Abstract
Recent studies from the Hawaiian Islands showed that pedogenic thresholds demarcate domains in which rock-derived nutrient dynamics remain similar across wide variations in rainfall. These thresholds appear related to certain aspects of N cycling, but the degree to which they correspond to patterns of biological N fixation (BNF)—the dominant input of N into less-managed ecosystems—remains unclear. We measured aboveground plant biomass, foliar nutrient concentrations, and foliar δ15N along a climate gradient on ~ 150,000-year-old basaltic substrate to characterize foliar N sources and spatially relate them to soil nutrients. Patterns in legume δ15N correspond to known pedogenic thresholds along the rainfall gradient, with low δ15N values (~ 0 to − 2‰) occurring in the dry, biologically inactive domain and the wet, highly weathered domain. Elevated δ15N in the middle, fertile domain suggests a greater reliance of legumes on soil N where it has accumulated over time. Non-legume face N deficiencies throughout most of the gradient while legumes maintain low C:N ratios via symbiotic BNF. However, legume abundance declines outside the fertile domain, limiting ecosystem N inputs. Breakpoints in legume δ15N data suggest that P (and potentially other nutrients) limits BNF and, by extension, legume abundance in wet region. Nutrients may also constrain legume abundance in the dry domain, but pedogenic effects could not be isolated from climatic constraints at the dry sites. We conclude that pedogenic thresholds defined by climate can be informative of foliar δ15N patterns in cases where legumes are not directly constrained by climate, land use, or other external factors.
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Amundson R, Austin AT, Schuur EAG et al (2003) Global patterns of the isotopic composition of soil and plant nitrogen. Global Biogeochem Cycles 17:1031. https://doi.org/10.1029/2002GB001903
Arnold JD (1976) The effects of fertilizer-herbicide interaction on the control of honey mesquite (Prosopis glandulosa). PhD thesis, Texas Tech University, 82 pp
Baker PJ, Scowcroft PG, Ewel JJ (2009) Koa (Acacia koa) ecology and silviculture. USDA General Technical Report PSW-GTR-21, Albany, 129 pp
Bateman JB, Chadwick OA, Vitousek PM (2019) Quantitative analysis of pedogenic thresholds and domains in volcanic soils. Ecosystems 22:1633–1649. https://doi.org/10.1007/s10021-019-00361-1
Bordeleau LM, Prévost D (1994) Nodulation and nitrogen fixation in extreme environments. Plant Soil 161:115–125. https://doi.org/10.1007/BF02183092
Campo J, Dirzo R (2003) Leaf quality and herbivory responses to soil nutrient addition in secondary tropical dry forests of Yucatán, Mexico. J Trop Ecol 19:525–530. https://doi.org/10.1017/S0266467403003572
Canfield DE, Glazer AN, Falkowski PG (2010) The evolution and future of earth’s nitrogen cycle. Science 330:192–196. https://doi.org/10.1126/science.1186120
Chadwick OA, Chorover J (2001) The chemistry of pedogenic thresholds. Geoderma 100:321–353. https://doi.org/10.1016/S0016-7061(01)00027-1
Chadwick OA, Gavenda RT, Kelly EF et al (2003) The impact of climate on the biogeochemical functioning of volcanic soils. Chem Geol 202:195–223. https://doi.org/10.1016/j.chemgeo.2002.09.001
Chadwick OA, Kelly EF, Hotchkiss SC, Vitousek PM (2007) Precontact vegetation and soil nutrient status in the shadow of Kohala Volcano, Hawaii. Geomorphology 89:70–83. https://doi.org/10.1016/j.geomorph.2006.07.023
Chemisquy MA, Giussani LM, Scataglini MA et al (2010) Phylogenetic studies favour the unification of Pennisetum, Cenchrus and Odontelytrum (Poaceae): a combined nuclear, plastid and morphological analysis, and nomenclatural combinations in Cenchrus. Ann Bot 106:107–130. https://doi.org/10.1093/aob/mcq090
Colman RL, O’Neill GH (1978) Seasonal variation in the potential herbage production and response to nitrogen by kikuyu grass (Pennisetum clandestinum). J Agric Sci 91:81–90. https://doi.org/10.1017/S0021859600056641
Craine JM, Elmore AJ, Aidar MPM et al (2009) Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phytol 183:980–992. https://doi.org/10.1111/j.1469-8137.2009.02917.x
