Ecological Applications, 12(4), 2002, pp. 937±947 ᭧ 2002 by the Ecological Society of America

NET ECOSYSTEM PRODUCTION: A COMPREHENSIVE MEASURE OF NET ACCUMULATION BY ECOSYSTEMS

J. T. RANDERSON,1,6 F. S . C HAPIN, III,2 J. W. HARDEN,3 J. C. NEFF,4 AND M. E. HARMON5 1Divisions of Engineering and Applied Science and Geological and Planetary Sciences, California Institute of Technology, Mail Stop 100-23, Pasadena, California 91125 USA 2Institute for Arctic Biology, 311 Irvine 1 Building, University of Alaska, Fairbanks, Fairbanks, Alaska, 99775 USA 3U.S. Geological Survey, Mail Stop 962, 345 Middle®eld Road, Menlo Park, California 94025 USA 4U.S. Geological Survey, Mail Stop 980, Denver Federal Center, Denver, Colorado 80225 USA 5Department of Forest Science, Oregon State University, Corvallis, Oregon 97331-57521 USA

Abstract. The conceptual framework used by ecologists and biogeochemists must allow for accurate and clearly de®ned comparisons of carbon ¯uxes made with disparate tech- niques across a spectrum of temporal and spatial scales. Consistent with usage over the past four decades, we de®ne ``net ecosystem production'' (NEP) as the net carbon accu- mulation by ecosystems. Past use of this term has been ambiguous, because it has been used conceptually as a measure of carbon accumulation by ecosystems, but it has often been calculated considering only the balance between gross (GPP) and ecosystem respiration. This calculation ignores other carbon ¯uxes from ecosystems (e.g., leaching of dissolved carbon and losses associated with disturbance). To avoid conceptual ambiguities, we argue that NEP be de®ned, as in the past, as the net carbon accumulation by ecosystems and that it explicitly incorporate all the carbon ¯uxes from an ecosystem, including autotrophic respiration, heterotrophic respiration, losses associated with distur- bance, dissolved and particulate carbon losses, volatile organic compound emissions, and lateral transfers among ecosystems. Net biome productivity (NBP), which has been proposed to account for carbon loss during episodic disturbance, is equivalent to NEP at regional or global scales. The multi-scale conceptual framework we describe provides continuity be- tween ¯ux measurements made at the scale of soil pro®les and chambers, forest inventories, eddy covariance towers, aircraft, and inversions of remote atmospheric ¯ask samples, al- lowing a direct comparison of NEP estimates made at all temporal and spatial scales.

Key words: atmospheric CO2; biosphere±atmosphere ¯uxes; carbon accumulation by ecosystems, measuring; carbon balance; disturbance; net biome production; net ecosystem production; net primary production; scaling.

INTRODUCTION creasing need to de®ne carbon budgets at regional and Some of the biogeochemical processes that affect the continental scales (Steffen et al. 1998). Unfortunately, carbon balance of terrestrial ecosystems include pho- direct measurements of carbon ¯uxes at regional to tosynthesis (Farquhar et al. 1980, Collatz et al. 1991), global scales are dif®cult with current technology (Tans plant respiration (Ryan 1991), microbial respiration 1993) so estimates of regional- and continental-scale C ¯uxes require the integration of remote atmosphere (Parton et al. 1993), leaching losses (Neff and Asner and satellite observations with ®eld measurements and 2001), erosion (Stallard 1998), herbivory (McNaugh- experimental manipulations (Running et al. 1999). ton et al. 1989), ®re (Crutzen and Andreae 1990), ice- Initial investigations of biosphere±atmosphere car- sheet expansion and retreat (Harden et al. 1992, Schles- bon exchange made the assumption that the net ¯ux inger 1997), and rates of rock weathering (Berner can be approximated as the balance between photo- 1993). Human appropriation and modi®cation of the synthesis and respiration (Keeling 1961, Machta 1972, earth's surface over the last several centuries has al- Pearman and Hyson 1980, Fung et al. 1983). This was tered many of these processes, with consequences for sensible given that many diurnal and seasonal patterns net ecosystem carbon ¯uxes, atmospheric mass bal- of atmospheric CO2 concentration can be explained by ance, and inputs to oceans (Vitousek et al. 1986, considering only these two processes (Denning et al. Houghton 1996, DeFries et al. 1999). With attention 1996, Heimann et al. 1998). However, analysis of in- focused by the Kyoto Protocol (Schulze et al. 2000) terannual and decadal dynamics in atmospheric CO2 and subsequent international dialogue on carbon emis- driven by changes within the terrestrial biosphere re- sions from individual nations, there has been an in- quires consideration of additional processes including ®re, (DOC) and dissolved in- Manuscript received 12 June 2001; revised 1 October 2001; accepted 4 October 2001; ®nal version received 13 November organic carbon (DIC) losses in rivers, erosion, and 2001. land-use changes such as agriculture and timber harvest 6 E-mail: [email protected] (Canadell et al. 2000, Pacala et al. 2001). 937 938 J. T. RANDERSON ET AL. Ecological Applications Vol. 12, No. 4

TABLE 1. Summary of contemporary terrestrial ecosystem carbon ¯uxes.

