Who is the new sheriff in town regulating boreal forest growth?

Climate change appears to be altering boreal forests. One recently observed symptom of these changes has been an apparent weakening of the positive relationship between high-latitude boreal tree growth and temperature at some sites (D'Arrigo et al 2008). This phenomenon is referred to as the 'divergence problem' or 'divergence effect' and is thought to reflect a non-linear relationship between temperature and tree growth, where recent warming has allowed other factors besides growing-season temperature to emerge as dominant regulators of annual growth rates. Figure 1 demonstrates this divergence phenomenon with records of tree-ring widths collected from 59 populations of white spruce in Alaska 1. Key tendencies among these populations include: (1) growth is most sensitive to temperature during relatively cold growing seasons (figure 1(a)), (2) populations at colder sites are more sensitive to temperature than those at warmer sites are (figure 1(a)), and (3) growth at warmer sites may respond negatively to increased temperature beyond some optimal growing-season temperature (figure 1(b)). Since temperature is rising rapidly at high latitudes, one interpretation of figures 1(a) and (b) is that warming has promoted increased growth at colder sites, but caused growth to plateau or slow at warmer sites. Corroborating this interpretation, satellite imagery and tree-ring data indicate increasing vegetation productivity near the forest-tundra boundary but declining productivity in warmer regions within forest interiors (e.g., Bunn and Goetz 2006, Beck and Goetz 2011, Beck et al 2011, Berner et al 2011). Will continued warming cause a northward migration of boreal forests, with mortality in the warmer, southern locations and expansion into the colder tundra? This question is difficult to answer because many factors besides temperature influence boreal forest dynamics. Widespread productivity declines within interior boreal forests appear to be related to warming-induced drought stress (Barber et al 2000). Notably, this response may be more complicated than simply a decline in soil moisture. Even when soil moisture is plentiful, warming can negatively impact plant growth and survival by causing increased respiratory consumption of stored carbohydrates (McDowell 2011) and decreased stomatal conductance due to hydraulic limitation (Flexas et al 2004). Some degree of acclimation may be occurring, as white spruce populations that experience moderate temperatures and precipitation have lower optimal growth temperatures than populations at warmer, drier sites do (figure 1(c)). Yet, populations at the warmest or driest sites show strong growth declines during warm periods, consistent with a decline in the viability of these populations in some regions (Goetz et al 2005, Beck and Goetz 2011, Beck et al 2011). Can interior boreal forests acclimate to the current era's rapid warming? Or will temperatures within interior boreal forests outpace or extend beyond the adaptive capabilities of boreal tree species? The answer remains a mystery, partly because important aspects of acclimation are still poorly understood, and partly because of other important processes such as wildfire and increases in CO2 concentration, nitrogen deposition, growing-season length, and tropospheric ozone concentration. Figure 1. Relationships between white spruce tree-ring widths and climate at 59 sites in Alaska. (a) Annual correlation between ring-width index and June–July average temperature during years when June--July temperature was colder (blue bars) and warmer (red bars) than average. Pairs of bars represent the coldest 20 sites (left), 19 sites with intermediate temperature (middle) and the warmest 20 sites (right). (b) Spline curves that represent the best-fit relationship between temperature (x-axis) and ring-width index variability (y-axis) at cold sites (blue line), intermediate sites (black line) and warm sites (orange line). (c) Same as (b) but for the wettest 20 sites (green line), 19 sites with intermediate annual precipitation (black line) and the driest 20 sites (brown line). Error bars in (a)–(c) are standard errors. Perhaps an even bigger mystery is what the future has in store at the cold ecotone where boreal forest gives way to arctic tundra. Just as for warmer sites, there tends to be a temperature threshold at cold and intermediate sites, above which further warming no longer positively influences growth rate (figures 1(a) and (b)). Rather than reverse sign once this threshold is surpassed, growth–temperature relationships at cold and intermediate sites tend to simply disappear or at least diminish. This is because metabolic rates are slow in the cold, but are optimal under moderately