surficial. The system itzer et al., 2008) underscores the point that belowground processes below 20 or 30 cm is presumed to change at such slow rates that are relatively poorly and superficially characterized. sampling is not required. A third example is an international project of the late 1980s and Although organic carbon inputs and outputs are most rapid in 1990s, the Integrated Forest Study (IFS). This project was surficial layers of soil, the relative balance of organic carbon inputs organized to investigate how industrial air pollution and resultant and outputs in surface layers may contrast with that at depth acid deposition were acidifying the environment, diminishing the (Trumbore et al., 1995; Richter et al., 1999; Gaudinski et al., 2001; availability of soil nutrients and influencing productivity and long- Mobley et al., 2014). Temporal changes in subsoil organic carbon term functioning of terrestrial ecosystems. The IFS was organized have not been well addressed (Jenkinson et al., 2008; Rumpel & in part as an updated version of the IBP and included 17 sites across K€ogel-Knabner, 2011; Mobley et al., 2014) and yet they may be North America and Europe. The depths of belowground sampling highly significant to local and global carbon cycles. Relatively small were conceptually taken to be rooting depths, but in contrast with changes in organic carbon concentrations in large volumes of IBP, the IFS sampling depths were precisely quantified, ranging subsoil may be hard to detect, but may still amount to substantial from 41 to > 120 cm, with the median depth of sampling of c. changes in carbon content. For example, over a century, a gain or 60 cm. Johnson & Lindberg (1992) were well aware that: sampling loss of 0.1% soil organic carbon (SOC) in 100 cm of subsoil would depths and lower boundaries of the belowground ecosystems be difficult to detect, but the content of that SOC would be the greatly affected interpretations of the vulnerability of ecosystems to same order of magnitude as the rates of change in SOC contents acidic deposition, and belowground ecosystem data had large estimated by Post & Kwon (2000) and West & Post (2002) in the uncertainties. A major conclusion of the IFS project was that deep upper 20–30 cm of soil. This point was recently quantified by soil processes, such as nutrient release via mineral weathering and Mobley et al. (2014) who documented no net change in SOC in deep root uptake, were in much need of research (April & Newton, repeated samplings of the surficial 60 cm of mineral soil in 16 plots 1992). that were undergoing 50 yr of reforestation following long-term These three examples demonstrate the historic, unresolved cultivation. Remarkably, no net change in SOC across 60 cm was nature of lower boundary conditions of terrestrial ecosystems, and the net result of significant increases in organic carbon at 0–7.5 cm point directly to underlying boundaries being an important focus of and concurrent significant decreases in carbon at 35–60 cm. contemporary belowground studies. Recent and on-going research A second example of belowground sampling practices is from the demonstrates that lower ecosystem boundaries are deeper and more International Biological Program (IBP) conducted in the 1970s in open, diffuse, heterogeneous and temporally variable than we have 36 ecosystems in Europe, Asia and North America (Reichle, 1981; often assumed in the past (Richter & Yaalon, 2012). Deep cores Coleman, 2010). The objectives were to estimate fluxes and and excavations are revealing that subsoil nutrient and organic inventories of carbon and nutrients across a broad range of the matter supplies, even in rocky terrain, can be quantitatively and world’s terrestrial ecosystems. For the time, the IBP data were ecologically substantial down through several meters (Jobbagy & invaluable in their detail, revealing contents and dynamics of Jackson, 2001; Harrison et al., 2003, 2011; James et al., 2014). chemical elements of foliage, branches and boles of forest trees and Deep underlying bedrock chemistry can impart substantial effects