Craine JM, Elmore AJ, Wang L et al (2015) Convergence of soil nitrogen isotopes across global climate gradients. Sci Rep 5:8280. https://doi.org/10.1038/srep08280
Davies RB (2002) Hypothesis testing when a nuisance parameter is present only under the alternative: Linear model case. Biometrika 89:484–489. https://doi.org/10.1093/biomet/89.2.484
Dudley BD, Flint Hughes R, Ostertag R (2014) Groundwater availability mediates the ecosystem effects of an invasion of Prosopis pallida. Ecol Appl 24:1954–1971. https://doi.org/10.1890/13-1262.1
Elser JJ, Bracken MES, Cleland EE et al (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142. https://doi.org/10.1111/j.1461-0248.2007.01113.x
Evans RD (2001) Physiological mechanisms influencing plant nitrogen isotope composition. Trends Plant Sci 6:121–126. https://doi.org/10.1016/S1360-1385(01)01889-1
Gei M, Rozendaal DMA, Poorter L et al (2018) Legume abundance along successional and rainfall gradients in Neotropical forests. Nat Ecol Evol 2:1104–1111. https://doi.org/10.1038/s41559-018-0559-6
Giambelluca TW, Chen Q, Frazier AG et al (2013) Online rainfall atlas of Hawai‘i. Bull Am Meteorol Soc 94:313–316. https://doi.org/10.1175/BAMS-D-11-00228.1
Giambelluca TW, Shuai X, Barnes ML et al (2014) Evapotranspiration of Hawai‘i Final Report. US Army Corps of Engineers, Honolulu, 168 pp
Gibson A (1963) Physical environment and symbiotic nitrogen fixation. Aust J Biol Sci 18:295–310. https://doi.org/10.1071/bi9630028
Goh KM, Bruce GE (2005) Comparison of biomass production and biological nitrogen fixation of multi-species pastures (mixed herb leys) with perennial ryegrass-white clover pasture with and without irrigation in Canterbury, New Zealand. Agric Ecosyst Environ 110:230–240. https://doi.org/10.1016/j.agee.2005.04.005
Gutschick VP (1981) Evolved strategies in nitrogen acquisition by plants. Am Nat 118:607–637. https://doi.org/10.1086/283858
Hanger BC (1979) The movement of calcium in plants. Commun Soil Sci Plant Anal 10:171–193. https://doi.org/10.1080/00103627909366887
Hanselka CW, Hussey MA, Ibarra FF (2004) Buffelgrass. In: Moser LE, Burson BL, Sollenberger LE (eds) Warm-season (C4) grasses. American Society of Agronomy, Inc., Crop Science Society of America, Inc., Soil Science Society of America, Inc., Madison, pp 477–502
Houlton BZ, Sigman DM, Schuur EAG, Hedin LO (2007) A climate-driven switch in plant nitrogen acquisition within tropical forest communities. Proc Natl Acad Sci USA 104:8902–8906. https://doi.org/10.1073/pnas.0609935104
Jobbágy EG, Jackson RB (2001) The distribution of soil nutrients with depth: global patterns and the imprint of plants. Biogeochemistry 53:51–77. https://doi.org/10.1023/A:1010760720215
Kagawa AK, Vitousek PM (2012) The Ahupua‘a of Puanui: a resource for understanding Hawaiian Rain-Fed agriculture. Pacific Sci 66:161–172. https://doi.org/10.2984/66.2.6
Ladefoged TN, Graves MW (2011) The Leeward Kohala field system. In: Kirch PV (ed) Roots of conflict: soils, agriculture, and sociopolitical complexity in ancient Hawai‘i. School for Advanced Research Press, Santa Fe, pp 89–110
Ladefoged TN, Graves MW, Jennings RP (1996) Dryland agricultural expansion and intensification in Kohala, Hawai’i island. Antiquity 70:861–880. https://doi.org/10.1017/S0003598X0008412X
LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary production in terrestrial ecosystems is globally distributed. Ecology 89:371–379. https://doi.org/10.1890/06-2057.1
Lincoln N, Chadwick O, Vitousek P (2014) Indicators of soil fertility and opportunities for precontact agriculture in Kona, Hawai’i. Ecosphere 5:42. https://doi.org/10.1890/ES13-00328.1
Liu D, Zhu W, Wang X et al (2017) Abiotic versus biotic controls on soil nitrogen cycling in drylands along a 3200 km transect. Biogeosciences 14:989–1001. https://doi.org/10.5194/bg-14-989-2017
Mannetje L’t, Jones RM (1990) Pasture and animal productivity of buffel grass with Siratro, lucerne or nitrogen fertilizer. Trop Grasslands 24:269–281
Mariotti A (1983) Atmospheric nitrogen is a reliable standard for natural 15N abundance measurements. Nature 303:685–687. https://doi.org/10.1038/303685a0
Marshall K, Koseff C, Roberts AL et al (2017) Restoring people and productivity to Puanui: challenges and opportunities in the restoration of an intensive rain-fed Hawaiian field system. Ecol Soc 22:23. https://doi.org/10.5751/ES-09170-220223
