Photosynthetica 2021, 59(1):61-73 | DOI: 10.32615/ps.2020.079

Performing gas-exchange measurements on excised branches - evaluation and recommendations

J.E.C. MISSIK1, 2, A.C. OISHI3, M.C. BENSON1, V.J. MERETSKY1, R.P. PHILLIPS4, K.A. NOVICK1
1 O'Neill School of Public and Environmental Affairs, Indiana University - Bloomington, 702 N Walnut Grove Avenue, Bloomington, IN 47408, USA
2 Department of Civil and Environmental Engineering, Washington State University, PO Box 642910, Washington State University, Pullman, WA 99164, USA
3 Coweeta Hydrologic Lab, USDA Forest Service - Southern Research Station, 3160 Coweeta Lab Road, Otto, NC 28763, USA
4 Department of Biology, Indiana University - Bloomington, 1001 E. 3rd St., Bloomington, IN 47405, USA

In forest canopies, it is common to perform leaf-level gas-exchange measurements on recently excised branches, often without testing for excision-related biases. We conducted a formal test of excision effects using gas-exchange measurements from cut and uncut canopy branches of three deciduous hardwoods - sugar maple (Acer saccharum Marsh.), tulip poplar (Liriodendron tulipifera L.), and white oak (Quercus alba L.). Across all species, excision immediately reduced photosynthesis and stomatal conductance by 27-62% relative to pre-excision rates. In white oak, which had particularly long (> 100 cm) vessels, gas exchange was more impaired for shorter (~ 30 cm) as compared to longer (~ 100 cm) branches. Additional hypotheses linking branch height and species water-use strategy to excision bias were tested but not confirmed. A survey of 23 previously published studies confirms that our results are not without precedent. Excision-related biases should be considered when interpreting measurements performed on excised branches.

Additional key words: canopy physiology; cut branch; hydraulics; isohydricity; measurement bias; methodology.

Received: August 14, 2020; Revised: November 6, 2020; Accepted: November 19, 2020; Prepublished online: January 20, 2021; Published: March 18, 2021  Show citation

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MISSIK, J.E.C., OISHI, A.C., BENSON, M.C., MERETSKY, V.J., PHILLIPS, R.P., & NOVICK, K.A. (2021). Performing gas-exchange measurements on excised branches - evaluation and recommendations. Photosynthetica59(1), 61-73. doi: 10.32615/ps.2020.079
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References