New Phytologist (2015) 206: 900–912 Ó 2015 The Authors www.newphytologist.com New Phytologist Ó 2015 New Phytologist Trust New Phytologist Tansley review Review 905 on vegetative productivity and ecosystem evolution itself (Hahm et al., 2014), and the geochemical importance of underlying bedrock has even been extended to nitrogen (Morford et al., 2011). The phenomenon of hydraulic lift (Caldwell et al., 1998) demonstrates the remarkable ability of deep roots to extend hydrologic rooting depths, with roots efficiently taking up deep water via diurnal cycles based on water potential differences of plant cells and soil. Lastly, mycorrhizal research continues to expand our appre- ciation of the ecological significance of deep subsoils. Mycorrhizas are observed to tunnel through feldspars and hornblendes, presumably via organic acid dissolution, releasing rock-bound nutrients for biotic uptake (Hoffland et al., 2003). Although tree roots in deep C horizons and regolith may be physically excluded from the regolith matrix and confined to bedrock fractures, their ectomycorrhizal hyphae can proliferate throughout the regolith’s microporosity, enabling ecosystems to cycle water and nutrients from, in one case, a 4-m-deep rooting zone (Bornyasz et al., 2005).

V. The metabolism of ecosystems and critical zones Unresolved lower boundaries of ecosystems are perhaps best explored by considering ecosystem metabolism, the biological– Fig. 3 Aquatic ecosystem scientists Professors Edward A. Birge and Chancey physical–chemical process of energy flow through ecosystems and Juday sampling the water column on Lake Mendota at the University of CZs. In this section, we first consider why the study of ecosystem Wisconsin, c. 1917. Reprinted with permission from the Wisconsin History Society, Madison, WI, USA. metabolism accelerated first in the 1940s in aquatic ecosystems, decades before that in terrestrial systems. Terrestrial science finally coalesced around common approaches to metabolism in the 1960s, pollutant organic matter in river stretches (Vesilind et al., 2010), but even today we maintain that our understanding of terrestrial aquatic ecologists measured diurnal variations of aqueous oxygen to metabolism is limited by incomplete belowground data. We use the estimate ecosystem photosynthesis and respiration (Odum, 1956). propagation (Reiners & Driese, 2004) of belowground respiratory What was new was that ecosystem scientists quantified energy flow CO2 to help define the lower boundary of the ecosystem, and throughout the whole physical system. Odum’s (1956) classic therefore the congruence of the ecosystem and CZ concepts. illustration (Fig. 4) of stream metabolism depicts the ecosystem approach, showing photosynthetic inputs (‘P’) of organic reduc- tants and respiration (‘R’) of the various organisms. In Fig. 4, P is 1. Metabolism in aquatic and terrestrial ecosystems less than R because the stream respired a sizeable amount of Energy flow through ecosystems has excited scientists throughout allochthonous detritus (‘imports’), a clear demonstration of what the history of ecosystem ecology and biogeochemistry (Lindeman, Tansley (1935) had referred to as the overlapping and interlocking 1942; Odum, 1956; Gosz et al., 1978; Enquist et al., 2003; of ecosystems. DeLucia et al., 2005; Cole, 2013). Odum (1968) called eco- By the 1960s and 1970s, metabolism data had become sufficient energetics ‘the core of ecosystem analysis’ and Hutchinson (1940) to make first-order estimates of terrestrial energy flows in forests, and his students helped initiate ecosystem science with studies of grasslands and other terrestrial systems. Gases, water and solids of the metabolism of aquatic systems (Lindeman, 1942; Odum, terrestrial ecosystems are not as well mixed as they are in aquatic 1956). systems, and metabolic rates range by many orders of magnitude In the 1940s and 1950s, ecosystem metabolism was documented across plant and animal biomass, organic detritus, the decomposers in lakes, ponds, reefs, streams and rivers (Hagen, 1992), in part themselves, soil and underlying substrata. Gases and water flow because aquatic systems have characteristics that make them through complex networks that include vascular tissues, mycor- amenable to metabolic studies. Specifically, aqueous systems have rhizal hyphae and tortuous interconnections of pores within soil, relatively rapid and thorough mixing rates, the water column is regolith and the weathering bedrock itself with its fractures and relatively easy to sample (Fig. 3), many aquatic organisms have heterogeneous weathering zones. As a result of this complexity, small sizes and, despite great abundance, can be efficiently sampled, metabolism measurements in terrestrial ecosystems proved to be a and the gas–liquid phase boundary strongly constrains gas diffusion daunting task, with much work left to be accomplished even today. between the aqueous and atmosphere systems. In addition, by the In spite of these challenges, terrestrial primary productivity was 1930s, analytical instrumentation was available to estimate aquatic quantified in a number of ecosystems by the 1960s (Ovington, ecosystem photosynthesis and respiration. 1957; Rodin & Bazilevich, 1965; Woodwell & Whittaker, 1968). Following sanitary engineers, such as Harold Streeter and Earle In the 1970s, Lieth (1975) and Lieth & Whittaker (1975) compiled Phelps, who for decades had estimated heterotrophic oxidation of terrestrial carbon data and weighted them by area of the world’s