Acronym/ Concept symbol Global ¯ux De®nition Gross primary production GPP ϳ100±150 Pg C/yr carbon uptake by plants during pho- tosynthesis Autotrophic respiration Ra ϳ½ of GPP respiratory loss (CO2) by plants for construction, maintenance, or ion uptake Net primary production NPP ϳ½ of GPP GPP Ϫ Ra Heterotrophic respiration (on land) Rh ϳ82±95% of NPP respiratory loss (CO2) by the hetero- trophic community (herbivores, mi- crobes, etc.) Ecosystem respiration Re ϳ91±97% of GPP Ra ϩ Rh Non-CO2 losses ϳ2.8±4.9 Pg C/yr CO, CH4, isoprene, dissolved inor- ganic and organic carbon, erosion, etc; see Table 2. Non-respiratory CO2 losses (®re) ϳ1.6±4.2 Pg C/yr combustion ¯ux of CO2; see Table 2. Net ecosystem production NEP ϳϮ2.0 Pg C/yr accumulation within the ecosystem; de®ned in De®ning Net Ecosystem Production: A compre- hensive de®nition of NEP.

In part because of the rapid expansion of carbon With new assessments of volatile organic compound cycle analyses at regional to global scales, we are left (VOC), methane, ®re, and river ¯uxes, the sum of non- with ambiguities in our conceptual framework (see Ta- CO2 and non-respiratory losses from terrestrial eco- ble 1 for a summary of ecosystem ¯ux concepts). systems is substantial at stand, regional, and global Should net ecosystem production (NEP), which was scales. Combined, these ¯uxes represent a loss of initially approximated in the ®rst biosphere±atmo- ϳ10% of global net primary production (NPP) (Table sphere CO2 studies as the difference between photo- 2), and thus provide motivation for de®ning NEP solely synthesis and respiration, formally include all carbon in terms of carbon accumulation at all scales of inquiry. exchanges that in¯uence net carbon accumulation by A comprehensive de®nition of NEP an ecosystem (as the name ``net ecosystem production'' implies)? Alternatively, should NEP refer solely to the To reconcile carbon ¯ux measurements made with photosynthesis and respiration components (as sug- diverse techniques and across widely varying time and gested by some recent analyses, e.g., Schulze and Hei- space scales, NEP must be de®ned as the rate at which mann [1998], Steffen et al. [1998], and Buchmann and carbon (C) accumulates within an ecosystem (i.e., the Schulze and [1999])? change in carbon storage over some time interval):

DEFINING NET ECOSYSTEM PRODUCTION NEP ϭ dC/dt. (1) Historical perspective A critical element of this de®nition is that the ecosys- tem in consideration must have de®ned boundaries in The simultaneous de®nition of NEP as the carbon three dimensions (it must be possible to enclose the accumulation within ecosystems and as the difference ecosystem with a three-dimensional container or box). between gross primary production (GPP) and ecosys- For example, in a forest ecosystem, the top of the box tem respiration extends back in the ecological literature might be de®ned as the height of the tallest tree, while over four decades (Woodwell and Whittaker 1968, the bottom of the box might be de®ned as a speci®ed Woodwell and Botkin 1970, Reichle et al. 1975). These soil depth. Another critical feature of this de®nition is two de®nitions are equivalent when non-photosynthetic that the start and end times of the measurement period gains and non-respiratory losses to an ecosystem are (or interval of integration) must be speci®ed. Conser- negligible, and so in many applications over the last vation of mass requires that ¯uxes (F ) across the eco- few decades the two de®nitions have been used inter- system boundaries equal the rate of change in C within changeably. Increasing interest in the global carbon the ecosystem. Thus, NEP has the equivalent de®nition budget and the partitioning of land and ocean carbon (Olson 1963): sinks in the late 1970s focused attention on the need to quantify non-respiratory losses from terrestrial eco- NEP ϭ Finϩ F out systems, including ®re and river ¯uxes (Bolin et al. F F F F F 1979). As described by Lugo and Brown (1986), even ഠ GPP ϩ Re ϩ fireϩ leachingϩ erosion if the terrestrial biosphere were close to steady-state ϩ F ϩ F ϩ F ϩ ´´´. (2) carbon balance, a substantial biosphere±atmosphere hydrocarbons herbivory harvest

CO2 sink would be required to match river carbon Therefore, NEP encompasses all ¯uxes (Fi) across all losses. the boundaries of the ecosystem, independent of the August 2002 NET ECOSYSTEM PRODUCTION 939

TABLE 2. Global non-CO2 and non-respiratory carbon losses from terrestrial ecosystems.

