Abstract
Background and aims
Bark contains a substantial fraction of the nutrients stored in woody biomass, however the degree of functional coordination of bark, wood, and foliar nutrient pools, and its relationship to soil nutrient availability remains poorly understood.
Methods
Bark thickness and nitrogen, phosphorus, potassium, calcium, and magnesium concentrations were measured in 23 tree species present in two premontane wet tropical forests in western Panama differing in soil nutrient availability. Bark data were combined with existing wood and leaf data from the same species.
Results
Bark nutrients were positively correlated with leaf and wood nutrients for all elements. The low fertility site had both lower bark nutrient concentrations and thicker bark, driven primarily by species compositional differences between sites, and secondarily by intraspecific variation. Across species, bark nutrient concentration varied 4 to 25 fold, with the highest variation for calcium. Overall, bark accounted for the largest percent of Ca in above-ground biomass nutrient pools (22–82%) and a large fraction of the other nutrients studied (N: 6–53%, P: 5–50%, K: 4–40%, and Mg: 2–35%).
Conclusions
Bark represents a substantial, and highly variable, pool of biomass nutrients. The functional role of bark nutrients, the causes and consequences of this variation, and its relation to other bark traits, including bark thickness, deserve further study.
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Abbreviations
- Ca:
-
Calcium
- C:N:
-
Carbon to Nitrogen ratio
- DBH:
-
Diameter Breast Height
- LMA:
-
leaf mass per unit area
- Mg:
-
Magnesium
- N:
-
Nitrogen
- P:
-
Phosphorus
- K:
-
Potassium
References
Alban DH, Perala DA, Schlaegel BE (1978) Biomass and nutrient distribution in aspen, pine, and spruce stands on the same soil type in Minnesota. Can J For Res 8:290–299. https://doi.org/10.1139/x78-044
Alvarez-Clare S, Mack MC, Brooks M (2013) A direct test of nitrogen and phosphorus limitation to net primary productivity in a lowland tropical wet forest. Ecology 94:1540–1551
Arias D, Calvo-Alvarado J, Richter DD, Dohrenbusch A (2011) Productivity, aboveground biomass, nutrient uptake and carbon content in fast-growing tree plantations of native and introduced species in the southern region of Costa Rica. Biomass Bioenergy 35:1779–1788. https://doi.org/10.1016/j.biombioe.2011.01.009
Asner GP, Martin RE (2011) Canopy phylogenetic, chemical and spectral assembly in a lowland Amazonian forest. New Phytol 189:999–1012. https://doi.org/10.1111/j.1469-8137.2010.03549.x
Baltzer JL, Thomas SC (2010) A second dimension to the leaf economics spectrum predicts edaphic habitat association in a tropical forest. PLoS One 5:e13163–e13167. https://doi.org/10.1371/journal.pone.0013163
Bond WJ (2010) Do nutrient-poor soils inhibit development of forests? A nutrient stock analysis. Plant Soil 334:47–60. https://doi.org/10.1007/s11104-010-0440-0
Cai S, Kang X, Zhang L (2013) Allometric models for aboveground biomass of ten tree species in Northeast China. Ann For Res 56:105–122
Chave J, Andalo C, Brown S, Cairns MA, Chambers JQ, Eamus D, Fölster H, Fromard F, Higuchi N, Kira T, Lescure JP, Nelson BW, Ogawa H, Puig H, Riéra B, Yamakura T (2005) Tree allometry and improved estimation of carbon stocks and balance in tropical forests. Oecologia 145:87–99. https://doi.org/10.1007/s00442-005-0100-x