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Fig. 4 The first ecosystem metabolism estimates were in lakes, reefs, streams and rivers. Here, Odum’s (1956) diagram of ecosystem metabolism of flowing waters balances primary production (P) and imports of organic matter with respiration (R) and exports. The energy flow diagram contains organisms of five trophic levels (in boxes): primary producing plants, herbivores, decomposers, carnivores, and top carnivores. In the system illustrated, R > P as a result of imports from upstream. Copyright (2014) by the Association for the Sciences of Limnology and Oceanography, Inc.

major terrestrial ecosystems to make the first global estimates of terrestrial ecosystem metabolism. Globally, gross primary productivity, net primary productivity and soil respiration were estimated to be responsible for carbon fluxes of c. 120 9 1015,609 1015 and 9 15 1 60 10 gCyr , remarkably large fractions of the total CO2 of the atmosphere (c. 800 9 1015 gCyr1). Most notably, after nearly 40 yr of additional research of ecosystem carbon exchange from the tundra to the tropics in field-based and remote sensing research, these initial estimates of global terrestrial metabolism have proven to be robust. By the 1990s, some of the most important ecosystem studies tested the response of terrestrial metabolism to the rising CO2 of the global atmosphere in Free Air Carbon Exchange (FACE) experiments. In FACE experiments in deserts, croplands and forests, ecosystem metabolism has exhibited a strong dependence on CO2 concentrations in the aboveground atmosphere (Fig. 5), with metabolic effects highly significant belowground. Responses of the young temperate zone pine forest in Fig. 5 included soil CO2 Fig. 5 Some of the most important metabolism estimates in terrestrial effluxes (Rh), changes in activity of different microbial groups ecosystems come from field experiments of elevated CO2 (FACE dependent on soil carbon as an energy source (Billings & Ziegler, experiments) that test metabolic responses of ecosystems to future elevated

2008) and depth-dependent concentrations and carbon-isotope CO2 (DeLucia et al., 2005). Here, fluxes of energy are in units of 2 1 gradients of CO2 down to 200 cm (Andrews & Schlesinger, 2001; gCm yr in a young pine forest (Pinus taeda) at Duke Forest in North Oh & Richter, 2004; Bernhardt et al., 2006; Oh et al., 2005, 2007; Carolina, USA. GPP, gross primary productivity; NPP, net primary Jackson et al., 2009). productivity; Ra, autotrophic respiration; Rh, heterotrophic respiration; NEP, net ecosystem productivity. Numbers in light balloons indicate 1 metabolic fluxes in forests growing in ambient CO2 (c. 380 lll ), and dark balloons indicate metabolic fluxes in forests growing in elevated CO2 2. Towards a systems perspective of belowground (elevated by c. 200 lll 1 to c. 580 lll 1 or the atmospheric concentration in respiratory CO2 c. 2050). Reproduced with permission from John Wiley & Sons. From the earliest estimates of terrestrial primary production in the 1950s to the most recent FACE studies, terrestrial ecosystem fixed carbon exchanges rapidly with the atmosphere, little attention metabolism is largely understood to be an ecological process of has been paid to the propagation of CO2 downwards throughout land-to-atmosphere exchange. Although most photosynthetically soil and deep bedrock substrata. These fluxes of deep CO2 are

