Nitrogen-fixing red alder trees tap rock-derived nutrients

Steven S. Perakis; Julie C. Pett-Ridge

doi:10.1073/pnas.1814782116

New Research In

Edited by Thure E. Cerling, University of Utah, Salt Lake City, UT, and approved January 9, 2019 (received for review August 29, 2018)

This article has Letters. Please see:

Do cluster roots of red alder play a role in nutrient acquisition from bedrock? - June 04, 2019
Effect of alder on soil bacteria offers an alternative explanation to the role played by alder in rock weathering - August 29, 2019

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Reply to Lambers et al.: How does nitrogen-fixing red alder eat rocks?
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- Aug 29, 2019

Significance

Tree species that form symbioses with nitrogen-fixing bacteria can naturally fertilize forests by converting atmospheric nitrogen gas into plant-available forms. However, other mineral nutrients that plants require for growth are largely locked in bedrock, and are released only slowly into soil. We used strontium isotopes to trace nutrient sources for six common tree species in a temperate rainforest, including one species from a globally widespread genus known for high rates of biological nitrogen fixation. We found that trees capable of fixing atmospheric nitrogen gas were also best able to directly access mineral nutrients from bedrock. This gives nitrogen-fixing trees the unique ability to provide the full suite of essential nutrients required to fuel growth and carbon uptake in forest ecosystems.

Abstract

Symbiotic nitrogen (N)-fixing trees supply significant N inputs to forest ecosystems, leading to increased soil fertility, forest growth, and carbon storage. Rapid growth and stoichiometric constraints of N fixers also create high demands for rock-derived nutrients such as phosphorus (P), while excess fixed N can generate acidity and accelerate leaching of rock-derived nutrients such as calcium (Ca). This ability of N-fixing trees to accelerate cycles of Ca, P, and other rock-derived nutrients has fostered speculation of a direct link between N fixation and mineral weathering in terrestrial ecosystems. However, field evidence that N-fixing trees have enhanced access to rock-derived nutrients is lacking. Here we use strontium (Sr) isotopes as a tracer of nutrient sources in a mixed-species temperate rainforest to show that N-fixing trees access more rock-derived nutrients than nonfixing trees. The N-fixing tree red alder (Alnus rubra), on average, took up 8 to 18% more rock-derived Sr than five co-occurring nonfixing tree species, including two with high requirements for rock-derived nutrients. The increased access to rock-derived nutrients occurred despite spatial variation in community‐wide Sr sources across the forest, and only N fixers had foliar Sr isotopes that differed significantly from soil exchangeable pools. We calculate that increased uptake of rock-derived nutrients by N-fixing alder requires a 64% increase in weathering supply of nutrients over nonfixing trees. These findings provide direct evidence that an N-fixing tree species can also accelerate nutrient inputs from rock weathering, thus increasing supplies of multiple nutrients that limit carbon uptake and storage in forest ecosystems.

Trees can accelerate mineral weathering in soil and the release of essential nutrients from bedrock into ecosystems. There are many ways that trees promote weathering: by anchoring soils, by altering hydrologic cycling, by secreting organic acids and chelating agents, by reducing pH around root hairs, and by stimulating production of carbonic acid from root respiration and organic matter decomposition (1 ⇓–3). All essential nutrients that trees require can be provided by mineral weathering, including nitrogen (N) in some geologic settings (4). Typically, however, most N inputs to ecosystems originate from biological fixation and atmospheric deposition (5). Consequently, couplings between plant N nutrition and mineral weathering remain largely speculative (6, 7). Understanding links between plant N nutrition and mineral weathering could contribute to climate, food, fiber, and soil security while minimizing release of excess N to the environment (8).

Nitrogen is the nutrient that most commonly limits tree growth, soil fertility, and carbon (C) storage in forests worldwide (5, 9, 10). Nitrogen limitation occurs due to a combination of low N inputs relative to annual plant demands, and persistent N losses that constrain N accumulation and availability in soil (4 ⇓⇓–7). Nitrogen input from biological N fixation converts inert atmospheric N₂ gas into biologically available N in ecosystems. This evolutionary adaption to low N availability can eliminate N limitation in individual organisms, but less frequently eliminates community-wide N limitation (5, 11). An exception to this can occur in symbioses where woody plants support N-fixing bacteria in root nodules (hereafter “N fixers”). These symbioses can in some cases support exceptionally high rates of N fixation that exceed host plant N requirements, leading to excess N supply and community-wide N sufficiency that shifts nutrient limitation away from N toward other nutrients such as P and Ca (12, 13).