warmer conditions (Tjoelker et al 2009). As temperature increases into a range of variability that no longer limits metabolic rate, a host of other climatic and soil-related factors can limit or promote growth and seedling recruitment. At some cool treeline sites, rapidly rising temperatures may have already surpassed the level that supports optimal growth, as negative relationships have emerged between temperature and growth rate in most decades (McGuire et al 2010). In a recent contribution to this important body of research, Andreu-Hayles et al (2011) studied growth–temperature relations within a white spruce population growing at the northern treeline in Alaska. Consistent with observations elsewhere in boreal forests, Andreu-Hayles et al discovered that a positive and significant relationship between ring widths and June–July temperature during 1901–1950 disappeared during 1951–2000. Interestingly, ring widths and temperature both increased throughout the 20th century at this treeline site, in contrast to recent trends at many other sites in Alaska where warming is outpacing ring widths (e.g., D'Arrigo et al 2008). At the site studied by Andreu-Hayles et al, it seems recent warming has caused a release of white spruce growth from temperature limitation and there is now a new sheriff in town regulating annual growth rate. Who this new sheriff is, however, remains an open and important question. Another interesting result in the Andreu-Hayles et al study is that the relationship between temperature and density of tree-ring latewood (the dark band formed at the end of the growing season) was stable throughout the 20th century. This means that although temperature may no longer be the primary factor governing annual growth, it still has an important physiological impact at the end of the growing season. The stability of the latewood density–temperature relationship also offers a promising implication for dendroclimatic studies. While non-linear relationships between ring widths and temperature may make it difficult to use ring widths to infer information about historical temperature variability for some sites, Andreu-Hayles et al add to the evidence (e.g., Barber et al 2000, Davi et al 2003, D'Arrigo et al 2009) that latewood density may be particularly useful in reconstructing historical temperature at high latitudes. While the divergence problem and new contribution by Andreu-Hayles et al are interesting on their own, they are also important because they highlight the current limits to our understanding of the mechanisms driving boreal forest growth and survival. As Allen et al (2010) pointed out, understanding and predicting the consequences of climate changes on forests is emerging as a grand challenge for global change scientists. This is particularly true at high latitudes because boreal forests store ~32% of Earth's terrestrial forest carbon, more than twice that of temperate forests (Pan et al 2011). Will continued warming turn boreal forests into a sink or source of atmospheric CO2? And will boreal forest growth and distribution change enough to significantly impact the energy balance of high latitude landscapes and thereby influence large-scale atmospheric circulation? To answer these questions, it is critical to understand the factors influencing boreal forest growth under warmer conditions and how the relative contributions of these factors vary spatially. Our understanding of these factors can be improved through research campaigns that integrate field-measurements, remote sensing and ecological modeling (Goetz et al 2011). Field-studies that measure the physiological responses of trees to manipulations of environmental variables such as temperature, soil moisture, soil nutrients and insolation are critical for informing ecological models that predict forest responses to various scenarios of climate and environmental change. Remote sensing is critical in validating modeled projections of forest growth. At present, ecological models do poorly at characterizing observed trends in boreal-forest productivity in some regions (Beck et al 2011). It will be exciting in the coming years to see how field measurements, modeling and remote sensing can work together to resolve the mysteries of the divergence problem, how warming will influence the overall productivity and distribution of boreal forests, and how changes in boreal-forest characteristics may influence regional and global climates. References Allen C D et al 2010 A global overview of drought and head-induced tree mortality reveals emerging climate change risks for forests Forest Ecol. Manag. 