Author: Marshall J1
Reviewer: Gough C2
Measurement unit: µmol m-2 s-1 (or g-1 or m-3), µmol g-1 s-1; Measurement scale: tissue, plant, or plot; Equipment costs: €€€; Running costs: €; Installation effort: medium to high; Maintenance effort: -; Knowledge need: high; Measurement mode: manual measurement or data logger
Plant respiration is the carbon dioxide (CO2) efflux from vegetative tissues to the atmosphere. With plants globally respiring upwards of 60 gigatons of carbon per year (Schimel 1995), this flux is one of the largest contributors to atmospheric CO2 (Raich & Potter, 1995). Plant respiration converts roughly half of fixed photosynthate back into CO2 (Lambers et al., 2008; Amthor, 2010). The difference between photosynthesis and plant respiration represents net primary production.
Respiration occurs in all living plant tissues whether in darkness or in sunlight, but rates are especially sensitive to kinetic changes owing to temperature and tissue growth rates, increasing exponentially with temperature and linearly with growth rates. Climate and other global-change drivers such as elevated CO2 and nitrogen depostion can influence temperature and growth rates and thus respiration rates (Ryan, 1991; Hyvönen et al., 2007).
2.1.4.1 What and how to measure?
Gold standard
The sensitivity of the respiration rate to dynamic environmental conditions and its coupling with plant growth necessitates high frequency, continuous measurements if the goal is to disentangle the underlying drivers regulating plant respiration rates. For this reason, the gold standard is continuous measurements of CO2 efflux (Tarvainen et al., 2014). This requires either closed or open chambers mounted on or around the plant organ of interest (Field et al., 1989; Tamayo et al., 2001, see Special cases below). Closed chambers must be opened between measurements using some automated mechanism. Open chambers can remain closed, but they require a cooling mechanism if they are exposed to daytime sun. In theory, O2 influx could also be measured (Gonzalez et al., 2007), but in fact this is seldom done in terrestrial ecosystems because the background concentration in the atmosphere is so high that a change would be difficult to detect.
Bronze standard
The bronze standard is to use a portable gas-exchange system to take periodic point measurements manually at intervals. At its most basic, such a measurement can be treated as an index to be used as a basis for comparison within a study. However, due to the less frequent nature of manual measurements relative to those that are automated, and the potential for changing environmental conditions to bias measurements across plots and sites, manual measurements are generally less suitable for integrative estimates of whole-ecosystem plant respiration. Some standardisation of manual data collection (e.g., by time of day and season) should be considered in order to reduce environmental bias and the effects of co-occuring photosynthesis on plant respiration.
For climate-change experiments, it may be more useful to use manual spot measurements to calibrate, or to compare to general models that were parameterised elsewhere (e.g. Heskel et al., 2016). If annual scale summations are required, they can be derived from response functions scaled up using continuous abiotic data (e.g. Niinistö et al., 2011).
Also see protocol 2.2.3 on Soil CO2 and trace gas fluxes for more details on measuring gas fluxed from the soil.
Where to start
Start with Ryan’s description (Ryan, 1991), which is clear and interesting. Then read Heskel et al. (2016) or Reich et al. (2016) for a look at global patterns. If you want more of the physiology, Amthor (2010) is a good read.
2.1.4.2 Special cases, emerging issues, and challenges
Continuous measurements can be made with either open or closed chambers (Field et al., 1989; Tamayo et al., 2001). Open chambers rely on a continuous flow of gas and the measurement of the CO2 concentration difference between the inflow and the outflow. Open chambers have low sensitivity to leaks, but they require careful measurement of flow rates. Closed chambers rely on a timed mechanism to seal the chamber, followed by measurement of the rise in concentration over time, and then opening of the chamber after the measurement. Such chambers are sensitive to leaks and temperature increases during the measurement. In either case, chamber temperatures should be measured with some precision, especially if the chamber is in bright sunlight. Still better is some form of chamber cooling system, which prevents the temperature rise that would otherwise occur.
Continuous respiration measurements often rely on a commercial photosynthesis system that has been modified for continuous operation. Spot measurements can be made with most commercial gas-exchange systems provided that enough living tissue can be fitted into the chamber to yield a reliable measurement. Because respiration rates are often 10% or so of net photosynthetic rates, the measurement can challenge traditional gas-exchange systems, especially at low temperatures.
Respiration rates can be expressed relative to tissue mass, surface area, or volume. The best basis depends on the study objectives, but mass is often easiest to measure and is well correlated with respiring tissue quantity. However, there is a strong tradition of expressing leaf respiration per square metre (Heskel et al., 2016). In the interest of generating comparable data across studies, we suggest using mass as the default basis for all rates except for leaves, which should be expressed per m2.
When leaves or green stems are sunlit, respiration may be partly or completely offset by simultaneous photosynthesis. Photosynthetic stems may either refix respired CO2 internally, under the bark, or they may take CO2 from the surrounding atmosphere. For the former, it seems reasonable to measure with transparent chambers, which allow refixation to proceed as normal (Cernusak & Hutley, 2011). The latter should be treated as an alternative site for net photosynthesis and measured alongside the leaves (see protocol 2.1.3 Leaf-scale photosynthesis).