Mears PT (1970) Kikuyu—(Pennisetum clandestinum) as a Pasture Grass—a review. Trop Grasslands 4:139–152
Menge DNL, Wolf AA, Funk JL (2015) Diversity of nitrogen fixation strategies in Mediterranean legumes. Nat Plants 1:15064. https://doi.org/10.1038/nplants.2015.64
Miyazawa Y, Dudley BD, Hughes RF et al (2016) Non-native tree in a dry coastal area in Hawai’i has high transpiration but restricts water use despite phreatophytic trait. Ecohydrology 9:1166–1176. https://doi.org/10.1002/eco.1715
Mo Q, Li Z, Sayer EJ et al (2019) Foliar phosphorus fractions reveal how tropical plants maintain photosynthetic rates despite low soil phosphorus availability. Funct Ecol 33:503–513. https://doi.org/10.1111/1365-2435.13252
Mueller-Dombois D (1987) Forest dynamics in Hawaii. Trends Ecol Evol 2:216–220. https://doi.org/10.1016/0169-5347(87)90024-3
Muggeo VMR (2003) Estimating regression models with unknown break-points. Stat Med 22:3055–3071. https://doi.org/10.1002/sim.1545
Muggeo VMR (2008) Segmented: an R package to fit regression models with broken-line relationships. R News 8:20–25
Muhs DR (1984) Intrinsic thresholds in soil systems. Phys Geogr 5:99–110. https://doi.org/10.1080/02723646.1984.10642246
O’Hara GW (2001) Nutritional constraints on root nodule bacteria affecting symbiotic nitrogen fixation: a review. Aust J Exp Agric 41:417–433. https://doi.org/10.1071/EA00087
Osborne CP, Sack L (2012) Evolution of C4 plants: a new hypothesis for an interaction of CO2 and water relations mediated by plant hydraulics. Philos Trans R Soc B Biol Sci 367:583–600. https://doi.org/10.1098/rstb.2011.0261
Peay KG, von Sperber C, Cardarelli E et al (2017) Convergence and contrast in the community structure of Bacteria, Fungi and Archaea along a tropical elevation–climate gradient. FEMS Microbiol Ecol 93:fix045. https://doi.org/10.1093/femsec/fix045
Price JP, Jacobi JD, Gon SM III et al (2012) Mapping Plant Species Ranges in the Hawaiian Islands: Developing a Methodology and Associated GIS Layers. USGS Open-File Report 2012–1192, Reston, 34 pp
Reed SC, Cleveland CC, Townsend AR (2011) Functional ecology of free-living nitrogen fixation: a contemporary perspective. Annu Rev Ecol Evol Syst 42:489–512. https://doi.org/10.1146/annurev-ecolsys-102710-145034
Rose TJ, Kearney LJ, Erler DV et al (2018) Influence of growth stage and seed nitrogen on B values and potential contributions to error in estimating biological N2 fixation using the 15N natural abundance method. Plant Soil 425:389–399. https://doi.org/10.1007/s11104-018-3600-2
Ruschel AP, Vose PB, Victoria RL, Salati E (1979) Comparison of isotope techniques and non-nodulating isolines to study the effect of ammonium fertilization on dinitrogen fixation in soybean, Glycine max. Plant Soil 53:513–525. https://doi.org/10.1007/BF02140722
Sandli N, Svenning MM, Røsnes K, Junttila O (1993) Effect of nitrogen supply on frost resistance, nitrogen metabolism and carbohydrate content in white clover (Trifolium repens). Physiol Plant 88:661–667. https://doi.org/10.1111/j.1399-3054.1993.tb01386.x
Schwenke TG, Kerridge PC (2000) Relative responsiveness of some tropical pasture legumes to molybdenum. Trop Grasslands 34:91–98
Shearer G, Kohl DH (1986) N2-fixation in field settings: estimations based on natural 15N abundance. Aust J Plant Physiol 13:699–756
Sheffer E, Batterman SA, Levin SA, Hedin LO (2015) Biome-scale nitrogen fixation strategies selected by climatic constraints on nitrogen cycle. Nat Plants 1:15182. https://doi.org/10.1038/nplants.2015.182
Sherrod DR, Sinton JM, Watkins SE, Brunt KM (2007) Geologic Map of the State of Hawai‘i. USGS Open-File Report 2007–1089, Reston, 83 pp
Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton
Tomonari-Tuggle MJ (1988) North Kohala: perception of a changing community, a cultural resources study. Hawaiʻi Department of Land and Natural Resources, Honolulu, 261 pp
Unkovich MJ, Pate JS, Sanford P, Armstrong EL (1994) Potential precision of the δ15N natural abundance method in field estimates of nitrogen fixation by crop and pasture legumes in south-west Australia. Aust J Agric Res 45:119–132. https://doi.org/10.1071/AR9940119