Flux Flux range Source Components (Pg C/yr) (Pg C/yr) Reference

Non-CO2 losses Rivers dissolved organic carbon 0.40 0.20±0.90 Schlesinger and Melack (1981), Degens (1982), Degens et al. (1991), Meybeck (1982), Suchet and Probst (1995), Stallard (1998) dissolved inorganic carbon 0.30 ² particulate organic carbon 0.30 ² Volatile organic compounds, isoprene 0.50 ² Guenther et al. (1995) VOCs monoterpene 0.12 ² other reactive VOCs 0.26 ² other non-reactive VOCs 0.26 ² Methane natural sources 0.16 0.11±0.21 Prather et al. (1996) anthropogenic biosphere 0.27 0.20±0.35 Carbon monoxide, CO ®res 1.0 0.50±1.50 Bergamaschi et al. (2000) photochemical oxidation of 0.06 0.03±0.09 Schade and Crutzen (1999) organic matter thermal oxidation of organic 0.04 0.01±0.08 Schade et al. (1999) matter

Non-respiratory CO2 losses Fires ´´´ 3.0 1.6±4.2 Crutzen and Andreae (1990)

Total sum of non-CO2 and non- ´´´ 6.6 4.4±9.2 respiratory CO2 losses³ ² Range of estimates not available. ³ Total ¯ux is ϳ11% of global NPP at 60 Pg C/yr, which is ϳ6 times larger than the net terrestrial carbon ¯ux estimated by Prentice et al. (2001).

driving mechanism or the degree of biological regu- (GPP) and ecosystem respiration (Re; including both lation (Fig. 1). This de®nition must include all ¯uxes autotrophic and heterotrophic components) in which because, in many instances, it is dif®cult to distinguish CO2 diffuses directly through a cell membrane. Fluxes between C ¯uxes that are regulated solely by abiotic associated with ®re (F®re) and soil erosion (Ferosion) also or biotic processes. Clear examples of ¯uxes with direct are strongly regulated by biological and ecological pro- biological regulation include gross primary production cesses, though not necessarily at a cellular level. The

FIG. 1. Regulation of net ecosystem production (NEP) by processes in terrestrial ecosystems varies with the time±space scales. At longer timescales and larger spatial scales, dissolved organic and inorganic river ¯uxes (DOC/DIC), ®res, and erosion play critical roles in regulating ecosystem carbon balance. On shorter timescales, gross primary production (GPP) and ecosystem respiration (Re) are dominant processes. 940 J. T. RANDERSON ET AL. Ecological Applications Vol. 12, No. 4

®re ¯ux (F®re; which includes CO2, CO, CH4, VOCs, vious de®nitions of NEP although they have been fre- and particulates) needs to be included in this de®nition, quently inferred as a part of heterotrophic respiration so that NEP is equivalent to the ecosystem mass rate (Parton et al. 1993). Either we need still another con- of change over any timescale. cept that re¯ects total ecosystem C accumulation or (as we argue here) we need to explicitly include all C ex- The role of non-CO2 ¯uxes changes in NEP, so that this term truly re¯ects the net

Not all ecosystem C ¯uxes are in the form of CO2 C accumulation by ecosystems, as has been implied in gas. Leaching (Fleaching) and hydrocarbon emissions the past.

