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Nitrogen Oligotrophication in Northern Hardwood Forests Biogeochemistry (2018) 141:523–539 https://doi.org/10.1007/s10533-018-0445-y (0123456789().,-volV)(0123456789().,-volV) Nitrogen oligotrophication in northern hardwood forests Peter M. Groffman . Charles T. Driscoll . Jorge Dura´n . John L. Campbell . Lynn M. Christenson . Timothy J. Fahey . Melany C. Fisk . Colin Fuss . Gene E. Likens . Gary Lovett . Lindsey Rustad . Pamela H. Templer Received: 30 October 2017 / Accepted: 17 April 2018 / Published online: 12 May 2018 Ó Springer International Publishing AG, part of Springer Nature 2018 Abstract While much research over the past research at the Hubbard Brook Experimental Forest 30 years has focused on the deleterious effects of in New Hampshire, USA suggesting that N olig- excess N on forests and associated aquatic ecosystems, otrophication in forest soils is driven by increased recent declines in atmospheric N deposition and carbon flow from the atmosphere through soils that unexplained declines in N export from these ecosys- stimulates microbial immobilization of N and tems have raised new concerns about N oligotrophi- decreases available N for plants. Decreased available cation, limitations of forest productivity, and the N in soils can result in increased N resorption by trees, capacity for forests to respond dynamically to distur- which reduces litterfall N input to soils, further bance and environmental change. Here we show limiting available N supply and leading to further multiple data streams from long-term ecological declines in soil N availability. Moreover, N olig- otrophication has been likely exacerbated by changes in climate that increase the length of the growing Responsible Editor: Sujay Kaushal. P. M. Groffman (&) T. J. Fahey Advanced Science Research Center at the Graduate Department of Natural Resources, Cornell University, Center, City University of New York, New York, Ithaca, NY 14853, USA NY 10031, USA e-mail: [email protected] M. C. Fisk Department of Zoology, Miami University, Oxford, C. T. Driscoll OH 45056, USA Department of Civil and Environmental Engineering, Syracuse University, Syracuse, NY 13244, USA P. M. Groffman Á C. Fuss Á G. E. Likens Á G. Lovett Cary Institute of Ecosystem Studies, Millbrook, J. Dura´n NY 12545, USA Department of Life Sciences, Centre for Functional Ecology, University of Coimbra, Calc¸ada Martim de P. H. Templer Freitas, 3000-456 Coimbra, Portugal Department of Biology, Boston University, Boston, MA 02215, USA J. L. Campbell Á L. Rustad USDA Forest Service Northern Research Station, Durham, NH 03824, USA L. M. Christenson Vassar College, Poughkeepsie, NY 12604, USA 123 524 Biogeochemistry (2018) 141:523–539 season and decrease production of available N by we cannot define specific nutrient concentrations mineralization during both winter and spring. These associated with various trophic conditions (e.g., olig- results suggest a need to re-evaluate the nature and otrophic, mesotrophic, eutrophic) for terrestrial extent of N cycling in temperate forests and assess ecosystems, we can examine quantitative changes in how changing conditions will influence forest ecosys- multiple measures of N flux and availability that serve tem response to multiple, dynamic stresses of global as symptoms or indices of oligotrophication. Similar environmental change. analyses have long been done to evaluate N richness in different ecosystem types (Pastor et al. 1984; Vitousek Keywords Climate change Á Carbon Á Dissolved et al. 1979) or in response to changes in atmospheric organic carbon Á Hubbard Brook Experimental Forest Á CO2 manipulations (Zak et al. 2003). We hope that this Nitrogen examination begins a discussion of specific classifi- cations of trophic state for terrestrial systems as these have been very useful in aquatic systems and terres- trial ecosystems around the world are in a dynamic Introduction state of increasing or decreasing N richness (Battye et al. 2017). In most temperate forest ecosystems, N is a limiting The great challenge posed by the emergence of N nutrient that constrains net primary production oligotrophication is understanding how ecosystems (LeBauer and Treseder 2008; Vitousek and Howarth are responding to decreases in anthropogenic reactive 1991). However, in excess, N can contribute to N deposition and the availability of key nutrients such environmental problems, such as acidification, as N, while simultaneously experiencing changes in eutrophication, and loss of biodiversity (Davidson atmospheric chemistry (e.g., sulfur deposition, ele- et al. 2012). In recent decades, much research has vated concentrations of carbon dioxide (CO2), ozone), focused on anthropogenic activities that increase climate, and community composition (pests, patho- inputs of ‘‘reactive’’ N to forests