Foliar C/N stoichiometry in urban forest trees on a global scale

Abstract

Foliar C/N stoichiometry is an indicator of geochemical cycling in forest ecosystems, but the driving changes for its response to urbanization at the wide scale is not clear. In this study, data on tree-leaf C and N stoichiometry were collected in papers from across 105 tree species from 82 genera and 46 families. The foliar C/N of urban forest trees varied among different climate zones and tree taxonomic variation and tended to be higher in trees of urban forests near the equator and in eastern regions, mainly driven by lowered foliar N concentration. Neither the foliar C concentration nor foliar C/N for trees of urban forests was statistically higher than those of rural forests. For variation by taxonomic classification, C₄ species Amaranthus retroflexus and Chenopodium ambrosoides (Amaranthaceae) had lower foliar C/N than did other species and families. Myrsine guianensis (Primulaceae) and Myconia fallax (Asteraceae) had the highest foliar C/N. Therefore, urbanization has not caused a significant response in forest trees for foliar C/N. The change in foliar N concentration was globally the main force driving of the differences in foliar C/N for most tree species in urban forests. More work is needed on foliar C/N in trees at cities in polar regions and the Southern Hemisphere.

Keywords

Ecosystem cycling / City habitat / Isometric scaling / Suburb / Remote town / N deposition

References

[1] Alfani A, Baldantoni D, Maisto G, Bartoli G, De Santo AV. Temporal and spatial variation in C, N, S and trace element contents in the leaves of Quercus ilex within the urban area of Naples. Environ Pollut, 2000, 109: 119-129.

[2] Bui EN, Henderson BL. C:N:P stoichiometry in Australian soils with respect to vegetation and environmental factors. Plant Soil, 2013, 373: 553-568.

[3] Bukata AR, Kyser TK. Carbon and nitrogen isotope variations in tree-rings as records of perturbations in regional carbon and nitrogen cycles. Environ Sci Technol, 2007, 41: 1331-1338.

[4] Caldararu S, Purves DW, Palmer PI. Phenology as a strategy for carbon optimality: a global model. Biogeosciences, 2014, 11: 763-778.

[5] Carreiro MM, Tripler CE. Forest remnants along urban-rural gradients: examining their potential for global change research. Ecosystems, 2005, 8: 568-582.

[6] Chen FS, Fahey TJ, Yu MY, Gan L. Key nitrogen cycling processes in pine plantations along a short urban-rural gradient in Nanchang, China. For Ecol Manage, 2010, 259: 477-486.

[7] Cleveland CC, Townsend AR, Taylor P, Alvarez-Clare S, Bustamante MMC, Chuyong G, Dobrowski SZ, Grierson P, Harms KE, Houlton BZ, Marklein A, Parton W, Porder S, Reed SC, Sierra CA, Silver WL, Tanner EVJ, Wieder WR. Relationships among net primary productivity, nutrients and climate in tropical rain forest: a pan-tropical analysis. Ecol Lett, 2011, 14: 939-947.

[8] Cobley LAE, Pataki DE, McCarthy HR, Martin SA, Ehleringer JR. Housing age and affluence influence plant and soil nitrogen and carbon cycles in two semiarid cities. J Geophys Res Biogeosci, 2018, 123: 3178-3192.

[9] Craven D, Braden D, Ashton MS, Berlyn GP, Wishnie M, Dent D. Between and within-site comparisons of structural and physiological characteristics and foliar nutrient content of 14 tree species at a wet, fertile site and a dry, infertile site in Panama. For Ecol Manag, 2007, 238: 335-346.

[10] Drake BG, GonzalezMeler MA, Long SP. More efficient plants: a consequence of rising atmospheric CO₂?. Annu Rev Plant Physiol Plant Molec Biol, 1997, 48: 609-639.

[11] Enloe HA, Lockaby BG, Zipperer WC, Somers GL. Urbanization effects on leaf litter decomposition, foliar nutrient dynamics and aboveground net primary productivity in the subtropics. Urban Ecosyst, 2015, 18: 1285-1303.