(Fhydrocarbons) contribute signi®cantly to NEP in many ecosystems. For example, in boreal peatlands and arctic Disturbance and NEP tundra, vertical and lateral ¯uxes of dissolved organic All of the ¯ux components that contribute to NEP carbon (DOC), dissolved inorganic carbon (DIC), and de®ned in Eq. 2 are either a direct result of disturbance methane are as much as 5% to 10% of the net ecosys- events or are responding to a complex history of mul- tem±atmosphere CO ¯ux (Waddington and Roulet 2 tiple disturbances that leave a long-term biological leg- 1997, King et al. 1998, Reeburgh et al. 1998). In tundra acy (Reichle et al. 1975). ecosystems, the inclusion of dissolved CO and meth- 2 ``Disturbance'' is frequently de®ned as a relatively ane ¯uxes in calculations of NEP reduced carbon up- discrete event that induces widespread mortality of the take rates by 20% relative to the ecosystem±atmosphere dominant species within an ecosystem (e.g., Aber and CO ¯ux (Kling et al. 1992). Isoprene, terpene, and 2 Melillo 1991). Climate variability, N deposition, and other volatile organic compound (VOC) emissions also stimulation of plant growth by elevated levels of at- contribute to NEP (Lerdau 1991, Monson et al. 1991, mospheric CO are often considered as separate pro- Guenther et al. 1995). 2 cesses (in terms consequences for C ¯uxes), though While stream ¯uxes of DOC are generally within the they also have the potential to cause stand-leveling range of 0±10 g C´mϪ2´yrϪ1 and average ϳ5g mortality events (Neilson 1993) and thus also have the C´mϪ2´yrϪ1, there is large variability (2±52 g potential to serve as agents of disturbance. C´mϪ2´yrϪ1) across ecosystems (Hope et al. 1994). Rates As with the de®nition of NEP described above, a of DOC ¯ux are also substantially higher in soils than comprehensive de®nition of disturbance should be in streams, indicating the need to explicitly de®ne a based on clearly de®ned spatial boundaries and time vertical (depth) ecosystem boundary in NEP calcula- intervals. Here we suggest following the framework tions (Neff and Asner 2001). The impact of soluble developed by Pickett et al. (1989). Pickett et al. (1989) carbon ¯uxes on carbon balance may be especially im- de®ne the ecological concept of disturbance as a change portant in streams draining boreal forests and in areas in the minimal structure of a system caused by an ex- with substantial wetland cover (e.g., Moore 1989, Hope ternal agent. Applying these concepts at the ecosystem et al. 1994, Waddington and Roulet 1997). Particulate scale, minimal structure includes the species compo- C losses can also be substantial in some ecosystems, sition, the distribution of plant functional types, and particularly following disturbance (Bormann et al. canopy architecture. Stand-leveling wind storms, ®res, 1974, Stallard et al. 1998). Are these losses signi®cant mortality induced by insect outbreaks, stand-killing when integrated to the global scale? A 1 Pg C/yr net droughts, and harvesting by humans all fundamentally terrestrial ¯ux evenly distributed over all biomes cor- alter this minimal structure and originate from a dif- responds to approximately a 10 g C´mϪ2´yrϪ1 ¯ux. Thus, ferent level of ecological organization, thus qualifying when integrated, stream and river losses are compa- as external agents. At the biome scale, a change in the rable in magnitude to the net terrestrial ¯ux (Prentice disturbance regime from climate change or humans et al. 2001). may constitute an external agent, with the ensemble of Carbon can also be removed or delivered to an eco- vegetation types and stand ages de®ning the minimum system by lateral transfer of organic material, as me- structure. diated by herbivores (Fherbivory) (McNaughton et al. 1989) or harvest (F ) (Harmon et al. 1990). In many harvest Human impacts on NEP cases herbivores are an internal component of an eco- system, and will not cause a net transfer of C across Humans affect all of the NEP components on the the three-dimensional shape de®ned for the purpose of right-hand side of Eq. 2 by modifying the atmospheric the NEP measurement. In other cases, herbivores may composition, nutrient levels, climate, erosion rates, and transfer C across the prede®ned spatial boundaries of disturbance regime. Examples of ¯uxes associated with the ecosystem, and thus contribute to NEP. Possible humans include the removal of crops in agricultural situations where this might occur include mass migra- ecosystems for use in distant feedlots and cities, the tions, insect outbreaks, or agricultural grazing, or in lateral transfer of wood from forests to paper mills, any situation where the de®ned ecosystem is small as from paper mills to suburban and urban areas, and then compared to the size of a typical herbivore. These com- to land®lls, and the altered heterotrophic respiration of ponents have not been explicitly incorporated into pre- plowed soils when disturbance reduces the protection August 2002 NET ECOSYSTEM PRODUCTION 941 of soil organic carbon from microbial attack (Kurz et duced changes in the disturbance regime become crit- al. 1995, Barlaz 1998, Skog and Nicholson 1998). ical regulators of NEP (Schulze and Heimann 1998, Canadell et al. 2000). The dominant components of NEP vary with scale At the global scale, the integral of NEP over the

As indicated in the discussion above, NEP poten- entire land surface (NEPglobal) represents the change in tially involves different processes and forms of carbon the total mass balance of the terrestrial biosphere, in-