New Phytologist (2015) 206: 900–912 Ó 2015 The Authors www.newphytologist.com New Phytologist Ó 2015 New Phytologist Trust New Phytologist Tansley review Review 907 examples of the propagation of ecosystem effects by Reiners & (a) A Driese (2004) and of Tansley’s ‘overlapping and interlocking’ of E ecosystems. We assert that the downward propagation of respira- B tory CO2 and its biological, chemical and physical effects are integral to the functioning of terrestrial ecosystems and CZs, and are key to understanding the congruence of the two concepts. At the Calhoun CZO in the warm temperate zone of North Soil horizons America’s Southern Piedmont, forest respiration rates are highest in surficial O and A horizons, even though O and A horizon CO2 C concentrations are the lowest of the entire soil and weathering profile (Richter & Markewitz, 2001). The soil’s A horizon, home to (m) Soil depth the most densely rooted and most biologically active volumes of the mineral soil’s decomposition system, has well-developed macrop- orosity that allows respired CO2 to rapidly diffuse and escape to the aboveground atmosphere. At deeper depths, however, although respiration rates are diminished, concentrations of CO2 increase by orders of magnitude as a result of pore network tortuosity, which decreases gas diffusivity and greatly increases CO2 residence time. Soil CO2 (%) From the Calhoun soil surface to c.4–6 m, the apparent depth of (b) maximum CO2 concentrations (called here Zmax), CO2 increases by c. 100-fold (Fig. 6a). Despite a large and rich literature devoted to belowground CO2 production, diffusion and fluxes, there are only the beginnings of research into CO2 dynamics above and below Zmax (e.g. Oh et al., 2005; Johnson et al., 2008). Oh et al. (2005) modeled belowground CO2 concentrations in the upper 10 m of soil (Fig. 7) using physical and biological properties corresponding generally to Calhoun soil profiles, whose CO observations are illustrated in 2 (m) Soil depth Fig. 6. In the upper meters of soil above Zmax, modeled [CO2] closely tracked observed concentrations (Figs 6, 7). From 6 to 10 m and presumably all the way down to 30 m, where the weathering profiles meet unweathered granite, modeled patterns of declining [CO2] depict a downward propagation of CO2. Although not yet measured, such a dynamic would represent highly significant Fig. 6 Average concentrations of CO2 in soil atmospheres of the Calhoun biogeochemistry that is yet to be much discussed in the ecosystem, Experimental Forest under an approximately 40-yr-old loblolly pine forest. soil or CZ literature. (a) Data averaged over 4 yr of bi- and tri-weekly collections from eight gas reservoirs per depth, except at 5.5 m depth, where there were four reservoirs Two factors can drive the reversal of [CO2] below Zmax (Fig. 7). (Richter & Markewitz, 2001). Reproduced with permission from Cambridge First, soil respiration rates diminish to near insignificance below University Press. (b) Periodically measured CO2 data plotted with Matlab. Zmax. Second, silicate mineral weathering becomes a sink for CO2 The depth of maximum CO2 concentration is called Zmax, which these data below Zmax, and this sink drives diffusion of CO2 downwards. At the suggest is c.4–6m. Calhoun CZO, a 70-m-deep core through a zero-order interfluve (Bacon et al., 2012; Brecheisen & Richter, 2014) traversed 30 m of In Calhoun’s deep weathering profile, the pH ranges from 3.7 to soil and saprolite, and 40 m of unweathered granite bedrock. The 4.2 (in 0.01 M CaCl2) in all samples from 0 to 10 m, but gradually solid core materials had strongly depth-dependent pH, exchange- increases to pH 5.5 in samples taken from 16.8 to 18.3 m (Bacon able cations, tauNa and tauCa, all of which demonstrated advanced et al., 2012). The chemistry of soil water collected from within this > > weathering to 10 m depths. At Calhoun, the CO2 sink at 10 m profile tells a similar story (Markewitz et al., 1998; Richter & can be represented with equations that describe how CO2 Markewitz, 2001). Throughout the upper 6 m of soil, soil water is l 1 consumption is tied to the weathering dissolution of albite dilute and marked with low HCO3 alkalinity (33 mol l at a (NaAlSi3O8), with reaction products being kaolinite depth of 6 m). The Calhoun soil is an advanced weathering stage [Al2Si2O5(OH)4], soluble sodium bicarbonate and silica: soil with no weatherable minerals to react with carbonic acid, despite high concentrations of CO2 (Fig. 5). However, water CO þ H O $ H CO collected from c. 25 m below the soil surface from a deep 2 2 2 3 > groundwater seep was 15-fold more concentrated in HCO3