Condit R, Engelbrecht BMJ, Pino D, Perez R, Turner BL (2013) Species distributions in response to individual soil nutrients and seasonal drought across a community of tropical trees. PNAS 110:5064–5068. https://doi.org/10.1073/pnas.1218042110
Cornwell WK, Cornelissen JHC, Allison SD et al (2009) Plant traits and wood fates across the globe: rotted, burned, or consumed? Glob Chang Biol 15:2431–2449. https://doi.org/10.1111/j.1365-2486.2009.01916.x
Dalling JW, Heineman K, Lopez OR, Wright SJ, Turner BL (2016) Nutrient availability in tropical rain forests: the paradigm of phosphorus limitation. In: Goldstein G, Santiago L (eds) Tropical tree physiology: adaptations and responses in a changing environment. Springer International Publishing, Basel, pp 261–273
Day FP, Monk CD (1977) Seasonal nutrient dynamics in the vegetation on a southern Appalachian watershed. Am J Bot 64:1126. https://doi.org/10.2307/2442169
Dell B, Jones S, Wilson SA (1987) Phosphorus nutrition of jarrah (Eucalyptus marginata) seedlings. Plant Soil 97:369–379. https://doi.org/10.1007/bf02383227
Dossa GGO, Paudel E, Cao K, Schaefer D, Harrison RD (2016) Factors controlling bark decomposition and its role in wood decomposition in five tropical tree species. Sci Rep 6:1–9. https://doi.org/10.1038/srep34153
Dossa GGO, Schaefer D, Zhang J-L, Tao JP, Cao KF, Corlett RT, Cunningham AB, Xu JC, Cornelissen JHC, Harrison RD (2018) The cover uncovered: bark control over wood decomposition. J Ecol 106:1–14. https://doi.org/10.1111/1365-2745.12976
Fearnside PM (1997) Wood density for estimating forest biomass in Brazilian Amazonia. For Ecol Manag 90:59–87. https://doi.org/10.1016/s0378-1127(96)03840-6
Franceschi VR, Krokene P, Christiansen E, Krekling T (2005) Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytol 167:353–375. https://doi.org/10.1111/j.1469-8137.2005.01436.x
Freschet GT, Aerts R, Cornelissen JHC (2012) A plant economics spectrum of litter decomposability. Funct Ecol 26:56–65. https://doi.org/10.1111/j.1365-2435.2011.01913.x
Fromm J (2010) Wood formation of trees in relation to potassium and calcium nutrition. Tree Physiol 30:1140–1147. https://doi.org/10.1093/treephys/tpq024
Fyllas NM, Patiño S, Baker TR, Bielefeld Nardoto G, Martinelli LA, Quesada CA, Paiva R, Schwarz M, Horna V, Mercado LM, Santos A, Arroyo L, Jiménez EM, Luizão FJ, Neill DA, Silva N, Prieto A, Rudas A, Silviera M, Vieira ICG, Lopez-Gonzalez G, Malhi Y, Phillips OL, Lloyd J (2009) Basin-wide variations in foliar properties of Amazonian forest: phylogeny, soils and climate. Biogeosciences 6:2677–2708. https://doi.org/10.5194/bg-6-2677-2009
Gautam MK, Tripathi AK, Manhas RK (2011) Assessment of critical loads in tropical Sal (Shorea robusta Gaertn. F.) forests of Doon Valley Himalayas, India. Water Air Soil Pollut 218:235–264. https://doi.org/10.1007/s11270-010-0638-z
Harrell FE, Dupont C (2018) Hmisc: Harrell Miscellaneous. R package version 4.1–1. https://CRAN.R-project.org/package=Hmisc. Accessed 13 July 2018
Harrington RA, Fownes JH, Vitousek PM (2001) Production and resource use efficiencies in N- and P-limited tropical forests: a comparison of responses to long-term fertilization. Ecosystems 4:646–657. https://doi.org/10.1007/s10021-001-0034-z
Hart P, Clinton PW, Allen RB et al (2003) Biomass and macro-nutrients (above-and below-ground) in a New Zealand beech (Nothofagus) forest ecosystem: implications for carbon storage and sustainable forest management. For Ecol Manag 174:281–294
Heineman KD, Turner BL, Dalling JW (2016) Variation in wood nutrients along a tropical soil fertility gradient. New Phytol 211:440–454. https://doi.org/10.1111/nph.13904