(i.e., not just CO2). These processes are best repre- cluding plants, soils, herbivores, etc. NEP at this scale sented and studied at certain scales. For example, dis- represents a transfer of C to ocean, atmosphere, and turbances such as ®re kill individual plants and con- lithosphere reservoirs. By de®nition all transfers are sume individual detritus parts, but are best considered internal, except the net ¯ow to the atmosphere, oceans, in the NEP context at the level of landscapes or at the or lithosphere. At the global scale, a clear de®nition of stand scale over very long time periods relative to the the borders of the terrestrial system is dif®cult given disturbance return interval. This is in part because the the dynamic mixing processes and CO2 ¯uxes that oc- probability of a ®re occurring increases with the extent cur at coastal margins and in estuaries. of the temporal or spatial scale. At ®ner scales ®res are irregular and they appear to add an unreasonable The minimal scale for NEP and often misleading variance in NEP. We suggest that Use of a multiscale de®nition of NEP raises the issue this feature of NEP could be addressed by explicitly of whether there is a minimal scale that emerges from de®ning the level that NEP is being reported by use of NEP as a property. We suggest that this minimum scale subscripts. This would then clarify the processes that is the same as the minimum scale for the de®nition of are usually included and excluded from the analysis. an ecosystem (Odum 1959). While most ecosystems Any scaling of NEP from one level to another would include some combination of heterotrophs and auto- then involve the addition of the processes that are most trophs, the temporary or permanent absence of light- appropriately studied at that scale. For example, NEP at harvesting (photosynthetic) organisms clearly does not the level of individual stands (NEPstand, with length scales preclude application of the ecosystem concept neither roughly from1mto1km)would require study of ¯uxes should it preclude characterization of the ecosystem associated with GPP (FGPP), ecosystem respiration (FRe), carbon balance with NEP. hydrocarbons (Fhydrocarbons), leaching (Fleaching), and erosion MEASUREMENTS OF NEP AND BIOSPHERE- (Ferosion), although over short time spans the latter three terms might be neglected for some purposes. Fluxes as- ATMOSPHERE CO2 EXCHANGE sociated with ®re (F®re), herbivory (Fherbivory), and har- On short timescales (typically less than a decade), it vest (Fharvest) may not be explicitly addressed at this is dif®cult to accurately measure changes in total eco- scale (unless a disturbance occurs during a sampling system carbon storage against large and heterogeneous interval). They would be seen at this scale as rare events stocks of C in soils and vegetation using Eq. 1. More that export C from the system. At larger scales, how- precision can be obtained by measuring ¯uxes across ever, some of these processes would be seen as internal the boundaries of the ecosystem via Eq. 2 (Fig. 2). Use transfers while others would emerge as substantial con- of Eq. 2 to estimate NEP requires that we identify and tributors to NEP (Fig. 1). measure the dominant components of the ¯ux. In prac-

Regional-scale estimates of NEP (NEPreg, with length tice, it also requires the conscious decision to neglect scales roughly from 1 km to 102 km) would include certain components, if they are believed to be small at ¯uxes from a mosaic of stands with different distur- the temporal or spatial scale of measurement. bance histories and intensities. At this level, NEP is At the time and space scale of eddy covariance ¯ux strongly regulated by direct CO2 losses from ®re and measurements, the dominant one-way components of other disturbances as well as ¯uxes associated with NEP are GPP and Re. This has led to the de®nition of

GPP and Re at various times following disturbance. It net ecosystem exchange (NEE) as the balance between would include CO2 emissions from crop burning, CO2 GPP and Re at half-hour to decadal time intervals (Wof- and organics that enter groundwater and are subse- sy et al. 1993). De®ned in this way, NEE is a partial quently emitted from lakes and streams, and CO2 emit- ¯ux out the top of a three-dimensional box enclosing ted from land®lls and feedlots that was derived from the ecosystem and is equivalent to NEP (Eq. 1 and 2) NPP transported laterally from other ecosystems. only at sites where other lateral and vertical C ¯uxes

For the case of biome-level NEP (NEPbiome, with are demonstrably small. NEP at eddy ¯ux tower sites length scales roughly from 102 km to 104 km), ®res, in managed forests also includes any lateral removal deforestation, erosion, and river DOC are signi®cant of coarse woody debris in the footprint area, in addition contributing processes, even on relatively short time to the ecosystem±atmosphere CO2 ¯ux. A tower in an scales (months to years). At this scale, the impact of eroding ®eld might record a net uptake of C, even any individual disturbance event may be small com- though NEP is at steady state, with ecosystem±atmo- pared with the ensemble of disturbance events that are sphere gains balanced by erosion losses (Harden et al. simultaneously occurring, and human- and climate-in- 1999). Moreover, the ecosystem boundaries should be 942 J. T. RANDERSON ET AL. Ecological Applications Vol. 12, No. 4

FIG. 2. The temporal and spatial domain of different techniques used to measure components of net ecosystem production