2H2CO3 þ 2NaAlSi3O8 þ H2O ! (Fig. 8). The increases in alkalinity were balanced by increases mainly in Na+ and Ca2+, but also in Mg2+ (Stumm & Morgan, ð Þ þ þ þ þ Al2Si2O5 OH 4 2Na 2HCO3 4SiO2 2012). Respiratory CO2 propagated deeply into this proﬁle thus

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CO2 (%) through the soils and into the aboveground atmosphere (Fig. 7). 0 1 2 3 4 5 Andrews & Schlesinger (2001) estimated the leaching of 0 alkalinity from the FACE pine forest (Fig. 5) to be only c.1% of total soil respiration. Nevertheless, plant life in the above-

2 ground ecosystem drives weathering reactions in the lowest reaches of the ecosystem by the biophysical magniﬁcation of CO2 partial pressures (Figs 6, 7), with strong seasonal and depth- 4 dependent waves of [CO2] propagating deeply through the belowground ecosystem (Richter & Markewitz, 1995; Baldocchi et al., 2006; Johnson et al., 2008; Jackson et al., 2009). The Depth (m) 6 biogeochemical result is carbonic acid weathering of rock-derived minerals that releases soluble nutrients to deep roots and drainage (1) Feb – – 8 (2) May waters and critically produces soil from the bottom up (3) Aug (Heimsath et al., 1997). Thus, the small fraction of the system’s (4) Nov total respiration that diffuses downwards can have an enormous 10 inﬂuence on ecosystem structure and function by helping to

Fig. 7 A model simulation of soil CO2 using system properties and fluxes generate the soil that ultimately supports the ecosystem itself. We comparable with those at the Calhoun pine forest illustrated in Fig. 6 (Oh submit that, although the lower boundary of the terrestrial et al., 2005). The figure is an excellent illustration of an ecosystem ecosystem may be diffuse, heterogeneous and open, the metab- propagation as in Reiners & Driese’s (2004) propagation of ecosystem olism of the terrestrial ecosystem demonstrates that the ecosys- influence (CO and carbonic acid) throughout the belowground ecosystem 2 tem’s lower boundary is the bottom of the CZ itself, the depth to and down into the weathering bedrock. Here, the depth of maximum CO2 concentration (Zmax) is modeled to be seasonally dependent and between 3 which biogeochemical signals penetrate the Earth’s surface. and 6 m. VI. Towards a more active biogeoscience Wet-only precipitation We began this review with the assertion that terrestrial ecosystems and Earth science’s CZ were congruent across spatial and temporal Throughfall scales of vegetation-clad weathering profiles and hillslopes to small O horizon catchments, landscapes, river basins, continents and the terrestrial Earth itself. We asserted that the congruence of concepts is most 0.15 m readily apparent viewed from Tansley’s ecosystem as ‘one physical Anions Cations system’ and Lindeman’s and Hutchinson’s conviction of the HCO Na 0.6 m 3 inseparability of the biotic–abiotic complex. From this perspective, X Cl X Ca Soil depth (m) Mg SO4 it is evident that terrestrial ecosystem scientists have important 1.75 m Org. Acids K NH unfinished business in the study of ecosystem metabolism, NO3 4 H specifically in quantifying the propagation and biogeochemical 6.0 m effects of plant-derived respiratory CO2 that diffuses throughout soils and deeply into weathering geologic substrata. Although these Seep metabolic processes may account for a relatively small fraction of –600 –500 –400 –300 –200 –100 0 100 200 300 400 500 600 total respiration belowground, they are fundamental for the biogeochemical effects that follow: the microbiological recycling of CO and the carbonic acid weathering that helps to produce the Cumulative concentrations (µeq l–1) 2 very soil on which the ecosystem depends (Richter & Markewitz, Fig. 8 Soil and seep water chemistry at Calhoun’s long-term soil experiment 1995). site illustrated in Fig. 6 and modeled in Fig. 7 (Richter & Markewitz, 2001). No weatherable minerals exist in the upper 10 m of these highly weathered Two implications follow from this congruence in concepts. First, Ultisols and thus, despite elevated CO2, HCO3 alkalinity is very low until given that ecosystems are open, three-dimensional systems, the deep in the weathering profile (< 50 leq l 1), with groundwater collected ecosystem is cut short if it includes too little of the belowground from a seep c. 25 m below the soil surface and containing > 10-fold the environment. Ecosystem resilience and sustainability cannot be – alkalinity as that of the water collected throughout 0 6 m. Reproduced with accurately gaged, nor can Tansley’s ecosystem vision be realized, if permission from Cambridge University Press. lower boundary conditions are not carefully evaluated. Today, opportunities abound to explore connections between upper and driving carbonic-acid weathering of Na-, Ca- and Mg-bearing lower components of CZ ecosystems, between soils and streams in minerals in the saprolite below Zmax (Richter & Markewitz, 2001; watersheds, and between CO2 derived from plants and deep Bacon et al., 2012). microbial communities, all to better resolve ecosystem and CZ Diffusion of CO2 downwards in the profile may account for a evolution and resilience. The biological and geological arms of the relatively small fraction of the total CO2 that diffuses upwards national science foundations of many nations now support