Excised tissues are sometimes used for respiration measurements. This greatly simplifies chamber insertion, but the cutting may induce artefacts. In particular, “wound” respiration may be induced by the cell damage and diffusion paths are disrupted. These effects can be minimised by waiting until the pulse of wound respiration recedes or by coating cut surfaces in liquid paraffin (Cernusak et al., 2001), respectively.
It should be recognised that plants acclimatise to changes in temperature, which tends to reduce respiration responses relative to measurements in a short-term temperature experiment (Reich et al., 2016). What this means is that short-term responses should not be scaled up into seasonal or annual responses. Leaves that develop under a new temperature regime are more able to acclimatise to that regime, so the best policy would be to focus on leaves produced since the temperature treatment began (Slot & Kitajima, 2015).
2.1.4.3 References
Theory, significance, and large datasets
Theory in Amthor (2010). Significance in Amthor (2010), Heskel et al. (2016), Hyvönen et al. (2007), and Slot & Kitajima (2015). Large datasets in Heskel et al. (2016)
More on methods and existing protocols
Cernusak et al. (2001), Field et al. (1989), Heskel et al. (2016), Tarvainen et al. (2014)
All references
Amthor, J. S. (2010). From sunlight to phytomass: on the potential efficiency of converting solar radiation to phyto-energy. New Phytologist, 188(4), 939-959.
Cernusak, L. A., & Hutley, L. B. (2011). Stable isotopes reveal the contribution of corticular photosynthesis to growth in branches of Eucalyptus miniata. Plant Physiology, 155(1), 515-523.
Cernusak, L. A., Marshall, J. D., Comstock, J. P., & Balster, N. J. (2001). Carbon isotope discrimination in photosynthetic bark. Oecologia, 128(1), 24-35.
Field, C. B., Ball, J. T., & Berry, J. A. (1989). Photosynthesis: principles and field techniques. In R. W. Pearcy, J. R. Ehleringer, H. A. Mooney, & P. W. Rundel (Eds.), Plant Physiological Ecology (pp. 209-253). Dordrecht: Springer.
Gonzalez, L., Bolaño, C., & Pelissier, F. (2007). Use of oxygen electrode in measurements of photosynthesis and respiration. In M. J. Regiosa Roger (Ed.), Handbook of Plant Ecophysiology Techniques (pp. 141-153). Dordrecht: Springer.
Heskel, M. A., O’Sullivan, O. S., Reich, P. B., Tjoelker, M. G., Weerasinghe, L. K., Penillard, A., … Atkin, O. K. (2016). Convergence in the temperature response of leaf respiration across biomes and plant functional types. Proceedings of the National Academy of Sciences USA, 113(14), 3832-3837.
Hyvönen, R., Ågren, G. I., Linder, S., Persson, T., Cotrufo, M. F., Ekblad, A., … Wallin, G. (2007). The likely impact of elevated CO2, nitrogen deposition, increased temperature and management on carbon sequestration in temperate and boreal forest ecosystems: a literature review. New Phytologist, 173(3), 463-480.
Lambers, H., Chapin, F. S., & Pons, T. L. (2008). Respiration. In Plant Physiological Ecology (pp. 101-150). Berlin: Springer.
Niinistö, S. M., Kellomäki, S., & Silvola, J. (2011). Seasonality in a boreal forest ecosystem affects the use of soil temperature and moisture as predictors of soil CO2 efflux. Biogeosciences, 8(11), 3169-3186.
Raich, J. W., & Potter, C. S. (1995) Global patterns of carbon dioxide emissions from soils. Global Biogeochemical Cycles, 9(1), 23–36.
Reich, P. B., Sendall, K. M., Stefanski, A., Wei, X., Rich, R. L., & Montgomery, R. A. (2016). Boreal and temperate trees show strong acclimation of respiration to warming. Nature, 531(7596), 633-636.
Ryan, M. G. (1991). Effects of climate change on plant respiration. Ecological Applications, 1(2), 157-167.
Schimel, D. S. (1995). Terrestrial ecosystems and the carbon cycle. Global Change Biology, 1(1), 77-91.
Slot, M., & Kitajima, K. (2015). General patterns of acclimation of leaf respiration to elevated temperatures across biomes and plant types. Oecologia, 177(3), 885-900.
Tamayo, P. R., Weiss, O., & Sánchez-Moreiras, A. M. (2001). Gas exchange techniques in photosynthesis and respiration infrared gas analyser. In M. J. Reigosa Roger (Ed.), Handbook of Plant Ecophysiology Techniques (pp. 113-139). Dordrecht: Springer.
Tarvainen, L., Räntfors, M., & Wallin, G. (2014). Vertical gradients and seasonal variation in stem CO2 efflux within a Norway spruce stand. Tree Physiology, 34(5), 488-502.
Author: Marshall J1
Reviewer: Gough C2
Affiliations
1 Department of Forest Ecology and Management, Swedish University of Agricultural Sciences, Umeå, Sweden.
2 Department of Biology, Virginia Commonwealth University, Richmond, USA