(NEP) in terrestrial ecosystems. Atmospheric-inversion methods have been applied to contemporary ¯ask CO2 measurements as well as ice-core records extending over the last 1000 years (Joos et al. 1999, Rayner et al. 1999). Eddy covariance ¯ux measurements from the Harvard Forest (Petersham, Massachusetts, USA) extend over one decade (Wofsy et al.1993). clearly de®ned in stand- and regional-scale ¯ux studies and large C losses associated with disturbance (Kas- by disturbance age, erosion setting, and other key var- ischke et al. 1995, Cohen et al. 1996). The C accu- iables that affect NEP as it is ``scaled up'' to regional mulation over any long time period depends on GPP or global estimates (e.g., Rapalee et al. 1998). (gross primary production) and the respiration of newly

For similar reasons, biosphere±atmosphere CO2 ¯ux- ®xed carbon, respiration and other loss pathways for es inferred from atmospheric model inversions of CO2 carbon that was ®xed prior to the last disturbance, and ¯ask or aircraft measurements (Rayner et al. 1999) are carbon losses associated with the disturbance event. also only partially representative of terrestrial NEP. At For example, NEP measurement following disturbance the global scale, river runoff contains DOC (dissolved includes variable proportions of recent and old soil C organic C) and DIC (dissolved inorganic C) of mixed (Trumbore and Harden 1997, Goulden et al. 1998). terrestrial and aquatic origin on the order of 0.2±0.9 Pg C/yr for DOC and 0.3 Pg C/yr for DIC (Schlesinger NEP AND NET BIOME PRODUCTION and Melack 1981, Degens 1982, Meybeck 1982, De- The new concept proposed by Schulze and gens et al. 1991, Suchet and Probst 1995). As previ- Heimann (1998) ously stated, if the terrestrial biosphere were at steady state, then this net hydrologic C transport would require To address the issue of disturbance (which was wide- a one-way atmosphere±biosphere ¯ux of the same mag- ly neglected in initial biosphere±atmosphere modeling nitude (Lugo and Brown 1986). Estimates of C accu- analyses and ®eld measurement programs), Schulze mulation within the terrestrial biosphere based on at- and Heimann (1998) proposed the concept of net biome mosphere-biosphere ¯uxes must account for these hy- production (NBP), de®ned as the regional net carbon drologic losses, and also assess the spatial domain and accumulation after considering C losses from ®re, har- timescale over which the land±ocean ¯ux returns to the vest, and other episodic disturbances. Speci®cally, the atmosphere in coastal margins and in the open ocean. NBP concept acknowledges that small but consistent

Atmospheric inversions of CO2 will also fail to properly rates of C accumulation over most of the land surface assign sources and sinks of total C when oxidation of (i.e., what occurs in most forests and grasslands) must

CH4, CO, and some VOCs occur in atmospheric regions be balanced by relatively infrequent, but large-mag- that are offset from their terrestrial sources. nitude releases associated with episodic disturbance On timescales greater than a decade, it is possible (e.g., Rapalee et al. 1998). The infrequent nature of to measure changes in total ecosystem C storage (Fig. these release events makes it dif®cult to design terres- 2). Chronosequences of stands of different ages show trial sampling programs that provide a true measure of decade-to-century scale increases in C stocks following the regional- or continental-scale C ¯ux (Schulze and clearing (Richter et al. 1999), glacial retreat (Crocker Heimann 1998). and Major 1955, Harden et al. 1992), ¯oodplain de- In the de®nition of NBP, Schulze and Heimann velopment (Yarie et al. 1998), ®re (Harden et al. 2000), (1998) distinguish between directional forcing (such as August 2002 NET ECOSYSTEM PRODUCTION 943