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programs, such as the International Long-Term Ecological Andrews JA, Schlesinger WH. 2001. Soil CO2 dynamics, acidification, and chemical weathering in a temperate forest with experimental CO2 enrichment. Research Program (ILTER), the international CZO programs – (Fig. 1), and in the USA the National Ecological Observatory Global Biogeochemical Cycles 15: 149 162. April R, Newton R. 1992. Mineralogy and mineral weathering. In: Johnson DW, Network (NEON), each of which can greatly benefit from the Lindberg SL, eds. Atmospheric deposition and forest nutrient cycling. New York, NY, recognition of the congruence of the ecosystem and CZ concepts. USA: Springer, 378–425. For example, although we expect much significant and timely data Bacon AR, Richter DdeB, Bierman PR, Rood DH. 2012. Coupling meteoric 10Be with pedogenic losses of 9Be to improve soil residence time estimates on an to soon flow from the USA’s NEON program, the explicit 2-m- – deep limit of belowground sampling (Loescher et al., 2014) ancient North American interfluve. Geology 40: 847 850. Baldocchi DB, Tang J, Xu L. 2006. How switches and lags in biophysical regulators terminates belowground ecological processes at a depth far too affect spatial–temporal variation of soil respiration in an oak–grass savanna. shallow for many ecosystems. Given the tens of thousands of Journal of Geophysical Research 111: G02008, doi: 10.1029/2005JG000063. sensors and samplers being installed in the 60 NEON sites across Band LE, McDonnell JJ, Duncan JM, Barros A, Bejan A, Burt T, Dietrich WE, Emanuel RE, Hwang T, Katul G et al. 2014. Ecohydrological flow networks in the USA, a relatively small number of additional sensors and – samplers at > 2 m depth can be installed to monitor moisture, the subsurface. Ecohydrology 7: 1073 1078. Banwart SA, Chorover J, Gaillardet J, Sparks D, White T, Anderson S, temperature and biogeochemistry, and thereby extend the ecosys- Aufdenkampe A, Bernasconi S, Brantley SL, Chadwick O et al. 2013. Sustaining tem to the full depth and volume of the CZ. The results would Earth’s critical zone basic science and interdisciplinary solutions for global challenges. almost certainly transform how we understand ecosystem dynamics Sheffield, UK: University of Sheffield. and evolution, and have major benefits for CZ science, given the Bazilevskaya E, Lebedeva M, Pavich M, Rother G, ParkinsonDY, Cole D, Brantley extensive and careful placement of NEON sites across North SL. 2013. Where fast weathering creates thin regolith and slow weathering creates thick regolith. Earth Surface Processes and Landforms 38: 847–858. America’s climatic and vegetative gradients. Bernhardt ES, Barber JJ, Pippen JS, Taneva L, Andrews JA, Schlesinger WH. 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