259 660–84 Andreu-Hayles L, D'Arrigo R, Anchukaitis K J, Beck P S A, Frank D and Goetz S 2011 Varying boreal forest response to Arctic environmental change at the Firth River, Alaska Environ. Res. Lett. 6 045503 Barber V A, Juday G P and Finney B P 2000 Reduced growth of Alaskan white spruce in the twentieth century from temperature-induced drought stress Nature 405 668–73 Beck P S A and Goetz S J 2011 Satellite observations of high northern latitude vegetation productivity changes between 1982 and 2008: ecological variability and regional differences Environ. Res. Lett. 6 045501 Beck P S A, Juday G P, Alix C, Barber V A, Winslow S E, Sousa E E, Heiser P, Herriges J D and Goetz S J 2011 Changes in forest productivity across Alaska consistent with biome shift Ecol. Lett. 14 373–9 Berner L T, Beck P S A, Bunn A G, Lloyd A H and Goetz S J 2011 High-latitude tree growth and satellite vegetation indices: correlations and trends in Russia and Canada (1982–2008) J. Geophys. Res. 116 G01015 Bunn A G and Goetz S J 2006 Trends in satellite-observed circumpolar photosynthetic activity from 1982 to 2003: the influence of seasonality, cover type, and vegetation density Earth Interact. 10 1–19 D'Arrigo R, Jacoby G, Buckley B, Sakulich J, Frank D, Wilson R, Curtis A and Anchukaitis K 2009 Tree growth and inferred temperature variability at the North American Arctic treeline Glob. Planet. Change 65 71–82 D'Arrigo R, Wilson R, Liepert B, Cherubini P 2008 On the 'divergence problem' in northern forests: a review of the tree-ring evidence and possible causes Glob. Planet. Change 60 289–305 Davi N K, Jacoby G C and Wiles G C 2003 Boreal temperature variability inferred from maximum latewood density and tree-ring width data, Wrangell Mountain region, Alaska Quatern. Res. 60 252–62 Flexas J, Bota J, Loreto F, Cornic G and Sharkey T 2004 Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants Plant Biol. 6 269–79 Goetz S J, Bunn A G, Fiske G J and Houghton R 2005 Satellite-observed photosynthetic trends across boreal North America associated with climate and fire disturbance Proc. Natl Acad. Sci. USA 102 13521–5 Goetz S J, Kimball J S, Mack M C and Kasischke E S 2011 Scoping completed for an experiment to assess vulnerability of Arctic and boreal ecosystems EOS Trans. Am. Geophys. Union 92 150–1 McDowell N G 2011 Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality Plant Physiol. 155 1051–9 McGuire A D, Ruess R W, Lloyd A, Yarie J, Clein J S and Juday G P 2010 Vulnerability of white spruce tree growth in interior Alaska in response to climate variability: dendrochronological, demographic, and experimental perspectives Canadian J. Forest Res. 40 1197–209 Pan Y et al 2011 A large and persistent carbon sink in the world's forests Science 333 988–93 Tjoelker M G, Oleksyn J, Lorenc-Plucinska G and Reich P B 2009 Acclimation of respiratory temperature responses in northern and southern populations of Pinus banksiana New Phytologist 181 218–29 1 Tree-ring data: ftp.ncdc.noaa.gov/pub/data/paleo/treering. Climate data: snap.uaf.edu/downloads/alaska-climate-datasets.

Climate change appears to be altering boreal forests. One recently observed symptom of these changes has been an apparent weakening of the positive relationship between high-latitude boreal tree growth and temperature at some sites (D'Arrigo et al 2008). This phenomenon is referred to as the 'divergence problem' or 'divergence effect' and is thought to reflect a non-linear relationship between temperature and tree growth, where recent warming has allowed other factors besides growing-season temperature to emerge as dominant regulators of annual growth rates. Figure 1 demonstrates this divergence phenomenon with records of tree-ring widths collected from 59 populations of white spruce in Alaska 1 . Key tendencies among these populations include: (1) growth is most sensitive to temperature during relatively cold growing seasons (figure 1(a)), (2) populations at colder sites are more sensitive to temperature than those at warmer sites are (figure 1(a)), and (3) growth at warmer sites may respond negatively to increased temperature beyond some optimal growing-season temperature ( figure 1(b)). Since temperature is rising rapidly at high latitudes, one interpretation of figures 1(a) and (b) is that warming has promoted increased growth at colder sites, but caused growth to plateau or slow at warmer sites. Corroborating this interpretation, satellite imagery and tree-ring data indicate increasing vegetation productivity near the forest-tundra boundary but declining productivity in warmer regions within forest interiors (e.g., Bunn and Goetz 2006, Beck and Goetz 2011, Beck et al 2011, Berner et al 2011.
Will continued warming cause a northward migration of boreal forests, with mortality in the warmer, southern locations and expansion into the colder tundra? This question is difficult to answer because many factors besides temperature influence boreal forest dynamics.