changing levels of atmospheric CO2 or temperature) In the case of harvest, ecosystems may experience se- and disturbance by episodic forcing (such as ®res and vere disturbance of the soil and canopy understory dur- harvest). According to Schulze and Heimann (1998), ing clearing (Black and Harden 1995) or harvest may directional forcing affects NEP (net ecosystem pro- be restricted to removal of berries or removal of dead duction) ¯uxes through changes in NPP and microbial wood for fuel (Hao and Liu 1994). Should the harvest and herbivore respiration. In contrast, episodic distur- ¯ux (associated with NBP according to Schulze and bance is said to only affect NBP because of the different Heimann [1998]) include the changes in soil respiration time scale and impact on ecosystem processes (fre- triggered by harvest removal or subsequent soil ero- quently decimating aboveground and belowground bio- sion? mass stocks) and the different measurement approach The implications of attempting to separate episodic required. NBP is considered as a downstream ¯ux at and directional forcing are severe. Previous estimates the landscape, regional, or continental scale, after of global NEP, based on the assumption that episodic stand-level ¯uxes of GPP, Ra, Rh, and NEP have been disturbances are associated only with the NBP ¯ux, are estimated. Here we question whether episodic distur- as high as 10 Pg C/yr into the land surface (Steffen et bances that are included in NBP can be partitioned al. 1998, Prentice et al. 2001). Yet, as shown in the conceptually or practically from processes that are in- examples above, it is unclear as to exactly what ¯uxes cluded in NEP. should be included when NEP is de®ned in this way. It is essential that we separate our theoretical paradigm Ambiguities introduced by the NBP concept of terrestrial C balance from our ability (or inability) The distinction between NEP and NBP has limita- to accurately measure the net ¯ux and its components. tions that compromise communication among biogeo- From a practical perspective, NEP and NBP are im- chemists, atmospheric scientists, and ecologists work- possible to measure separately (it is impossible to make ing at different scales. The limitations stem from three a pure measurement of NEP following the NBP±NEP sources: (1) The de®nition of NBP assumes episodic distinction presented in Schulze and Heimann [1998], disturbance and directional forcing can be distin- Buchmann and Schulze [1999], and Schulze et al. guished from one another, allowing an unambiguous [2000]). partitioning of ¯uxes between NEP and NBP. (2) The Disturbance is an integral and de®ning element of de®nition of NBP suggests that other terrestrial C ¯uxes all ecosystems. Therefore measurements of GPP, NPP,

(GPP, NPP, Re, and NEP; Table 1) can be estimated Ra, and Rh are impossible to consider outside the context (either measured or modeled) separately from episodic of both episodic disturbance and directional forcing. disturbance (and thus NBP). (3) The name and de®- For example, canopy photosynthetic capacity depends nition of NBP implies that episodic disturbance emerg- strongly on leaf nitrogen, which in turn, depends on es only as a regulator of C ¯uxes at continental or soil N availability and the cumulative history of dis- ``biome'' scales, as a downstream process from NEP. turbance events that have precipitated N loss (Field and We address these issues in the following paragraphs. Mooney 1986, Schulze et al. 1994). Likewise, ecosys- In many instances, episodic disturbances and direc- tem respiration ¯uxes critically depend on total eco- tional forcing cannot be easily separated, yet our frame- system carbon stocks and their distribution among live, work (and carbon accounting systems) must be rigorous labile, chemically recalcitrant, and physically protected enough to include this reality. For example, tempera- forms (Schimel et al. 1994). Again, past disturbance ture increases could be classi®ed as a directional forc- frequencies and intensities are critical regulators of the ing (and thus fall under NEP in the de®nition proposed distribution and amounts of C in these forms. The def- by Schulze and Heimann [1998]). Consider the case, inition of NBP does not emphasize the fundamental however, of a severe temperature or drought event that role of episodic disturbance in shaping ``upstream'' kills some of the vegetation. How much of this mor- ¯uxes (GPP, NPP, Ra, and Rh); the primary effect of tality must occur before the ¯ux is considered NBP disturbance is assumed to occur at very large spatial instead of NEP? If ®re is an annual occurrence, as in scales (Buchmann and Schulze 1999: Fig. 1). many grassland ecosystems, or consumes only a small Within every square meter of an ecosystem, the net fraction of the vegetation, as in many ground ®res, is C balance (and all of the one-way components) is in- this an episodic disturbance? Similar issues arise with ¯uenced by the cumulative history of multiple, pre- herbivory and wind damage. Low levels of insect her- vious disturbances. In the boreal forest, for example, bivory and wind damage are common in most ecosys- logs remain after ®re from trees that grew two or more tems, while outbreaks and hurricanes may be relatively ®re cycles previously and are still decomposing. Hard- infrequent. If an outbreak or windstorm does occur, at en et al. (2000) found that it was very dif®cult to dis- what level of severity does it constitute an episodic tinguish between heterotrophic respiration from the de- disturbance vs. a directional one? Low levels of her- composition of organic material exposed or killed dur- bivory are usually treated as a component of NPP, but ing the last major disturbance and microbial respiration if certain levels of herbivory are counted in NBP one of decomposing leaf and root litter derived from living needs to decide which form goes with which process. vegetation. 944 J. T. RANDERSON ET AL. Ecological Applications Vol. 12, No. 4