[12] Falxa-Raymond N, Palmer MI, McPhearson T, Griffin KL. Foliar nitrogen characteristics of four tree species planted in New York City forest restoration sites. Urban Ecosyst, 2014, 17: 807-824.

[13] Fan HB, Wu JP, Liu WF, Yuan YH, Hu L, Cai QK. Linkages of plant and soil C:N: P stoichiometry and their relationships to forest growth in subtropical plantations. Plant Soil, 2015, 392: 127-138.

[14] Fang YT, Yoh M, Koba K, Zhu WX, Takebayashi Y, Xiao YH, Lei CY, Mo JM, Zhang W, Lu XK. Nitrogen deposition and forest nitrogen cycling along an urban-rural transect in southern China. Glob Change Biol, 2011, 17: 872-885.

[15] Hawke DJ, Valiance JR. Microbial carbon concentration in samples of seabird and non-seabird forest soil: implications for leaf litter cycling. Pedobiologia, 2015, 58: 33-39.

[16] Imhoff ML, Bounoua L, DeFries R, Lawrence WT, Stutzer D, Tucker CJ, Ricketts T. The consequences of urban land transformation on net primary productivity in the United States. Remote Sens Environ, 2004, 89: 434-443.

[17] Jiang D, Geng Q, Li Q, Vogel J, Shi Z, Ruan H, Xu X. Nitrogen and phosphorus resorption in planted forests worldwide. Forests, 2019, 10: 201.

[18] Kagata H, Ohgushi T. Carbon-nitrogen stoichiometry in the tritrophic food chain willow, leaf beetle, and predatory ladybird beetle. Ecol Res, 2007, 22: 671-677.

[19] Kahan AY, Currie WS, Brown DG. Nitrogen and carbon biogeochemistry in forest sites along an indirect urban-rural gradient in southeastern Michigan. Forests, 2014, 5: 643-665.

[20] Kim C, Jeong J, Park JH, Ma HS. Growth and nutrient status of foliage as affected by tree species and fertilization in a fire-disturbed urban forest. Forests, 2015, 6: 2199-2213.

[21] Kiyosu Y, Kidoguchi M. Variations in the stable carbon isotope ratios of Zelkova serrata leaves from roadside trees in Toyama City, Japan. Geochem J, 2000, 34: 379-382.

[22] Knepp RG, Hamilton JG, Mohan JE, Zangerl AR, Berenbaum MR, DeLucia EH. Elevated CO₂ reduces leaf damage by insect herbivores in a forest community. New Phytol, 2005, 167: 207-218.

[23] Koyama L, Tokuchi N, Fukushima K, Terai M, Yamamoto Y. Seasonal changes in nitrate use by three woody species: the importance of the leaf-expansion period. Trees-Struct Funct, 2008, 22: 851-859.

[24] Li JF, Lu KD, Lv W, Li J, Zhong LJ, Ou YB, Chen DH, Huang X, Zhang YH. Fast increasing of surface ozone concentrations in Pearl River Delta characterized by a regional air quality monitoring network during 2006–2011. J Environ Sci-China, 2014, 26: 23-36.

[25] Li ZG, Xie CK, Chen D, Lu HY, Che SQ. Effects of land cover patterns on land surface temperatures associated with land use types along urbanization gradients in Shanghai, China. Pol J Environ Stud, 2020, 29: 713-725.

[26] Liu W, Zhan JY, Zhao F, Yan HM, Zhang F, Wei XQ. Impacts of urbanization-induced land-use changes on ecosystem services: a case study of the Pearl River Delta Metropolitan Region, China. Ecol Indic, 2019, 98: 228-238.

[27] Maisto G, Baldantoni D, De Marco A, Alfani A, De Santo AV. Ranges of nutrient concentrations in Quercus ilex leaves at natural and urban sites. J Plant Nutr Soil Sci, 2013, 176: 801-808.

[28] McGroddy ME, Daufresne T, Hedin LO. Scaling of C:N: P stoichiometry in forests worldwide: implications of terrestrial redfield-type ratios. Ecology, 2004, 85: 2390-2401.

