Soil and root respiration in mature Alaskan black spruce forests that vary in soil organic matter decomposition rates

Climate warming at high latitudes is expected to increase root and microbial respiration and thus cause an increase in soil respiration. We measured the root and microbial components of soil respiration near Fairbanks, Alaska, in 2000 and 2001, in three black spruce (Picea mariana (Mill) B.S.P.) forests. We hypothesized faster decomposition correlates with greater amounts of both root and microbial contributions to soil respiration. Contrary to our prediction, the site with the coolest summer soil temperatures and slowest decomposition (site identification “high-np”) had significantly (p < 0.05) greater growing season soil respiration (485 g C·m–2·year–1) than the two other sites (372 and 332 g C·m–2·year–1). Spruce C allocation to root respiration was significantly greater, and fine-root N concentration was 10% and 12% greater (p < 0.05) at high-np than at the other two sites. High-np spruce foliage was also more enriched in 13C and depleted in 15N, suggesting either lower available moisture or slower N turnover. Either factor could drive greater C allocation to roots; however, a literature review suggests moisture deficit corresponds to greater C allocation to roots in black spruce forests across the boreal ecosystem. Controls on spruce C allocation need to be resolved before making the generalization that soil respiration will increase with warming in this forest type. Résumé : Le réchauffement du climat aux latitudes élevées devrait augmenter la contribution tant des racines que des décomposeurs hétérotrophes à la respiration du sol. Les auteurs mesuré les composantes racinaires et hétérotrophes de la respiration du sol près de Fairbanks en Alaska, en 2000 et 2001, dans trois forêts d’épinette noire (Picea mariana (Mill.) B.S.P.) situées à différents endroits dans le paysage. Ils ont assumé qu’une décomposition plus rapide correspondrait à une plus grande contribution racinaire et hétérotrophe à la respiration du sol. Contrairement à leurs prédictions cependant, la respiration du sol pendant la saison de croissance était significativement plus élevée (p < 0,05) dans le site avec les températures estivales du sol les plus froides et la décomposition la plus lente (site ID « np-élevé ») (485 g C·m–2·an–1) que dans les deux autres sites (372 et 332 g C·m–2·an–1). L’allocation de C vers la respiration des racines était significativement plus élevée et la concentration de N dans les racines fines était 10 % et 12 % plus élevée (p < 0,05) dans le site np-élevé que dans les deux autres sites. Le feuillage de l’épinette dans le site np-élevé était également plus riche en 13C et plus pauvre en 15N; ce qui indiquait soit une plus faible disponibilité en eau, soit un remplacement plus lent de N. L’un ou l’autre de ces facteurs pourrait entraîner une plus forte allocation de C vers les racines. Cependant, une revue de la littérature indique qu’un déficit en eau correspond à une plus forte allocation de C vers les racines dans les forêts d’épinette noire partout dans l’écosystème boréal. Les facteurs qui contrôlent l’allocation de C chez l’épinette doivent être connus avant de pouvoir généraliser le fait que le réchauffement du climat entraînera une augmentation de la respiration du sol dans ce type de forêts. [Traduit par la Rédaction] 174 Vogel et al. Introduction Soil respiration generally increases with temperature, creating the possibility that the ongoing and predicted warming at high latitudes will increase soil respiration and decrease net boreal forest uptake of CO2 from the atmosphere (Goulden et al. 1998). Both root and microbial respiration contribute to soil respiration and correlate with temperature, but the activity of each has different implications for ecosystem carbon (C) balance. Root respiration in general consumes photosynthate recently fixed by the canopy (Högberg et al. 2001), thus this respiration has little influence on annual net ecosystem carbon balance and is sensitive to both canopy and soil conditions. Alternatively, microbial decomposition can affect ecosystem C balance by releasing CO2 from soil organic matter that ranges in age from recent (e.g., fine-root turnover) to years and millennia (e.g., litter and humified soil C) (Trumbore 2000). The decomposition of soil organic Can. J. For. Res. 35: 161–174 (2005) doi: 10.1139/X04-159 © 2005 NRC Canada 161 Received 8 April 2004. Accepted 14 September 2004. Published on the NRC Research Press Web site at http://cjfr.nrc.ca on 12 February 2005. J.G. Vogel1,2 and D.W. Valentine. Department of Forest Sciences, University of Alaska, P.O. Box 757200, Fairbanks, AK 99775-7200, USA. R.W. Ruess. Department of Biology and Wildlife, University of Alaska, P.O. Box 757000, Fairbanks, AK 99775-7200, USA. 1Corresponding author (e-mail: [email protected]). 