  1. Aranda I., Gil L., Pardos J.A.: Water relations and gas exchange in Fagus sylvatica L. and Quercus petraea (Mattuschka) Liebl. in a mixed stand at their southern limit of distribution in Europe. - Trees 14: 344-352, 2000. Go to original source...
  2. Beer C., Ciais P., Reichstein M. et al.: Temporal and among-site variability of inherent water use efficiency at the ecosystem level. - Global Biogeochem. Cy. 23: GB2018, 2009. Go to original source...
  3. Bernacchi C.J., Calfapietra C., Davey P.A. et al.: Photosynthesis and stomatal conductance responses of poplars to free-air CO2 enrichment (PopFACE) during the first growth cycle and immediately following coppice. - New Phytol. 159: 609-621, 2003. Go to original source...
  4. Bernacchi C.J., Rosenthal D.M., Pimentel C. et al.: Modeling the temperature dependence of C3 photosynthesis. - In: Laisk A., Nedbal L., Govindjee (ed.): Photosynthesis in silico: Understanding Complexity from Molecules to Ecosystems. Pp. 231-246. Springer, Dordrecht 2009. Go to original source...
  5. Bloomfield K.J., Domingues T.F., Saiz G. et al.: Contrasting photosynthetic characteristics of forest vs. savanna species (Far North Queensland, Australia). - Biogeosciences 11: 7331-7347, 2014. Go to original source...
  6. Brodribb T.J., McAdam S.A., Carins Murphy M.R.: Xylem and stomata, coordinated through time and space: Functional linkages between xylem and stomata. - Plant Cell Environ. 40: 872-880, 2017. Go to original source...
  7. Buckley T.N.: The control of stomata by water balance. - New Phytol. 168: 275-291, 2005. Go to original source...
  8. Campany C.E., Tjoelker M.G., von Caemmerer S., Duursma R.A.: Coupled response of stomatal and mesophyll conductance to light enhances photosynthesis of shade leaves under sunflecks. - Plant Cell Environ. 39: 2762-2773, 2016. Go to original source...
  9. Cano F.J., Sánchez-Gómez D., Rodríguez-Calcerrada J. et al.: Effects of drought on mesophyll conductance and photosyn-thetic limitations at different tree canopy layers. - Plant Cell Environ. 36: 1961-1980, 2013. Go to original source...
  10. Cochard H., Herbette S., Barigah T. et al.: Does sample length influence the shape of xylem embolism vulnerability curves? A test with the Cavitron spinning technique. - Plant Cell Environ. 33: 1543-1552, 2010. Go to original source...
  11. Dang Q.-L., Margolis H.A., Coyea M.R. et al.: Regulation of branch-level gas exchange of boreal trees: roles of shoot water potential and vapor pressure difference. - Tree Physiol. 17: 521-535, 1997. Go to original source...
  12. Dietze M.C., Vargas R., Richardson A.D. et al.: Characterizing the performance of ecosystem models across time scales: A spectral analysis of the North American Carbon Program site-level synthesis. - J. Geophys. Res.-Biogeo. 116: G04029, 2011. Go to original source...
  13. Domingues T.F., Meir P., Feldpausch T.R. et al.: Co-limitation of photosynthetic capacity by nitrogen and phosphorus in West Africa woodlands. - Plant Cell Environ. 33: 959-980, 2010. Go to original source...
  14. Ellsworth D.S., Liu X.: Photosynthesis and canopy nutrition of four sugar maple forests on acid soils in northern Vermont. - Can. J. For. Res. 24: 2118-2127, 1994. Go to original source...
  15. Ethier G.J., Livingston N.J., Harrison D.L. et al.: Low stomatal and internal conductance to CO2 versus Rubisco deactivation as determinants of the photosynthetic decline of ageing evergreen leaves. - Plant Cell Environ. 29: 2168-2184, 2006. Go to original source...
  16. Ewers B., Oren R., Kim H.S. et al.: Effects of hydraulic architecture and spatial variation in light on mean stomatal conductance of tree branches and crowns. - Plant Cell Environ. 30: 483-496, 2007. Go to original source...
  17. Flexas J., Ribas-Carbó M., Diaz-Espejo A. et al.: Mesophyll conductance to CO2: current knowledge and future pro- spects. - Plant Cell Environ. 31: 602-621, 2008. Go to original source...
