98 values less than 1.5 associated with a critical deficiency; how- ever, variation between species does exist. In agreement with the standards stipulated by Cresswell and Weir (1997), quadratic regression models ranging between 0.71 and 0.88 R2 values in all three tree species (Figure 6) indicate a foliar N content less than 1.5 is associated with reductions in Fv/Fm values of 0.8 (values associated with full photosynthetic functioning) (Björkman and Demmig 1987; Mohammed et al. 1995; Percival 2005). Foliar N content between 0.8% and 1.2% corresponds to Fv/Fm values of 0.6 which in turn relate to reduced survival and growth (Maki and Colombo 2001; Percival 2004). Results presented here are one of the first to quantify actual foliar N content with impair- ment of the leaf photosynthetic system and potential influence on future growth and survival. In conclusion, results of this study indicate that the chloro- phyll content SPAD meter potentially offers a useful nondestruc- tive, handheld system to aid in the evaluation of tree health. High correlations were obtained among SPAD readings, total leaf chlorophyll and carotenoid content, foliar N content, and leaf photosynthetic efficiency as measured by chlorophyll fluores- cence Fv/Fm values. A lower correlation between SPAD values and total chlorophyll/carotenoid content were obtained. In the case of Acer pseudoplatanus, Fagus sylvatica, and Quercus ro- bur, SPAD readings lower than 25 indicated impairment of the leaf photosynthetic process. However, critical chlorophyll meter values indicating reductions in tree vitality may vary among species and among cultivars within the same species (Hoel 1998). Likewise, the chlorophyll content of a leaf varies with age. Consequently, consistency in sample collection and sea- sonal timing may be necessary to develop species and cultivar calibration to correlate SPAD values with reductions in tree vi- tality (Hoel 1998). Acknowledgments. The authors are grate- ful for funding in part from the TREE Fund (John Z. Duling Grant). Percival et al.: Quantifying Nutrient Stress in Foliar Tissue Cresswell, G.C., and R.G. Weir. 1997. Plant Nutrient Disorders— Ornamental Plants and Shrubs. Inkata Press, Melbourne, Australia. pp. 132–221. Doncheva, S., V. Vassileva, G. Ignatov, S. Pandev, R. Dris, and R. Niskanen. 2001. Nitrogen deficiency, photosynthesis and chloro- plasts of pepper plants. Agriculture and Food Science in Finland 10:59–64. Escudero, A., and S. Mediavilla. 2003. Decline in photosynthetic nitro- gen use efficiency with leaf age and nitrogen, resorption as determi- nants of leaf life span. Journal of Ecology 91:880–889. Evans, J.R. 1983. Nitrogen and photosynthesis in the flag leaf of wheat. Plant Phvsiology. 72:297–302. ———. 1989. Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19. Filella, I., L. Serrano, J. Serra, and J. Peñuelas. 1995. Evaluating wheat nitrogen status with canopy reflectance indices and discriminant analysis. Crop Science 35:1400–1405. Follett, R.H., R.E. Follett, and A.D. Halvorson. 1992. Use of chlorophyll meter to evaluate the nitrogen status of dry land winter wheat. Com- munications in Soil Science and Plant Analysis 23:687–697. Gastal, F., G. Belanger, and G. Lemaire. 1992. A model of the leaf extension rate of tall fescue in response to nitrogen and temperature. Annals of Botany 70:437–442. Hall, D.O., and K.K. Rao. 1999. Photosynthesis. 6th Edition. Cambridge University Press, Cambridge, MA. pp. 174–180. Havaux, M. 1988. Carotenoids as membrane stabilizers in chloroplasts. Trends in Plant Science 4:147–151. Hendry, G.A.F., and A.H. Price. 1993. Stress indicators: Chlorophylls and carotenoids, pp. 148–152. In Hendry, G.A.F., and J.P. Grime (Eds.). Methods in Comparative Plant Ecology. Chapman and Hall, London, U.K. Hikosaka, K., and T. Hirose. 2000. Photosynthetic nitrogen use effi- ciency in species coexisting in a warm-temperate evergreen forest. Tree Physiology 20:1249–1254. Hirose, T., and M.J.A. Werger. 1987. Nitrogen use efficiency in instan- taneous and daily photosynthesis of leaves in the canopy of a Soli- dago altissima stand. Physiologia Plantarum 70:215–222. Hoel, B.O. 1998. Use of a hand held chlorophyll meter in winter wheat: Evaluation of different measuring positions on the leaves. Acta Ag- riculturae Scandinavica 48:222–228. LITERATURE CITED Anten, N.P.R., K. Hikosaka, and T. Hirose. 2000. Leaf Development and Canopy Growth. Sheffield Academic Press, Sheffield, UK. pp. 171–203. Bacci, L., M. De. Vincenzi, B. Rapi, B. Arca, and F. Benincasa. 1998. Two methods for the analysis of colorimetric components applied to plant stress monitoring. Computers and Electronics in Agriculture 19:167–186. Balasubramanian, V., A.C. Morales, R.T. Cruz, T.M. Thiyagarajan, R. Nagarajan, M. Babu, S. Abdulrachman, and L.H. Hai. 2000. Adap- tation of the chlorophyll meter (SPAD) technology for real-time N management in rice: A review. International Rice Research Institute 5:25–26. Björkman, O., and B. Demmig. 1987. Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170:489–504. Brown, S.B., J.D. Houghton, and G.A.F. Hendry. 1991. Chlorophyll breakdown, pp. 465–489. In Scheer, H. (Ed.). Chlorophylls. CRC Press, Boca Raton, FL. Buckland, S.M., A.H. Price, and G.A.F. Hendry. 1991. The role of ascorbate in drought-treated Cochlearia atlantica Pobed. and Arme- ria maritime (Mill.) Willd. The New Phytologist 119:155–160. ©2008 International Society of Arboriculture Jimenez, M.S., A.M. Gonzalez-Rodriguez, D. Morales, M.C. Cid, A.R. Socorro, and M. Caballero. 1997. Evaluation of chlorophyll fluores- cence as a tool for salt stress detection in roses. Photosynthetica 33:291–301. Kariya, K., A. Matsuzaki, and H. Machida. 1982. Distribution of chlo- rophyll content in leaf blade of rice plant. Nihon Sakumotsu Gakkai Kiji 51:134–135. Kitajima, M., and W.L. Butler. 1975. Quenching of chlorophyll fluo- rescence and primary photochemistry in chloroplasts by dibromothy- moquinone. Biochemistry Biophysical Acta 723:169–175. Kitao, M., T.T. Lei, and T. Koike. 1998. Application of chlorophyll fluorescence to evaluate Mn tolerance of deciduous broad-leaved tree seedlings native to northern Japan. Tree Physiology 18:135–140. Körner, C. 1989. The nutritional status of plants from high altitudes: A worldwide comparison. Oecologia 81:379–391. Kraus, T.E., and R.A. Fletcher. 1994. Paclobutrazol protects wheat seed- lings from heat and paraquat injury. Is detoxification of active oxygen involved? Plant & Cell Physiology 35:45–52. Larcher, W. 1995. Physiological Plant Ecology. 3rd Edition. Springer, London, U.K. Lawlor, D.W. 2001. Photosynthesis. 3rd Edition. Scientific Publishers Limited, Oxford, U.K. Lichtenthaler, H.K., and A.R. Wellburn. 1983. Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochemical Society Transmycological 11:591–593.
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