Christopher M. Gough

Controls on Annual Forest Carbon Storage: Lessons from the Past and Predictions for the Future

ABSTRACT The temperate forests of North America may play an important role in future carbon (C) sequestration strategies. New, multiyear, ecosystem-scale C cycling studies are providing a process-level understanding of the factors controlling annual forest C storage. Using a combination of ecological and meteorological methods, we quantified the response of annual C storage to historically widespread disturbances, forest succession, and climate variation in a common forest type of the upper Great Lakes region. At our study site in Michigan, repeated clear-cut harvesting and fire disturbance resulted in a lasting decrease in annual forest C storage. However, climate variation exerts a strong control on C storage as well, and future climate change may substantially reduce annual C storage by these forests. Annual C storage varies through ecological succession by rising to a maximum and then slowly declining in old-growth stands. Effective forest C sequestration requires the management of all C pools, including traditionally managed pools such as bole wood and also harvest residues and soils.

The role of canopy structural complexity in wood net primary production of a maturing northern deciduous forest.

The even-aged northern hardwood forests of the Upper Great Lakes Region are undergoing an ecological transition during which structural and biotic complexity is increasing. Early-successional aspen (Populus spp.) and birch (Betula papyrifera) are senescing at an accelerating rate and are being replaced by middle-successional species including northern red oak (Quercus rubra), red maple (Acer rubrum), and white pine (Pinus strobus). Canopy structural complexity may increase due to forest age, canopy disturbances, and changing species diversity. More structurally complex canopies may enhance carbon (C) sequestration in old forests. We hypothesize that these biotic and structural alterations will result in increased structural complexity of the maturing canopy with implications for forest C uptake. At the University of Michigan Biological Station (UMBS), we combined a decade of observations of net primary productivity (NPP), leaf area index (LAI), site index, canopy tree-species diversity, and stand age with canopy structure measurements made with portable canopy lidar (PCL) in 30 forested plots. We then evaluated the relative impact of stand characteristics on productivity through succession using data collected over a nine-year period. We found that effects of canopy structural complexity on wood NPP (NPPw) were similar in magnitude to the effects of total leaf area and site quality. Furthermore, our results suggest that the effect of stand age on NPPw is mediated primarily through its effect on canopy structural complexity. Stand-level diversity of canopy-tree species was not significantly related to either canopy structure or NPPw. We conclude that increasing canopy structural complexity provides a mechanism for the potential maintenance of productivity in aging forests.

Sustained carbon uptake and storage following moderate disturbance in a Great Lakes forest

Carbon (C) uptake rates in many forests are sustained, or decline only briefly, following disturbances that partially defoliate the canopy. The mechanisms supporting such functional resistance to moderate forest disturbance are largely unknown. We used a large-scale experiment, in which > 6700 Populus (aspen) and Betula (birch) trees were stem-girdled within a 39-ha area, to identify mechanisms sustaining C uptake through partial canopy defoliation. The Forest Accelerated Succession Experiment in northern Michigan, USA, employs a suite of C-cycling measurements within paired treatment and control meteorological flux tower footprints. We found that enhancement of canopy light-use efficiency and maintenance of light absorption maintained net ecosystem production (NEP) and aboveground wood net primary production (NPP) when leaf-area index (LAI) of the treatment forest temporarily declined by nearly half its maximum value. In the year following peak defoliation, redistribution of nitrogen (N) in the treatment forest from senescent early successional aspen and birch to non-girdled later successional species facilitated the recovery of total LAI to pre-disturbance levels. Sustained canopy physiological competency following disturbance coincided with a downward shift in maximum canopy height, indicating that compensatory photosynthetic C uptake by undisturbed, later successional subdominant and subcanopy vegetation supported C-uptake resistance to disturbance. These findings have implications for ecosystem management and modeling, demonstrating that forests may tolerate considerable leaf-area losses without diminishing rates of C uptake. We conclude that the resistance of C uptake to moderate disturbance depends not only on replacement of lost leaf area, but also on rapid compensatory photosynthetic C uptake during defoliation by emerging later successional species.

