Maintaining high rates of carbon storage in old forests: A mechanism linking canopy structure to forest function
Graphical abstract
Highlights
► Observed high C storage rates in old forests remain unexplained. ► We examine links between canopy structural complexity (rugosity) and LUE & NUE. ► Canopy structural complexity (rugosity) increased across 166 years of succession. ► LUE & NUE increased with rugosity sustaining ANPP into late succession. ► We provide a mechanistic basis for high C storage rates in old forests.
Introduction
Forests are an integral component of the Earth’s carbon (C) cycle, storing at present 2.4 Pg C annually in biomass and soils (Pan et al., 2011). Considerable uncertainty exists, however, in the future trajectory and magnitude of the terrestrial C sink as globally many aggrading forests approach maturity following clear-cut harvesting a century or more ago (Birdsey et al., 2006). With these regrowing forests advancing beyond the early aggrading phase of succession, an ecologically important transition is underway in which structurally and biologically simple forests dominated by short-lived early successional trees senesce and give way to more complex stands comprised of longer-lived, later successional species (Caspersen and Pacala, 2001, Birdsey et al., 2006). Widespread forest regrowth is leading to a reemergence of later successional forests in many regions, especially the naturally-regenerated, mixed-deciduous forests of North America and Eurasia (Caspersen et al., 2000, Luyssaert et al., 2010, Wang et al., 2011).
Investigations of forest net primary production (NPP) over the course of ecological succession support a general trend of declining production with forest age, but with important knowledge gaps for late successional, mixed forests (Gower et al., 1996, Ryan et al., 1997, Smith and Long, 2001, Law et al., 2003, Parker et al., 2004a, Pregitzer and Euskirchen, 2004, Gough et al., 2008a). Quantitative syntheses consistently report lower NPP in old-growth rather than young, aggrading forests (Pregitzer and Euskirchen, 2004, DeLucia et al., 2007, Luyssaert et al., 2008). These syntheses provide critical assessments of changes in NPP over time; however, the inference of their findings may not extend to temperate deciduous forests for two important reasons. First, coniferous forests dominate global syntheses and thus drive trends in and conclusions regarding old growth NPP. Secondly, mixed deciduous forests included in these syntheses were less than a century old, highlighting the lack of NPP data from mature mixed deciduous-conifer forests. Single-site empirical studies of mixed deciduous forest NPP from early through late succession have not been conducted; however, decadal studies of NPP in mixed deciduous forests entering mid-succession indicate NPP may increase, contrary to expectations derived from studies of coniferous forests (Urbanski et al., 2007, Gough et al., 2008a, Gough et al., 2010). Moreover, recent modeling studies report considerably different NPP trajectories among forest types, with some temperate deciduous broadleaf forests showing no decline in NPP after 100 years (Wang et al., 2011).
Reported patterns of C storage rates from aging stands are not consistent, showing trends in different directions with different proposed mechanisms (Ryan et al., 1997, Pregitzer and Euskirchen, 2004, DeLucia et al., 2007, Luyssaert et al., 2008). The mechanisms controlling successional trajectories of NPP in mixed-deciduous forests likely depart from those well described for many coniferous-dominated forests. Declines in production by very tall old-growth coniferous forests of the western US (Ryan et al., 1997, Binkley et al., 2006) and in a >100-years-old loblolly pine (Pinus taeda) forest reaching maturity (Drake et al., 2011) can be partially attributed to height-related limitations in hydraulic conductivity, but in shorter and more structurally and biologically diverse forests, height-related growth limitations may prove less prominent. Instead, increasing canopy structural complexity, which has been linked to forest production in a narrow range of stand ages, may sustain high rates of production in some mixed deciduous old-growth forests (Luyssaert et al., 2008, Gough et al., 2010, Hardiman et al., 2011) by improving light and nitrogen use efficiency.
