Background
The authors say that in an ecosystem where plant growth is limited by nitrogen (N) availability, "an increase in N has the potential to enhance photosynthetic rates and carbon (C) storage in trees," as has been reported by Melillo et al. (2002, 2011); and they state that "this can happen through increases in N deposition in precipitation (Melillo and Gosz, 1983; Thomas et al., 2009)," and that "increased N availability to plants can also occur in response to soil warming (Melillo et al., 1995, 2002, 2011) as N is moved from the soil where the C:N mass ratio in woody tissue is often less than 30:1, to the plants where the C:N mass ratio in woody tissue is 200-300:1 (Melillo et al., 2002, 2011)."

What was done
Butler et al. conducted a soil warming study within the Harvard Forest in central Massachusetts (USA), where they increased soil temperature 5°C above ambient using buried resistance cables as described by Melillo et al. (2002, 2011), and where for a period of seven years they measured various biogeochemical and plant responses in 900-m² heated and control areas, in order to see "how a temperate forest ecosystem is affected by warming-induced changes in the N cycle."

What was learned
The thirteen U.S. scientists state that "since the start of the experiment, we have documented a 45% average annual increase in net nitrogen mineralization." And they say that they have seen "no evidence of increases in gaseous or solution N losses from the heated area relative to the control," which means, as they describe it, that "the system has maintained a closed N cycle in spite of warming."

So where did the extra plant-available nitrogen go? Quoting the researchers, "the warming-induced increase of available nitrogen resulted in increases in the foliar nitrogen content and the relative growth rate of trees in the warmed area." And with respect to the generality of these findings, Butler et al. indicate that "the increase in N mineralization in response to warming that we documented in this study has also been observed in other studies; some in forests (Peterjohn et al., 1994; Hartley et al., 1999; Rustad et al., 2001; Melillo et al., 2002), some in grasslands (Shaw and Harte, 2001) and some in tundra (Chapin et al., 1995)."

What it means
With respect to the increases in leaf N concentration of the trees growing within the heated area of the Harvard Forest, the U.S. research team additionally writes that "leaf N is positively correlated to photosynthetic rate and carbon storage in many plants growing across the globe (Field and Mooney, 1986; Reich et al., 1994, 1995, 1997; Ollinger et al., 2008)," and they say that this relationship suggests that "the increases in leaf N we see with warming likely correspond to increases in C assimilation in the heated area." And they go on to say that "coupled with increases in leaf N, warming leads to general increases in the relative growth rate of trees, particularly for red maple," adding that "recent studies have shown that red maple saplings increase in relative growth rate with increasing N availability," citing Finzi and Canham (2000) and Zaccherio and Finzi (2007).

What is of most interest of all, however, is Butler et al.'s statement that "interactions between increasing temperatures and other factors predicted to change in the future, such as CO2 concentrations, could reinforce the ecosystem responses to warming alone," as they note that "Bazazz and Miao (1993) found that, when N was added to seedlings in growth chambers at Harvard Forest with elevated CO2 (700 ppm), the biomass of red maple and red oak increased significantly relative to controls."

In light of this additional fact, the U.S. research team concludes that "as CO2 concentrations increase and warming stimulates increases in N availability, it is possible that we may see further increases in growth rates of these species." And, as they continue, that is likely why "results from Duke University's Free-Air Carbon Dioxide Enrichment (FACE) experiment in North Carolina show red maples also benefiting from CO2 enrichment (Mohan et al., 2007)," while growing in a forest soil described by Finzi and Schlesinger (2003) as being in "a state of acute nutrient deficiency that can only be reversed with fertilization."

Apparently, however, nature herself - via warming - can provide the needed nitrogen for CO2-enhanced tree growth even in extremely nutrient-deficient soil.

Bye, bye, progressive nitrogen limitation hypothesis!!!

References
Chapin, S.F., Shaver, G.R., Giblin, A.E., Nadelhoffer, K.J. and Laundre, J.A. 1995. Responses of arctic tundra to experimental and observed changes in climate. Ecology 76: 694-711.

Field, C. and Mooney, H.A. 1986. The photosynthesis-nitrogen relationship in wild plants. In: Givnish, T.J. (Ed.). On the Economy of Plant Form and Function. Cambridge University Press, Cambridge, United Kingdom, pp. 25-55.

Finzi, A.C. and Canham, C.D. 2000. Sapling growth in response to light and nitrogen availability in a southern New England forest. Forest Ecology and Management 131: 153-165.