Joint control of terrestrial gross primary productivity by plant phenology and physiology

Significance Terrestrial gross primary productivity (GPP), the total photosynthetic CO2 fixation at ecosystem level, fuels all life on land. However, its spatiotemporal variability is poorly understood, because GPP is determined by many processes related to plant phenology and physiological activities. In this study, we find that plant phenological and physiological properties can be integrated in a robust index—the product of the length of CO2 uptake period and the seasonal maximal photosynthesis—to explain the GPP variability over space and time in response to climate extremes and during recovery after disturbance. Terrestrial gross primary productivity (GPP) varies greatly over time and space. A better understanding of this variability is necessary for more accurate predictions of the future climate–carbon cycle feedback. Recent studies have suggested that variability in GPP is driven by a broad range of biotic and abiotic factors operating mainly through changes in vegetation phenology and physiological processes. However, it is still unclear how plant phenology and physiology can be integrated to explain the spatiotemporal variability of terrestrial GPP. Based on analyses of eddy–covariance and satellite-derived data, we decomposed annual terrestrial GPP into the length of the CO2 uptake period (CUP) and the seasonal maximal capacity of CO2 uptake (GPPmax). The product of CUP and GPPmax explained >90% of the temporal GPP variability in most areas of North America during 2000–2010 and the spatial GPP variation among globally distributed eddy flux tower sites. It also explained GPP response to the European heatwave in 2003 (r2 = 0.90) and GPP recovery after a fire disturbance in South Dakota (r2 = 0.88). Additional analysis of the eddy–covariance flux data shows that the interbiome variation in annual GPP is better explained by that in GPPmax than CUP. These findings indicate that terrestrial GPP is jointly controlled by ecosystem-level plant phenology and photosynthetic capacity, and greater understanding of GPPmax and CUP responses to environmental and biological variations will, thus, improve predictions of GPP over time and space.

Evaluation of leaf-to-canopy upscaling methodologies against carbon flux data in North America

Despite the wide acceptance of the “big-leaf” upscaling strategy in evapotranspiration modeling (e.g., the Penman-Monteith model), its usefulness in simulating canopy photosynthesis may be limited by the underlying assumption of homogeneous response of carbon assimilation light-response kinetics through the canopy. While previous studies have shown that the separation of the canopy into sunlit and shaded parts (i.e., two-leaf model) is typically more effective than big-leaf models for upscaling photosynthesis from leaf to canopy, a systematic comparison between these two upscaling strategies among multiple ecosystems has not been presented. In this study, gross primary productivity was modeled using two-leaf and big-leaf upscaling approaches in the Boreal Ecosystem Productivity Simulator for shrublands, broadleaf, and conifer forest types. When given the same leaf-level photosynthetic parameters, the big-leaf approach significantly underestimated canopy-level GPP while the two-leaf approach more closely predicted both the magnitude and day-to-day variability in eddy covariance measurements. The underestimation by the big-leaf approach is mostly caused by its exclusion of the photosynthetic contributions of shaded leaves. Tests of the model sensitivity to a foliage clumping index revealed that the contribution of shaded leaves to the total simulated productivity can be as high as 70% for highly clumped stands and seldom decreases below ∼40% for less-clumped canopies. Our results indicate that accurate upscaling of photosynthesis across a broad array of ecosystems requires an accurate description of canopy structure in ecosystem models.

Species‐specific transpiration responses to intermediate disturbance in a northern hardwood forest

Intermediate disturbances shape forest structure and composition, which may in turn alter carbon, nitrogen, and water cycling. We used a large-scale experiment in a forest in northern lower Michigan where we prescribed an intermediate disturbance by stem girdling all canopy-dominant early successional trees to simulate an accelerated age-related senescence associated with natural succession. Using 3 years of eddy covariance and sap flux measurements in the disturbed area and an adjacent control plot, we analyzed disturbance-induced changes to plot level and species-specific transpiration and stomatal conductance. We found transpiration to be ~15% lower in disturbed plots than in unmanipulated control plots. However, species-specific responses to changes in microclimate varied. While red oak and white pine showed increases in stomatal conductance during postdisturbance (62.5 and 132.2%, respectively), red maple reduced stomatal conductance by 36.8%. We used the hysteresis between sap flux and vapor pressure deficit to quantify diurnal hydraulic stress incurred by each species in both plots. Red oak, a ring porous anisohydric species, demonstrated the largest mean relative hysteresis, while red maple, bigtooth aspen, and paper birch, all diffuse porous species, had the lowest relative hysteresis. We employed the Penman-Monteith model for LE to demonstrate that these species-specific responses to disturbance are not well captured using current modeling strategies and that accounting for changes to leaf area index and plot microclimate are insufficient to fully describe the effects of disturbance on transpiration.