[29] Milanović S, Lazarevic J, Popovic Z, Miletic Z, Kostic M, Radulovic Z, Karadzic D, Vuleta A. Preference and performance of the larvae of Lymantria dispar (Lepidoptera: Lymantriidae) on three species of European oaks. Eur J Entomol, 2014, 111: 371-378.

[30] Nikula S, Vapaavuori E, Manninen S. Urbanization-related changes in European aspen (Populus tremula L.): leaf traits and litter decomposition. Environ Pollut, 2010, 158: 2132-2142.

[31] Oldfield EE, Felson AJ, Wood SA, Hallett RA, Strickland MS, Bradford MA. Positive effects of afforestation efforts on the health of urban soils. For Ecol Manage, 2014, 313: 266-273.

[32] Oleksyn J, Kloeppel BD, Lukasiewicz S, Karolewski P, Reich PB. Ecophysiology of horse chestnut (Aesculus hippocastanum L.) in degraded and restored urban sites. Pol J Ecol, 2007, 55: 245-260.

[33] Orians CM, Fritz RS, Hochwender CG, Albrectsen BR, Czesak ME. How slug herbivory of juvenile hybrid willows alters chemistry, growth andsubsequent susceptibility to diverse plant enemies. Ann Bot, 2013, 112: 757-765.

[34] Pacaldo RS, Volk TA, Briggs RD. Greenhouse gas potentials of shrub willow biomass crops based on below- and aboveground biomass inventory along a 19-year chronosequence. BioEnergy Res, 2013, 6: 252-262.

[35] Pellegrini AFA, Hoffmann WA, Franco AC. Carbon accumulation and nitrogen pool recovery during transitions from savanna to forest in central Brazil. Ecology, 2014, 95: 342-352.

[36] Radwanski D, Gallagher F, Vanderklein DW, Schafer KVR. Photosynthesis and aboveground carbon allocation of two co-occurring poplar species in an urban brownfield. Environ Pollut, 2017, 223: 497-506.

[37] Rao P, Hutyra LR, Raciti SM, Finzi AC. Field and remotely sensed measures of soil and vegetation carbon and nitrogen across an urbanization gradient in the Boston metropolitan area. Urban Ecosyst, 2013, 16: 593-616.

[38] Reich PB, Oleksyn J. Global patterns of plant leaf N and P in relation to temperature and latitude. Proc Natl Acad Sci USA, 2004, 101: 11001-11006.

[39] Rong QQ, Liu JT, Cai YP, Lu ZH, Zhao ZZ, Yue WC, Xia JB. Leaf carbon, nitrogen and phosphorus stoichiometry of Tamarix chinensis Lour. in the Laizhou Bay coastal wetland. China Ecol Eng, 2015, 76: 57-65.

[40] Sack L, Grubb PJ, Maranon T. The functional morphology of juvenile plants tolerant of strong summer drought in shaded forest understories in southern Spain. Plant Ecol, 2003, 168: 139-163.

[41] Salehi A, Ghorbanzadeh N, Salehi M. Soil nutrient status, nutrient return and retranslocation in poplar species and clones in northern Iran. iForest, 2013, 6: 6.

[42] Sardans J, Rivas-Ubach A, Penuelas J. Factors affecting nutrient concentration and stoichiometry of forest trees in Catalonia (NE Spain). For Ecol Manage, 2011, 262: 2024-2034.

[43] Sardans J, Rivas-Ubach A, Penuelas J. The C:N: P stoichiometry of organisms and ecosystems in a changing world: a review and perspectives. Perspect Plant Ecol Evol Syst, 2012, 14: 33-47.

[44] Searle SY, Turnbull MH, Boelman NT, Schuster WSF, Yakir D, Griffin KL. Urban environment of New York City promotes growth in northern red oak seedlings. Tree Physiol, 2012, 32: 389-400.

[45] Shen WJ, Wu JG, Grimm NB, Hope D. Effects of urbanization-induced environmental changes on ecosystem functioning in the phoenix metropolitan region, USA. Ecosystems, 2008, 11: 138-155.