Non-N mineral nutrients such as P and Ca are taken up by plants from soil, yet are supplied ultimately to ecosystems by atmospheric deposition and bedrock weathering (5 ⇓–7, 12, 14). Atmospheric deposition typically provides most non-N nutrients only sparingly relative to potential inputs from bedrock. As a result, non-N mineral nutrients are often considered “rock-derived,” and their availability depends on internal ecosystem processes that influence weathering inputs. Both plant (1 ⇓–3) and microbial (15, 16) processes can accelerate mineral weathering in ecosystems, including several pathways that involve combined effects of plants and microbes (15 ⇓⇓–18). In forests, there is particular interest in whether certain classes of trees or mycorrhizal symbioses can accelerate weathering and uptake of rock-derived nutrients (17, 18). Early syntheses of terrestrial biogeochemistry theorized that symbiotic N-fixing trees may be one class of plant−microbial symbioses that can accelerate mineral weathering to release P and metallic cations for biotic uptake (6, 7). If true, such a role would place N fixers at a nexus of ecosystem nutrient sourcing, with potential for feedbacks between fixed N and rock-derived nutrients that regulate soil fertility, plant growth, and ecosystem C storage.

We used radiogenic Sr isotopes, ⁸⁷Sr/⁸⁶Sr (14, 18 ⇓–20), to identify nutrient sources for six codominant tree species in a temperate rainforest in Oregon. Our prior work in this region established two distinct and well-constrained end-members of potential Sr sources to forests: atmospheric inputs of Sr from the nearby Pacific Ocean and mineral weathering inputs of rock-derived Sr from local basalt (20). These two sources are equally important, on average, in supplying Sr to forest ecosystems across the region (average rock-derived Sr = 48% of total, range = 14 to 90%, SE = 8, n = 11; ref. 20). However, potential differences among dominant tree species in Sr sources within these forests have not been examined. By comparing Sr isotopes in foliage to known end-members, we determined the proportions of atmospheric vs. rock-derived nutrient sources taken up by individual trees in mixed-species plots. We established six replicate study plots across a 15-ha study forest, with each plot containing all six tree species within a <0.1-ha area. The species consisted of one actinorhizal N-fixing angiosperm that also forms symbioses with ectomycorrhizal fungi, one additional nonfixing angiosperm with arbuscular mycorrhizae, three nonfixing gymnosperms with ectomycorrhizae, and one nonfixing gymnosperm with arbuscular mycorrhizae (Table 1). The soil has high N levels (Table 2) typical of the region, and which lead to incipient Ca and P limitation of forest growth (13). Naturally high N availability in these forests shapes nutrient cycles in a manner similar to high inputs of N from anthropogenic deposition (21, 22), and provides context for broader identification of how ecosystem N enrichment alters cycles of rock-derived nutrients.

View this table:

Table 1.

Tree species characteristics and foliar chemical and isotopic values in a temperate rainforest

View this table:

Table 2.

Mineral soil (0 cm to 10 cm) properties across the forest

Results and Discussion

We found that N-fixing red alder trees (species code ALRU) obtained significantly more rock-derived Sr than all five codominant nonfixing trees in this mixed temperate rainforest (ANOVA, P < 0.001). In a two-source mixing calculation comparing atmospheric vs. bedrock Sr contributions (Methods and Eq. 1), N-fixing alder displayed a bedrock source of Sr (average = 66% bedrock-derived Sr, SE = 4%) that averaged 8 to 18% greater than nonfixing tree species (range: 48 to 58%; Fig. 1A). Similar calculations to determine Ca sources using Sr isotopes and end-member Ca/Sr ratios likewise suggest that N-fixing red alder relied 7 to 16% more on rock-derived Ca (average = 77%, SE = 3%) than nonfixing tree species (average = 67%, range: 61 to 70%; Fig. 1B). These Ca source calculations are unaffected by Ca/Sr fractionation during biological uptake (Methods, Eq. 2, and ref. 19). Our measured species differences in Sr and Ca sources likely underestimate true differences, due to lateral litterfall mixing and nutrient recycling among neighboring trees (23). Our findings broaden the current view of how symbiotic N-fixing trees influence ecosystem nutrient inputs, from a focus on increased N supply (5, 9 ⇓⇓–12), to a recognition that N fixers can also accelerate nutrient inputs from rock weathering.

