The contribution of respiration in tree stems to the Dole Effect

Biogeosciences, 9, 4037–4044, 2012 www.biogeosciences.net/9/4037/2012/ doi:10.5194/bg-9-4037-2012 © Author(s) 2012. CC Attribution 3.0 License. Biogeosciences The contribution of respiration in tree stems to the Dole Effect A. Angert1 , J. Muhr2 , R. Negron Juarez3 , W. Alegria Muñoz4 , G. Kraemer4 , J. Ramirez Santillan4 , J. Q. Chambers5 , and S. E. Trumbore2 1 The Institute of Earth Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel 2 Department of Biogeochemical Processes, Max-Planck Institute for Biogeochemistry, Jena, Germany 3 Ecology and Evolutionary Biology, Tulane University, 400 Lindy Boggs, New Orleans, LA, USA 4 Universidad Nacional de la Amazonı́a Peruana, Facultad de Ciencias Forestales, Iquitos, Peru 5 Lawrence Berkeley National Laboratory, Climate Sciences Department, Berkeley, CA, USA Correspondence to: A. Angert () Received: 16 January 2012 – Published in Biogeosciences Discuss.: 24 January 2012 Revised: 11 September 2012 – Accepted: 27 September 2012 – Published: 22 October 2012 Abstract. Understanding the variability and the current value of the Dole Effect, which has been used to infer past changes in biospheric productivity, requires accurate information on the isotopic discrimination associated with respiratory oxygen consumption in each of the biosphere components. Respiration in tree stems is an important component of the land carbon cycle. Here we measured, for the first time, the discrimination associated with tree stem oxygen uptake. The measurements included tropical forest trees, which are major contributors to the global fluxes of carbon and oxygen. We found discrimination in the range of 12.6–21.5 ‰, indicating both diffusion limitation, resulting in O2 discrimination values below 20 ‰, and alternative oxidase respiration, which resulted in discrimination values greater than 20 ‰. Discrimination varied seasonally, between and within tree species. Calculations based on these results show that variability in woody plants discrimination can result in significant variations in the global Dole Effect. 1 Introduction The Dole Effect is defined as the difference between the average isotopic composition of oxygen in seawater (H2 O), and the oxygen in atmospheric O2 . The magnitude of the Dole effect depends mainly on three factors: the isotopic composition of leaf water from which O2 is produced on land (Farquhar et al., 1993; Gillon and Yakir, 2001), the possible isotopic discrimination during release of O2 from H2 O during photosynthesis (Eisenstadt et al., 2010; Luz and Barkan, 2011); and the discrimination against the heavier isotope in respiratory oxygen consumption (Lane and Dole, 1956; Guy et al., 1989, 1993). The Dole Effect was suggested to be a useful tracer for paleo-changes in the ratio of ocean to land productivity (Bender et al., 1994; Blunier et al., 2002). However, this use is based on the assumption of significantly different isotopic effects of the land and the oceans. New findings, including indications for significant discrimination during marine photosynthesis and the effect of diffusion in soils on the effective respiratory discrimination, have resulted in a decreased estimated difference between the terrestrial and marine Dole Effects, making it easier to explain why there have not been large shifts in the Dole Effect between glacial and interglacial times (Luz and Barkan, 2011). As shown by previous studies (Angert et al., 2001, 2003; Angert and Luz, 2001), when the diffusion of O2 from the atmosphere to the consumption site inside roots and soil aggregates is restricted, the effective discrimination of the soil system depends not only on the intrinsic discrimination in the respiration processes, but also on the discrimination in diffusion, and on the internal oxygen concentration at the consumption site. This effect of diffusion on the discrimination in O2 uptake is similar to the well known isotopic effect which takes place in CO2 diffusion and uptake in leaves (Farquhar et al., 1982). Overall, the effect of diffusion tends to lower the effective discrimination of O2 uptake in soils (Angert et al., 2003). However, observations in temperate and boreal forest soils demonstrated that a second process must also act to explain the observed δ 18 O-O2 in soil pore space. This process is Published by Copernicus Publications on behalf of the European Geosciences Union. 4038 A. Angert et al.: Respiration in tree-stems to the Dole Effect respiration through the alternative oxidase pathway (AOX). The discrimination of AOX respiration is ∼ 30 ‰, which is considerably higher than the ∼ 20 ‰ discrimination in “normal” dark respiration through the cytochrome oxidase pathway (COX) (Ribas-Carbo et al., 1995). High discrimination values (22.5 ± 3.6 %) were found in boreal soils (Angert et al., 2003), and can be explained by a large fraction of respiration which goes through the AOX in plant roots. The emission of CO2 from aboveground woody tissues amounts to ∼ 16 % of the forest annual gross photosynthesis flux (Litton et al., 2007; Ryan et al., 1997; Waring et al., 1998) while belowground woody tissues contribute a similar amount. As a result, the discrimination in woody tissue O2 uptake may have a significant impact on the global contribution of land to the Dole Effect. To date there have been no measurements of O2 isotope discrimination in tree wood respiration processes. Here we report the first measurements based on stem O2 influx for 6 tree species, representing 4 different plant families, including trees from tropical forests that contribute ∼ 40 % of global land primary production (Beer et al., 2010). Our results suggest that, as with soil respiration, both the effects of diffusion on one hand, and AOX activity on the other, control the isotopic effects in stem O2 uptake. 2 2.1 Methods Sites and trees Trees from two sites were sampled. The first site was the Givat-Ram campus of the Hebrew University of Jerusalem (HUJI, 31◦ 460 1500 N 35◦ 110 5100 E). At this site we have performed experiments on the following trees: one Apple (Malus domestica), one Stone Pine (Pinus pinea L.), and one Aleppo Pine (Pinus halepensis Mill.). Experiments at this site were conducted from April 2010 to March 2011. The second site was the UNAP site, located at the Center for Research and Forest Learning (CIEFOR) of the National University of the Peruvian Amazon (UNAP) in the community of Puerto Almendras, which is located 16 km southwest of the city of Iquitos, Peru. CIEFOR is centered over 3◦ 490 5300 N, 73◦ 220 2800 W, encompasses a forested area of 1300 ha and belongs to the Faculty of Forest Engineering (FCF)-UNAP. For the base period 1971–2000 the mean annual rainfall is ∼ 3000 mm (http://www.senamhi.gob.pe/), and the maximum, minimum, and average temperatures are 26.3 ◦ C, 25.9 ◦ C, and 25.2 ◦ C, respectively (Brohan et al., 2006). All the experiments in this study were conducted on a total of nine trees from the fol (...truncated)