Helmisaari H-S, Siltala T (1989) Variation in nutrient concentrations of Pinus sylvestris stems. Scand J For Res 4:443–451. https://doi.org/10.1080/02827588909382580
Jager MM, Richardson SJ, Bellingham PJ, Clearwater MJ, Laughlin DC (2015) Soil fertility induces coordinated responses of multiple independent functional traits. J Ecol 103:374–385. https://doi.org/10.1111/1365-2745.12366
John R, Dalling JW, Harms KE, Yavitt JB, Stallard RF, Mirabello M, Hubbell SP, Valencia R, Navarrete H, Vallejo M, Foster RB (2007) Soil nutrients influence spatial distributions of tropical tree species. PNAS 104:864–869
Johnson CE, Siccama TG, Denny EG, Koppers MM, Vogt DJ (2014) In situ decomposition of northern hardwood tree boles: decay rates and nutrient dynamics in wood and bark. Can J For Res 44:1515–1524. https://doi.org/10.1139/cjfr-2014-0221
Jordan CF, Kline JR (1977) Transpiration of trees in a tropical rainforest. J Appl Ecol 14:853–860. https://doi.org/10.2307/2402816
Karla YP (1998) Handbook of reference methods for plant analysis. CRC Press, Boca Raton
Legendre P (2018) lmodel2: Model II Regression. In: httpsCRAN.R-project.orgpackagelmodel. Accessed 13 July 2018
Leigh EG Jr (1999) Tropical Forest ecology: a view from Barro Colorado Island. Oxford University Press, New York
Martin AR, Erickson DL, Kress WJ, Thomas SC (2014) Wood nitrogen concentrations in tropical trees: phylogenetic patterns and ecological correlates. New Phytol 204:484–495. https://doi.org/10.1111/nph.12943
Miles PD, Smith WB (2009) Specific gravity and other properties of wood and bark for 156 tree species found in North America. U.S. Department of Agriculture, Forest Service, Northern Research Station, Newtown Square. NRS-38
Mirmanto E, Proctor J, Green J, Nagy L, Suriantata (1999) Effects of nitrogen and phosphorus fertilization in a lowland evergreen rainforest. Philos Trans R Soc Lond Ser B Biol Sci 354:1825–1829. https://doi.org/10.1098/rstb.1999.0524
Muller-Landau HC (2004) Interspecific and inter-site variation in wood specific gravity of tropical trees. Biotropica 36:20–32
Netzer F, Schmid C, Herschbach C, Rennenberg H (2017) Phosphorus-nutrition of European beech (Fagus sylvatica L.) during annual growth depends on tree age and P-availability in the soil. Environ Exp Bot 137:194–207. https://doi.org/10.1016/j.envexpbot.2017.02.009
Nichols CP, Drewe JA, Gill R, Goode N, Gregory N (2016) A novel causal mechanism for grey squirrel bark stripping: the calcium hypothesis. For Ecol Manag 367:12–20. https://doi.org/10.1016/j.foreco.2016.02.021
Oksanen J, Blanchet FG, Friendly M et al (2018) Vegan: community ecology package. R package version 2.5–1. https://CRAN.R-project.org/package=vegan. Accessed 13 July 2018
Ordoñez JC, van Bodegom PM, Witte J-PM, Wright IJ, Reich PB, Aerts R (2009) A global study of relationships between leaf traits, climate and soil measures of nutrient fertility. Glob Ecol Biogeogr 18:137–149. https://doi.org/10.1111/j.1466-8238.2008.00441.x
Paine CET, Stahl C, Courtois EA, Patiño S, Sarmiento C, Baraloto C (2010) Functional explanations for variation in bark thickness in tropical rain forest trees. Funct Ecol 24:1202–1210. https://doi.org/10.1111/j.1365-2435.2010.01736.x
Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290. https://doi.org/10.1093/bioinformatics/btg412
Pausas JG (2015) Bark thickness and fire regime. Funct Ecol 29:315–327. https://doi.org/10.1111/1365-2435.12372