Canopy complexity, the vertical and horizontal heterogeneity of leaf area distribution within the canopy, can strongly influence light interception (Walcroft et al., 2005) and light use efficiency (Duursma and Makela, 2007) with significant consequences for NPP as forests age. Canopy structural complexity increases through forest development and succession due to disturbances that rearrange canopy leaf area; these changes are evident in the topography of the outer canopy surface in stands differing in age by more than a century (Ishii et al., 2004, Parker et al., 2004a, Chmura et al., 2007, Ishii and Asano, 2010). In contrast, leaf area index (LAI) tends to saturate early in stand development upon crown closure for many forest types and, barring severe disturbance, remains stable for long periods (Gough et al., 2007, Hardiman et al., 2011, He et al., 2012). Given the insensitivity of LAI to stand age, LAI is not a robust candidate to explain long-term trends in forest NPP, suggesting that leaf area arrangement may be more important than leaf area quantity in determining NPP. Structurally complex canopies have relatively greater canopy surface area exposed to incident radiation (Parker et al., 2004b, Walcroft et al., 2005, Duursma and Makela, 2007) and have lower albedo (Ogunjemiyo et al., 2005) indicating greater light interception. Within-canopy spatial partitioning by the complex assemblages of species and age cohorts often seen in late successional temperate forests can promote high canopy photosynthetic capacity in wide-ranging light conditions (Niinemets, 2007, Niinemets, 2010). Canopy light use efficiency (LUE, the ratio NPP to fAPAR, Haxeltine and Prentice, 1996) is determined by within-canopy spatial, temporal, and physiological differentiation of foliage and canopy structures in response to contrasting light levels (Chapin et al., 2002, Niinemets, 2007) and is known to vary with forest composition (Ahl et al., 2004). We therefore hypothesized that, barring limitation by other resources, increased light availability to foliage in the interior of the canopy resulting from reorganization of canopy structure will increase C assimilation rates. We also hypothesized that nitrogen use efficiency (NUE, the ratio of NPP to canopy N, Finzi et al., 2007) should increase with canopy structural complexity since as more light infiltrates deep into the canopy, low-lying foliage can maximize photosynthetic output relative to foliar N concentrations (Rocha et al., 2004). These hypotheses form the basis for a novel physiological explanation for previously observed linkages between canopy structural complexity and carbon storage rates and may explain sustained high C storage observed in some mid-late successional temperate forests.
To understand changes in canopy structural complexity and NPP, we studied passively managed forest plots in Northern Lower Michigan varying in age over >160 years of development. We evaluated the effects of changing canopy structural complexity on light and nitrogen use efficiencies, and thus on forest C storage potential. To do so, we combined ground-based near-surface remote sensing of canopy structure with biometric C storage accounting methods and chemical analysis of foliage.
Section snippets
Study area and plots
We conducted this study from 2005 through 2011 at the University of Michigan Biological Station (UMBS) located in northern Lower Michigan (45°35.5′N, 84°43′W). This site in the Upper Great Lakes region is located in the transition zone between Northern mixed deciduous and boreal forests. Forests throughout this region were subject to clear-cutting and slash-fueled wildfires in the early 1900s (Frelich and Reich, 1995, USDA, 2001), with few, mostly small remnants of uncut or selectively cut
ANPP, LAI, and canopy structure
Components of aboveground stand production (ANPPW and ANPPL) were both normal, unimodal distributions, though ANPPW was slightly positively skewed and ANPPL was slightly negatively skewed. Mean leaf to wood production ratio (LWR) was 1.04 for all plots (Table 1). We observed lowest LWR values in late successional plots (between 0.3 and 0.5; Fig. 1). In the five plots established via experimental cutting and burning we observed the highest LWR values (0.7–2.4) and these stands formed a smooth
Canopy structure and function
The relationships between LUE, NUE, and rugosity reported here provide evidence for a functional linkage between canopy structure and ecosystem carbon storage functioning. Canopies of older forests were more structurally complex, with higher rates of ANPP per unit light absorbed by the canopy and per unit foliar N than stands with structurally simple canopies. While we characterized LUE and NUE in a subset of our study plots, these plots spanned the range of variation in both ANPP and rugosity
Acknowledgements
We thank Christoph Vogel, Michael Grant, Kyle Maurer, Bryce Bredell, Amalia Spankowski, and Nate Lada for assistance with analysis, data collection, and fieldwork. We thank two anonymous reviewers for comments which greatly improved this manuscript. The UMBS flux site was established with support by the U.S. Department of Energy’s Office of Science (DoE BER) Grant # DE-SC0006708 and # DE-FC03-90ER610100. The site is supported by the DoE under Awards No. DE-FC02-06ER64158 & DE-SC0007041 and by
References (69)
- et al.