through increases in gens, invasive species) (Groffman et al. 2013; Holmes emissions and atmospheric deposition (Galloway et al. and Likens 2016; Keenan et al. 2014; Loehle et al. 2008) and the ability of these inputs to accelerate 2016; Niu et al. 2016; Rosi-Marshall et al. 2016;Xu forests toward a condition of N saturation, with et al. 2016). For example, recent findings suggest that adverse consequences on soils, plant growth, and environmental ‘‘deacidification’’ is catalyzing marked aquatic ecosystems (Aber et al. 1989, 2003; Stoddard increases in decomposition of forest soil organic 1994). However, atmospheric N deposition is now horizons (forest floor) and the flow of C to soil declining over large areas of North America (Eshle- microbial populations responsible for production and man et al. 2013; Lloret and Valiela 2016) and there consumption of reactive N (Johnson et al. 2014; have been remarkable declines in N export from non- Oulehle et al. 2011, 2017). Further challenges come aggrading northern hardwood forests that cannot be from the manipulative nature of most research focused explained by declines in atmospheric deposition alone on understanding the effects of global changes on (Bernal et al. 2012; Bernhardt et al. 2005; Driscoll forest nutrient cycling. For example, while studies in et al. 2016; Fuss et al. 2015; Goodale et al. 2003; diverse ecosystems have demonstrated that changing Likens 2013; Martin et al. 2000; McLauchlan et al. climate can substantially alter C and N cycles and 2007; Rosi-Marshall et al. 2016; Yanai et al. 2013). budgets (Hofmockel et al. 2011; Luo et al. 2011; Now, concerns about N saturation and over supply are Melillo et al. 2011; Pendall et al. 2008; Phillips et al. being replaced with concerns about N oligotrophica- 2011), most of this research has emerged from tion causing N limitation of forest productivity and manipulation experiments (i.e., Free-Air Carbon diox- diminished capacity of ecosystems to dynamically ide Enrichment; FACE). Effects of elevated atmo- respond to disturbance and environmental change spheric CO2 on unmanipulated forests have been (Dura´n et al. 2016; Elmore et al. 2016). difficult to detect (Aber and Driscoll 1997) due to the We refer to the changing state of N limitation in challenge of evaluating effects of relatively small temperate forests as ‘‘oligotrophication,’’ borrowing a (albeit sustained) flows of C from the atmosphere term from aquatic sciences (Hutchinson 1973). While 123 Biogeochemistry (2018) 141:523–539 525 through trees to soil, and the complex interactions increases in intense rainfall events (Morse et al. between C and N in the soil (Zak et al. 2011). 2014, 2015a, b; Wexler et al. 2014). Finally, new Analyses of climate change effects on forest C and analyses suggest that changes in soil C fluxes may be N dynamics have largely focused on temperature and linked to declines in N availability and export. precipitation during the growing season. However, Specifically, long-term increases in forest floor C:N processes during the dormant season have been shown ratio (Yanai et al. 2013), labile C, and dissolved to be a key driver of N oligotrophication (Dura´n et al. organic carbon (DOC) flux all suggest that increases in 2014, 2016; Elmore et al. 2016). Subtle and indirect atmospheric CO2 and/or deacidification effects on effects of climate change on snow depth and soil frost decomposition and plant mycorrhizal status (Battles and changes in plant-microbial interactions during et al. 2014; Juice et al. 2006) are increasing C flow seasonal transitions may have more pronounced from the atmosphere through plants into the soil, effects on ecosystem C and N cycles than changes which should reduce N mineralization and availability associated with mean annual temperature or precipi- (Hart et al. 1994). tation (Campbell et al. 2005; Groffman et al. 2012). In this paper, we synthesize data from multiple Changes during winter can be particularly important sources to advance the idea that multiple components as warmer temperatures decrease the depth and of environmental change are driving the northern duration of snowpack, potentially increasing soil hardwood forests at HBR toward a condition of N freezing severity, which in turn affects microbial, soil oligotrophication by two mechanisms (Fig. 1). First, and plant ecosystem processes (Brooks et al. 2011; we argue that increased C flow (caused by both Martz et al. 2016), not only during the winter, but also increased atmospheric CO2 and recovery from acid in the following growing season (Dura´n et al. rain) stimulates microbial immobilization and 2014, 2016; Liu et al. 2016; Sorensen et al. 2016b). decreases available N production via mineralization. However, the complex nature of snowpack and soil This reduction in available
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