  18. Ginn S.E., Seiler J.R., Cazell B.H., Kreh R.E.: Physiological and growth responses of eight-year-old loblolly pine stands to thinning. - For. Sci. 37: 1030-1040, 1991.
  19. Hacke U.G., Sperry J.S.: Functional and ecological xylem anatomy. - Persp. Plant Ecol. Evol. Syst. 4: 97-115, 2001. Go to original source...
  20. Han Q.: Height-related decreases in mesophyll conductance, leaf photosynthesis and compensating adjustments associated with leaf nitrogen concentrations in Pinus densiflora. - Tree Physiol. 31: 976-984, 2011. Go to original source...
  21. Hanson D.T., Green L.E., Pockman W.: Spatio-temporal decoupling of stomatal and mesophyll conductance induced by vein cutting in leaves of Helianthus annuus. - Front. Plant Sci. 4: 365, 2013. Go to original source...
  22. Huxman T.E., Turnipseed A.A., Sparks J.P. et al.: Temperature as a control over ecosystem CO2 fluxes in a high-elevation, subalpine forest. - Oecologia 134: 537-546, 2003. Go to original source...
  23. Joesting H.M., McCarthy B.C., Brown K.J.: Determining the shade tolerance of American chestnut using morphological and physiological leaf parameters. - Forest Ecol. Manag. 257: 280-286, 2009. Go to original source...
  24. Koch G.W., Sillett S.C., Jennings G.M., Davis S.D.: The limits to tree height. - Nature 428: 851-854, 2004. Go to original source...
  25. Kwon H., Choi M.: Generalized hydromechanical model for stomatal responses to hydraulic perturbations. - J. Theor. Biol. 340: 119-130, 2014. Go to original source...
  26. Lange O., Führer G., Gebel J.: Rapid field determination of photosynthetic capacity of cut spruce twigs (Picea abies) at saturating ambient CO2. - Trees 1: 70-77, 1986. Go to original source...
  27. Law B.E., Sun O., Campbell J. et al.: Changes in carbon storage and fluxes in a chronosequence of ponderosa pine. - Glob. Change Biol. 9: 510-524, 2003. Go to original source...
  28. LeBauer D.S., Wang D., Richter K.T. et al.: Facilitating feedbacks between field measurements and ecosystem models. - Ecol. Monogr. 83: 133-154, 2013. Go to original source...
  29. Leuning R., Kelliher F.M., De Pury D.G.G., Schulze E.-D.: Leaf nitrogen, photosynthesis, conductance and transpiration: scaling from leaves to canopies. - Plant Cell Environ. 18: 1183-1200, 1995. Go to original source...
  30. Lichtenthaler H.K., Aè A., Marek M.V. et al.: Differences in pigment composition, photosynthetic rates and chlorophyll fluorescence images of sun and shade leaves of four tree species. - Plant Physiol. Bioch. 45: 577-588, 2007. Go to original source...
  31. Long S.P., Bernacchi C.J.: Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. - J. Exp. Bot. 54: 2393-2401, 2003. Go to original source...
  32. Long S.P., Farage P.K., Garcia R.L.: Measurement of leaf and canopy photosynthetic CO2 exchange in the field. - J. Exp. Bot. 47: 1629-1642, 1996. Go to original source...
  33. Marler T.E., Mickelbart M.V.: Repeated mechanical stress from leaf cuvette influences leaf gas exchange. - HortScience 27: 432-434, 1992. Go to original source...
  34. Martínez-Vilalta J., Poyatos R., Aguadé D. et al.: A new look at water transport regulation in plants. - New Phytol. 204: 105-115, 2014. Go to original source...
  35. Masarovièová E., ©tefanèík L.: Some ecophysiological features in sun and shade leaves of tall beech trees. - Biol. Plantarum 32: 374-387, 1990. Go to original source...
  36. McAdam S.A., Brodribb T.J.: The evolution of mechanisms driving the stomatal response to vapor pressure deficit. - Plant Physiol. 167: 833-843, 2015. Go to original source...
  37. Meng F.-R., Arp P.A.: Net photosynthesis and stomatal conductance of red spruce twigs before and after twig detachment. - Can. J. For. Res. 23: 716-721, 1992. Go to original source...
  38. Miyazawa Y., Tateishi M., Komatsu H. et al.: Are measurements from excised leaves suitable for modeling diurnal patterns of gas exchange of intact leaves? - Hydrol. Process. 25: 2924-2930, 2011. Go to original source...
