Biodiversity

Abstract

Global climate change is expected to affect terrestrial ecosystems in a variety of ways. Some of the more well-studied effects include the biogeochemical feedbacks to the climate system that can either increase or decrease the atmospheric load of greenhouse gases such as carbon dioxide and nitrous oxide. Less well-studied are the effects of climate change on the linkages between soil and plant processes. Here, we report the effects of soil warming on these linkages observed in a large field manipulation of a deciduous forest in southern New England, USA, where soil was continuously warmed 5°C above ambient for 7 years. Over this period, we have observed significant changes to the nitrogen cycle that have the potential to affect tree species composition in the long term. Since the start of the experiment, we have documented a 45% average annual increase in net nitrogen mineralization and a three-fold increase in nitrification such that in years 5 through 7, 25% of the nitrogen mineralized is then nitrified. 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. Acer rubrum (red maple) trees have responded the most after 7 years of warming, with the greatest increases in both foliar nitrogen content and relative growth rates. Our study suggests that considering species-specific responses to increases in nitrogen availability and changes in nitrogen form is important in predicting future forest composition and feedbacks to the climate system.

Introduction

Climate change is predicted to play a significant role in altering the function and structure of forest ecosystems (Melillo et al. 1990). Many studies have addressed how changes in major processes such as photosynthesis and plant and microbial respiration are projected to affect ecosystem carbon (C) balance (e.g., Melillo et al. 1993, 2002, 2011; Ryan 1991; Ainsworth and Long 2005), water balance (Zavaleta et al. 2003), and cycling rates of key nutrients including nitrogen (N) and phosphorus (P) (Van Cleve et al. 1990; Peterjohn et al. 1994; Rustad et al. 2001; Melillo et al. 2002). A growing number of studies have examined how these functional changes within ecosystems can feedback to the climate system (Peterjohn et al. 1994; Shaver et al. 2000; Field et al. 2007; Melillo et al. 2011).

Direct and indirect feedbacks to the climate system as a result of warming are predicted to occur, with the direction (positive or negative) and magnitude being dependent on specific ecosystem conditions such as nutrient availability, moisture regime and species composition (Shaver et al. 2000; Field et al. 2007). In addition, ecosystem responses can vary over time, as organisms acclimate to changes in the environment or as community shifts in composition. For example, increased microbial activity, a characteristic response to warming, can further drive climate change by accelerating the decay of soil organic matter and thereby releasing carbon dioxide (CO₂), a greenhouse gas, to the atmosphere (Peterjohn et al. 1994; Rustad and Fernandez 1998; Shaver et al. 2000; Luo et al. 2001; Rustad et al. 2001; Melillo et al. 2002, 2011; Eliasson et al. 2005). This response to warming is reported to decrease over time as labile carbon is depleted or as the microbial communities adapt to warmer conditions (Melillo et al. 2002, 2011; Bradford et al. 2008). However, over the long term, it is unclear if warming will cause additional changes in ecosystems, further altering the magnitude or direction of the microbial community’s response to climate change. Varying and interacting responses of ecosystem processes to warming make it difficult to predict the overall scale and direction of long-term feedbacks to the climate system.

A number of climate change experiments in forests (e.g., Peterjohn et al. 1994; Rustad et al. 2001) have also shown that soil warming increases net N mineralization, the transformation of organically bound N to ammonium (NH₄⁺) and nitrification, the transformation of NH₄⁺ to nitrate (NO₃⁻). With increases in nitrification, ecosystems could experience gaseous and solution losses of N, potentially affecting water quality and creating a positive feedback to the climate system (Aber et al. 1989).

In an ecosystem where plant growth is limited by N availability, an increase in N has the potential to enhance photosynthetic rates and carbon storage in trees (Melillo et al. 2002, 2011). This can happen through increases N deposition in precipitation (Melillo and Gosz 1983; Thomas et al. 2009). 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 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). Warming responses that cause enhanced carbon storage in woody tissue produce negative feedbacks to the climate system, which consequently slow the rate of atmospheric CO₂ accumulations (Melillo et al. 2011).

Changes in N cycling in response to warming are also likely to have long-term consequences for plant community structure. Tree species vary in their abilities to acquire and retain N based on characteristics such as root morphology and physiology (Marschner and Dell 1994), fungal associations (Lambers et al. 2008), preferred form of N uptake (NO₃ vs. NH₄ vs. amino acids; Schimel and Bennett 2004; Finzi and Berthrong 2005) and N resorption efficiency (Killingbeck 1996; Kobe et al. 2005). As human-induced environmental changes continue to affect forest ecosystems, species-specific strategies and responses to changes in the N cycle may become increasingly important in determining plant–soil interactions, forest species composition and the associated long-term feedbacks to the climate system.

Models that project the redistribution of tree species in response to climate change have often used a “climate envelope” approach, with species tracking shifts in key climate parameters including temperature and moisture over space and time (e.g., VEMAP Members 1995; Iverson and Prasad 1998; Iverson et al. 2008; Mohan et al. 2009). Climate-driven changes in the nitrogen cycle have not routinely been considered in vegetation redistribution models. A recent review by Ostle et al. (2009) argues that this may be a serious omission and urges that this potential shortcoming be addressed in new modeling efforts.

Here, we report the results of a large soil warming study at the Harvard Forest in central Massachusetts, USA, designed to explore the complex links among climate change, ecosystem biogeochemistry and plant responses. In a mixed deciduous stand, we have increased soil temperature 5°C using buried resistance cables (Melillo et al. 2002, 2011). For 7 years, we measured biogeochemical and plant responses in 900-m² heated and control (unwarmed) areas to examine how a temperate forest ecosystem is affected by warming-induced changes in the N cycle. Our measurements have included in situ net N mineralization and nitrification, soil–water N concentrations, nitrous oxide (N₂O) emissions from the soil surface to the atmosphere, N concentration in green leaves and leaf litter, nitrate reductase activity in leaves of dominant species, and growth responses of the canopy trees. By examining how warming influences various fluxes and pools of N within the ecosystem, we document some short- and longer-term effects on ecosystem structure and function.

Materials and methods