Pellegrini AFA, Anderegg WRL, Paine CET, Hoffmann WA, Kartzinel T, Rabin SS, Sheil D, Franco AC, Pacala SW (2017) Convergence of bark investment according to fire and climate structures ecosystem vulnerability to future change. Ecol Lett 20:307–316. https://doi.org/10.1111/ele.12725
Pinard MA, Huffman J (1997) Fire resistance and bark properties of trees in a seasonally dry forest in eastern Bolivia. J Trop Ecol 13:727–740
Poorter L, McNeil A, Hurtado V-H, Prins HHT, Putz FE (2014) Bark traits and life-history strategies of tropical dry- and moist forest trees. Funct Ecol 28:232–242. https://doi.org/10.1111/1365-2435.12158
Prada CM, Morris A, Andersen KM, Turner BL, Caballero P, Dalling JW (2017) Soils and rainfall drive landscape-scale changes in the diversity and functional composition of tree communities in premontane tropical forest. J Veg Sci 28:859–870. https://doi.org/10.1111/jvs.12540
Rennenberg H, Wildhagen H, Ehlting B (2010) Nitrogen nutrition of poplar trees. Plant Biol 12:275–291
Richardson SJ, Laughlin DC, Lawes MJ, Holdaway RJ, Wilmshurst JM, Wright M, Curran TJ, Bellingham PJ, McGlone MS (2015) Functional and environmental determinants of bark thickness in fire-free temperate rain forest communities. Am J Bot 102:1590–1598. https://doi.org/10.3732/ajb.1500157
Rosell JA, Gleason S, Méndez-Alonzo R, Chang Y, Westoby M (2014) Bark functional ecology: evidence for tradeoffs, functional coordination, and environment producing bark diversity. New Phytol 201:486–497. https://doi.org/10.1111/nph.12541
Sandel B, Gutiérrez AG, Reich PB, Schrodt F, Dickie J, Kattge J (2015) Estimating the missing species bias in plant trait measurements. J Veg Sci 26:828–838. https://doi.org/10.1111/jvs.12292
Scatena FN, Silver W, Siccama T, Johnson A, Sanchez MJ (1993) Biomass and nutrient content of the bisley experimental watersheds, Luquillo experimental forest, Puerto-Rico, before and after hurricane Hugo, 1989. Biotropica 25:15–27
Shorohova E, Kapitsa E, Kazartsev I, Romashkin I, Polevoi A, Kushnevskaya H (2016) Tree species traits are the predominant control on the decomposition rate of tree log bark in a mesic old-growth boreal forest. For Ecol Manag 377:36–45. https://doi.org/10.1016/j.foreco.2016.06.036
Slik JWF, Aiba S-I, Brearley FQ, Cannon CH, Forshed O, Kitayama K, Nagamasu H, Nilus R, Payne J, Paoli G, Poulsen AD, Raes N, Sheil D, Sidiyasa K, Suzuki E, van Valkenburg JLCH (2010) Environmental correlates of tree biomass, basal area, wood specific gravity and stem density gradients in Borneo’s tropical forests. Glob Ecol Biogeogr 19:50–60. https://doi.org/10.1111/j.1466-8238.2009.00489.x
Stone EL, Boonkird S-A (1963) Calcium accumulation in the bark of Terminalia spp. in Thailand. Ecology 44:586–588. https://doi.org/10.2307/1932543?refreqid=search-gateway:9eb163eade8877b10909b4e6ce0166d5
Tanner E (1985) Jamaican montane forests: nutrient capital and cost of growth. J Ecol 73:553–568
Tanner E, Vitousek PM, Cuevas E (1998) Experimental investigation of nutrient limitation of forest growth on wet tropical mountains. Ecology 79:10–22
Townsend AR, Cleveland CC, Asner GP, Bustamante MMC (2007) Controls over foliar N:P ratios in tropical rain forests. Ecology 88:107–118. https://doi.org/10.2307/27651072?refreqid=search-gateway:4e458cd2cfffac311ffc4f8d7b2b6d59
Uhl C, Jordan CF (1984) Succession and nutrient dynamics following forest cutting and burning in Amazonia. Ecology 65:1476–1490