Fig. 1.

Percent rock-derived (A) Sr and (B) Ca in six tree species in a mixed-species temperate rainforest. Values are determined from two end-member mixing calculations that partition atmospheric and rock-derived sources (Sr, Eq. 1; Ca, Eq. 2). Tree species values are means and SEs from six mixed-species plots. Asterisks indicate that rock-derived nutrient sources are significantly greater in ALRU (N-fixing red alder) and significantly lower in TSHE (western hemlock) compared with other tree species (P < 0.001). Shaded areas span the full range of rock-derived Sr and Ca sources measured in the mineral soil exchangeable pool across the forest. See Table 1 for species codes.

Spatial variability in bedrock Sr inputs across landscape positions can obscure tree species differences in Sr sources (24). We observed significant spatial variability in Sr sources across the forest (ANOVA, P < 0.001), with average values of rock-derived Sr ranging from 44 to 64% among mixed-species plots. This 20% range in Sr sources due to spatial variability among plots was comparable to the 18% range observed among tree species. Despite these significant sources of variability, most individual tree species displayed Sr source patterns that tracked co-occurring species across the forest (Fig. 2A, P < 0.05 for all species except Sitka spruce). This tracking among tree species implies a coherent community-level shift in plant nutrient sources in response to spatial variation in bedrock Sr inputs. As the tree community shifted its Sr sources across the site, however, it maintained consistent rankings of tree species reliance on rock-derived Sr, with N-fixing alder relying most on rock-derived Sr in five of six mixed-species plots, and nonfixing western hemlock (species code TSHE) relying least on rock-derived Sr in all six plots (Fig. 2B). These consistent rankings highlight distinct species-level strategies of nutrient acquisition, particularly for N-fixing alder and nonfixing hemlock, that are maintained across spatial variation in forest Sr sources.

Fig. 2.

Percent rock-derived Sr and Sr isotope values for individual trees (A) regressed against the mean % rock-derived Sr of all other species in each plot and (B) compared among species in each plot. In A, solid lines show linear regressions for ACMA, ALRU, PSME, THPL, and TSHE (all P < 0.05), indicating coherent tracking in Sr sources across the forest. In B, lines connect species across mixed-species plots, and the average of all six species is shown, as are individual mineral soil exchangeable Sr isotope values (n = 8) from a transect across the site.

Comparison of Sr isotopes in plants and soil exchangeable pools further reveals a distinct strategy of nutrient acquisition in N-fixing red alder that is targeted to uptake of rock-derived nutrients. The largest immediate source of “plant available” base cation nutrients in forests typically occurs in the soil exchangeable pool, a loosely held reservoir where nutrients are recycled before plant uptake (25). In the forests studied here, the soil exchangeable pool of Sr is well mixed and biologically available, displays negligible Sr isotope variation with depth, and covaries closely with foliar Sr isotopes across a wide range of site conditions and soil fertility (slope = 1.03, r² = 0.97, n = 22; ref. 20). Similarly, all species of nonfixers that we examined exhibited considerable overlap of foliage with soil exchangeable Sr isotope values (Fig. 2B). This overlap is typical in forests and highlights the important role of nutrient recycling within ecosystems in supplying nutrients to trees (5 ⇓–7, 18). In contrast, N-fixing red alder was the only tree species whose foliage differed significantly from soil exchangeable Sr isotope values (Fig. 2B; ANOVA, P < 0.05). Red alder foliage was instead biased toward the signature of mineral weathering, implying direct uptake of rock-derived nutrients. This diminished dependence on soil exchangeable Sr, in combination with red alder’s distinct foliar Sr isotope values compared with other species, provides field evidence that N fixers can directly access rock-derived nutrients. By both fixing atmospheric N and taking up nutrients directly from mineral weathering, N fixers may therefore short-circuit the usual reliance of trees on internally recycled nutrients in forests.