Reconciling NBP with NEP manuscript, it is critical to clearly de®ne the boundaries Because of the ambiguities created by distinguish- of the region considered for C balance and to evaluate ing between NBP and NEP, we suggest a conceptual the impacts of previous disturbances on current rates framework where NBP is equivalent to a compre- of C uptake or loss at all spatial and temporal scales. hensive de®nition of NEP (see De®ning NEP: A com- Without consideration of these two issues, the account- prehensive de®nition, above) at regional or global ing requirements de®ned in the Kyoto Protocol for the scales. Thus, NBP also represents the total mass bal- inclusion of terrestrial C ¯uxes in a broader C restric- ance of terrestrial C: tion cannot be met. NBP ϭ NEP ϭ dC/dt. (3) CONCLUSIONS Is the concept of ``net biome productivity'' then nec- 1) A robust de®nition of net ecosystem production essary? Given the conceptual framework described by (NEP) should be based on a full ecosystem mass bal- ecologists over the last few decades (Woodwell and ance and include non-CO and non-respiratory com- Whittaker 1968, Reichle et al. 1975, Lugo and Brown 2 1986, Aber and Melillo 1991), NBP does not represent ponents of the C ¯ux and clearly de®ned temporal and a quantity that is fundamentally different from NEP. spatial boundaries. De®ned in this way, NEP provides However, the NBP concept is extremely useful because an unambiguous measure of change in C storage that it highlights the role of rapid episodic ¯uxes in shaping is conceptually consistent across all spatial and tem- NEP at very large scales and the challenges of extrap- poral scales, from an individual plot to the entire ter- olating terrestrial C measurements made at individual restrial biosphere. In our view, de®nitions of NEP sole- sites (where these rapid episodic ¯uxes are not easily ly based on the difference between NPP and Rh or GPP measured). NBP also highlights the non±negligible and Re encourages a perspective in which other C trans- contribution of lateral (harvest) ¯uxes out of ecosys- fers are ignored at the local scale, and thus reconciling tems that may be very dif®cult to quantify at individual carbon mass balance with ocean and atmosphere res- sites. ervoirs becomes dif®cult at the global scale. While there is value in the NBP concept, we believe 2) Disturbance is an integral property of all ecosys- that it is impossible to attempt to partition ¯uxes from tems. It affects all one-way C ¯uxes including GPP, Ra , the terrestrial biosphere in terms of their origin as either and Rh, and hydrologic ¯uxes at all spatial and temporal arising solely from episodic disturbance or directional scales. It does not emerge as a regulator solely at re- forcing from climate or other processes, or to make a gional or biome scales. unique distinction between NEP and NBP. 3) Net biome production (NBP) as previously de- ®ned by Schulze and Heimann (1998) cannot be dis- NEP, NBP, AND CARBON MANAGEMENT tinguished from NEP in many instances because epi- The relevance of disturbance effects on carbon ex- sodic disturbance is frequently impossible to distin- change is also important to the development of C emis- guish from directional forcing and because most C ¯ux- sion restrictions in the Kyoto Protocol.7 Article 3.4 of es respond to disturbance over a wide range of temporal the protocol includes the possibility that ecosystem- scales. management activities focused on containing distur- 4) Equivalent mass-balance de®nitions of the two bances such as ®re and pest outbreaks could be con- terms ``NBP'' and ``NEP'' allows for a consistent treat- sidered for carbon uptake credits. At the scale of coun- ment of carbon in political frameworks for taxation, tries or continents, disturbance-associated C ¯uxes are and for ef®cient comparison of ¯uxes at various spatial very large. For example, the direct loss of C during and temporal scales and between models and ®eld ob- boreal forest ®res is predicted to reach as high as 0.8 servations. Pg C/yr over the next 30±100 yr (Kasischke et al. 1995). Reductions in the rates of these emissions could, ACKNOWLEDGMENTS in theory, qualify for C credits. The amount of C that We wish to thank C. Field and I. Fung for discussions on could be affected by such policy decisions is signi®- this topic and support from NSF-Long Term Studies to the cant. For example it has been suggested that a 5% Bonanza Creek and Andrews Forest LTERs. J. Randerson reduction in ®re-induced C losses in United States received support from a National Space and Science Admin- could yield a 0.5 Pg C/yr reduction in C emissions istration MDAR grant NAG5-9462 and a U.S. Department of Energy Alexander Hollaender Fellowship to Lawrence Berke- (Sohngen and Haynes 1997). ley National Laboratory and the University of California at The critical issues involving NEP (net ecosystem Berkeley. production) and NBP (not biome production) estimates from a policy perspective are based on the need to LITERATURE CITED document changes in C storage associated with man- Aber, J. D., and J. M. Melillo. 1991. Terrestrial ecosystems. agement activities. For the reasons discussed in this Saunders College Publications, Philadelphia, Pennsylvania, USA. 7 URL: ͗http://www.unfccc.de/resource/convkp.html͘ Barlaz, M. A. 1998. Carbon storage during biodegradation August 2002 NET ECOSYSTEM PRODUCTION 945

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