Finzi, A.C. and Schlesinger, W.H. 2003. Soil-nitrogen cycling in a pine forest exposed to 5 years of elevated carbon dioxide. Ecosystems 6: 444-456.

Hartley, A.E., Neill, C., Melillo, J.M., Crabtree, R. and Bowles, F.P. 1999. Plant performance and soil nitrogen mineralization in response to simulated climate change in subarctic dwarf shrub heath. Oikos 86: 331-343.

Melillo, J.M., Butler, S., Johnson, J., Mohan, J., Steudler, P., Lux, H., Burrows, E., Bowles, F., Smith, R., Scott, L., Vario, C., Hill, T., Burton, A., Zhou, Y.-M. and Tang, J. 2011. Soil warming, carbon-nitrogen interactions, and forest carbon budgets. Proceedings of the National Academy of Sciences USA 108: 9508-9512.

Melillo, J.B. and Gosz, J.R. 1983. Interactions of biogeochemical cycles in forest ecosystems. In: Bolin, B. and Cook, R.B. (Eds.). The Major Biogeochemical Cycles and Their Interactions. Wiley, New York, New York, United States, pp. 177-222.

Melillo, J.M., Kicklighter, D.W., McGuire, A.D., Peterjohn, W.T. and Newkirk, K. 1995. Global change and its effects on soil organic carbon stocks. In: Zepp, R. and Sonntag, C. (Eds.). Report of the Dahlem Workshop on the Role of Nonliving Organic Metter in the Earth's Carbon Cycle. Wiley, Chichester, West Sussex, United Kingdom, pp. 175-189.

Melillo, J.M., Steudler, P.A., Aber, J.D., Newkirk, K., Lux, H., Bowles, F.P., Catricala, C., Magill, A., Ahrens, T. and Morrisseau, S. 2002. Soil warming and carbon-cycle feedbacks to the climate system. Science 298: 2173-2176.

Mohan, J.E., Clark, J.S. and Schlesinger, W.H. 2007. Long-term CO2 enrichment of a forest ecosystem: implications for forest regeneration and succession. Ecological Applications 17: 1198-1212.

Ollinger, S.V., Richardson, A.D., Martin, M.E., Hollinger, D.Y., Frolking, S.E., Reich, P.B., Plourde, L.C., Katul, G.G., Munger, J.W., Oren, R., Smith, M.-L., Paw, U.K.T., Bolstad, P.V., Cook, B.D., Day, M.C., Martin, T.A., Monson, R.K. and Schid, H.P. 2008. Canopy nitrogen, carbon assimilation, and albedo in temperate and boreal forests: functional relations and potential climate feedbacks. Proceedings of the National Academy of Sciences USA 105: 19,336-19.341.

Peterjohn, W.T., Melillo, J.M., Steudler, P.A., Newkirk, K.M., Bowles, F.P. and Aber, J.D. 1994. The response of trace gas fluxes and N availability to elevated soil temperatures. Ecological Applications 4: 617-625.

Reich, P.B., Kloeppel, B.D., Ellsworth, D.S. and Walters, M.B. 1995. Different photosynthesis-nitrogen relations in deciduous hardwood and evergreen coniferous tree species. Oecologia 104: 24-30.

Reich P.B., Walters, M.B. and Ellsworth, D.S. 1997. From tropics to tundra: global convergence in plant functioning. Proceedings of the National Academy of Sciences USA 94: 13,730-13,734.

Reich, P.B., Walters, M.B., Ellsworth, D.S. and Uhl, C. 1994. Photosynthesis-nitrogen relations in Amazonian tree species. Oecologia 97: 62-72.

Rustad, L., Campbell, J.L., Marion, G.M., Norby, R.J., Mitchell, M.J., Hartley, A.E., Cornelissen, J.H.C. and Gurevitch, C. 2001. A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126: 543-562.

Shaw, R.M. and Harte, J. 2001. Response of nitrogen cycling to simulated climate change: differential responses along a subalpine ecotone. Global Change Biology 7: 193-210.

Thomas, R.Q., Canham, C.D., Weathers, K.C. and Goodale, C.L. 2009. Increased tree carbon storage in response to nitrogen deposition in the US. Nature Geoscience 3: 13-17.

Zaccherio, M.T. and Finzi, A.C. 2007. Atmospheric deposition may affect northern hardwood forest composition by altering soil nutrient supply. Ecological Applications 17: 1929-1941.