Net primary production of a temperate deciduous forest exhibits a threshold response to increasing disturbance severity

The global carbon (C) balance is vulnerable to disturbances that alter terrestrial C storage. Disturbances to forests occur along a continuum of severity, from low-intensity disturbance causing the mortality or defoliation of only a subset of trees to severe stand- replacing disturbance that kills all trees; yet considerable uncertainty remains in how forest production changes across gradients of disturbance intensity. We used a gradient of tree mortality in an upper Great Lakes forest ecosystem to: (1) quantify how aboveground wood net primary production (ANPP,) responds to a range of disturbance severities; and (2) identify mechanisms supporting ANPPw resistance or resilience following moderate disturbance. We found that ANPPw declined nonlinearly with rising disturbance severity, remaining stable until >60% of the total tree basal area senesced. As upper canopy openness increased from disturbance, greater light availability to the subcanopy enhanced the leaf-level photosynthesis and growth of this formerly light-limited canopy stratum, compensating for upper canopy production losses and a reduction in total leaf area index (LAI). As a result, whole-ecosystem production efficiency (ANPPw/LAI) increased with rising disturbance severity, except in plots beyond the disturbance threshold. These findings provide a mechanistic explanation for a nonlinear relationship between ANPPw, and disturbance severity, in which the physiological and growth enhancement of undisturbed vegetation is proportional to the level of disturbance until a threshold is exceeded. Our results have important ecological and management implications, demonstrating that in some ecosystems moderate levels of disturbance minimally alter forest production.

Can EVI-derived land-surface phenology be used as a surrogate for phenology of canopy photosynthesis?

Canopy phenology plays a prominent role in determining the timing and magnitude of carbon uptake by many ecosystems. The Moderate Resolution Imaging Spectroradiometer (MODIS) Global Land Cover Dynamics product developed from the enhanced vegetation index (EVI) provides broad spatial and temporal coverage of land-surface phenology (LSP), and may serve as a useful proxy for the phenology of canopy photosynthesis. Here, we compare the MODIS growing season start and end dates (SOS and EOS) with the seasonal phenology of canopy photosynthesis estimated using the eddy covariance approach. Using 153 site-years obtained from the Ameriflux database, we calculated the SOS and EOS of gross primary production (GPP) and canopy photosynthesis capacity (CPC) for seven different boreal and temperate vegetation types. CPC is GPP at maximum radiation, estimated by fitting half-hourly GPP and radiation to a rectangular hyperbolic function. We found large mean absolute differences of up to 53 days, depending on vegetation type, between the phenology of canopy development and photosynthesis, indicating that remotely sensed LSP is not a robust surrogate of seasonal changes in GPP, particularly for evergreen needleleaf forests. This limited correspondence of ecosystem carbon uptake with the MODIS LSP product points to the need for improved remotely sensed proxies of GPP phenology.

Lawn soil carbon storage in abandoned residential properties: an examination of ecosystem structure and function following partial human-natural decoupling.

Residential abandonment is on the rise in many urban areas, with unknown implications for ecosystem structure and function on land slated for partial or full restoration to native habitat. Partial decoupling of human and natural systems could reduce disturbance (e.g., trampling, recreational traffic) and modify vegetation structure in a way that alters soil carbon storage, an ecosystem function that many municipalities consider a management objective of growing importance. We quantified soil carbon percent and mass to 10 cm depth and examined vegetation structure in 50 vacant and 10 occupied residential lawns located in Richmond, VA, with the principal objective of determining whether occupancy status alters trajectories of soil carbon storage or its correspondence with household economic/demographic indicators and vegetation cover. Abandoned residential lawns supported significantly less grass cover, but these declines were largely offset by increases in emergent overstory (>1 m height) vegetation cover. Soil carbon percent and mass did not differ between lawns of occupied and abandoned residences, even though significant, but highly uncertain, increases in soil carbon mass occurred in the first decade following vacancy. Instead, all residential lawns exhibited similar significant increases in soil carbon percent and mass with increasing residence age and neighborhood affluence, the former indicating annual carbon accretion rates of 20 g m(-2). We conclude that in this early stage of vacancy, soil carbon storage is already subtly responding to declines in human intervention, with reduced soil disturbance and sustained vegetation cover in abandoned lawns playing likely roles in emerging soil carbon storage trajectories.

Multivariate Conditional Granger Causality Analysis for Lagged Response of Soil Respiration in a Temperate Forest

Ecological multivariate systems offer a suitable data set on which to apply recent advances in information theory and causality detection. These systems are driven by the interplay of various environmental factors: meteorological and hydrological forcing, which are often correlated with each other at different time lags; and biological factors, primary producers and decomposers with both autonomous and coupled dynamics. Here, using conditional spectral Granger causality, we quantify directional causalities in a complex atmosphere-plant-soil system involving the carbon cycle. Granger causality is a statistical approach, originating in econometrics, used to identify the presence of linear causal interactions between time series of data, based on prediction theory. We first test to see if there was a significant difference in the causal structure among two treatments where carbon allocation to roots was interrupted by girdling. We then expanded the analysis, introducing radiation and soil moisture. The results showed a complex pattern of multilevel interactions, with some of these interactions depending upon the number of variables in the system. However, no significant differences emerged in the causal structure of above and below ground carbon cycle among the two treatments.