Vitousek PM, Chadwick OA (2013) Pedogenic thresholds and soil process domains in basalt-derived soils. Ecosystems 16:1379–1395. https://doi.org/10.1007/s10021-013-9690-z
Vitousek PM, Field CB (1999) Ecosystem constraints to symbiotic nitrogen fixers: a simple model and its implications. Biogeochemistry 46:179–202. https://doi.org/10.1007/978-94-011-4645-6
Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: How can it occur? Biogeochemistry 13:87–115. https://doi.org/10.1007/BF00002772
Vitousek PM, Aber JD, Howarth RH et al (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–750. https://doi.org/10.1038/nn1891
Vitousek PM, Cassman K, Cleveland C et al (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57–58:1–45. https://doi.org/10.1023/A:1015798428743
Vitousek PM, Ladefoged TN, Kirch PV et al (2004) Soils, agriculture, and society in precontact Hawaiʻi. Science 304:1665–1669. https://doi.org/10.1126/science.1099619
Vitousek PM, Menge DNL, Reed SC, Cleveland CC (2013) Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems. Philos Trans R Soc B 368:1–9. https://doi.org/10.1098/rstb.2013.0119
Vitousek P, Dixon JL, Chadwick OA (2016) Parent material and pedogenic thresholds: observations and a simple model. Biogeochemistry 130:147–157. https://doi.org/10.1007/s10533-016-0249-x
Vitousek PM, Paulus EL, Chadwick OA (2019) Nitrogen dynamics along a climate gradient on geologically old substrate, Kauaʻi, Hawaiʻi. Oecologia 189:211–219. https://doi.org/10.1007/s00442-018-4285-1
Vitousek PM, Bateman JB, Chadwick OA (2021) A “toy” model of biogeochemical dynamics on climate gradients. Biogeochemistry 154:183–210. https://doi.org/10.1007/s10533-020-00734-y
von Sperber C, Chadwick OA, Casciotti KL et al (2017) Controls of nitrogen cycling evaluated along a well-characterized climate gradient. Ecology 98:1117–1129. https://doi.org/10.1002/ecy.1751
Wang C, Wang X, Liu D et al (2014) Aridity threshold in controlling ecosystem nitrogen cycling in arid and semi-arid grasslands. Nat Commun 8:110. https://doi.org/10.1038/ncomms5799
Young J (1992) Phylogenetic classification of nitrogen-fixing organisms. In: Stacey G, Burris RH, Evans HJ (eds) Biological nitrogen fixation. Chapman and Hall Inc, New York, p 960
Acknowledgements
This work was supported by United States National Science Foundation grant ETBC1020791 to Stanford University. MWB, AEB, and CEB were supported by the Stanford Vice Provost for Undergraduate Education (VPUE) Biology and Stanford Earth Summer Undergraduate Research (SESUR) programs. MWB received additional funding from an Undergraduate Advising and Research (UAR) Small Grant and a Volpert Scholarship, both from Stanford University. We thank Isabella Badia-Bellinger, Natasha Batista, Duncan Coleman, Mark Matten, Tyler McIntosh, and Ryan Petterson for assistance in the field and Scott Fendorf for providing valuable input on the thesis from which this article was derived. Juan Lezama Pacheco, Guangchao Li, David Mucciarone, and Douglas Turner are gratefully acknowledged for their assistance with the laboratory analyses. We also thank Parker Ranch, Ponoholo Ranch, and Kamehameha Schools for access to the research sites, and the Hawai‘i Preparatory Academy for access to equipment and facilities.
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This work was funded by National Science Foundation (Grant no. ETBC1020791); Stanford University (Grant no. VPUE-2015, SESUR-2015, Volpert Scholarship)
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MWB, AEB, CEB, and PMV designed the study. All authors conducted the fieldwork. MWB, CvS, and ELP conducted the laboratory analyses. MWB analyzed the data and wrote the article with contributions from ELP, CvS, KM, and PMV.
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Communicated by Duncan Menge.
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Burnett, M.W., Bobbett, A.E., Brendel, C.E. et al. Foliar ẟ15N patterns in legumes and non-N fixers across a climate gradient, Hawaiʻi Island, USA. Oecologia 198, 229–242 (2022). https://doi.org/10.1007/s00442-021-05089-1
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DOI: https://doi.org/10.1007/s00442-021-05089-1