Heterogeneity of light use efficiency in a northern Wisconsin forest: implications for modeling net primary production with remote sensing
Remote Sens. Environ.
(2004) - et al.
Crown structure and biomass allocation patterns modulate aboveground productivity in young loblolly pine and slash pine
For. Ecol. Manage.
(2007) - et al.
Forest management for mitigation and adaptation to climate change: insights from long-term silviculture experiments
For. Ecol. Manage.
(2011) - et al.
Influence of foliar density profile on canopy flow: a large-eddy simulation study
Agric. For. Meteorol.
(2008) - et al.
Multi-year convergence of biometric and meteorological estimates of forest carbon storage
Agric. For. Meteorol.
(2008) - et al.
Wood net primary production resilience in an unmanaged forest transitioning from early to middle succession
For. Ecol. Manage.
(2010) - et al.
Measurements of branch area and adjusting leaf area index indirect measurements
Agric. For. Meteorol.
(1998) - et al.
Surface lidar remote sensing of basal area and biomass in deciduous forests of eastern Maryland, USA
Remote Sens. Environ.
(1999) - et al.
Age-related decline in forest productivity: pattern and process
- et al.
Age-related decline in forest growth: an emergent property
For. Ecol. Manage.
(2001)
Radiative transfer and carbon assimilation in relation to canopy architecture, foliage area distribution and clumping in a mature temperate rainforest canopy in New Zealand
Agric. For. Meteorol.
Relationships between net primary productivity and stand age for several forest types and their influence on China’s carbon balance
J. Environ. Manage.
Tree-girdling to separate root and heterotrophic respiration in two Eucalyptus stands in Brazil
Oecologia
Forest carbon management in the United States: 1600–2100
J. Environ. Qual.
Exploring the effects of microscale structural heterogeneity of forest canopies using large-eddy simulations
Bound.-Lay. Meteorol.
Pattern and Process in a Forested Ecosystem: Disturbance, Development, and the Steady State Based on the Hubbard Brook Ecosystem Study
Different responses to gaps among shade-tolerant tree species
Ecology
Active and passive forest management for multiple values
Northwest. Nat.
Successional diversity and forest ecosystem function
Ecol. Res.
Contributions of land-use history to carbon accumulation in US forests
Science
Principles of Terrestrial Ecosystem Ecology
Rank transformations as a bridge between parametric and nonparametric statistics
Am. Stat.
Resource Strategies of Wild Plants
Respiratory carbon losses and the carbon-use efficiency of a northern hardwood forest, 1999–2003
New Phytol.
Forest carbon use efficiency: is respiration a constant fraction of gross primary production?
Global Change Biol.
Root biomass of regenerating aspen (Populus tremuloides) stands of different densities in Alberta
Can. J. For. Res.
Characterizing the performance of ecosystem models across time scales: a spectral analysis of the North American carbon program site-level synthesis
J. Geophys. Res.-Biogeosci.
Mechanisms of age-related changes in forest production: the influence of physiological and successional changes
Global Change Biol.
Forest canopy properties and variation in aboveground net primary production over upper great lakes landscapes
Ecosystems
Summary models for light interception and light-use efficiency of non-homogeneous canopies
Tree Physiol.
Increases in nitrogen uptake rather than nitrogen-use efficiency support higher rates of temperate forest productivity under elevated CO2
Proc. Natl. Acad. Sci. USA
Spatial patterns and succession in a Minnesota Southern-Boreal Forest
Ecol. Monogr.
Estimating plot-level tree structure in a deciduous forest by combining allometric equations, spatial wavelet analysis and airborne LiDAR
Remote Sens. Lett.
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These authors contributed equally to this work.