Unger M, Homeier J, Leuschner C (2013) Relationships among leaf area index, below-canopy light availability and tree diversity along a transect from tropical lowland to montane forests in NE Ecuador. Trop Ecol 54:33–45
Van Lear DH, Waide JB, Teuke MJ (1984) Biomass and nutrient content of a 41-year-old loblolly-pine (Pinus-Taeda L) plantation on a poor site in South-Carolina. For Sci 30:395–404
Vitousek PM, Sanford RL (1986) Nutrient cycling in moist tropical forest. Annu Rev Ecol Syst 17:137–167
Wang D, Bormann FH, Lugo AE, Bowden RD (1991) Comparison of nutrient-use efficiency and biomass production in five tropical tree taxa. For Ecol Manag 46:1–21. https://doi.org/10.1016/0378-1127(91)90241-m
Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten W, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633. https://doi.org/10.1126/science.1094875
Webb CO, Donoghue MJ (2005) Phylomatic: tree assembly for applied phylogenetics. Mol Ecol Notes 5:181–183
Weedon JT, Cornwell WK, Cornelissen JHC, Zanne AE, Wirth C, Coomes DA (2009) Global meta-analysis of wood decomposition rates: a role for trait variation among tree species? Ecol Lett 12:45–56. https://doi.org/10.1111/j.1461-0248.2008.01259.x
Westman WE, Rogers RV (1977) Nutrient stocks in a subtropical eucalypt forest, north Stradbroke Island. Austral Ecol 2:447–460. https://doi.org/10.1111/j.1442-9993.1977.tb01160.x
Wetzel S, Greenwood JS (1991) A survey of seasonal bark proteins in eight temperate hardwoods. Trees 5:153–157. https://doi.org/10.1007/BF00204337
Wetzel S, Demmers C, Greenwood JS (1989) Seasonally fluctuating bark proteins are a potential form of nitrogen storage in three temperate hardwoods. Planta 178:275–281. https://doi.org/10.1007/BF00391854
Whittaker RH, Woodwell GM (1969) Structure, production and diversity of the oak-pine forest at Brookhaven, New York. J Ecol 57:155. https://doi.org/10.2307/2258214
Whittaker RH, Bormann FH, Likens GE, Siccama TG (1974) The Hubbard brook ecosystem study: forest biomass and production. Ecol Monogr 44:233–254. https://doi.org/10.2307/1942313
Whittaker RH, Likens GE, Bormann FH, Easton JS, Siccama TG (1979) The Hubbard brook ecosystem study: forest nutrient cycling and element behavior. Ecology 60:203–220. https://doi.org/10.2307/1936481
Woodwell GM, Whittaker RH, Houghton RA (1975) Nutrient concentrations in plants in the Brookhaven oak-pine forest. Ecology 56:318–332. https://doi.org/10.2307/1934963?refreqid=search-gateway:adfd5665bc8a461b5e71201b47917409
Wright JS, Kitajima K, Kraft NJB et al (2010) Functional traits and the growth-mortality trade-off in tropical trees. Ecology 91:3664–3674. https://doi.org/10.1890/09-2335.1
Zanne AE, Oberle B, Dunham KM, Milo AM, Walton ML, Young DF (2015) A deteriorating state of affairs: how endogenous and exogenous factors determine plant decay rates. J Ecol 103:1421–1431. https://doi.org/10.1111/1365-2745.12474
Acknowledgements
This work was supported by National Science Foundation Integrative Graduate Education and Research Traineeship Fellowship (1069157) and the National Science Foundation Doctoral Dissertation Improvement Grant (DEB-1311379). We thank Bady Garcia and Fredy Miranda for field assistance and Charles Tam and Zhaodi Liao for lab assistance.
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Jones, J.M., Heineman, K.D. & Dalling, J.W. Soil and species effects on bark nutrient storage in a premontane tropical forest. Plant Soil 438, 347–360 (2019). https://doi.org/10.1007/s11104-019-04026-9
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DOI: https://doi.org/10.1007/s11104-019-04026-9