  39. Monson R.K., Trahan N., Rosenstiel T.N. et al.: Isoprene emission from terrestrial ecosystems in response to global change: minding the gap between models and observations. - Philos. T. Roy. Soc. A 365: 1677-1695, 2007. Go to original source...
  40. Niinemets Ü., Cescatti A., Rodeghiero M., Tosens T.: Leaf internal diffusion conductance limits photosynthesis more strongly in older leaves of Mediterranean evergreen broad-leaved species. - Plant Cell Environ. 28: 1552-1566, 2005. Go to original source...
  41. Pan Y., Birdsey R.A., Fang J. et al.: A large and persistent carbon sink in the world's forests. - Science 333: 988-993, 2011. Go to original source...
  42. Pou A., Medrano H., Flexas J., Tyerman S.D.: A putative role for TIP and PIP aquaporins in dynamics of leaf hydraulic and stomatal conductances in grapevine under water stress and re-watering. - Plant Cell Environ. 36: 828-843, 2013. Go to original source...
  43. Roman D.T., Novick K.A., Brzostek E.R. et al.: The role of isohydric and anisohydric species in determining ecosystem-scale response to severe drought. - Oecologia 179: 641-654, 2015. Go to original source...
  44. Salleo S., Nardini A., Pitt F., Lo Gullo M.A.: Xylem cavitation and hydraulic control of stomatal conductance in laurel (Laurus nobilis L.). - Plant Cell Environ. 23: 71-79, 2000. Go to original source...
  45. Santiago L.S., Mulkey S.S.: A test of gas exchange measurements on excised canopy branches of ten tropical tree species. - Photosynthetica 41: 343-347, 2003. Go to original source...
  46. Schäfer K.V.R., Oren R., Ellsworth D.S. et al.: Exposure to an enriched CO2 atmosphere alters carbon assimilation and allocation in a pine forest ecosystem. - Glob. Change Biol. 9: 1378-1400, 2003. Go to original source...
  47. Schuster W., Monson R.: An examination of the advantages of C3-C4 intermediate photosynthesis in warm environments. - Plant Cell Environ. 13: 903-912, 1990. Go to original source...
  48. Sperry J.S., Wang Y., Wolfe B.T. et al.: Pragmatic hydraulic theory predicts stomatal responses to climatic water deficits. - New Phytol. 212: 577-589, 2016. Go to original source...
  49. Urban O., ©prtová M., Ko¹vancová M. et al.: Comparison of photosynthetic induction and transient limitations during the induction phase in young and mature leaves from three poplar clones. - Tree Physiol. 28: 1189-1197, 2008. Go to original source...
  50. Valladares F., Allen M.T., Pearcy R.W.: Photosynthetic responses to dynamic light under field conditions in six tropical rainforest shrubs occuring along a light gradient. - Oecologia 111: 505-514, 1997. Go to original source...
  51. Walker A.P., Beckerman A.P., Gu L. et al.: The relationship of leaf photosynthetic traits - Vcmax and Jmax - to leaf nitrogen, leaf phosphorus, and specific leaf area: a meta-analysis and modeling study. - Ecol. Evol. 4: 3218-3235, 2014. Go to original source...
  52. Warren C.R.: Why does photosynthesis decrease with needle age in Pinus pinaster? - Trees 20: 157-164, 2006. Go to original source...
  53. Warren C.R., Ethier G.J., Livingston N.J. et al.: Transfer conductance in second growth Douglas-fir (Pseudotsuga menziesii (Mirb.) Franco) canopies. - Plant Cell Environ. 26: 1215-1227, 2003. Go to original source...
  54. Warren J.M., Jensen A.M., Medlyn B.E. et al.: Carbon dioxide stimulation of photosynthesis in Liquidambar styraciflua is not sustained during a 12-year field experiment. - AoB Plants 7: plu074, 2015. Go to original source...
  55. Woodruff D.R., Bond B.J., Meinzer F.C.: Does turgor limit growth in tall trees? - Plant Cell Environ. 27: 229-236, 2004. Go to original source...
  56. Yi K., Dragoni D., Phillips R.P. et al.: Dynamics of stem water uptake among isohydric and anisohydric species experiencing a severe drought. - Tree Physiol. 37: 1379-1392, 2017. Go to original source...
  57. Zhang J., Marshall J.D., Jaquich B.C.: Genetic differentiation in carbon isotope discrimination and gas exchange in Pseudotsuga menziesii: A common garden experiment. - Oecologia 93: 80-87, 1993. Go to original source...