2Present address: Department of Botany, University of Florida, 220 Bartram Hall, Gainesville, FL 32611, USA. matter could drive a significant increase in atmospheric CO2 because boreal soils store about 182 Pg of soil C (Post et al. 1982), equivalent to 24% of the current atmospheric pool. Separating the root and microbial components of soil respiration is critical to monitoring the destabilization of soil C pools (Hanson et al. 2000), determining the relative sensitivities of roots and microbes to temperature or moisture (Boone et al. 1998; Melillo et al. 2002), and ultimately predicting how soil respiration will respond to a changing climate. Decomposition in boreal forests is very often temperature limited (Van Cleve et al. 1983), and a general hypothesis is that with soil warming, microbial decomposition will increase, releasing more nutrients to the plants, stimulating photosynthesis, and increasing overall plant productivity, including roots. If true, soil respiration should increase because of the stimulated contribution of both roots and microbes. However, experiments in other ecosystems indicate that soil respiration enhancement is not sustained at high levels in response to warming (Jarvis and Linder 2000; Rustad et al. 2001; Melillo et al. 2002). Root respiration may decrease or stay the same with warming because of temperature acclimation or changing plant C allocation. Roots acclimate to warmer average temperatures by respiring less at a given temperature (Sowell and Spomer 1986; Tjoelker et al. 1999; Luo et al. 2001). Also, plants often decrease overall allocation to roots with increased nutrient availability (Haynes and Gower 1995). Microbes may also appear to acclimate to temperature (Flanagan and Veum 1974), but this may instead result from the relatively quick depletion of easily decomposed soil organic matter (Melillo et al. 2002). Although soil-warming experiments provide direct evidence of the potential influence of climate change on decomposition and soil respiration, natural climate gradients can be useful for examining whether predictions of the final carbon cycling characteristics of a forest are accurate. We used this approach, selecting a common overstory–understory species association found in the North American boreal forest. Black spruce (Picea mariana (Mill) B.S.P.), the overstory species, occurs across the entire mean annual temperature range (7 to –11 °C) of the North American boreal biome, is the most prevalent and wide-ranging tree species in the boreal forest (Burns and Honkala 1990), and is the most common in boreal Alaska (Labau and van Hees 1990). The greatest amounts of soil C occur under black spruce (Van Cleve et al. 1983; Gower et al. 1997), partly because of its poor tissue quality and predominance in wet, cool soils. Also, bryophytes can cover 100% of the forest floor underneath spruce, drastically lowering soil temperatures through the insulating properties of their tissue (Van Cleve et al. 1983). Our objectives were to examine the relationship between decomposition and the two components of soil respiration, microbial and root respiration. We hypothesized that warmers soils favor faster decomposition and also higher rates of all components of soil respiration. Alternatively, a warmer soil and faster decomposition may cause temperature acclimation in roots or decreased available organic matter for microbes, resulting in similar or lower soil respiration across a decomposition gradient. Possible physiological explanations for root respiration patterns are examined in the context of foliage and fine-root N concentration and foliar isotopic differences in δ13C and δ15N. We also measured moss gross photosynthesis and modeled moss respiration to constrain the influence of these on soil respiration results. Materials and methods Study areas We selected a soil temperature gradient in a homogeneous vegetation type and therefore located similar black spruce forests near Fairbanks, Alaska, that varied in aspect and elevation. Sites included a high-elevation area with no permafrost (high-np), a mid-elevation deep permafrost area (mid-dp), and a low-elevation shallow permafrost (low-sp) area (Table 1). High-np is part of the Bonanza Creek Long Term Ecological Research (LTER) study within the Bonanza Creek Experimental Forest (64°48′N, 147°52′W). No two sites are greater than 30 km apart. Seasonal variation in daily mean air temperatures is extreme, ranging from –24.9 °C in January to 16.4 °C June, with a mean average temperature of –3.3 °C. Local variation in temperature occurs, driven by adiabatic altitude–temperature lapse rates, winter temperature inversions, and topographical sun-shading. The winter cold-air inversions driven by altitude are especially extreme, with high elevations being up to 30 °C warmer on winter days. Annual precipitation (269 mm) is less than potential evapotranspiration (466 mm), and 65% of precipitation occurs during the growing season (Viereck et al. 1993). Black spruce is the only canopy species, and feathermoss forms a near-continuous carpet. Feathermoss is a generic term for two species, Hylocomium splendens (Hedw.) B.S.G. and Pleurozium schreberi (Brid.) Mitt. The two species did not vary significantly in relative proportions among sites. Other cryptogams and bryophytes occupy <15% of the forest floor. Common to the understory of all sites are Vaccinium vitis-idaea L. and Cornus canadensis (L.) Graebn. The two low-elevation sites experience a mid-June flush of Equisetum palustre L., and high-np has three Alnus crispa (Ait.) Pursh bushes within the study area. The average diameter and stand density of the spruce are similar among the three sites, but variations occur in age and depth to permafrost (Table 1). © 2005 NRC Canada 162 Can. J. For. Res. Vol. 35, 2005 High-np Mid-dp Low-sp