Widespread productivity declines within interior boreal forests appear to be related to warming-induced drought stress (Barber et al 2000). Notably, this response may be more complicated than simply a decline in soil moisture. Even when soil moisture is plentiful, warming can negatively impact plant growth and survival by causing increased respiratory consumption of stored carbohydrates (McDowell 2011) and decreased stomatal conductance due to hydraulic limitation (Flexas et al 2004). Some degree of acclimation may be occurring, as white spruce populations that experience moderate temperatures and precipitation have lower optimal growth temperatures than populations at warmer, drier sites do ( figure 1(c)). Yet, populations at the warmest or driest sites show strong growth declines during warm periods, consistent with a decline in the viability of these populations in some regions (Goetz et al 2005, Beck and Goetz 2011, Beck et al 2011. Can interior boreal forests acclimate to the current era's rapid warming? Or will temperatures within interior boreal forests outpace or extend beyond the adaptive capabilities of boreal tree species? The answer remains a mystery, partly because important aspects of acclimation are still poorly understood, and partly because of other important processes such as wildfire and increases in CO 2 concentration, nitrogen deposition, growing-season length, and tropospheric ozone concentration. Perhaps an even bigger mystery is what the future has in store at the cold ecotone where boreal forest gives way to arctic tundra. Just as for warmer sites, there tends to be a temperature threshold at cold and intermediate sites, above which further warming no longer positively influences growth rate (figures 1(a) and (b)). Rather than reverse sign once this threshold is surpassed, growth-temperature relationships at cold and intermediate sites tend to simply disappear or at least diminish. This is because metabolic rates are slow in the cold, but are optimal under moderately warmer conditions (Tjoelker et al 2009). As temperature increases into a range of variability that no longer limits metabolic rate, a host of other climatic and soil-related factors can limit or promote growth and seedling recruitment. At some cool treeline sites, rapidly rising temperatures may have already surpassed the level that supports optimal growth, as negative relationships have emerged between temperature and growth rate in most decades (McGuire et al 2010).
In Another interesting result in the Andreu-Hayles et al study is that the relationship between temperature and density of tree-ring latewood (the dark band formed at the end of the growing season) was stable throughout the 20th century. This means that although temperature may no longer be the primary factor governing annual growth, it still has an important physiological impact at the end of the growing season. The stability of the latewood density-temperature relationship also offers a promising implication for dendroclimatic studies. While non-linear relationships between ring widths and temperature may make it difficult to use ring widths to infer information about historical temperature variability for some sites, Andreu-Hayles et al add to the evidence (e.g., Barber et al 2000, Davi et al 2003, D'Arrigo et al 2009) that latewood density may be particularly useful in reconstructing historical temperature at high latitudes.
While the divergence problem and new contribution by Andreu-Hayles et al are interesting on their own, they are also important because they highlight the current limits to our understanding of the mechanisms driving boreal forest growth and survival. As Allen et al (2010) pointed out, understanding and predicting the consequences of climate changes on forests is emerging as a grand challenge for global change scientists. This is particularly true at high latitudes because boreal forests store ∼32% of Earth's terrestrial forest carbon, more than twice that of temperate forests (Pan et al 2011). Will continued warming turn boreal forests into a sink or source of atmospheric CO 2 ? And will boreal forest growth and distribution change enough to significantly impact the energy balance of high latitude landscapes and thereby influence large-scale atmospheric circulation?
To answer these questions, it is critical to understand the factors influencing boreal forest growth under warmer conditions and how the relative contributions of these factors vary spatially. Our understanding of these factors can be improved through research campaigns that integrate field-measurements, remote sensing and ecological modeling (Goetz et al 2011). Field-studies that measure the physiological responses of trees to manipulations of environmental variables such as temperature, soil moisture, soil nutrients and insolation are critical for informing ecological models that predict forest responses to various scenarios of climate and environmental change. Remote sensing is critical in validating modeled projections of forest growth. At present, ecological models do poorly at characterizing observed trends in boreal-forest productivity in some regions (Beck et al 2011). It will be exciting in the coming years to see how field measurements, modeling and remote sensing can work together to resolve the mysteries of the divergence problem, how warming will influence the overall productivity and distribution of boreal forests, and how changes in boreal-forest characteristics may influence regional and global climates.