[46] Sheng PF, Guo XH. The Long-run and short-run impacts of urbanization on carbon dioxide emissions. Econ Model, 2016, 53: 208-215.

[47] Shi X, Sun HJ, Pan HW, Chen YT, Jiang ZP, Liu JF, Wang SF. Growth and efficiency of nutrient removal by Salix jiangsuensis J172 for phytoremediation of urban wastewater. Environ Sci Pollut Res, 2016, 23: 2715-2723.

[48] Slot M, Rey-Sanchez C, Gerber S, Lichstein JW, Winter K, Kitajima K. Thermal acclimation of leaf respiration of tropical trees and lianas: response to experimental canopy warming, and consequences for tropical forest carbon balance. Glob Change Biol, 2014, 20: 2915-2926.

[49] Turnbull MH, Griffin KL, Fyllas NM, Lloyd J, Meir P, Atkin OK. Separating species and environmental determinants of leaf functional traits in temperate rainforest plants along a soil-development chronosequence. Funct Plant Biol, 2016, 43: 751-765.

[50] United Nation (2018) Department of Economic and Social Affairs, Population Division. The World's Cities in 2018—Data Booklet (ST/ESA/SER.A/417)

[51] van Rensburg L, Kruger GHJ, Ubbink B, Scholes MC, Peacock J. A phytocentric perspective of Asterolecanium quercicola Bouche infestation on Quercus robur L trees along an urbanization gradient. S Afr J Bot, 1997, 63: 25-31.

[52] Wang SJ, Gao S, Li SJ, Feng KS. Strategizing the relation between urbanization and air pollution: empirical evidence from global countries. J Clean Prod, 2020, 243: 10.

[53] Wang Y, Chen LL, Kubota J. The relationship between urbanization, energy use and carbon emissions: evidence from a panel of Association of Southeast Asian Nations (ASEAN) countries. J Clean Prod, 2016, 112: 1368-1374.

[54] Yang Y, Luo Y. Carbon : nitrogen stoichiometry in forest ecosystems during stand development. Glob Ecol Biogeogr, 2011, 20: 354-361.

[55] Yang HI, Park HJ, Lee KS, Lim SS, Kwak JH, Lee SI, Chang SX, Lee SM, Choi WJ. Delta C-13, delta N-15, N concentration, C/N, and Ca/Al of Pinus densiflora foliage in Korean cities of different precipitation pH and atmospheric NO and SO levels. Ecol Indic, 2018, 88: 27-36.

[56] Yarie J, Van Cleve K. Effects of carbon, fertilizer, and drought on foliar chemistry of tree species in interior Alaska. Ecol Appl, 1996, 6: 815-827.

[57] Zhang D, Zheng HF, Ren ZB, Zhai C, Shen GQ, Mao ZX, Wang PJ, He XY. Effects of forest type and urbanization on carbon storage of urban forests in Changchun, Northeast China. Chin Geogr Sci, 2015, 25: 147-158.

[58] Zhang L, Jacob DJ, Knipping EM, Kumar N, Munger JW, Carouge CC, van Donkelaar A, Wang YX, Chen D. Nitrogen deposition to the United States: distribution, sources, and processes. Atmos Chem Phys, 2012, 12: 4539-4554.

[59] Zhang XL, Wu S, Yan XD, Chen ZJ. A global classification of vegetation based on NDVI, rainfall and temperature. Int J Climatol, 2017, 37: 2318-2324.

[60] Zhao N, He NP, Wang QF, Zhang XY, Wang RL, Xu ZW, Yu GR. The altitudinal patterns of leaf C:N:P stoichiometry are regulated by plantgrowth form, climate and soil on Changbai Mountain China. PLoS One, 2014, 9: 9.

[61] Zhao YH, Zhang L, Chen YF, Liu XJ, Xu W, Pan YP, Duan L. Atmospheric nitrogen deposition to China: a model analysis on nitrogen budget and critical load exceedance. Atmos Environ, 2017, 153: 32-40.

[62] Zheng SX, Shangguan Z. Spatial patterns of leaf nutrient traits of the plants in the Loess Plateau of China. Trees-Struct Funct, 2007, 21: 357-370.