The most likely mechanism for a stronger signal of rock-derived Sr in N-fixing alder is increased mineral weathering in the rooting zone caused by nitric acid. Acids often enhance mineral weathering and mobilize rock-derived nutrients in soil (1 ⇓–3, 26), but may or may not alter soil pH depending on the acid buffering status (27). The generation of nitric acid in soil under red alder results from very high rates of N fixation relative to demands (28 ⇓–30). This leads to excess soil N as ammonium that is oxidized by soil microorganisms during nitrification to nitrate and acidic protons (i.e., nitric acid). Excess N from biological fixation, atmospheric deposition, and agricultural fertilization can all produce nitric acid. Nitric acid is a strong acid compared with carbonic and organic acid weathering agents (1 ⇓–3, 15 ⇓–17, 29), and is very effective at mobilizing exchangeable soil cations (e.g., Sr and Ca) and stimulating coupled cation and nitrate leaching (20 ⇓–22, 29, 30), as well as enhancing mineral dissolution (31). However, without isotopic tracers, it can be difficult to resolve whether acids mobilize cations from the soil exchangeable pool vs. stimulate mineral weathering (18, 29 ⇓⇓⇓–33). Our Sr isotope evidence that N-fixing alder directly accesses rock-derived nutrients implicates enhanced mineral weathering in the rooting zone of trees. The mineral weathering likely occurs on minerals mixed throughout soil rather than unweathered bedrock at depth, because rooting depths are consistently shallow (<1 m deep; refs. 34 ⇓–36) compared with the depth of fresh competent bedrock (>8 m; ref. 20).

Other possible causes of greater uptake of rock-derived Sr in N-fixing alder have less support. We excluded the possibility that N fixers occupied areas with intrinsically high rock-derived Sr by sampling mixed plots containing all focal tree species across a heterogeneous forest (Fig. 2). Mineral soil rooting depths of our study species are generally shallow (<1 m) and overlapping (34 ⇓–36), and occupy a zone where soil exchangeable Sr isotopes display negligible depth variation (20). Ectomycorrhizal fungi can enhance mineral weathering in some tree species (16 ⇓–18), but this effect is equivocal in alder (37). Furthermore, ectomycorrhizae were not unique to alder, as four of the six tree species studied support ectomycorrhizae, including western hemlock that relied more on atmospheric Sr (Table 1). The divergence in Sr sources between western hemlock and red alder is notable because both species produce highly acidic organic matter (35) that could promote weathering. Western hemlock’s weaker signal of weatherable Sr may reflect some uptake of atmospheric Sr from surface organic soil (36) as well as low weathering rates in mineral soil due to a lack of nitric acid generation (38). Finally, we are unaware of evidence that N-fixing trees directly exude more organic acids for mineral weathering compared with nonfixers, although such a mechanism could complement nitric acid weathering. We note, however, that exudate production from live N-fixing trees would be only transient compared with long-term legacies of soil N saturation that sustain excess nitrification and nitric acid generation across this landscape (20−22).

Our findings shed light on how N-fixing alder accelerates mineral weathering in the rooting zone to increase nutrient supply in our forests. By coupling Sr isotope data of foliage, bedrock, and atmospheric deposition to rates of atmospheric Sr input in mass balance calculations (Methods and Eq. 3), we find that N-fixing alder accelerates mineral weathering input of nutrients by 64% compared with nonfixing trees. This input flux is limited only to the rooting zone of soil, whereas larger-scale weathering fluxes that supply stream export are not addressed in our study. The substantial increase in mineral weathering by N-fixing alder helps explain how this species takes up 65% more P and 200% more Ca than nonfixing Douglas-fir (9). Enhanced access to P is most likely important to N fixers (5, 12), and is used to increase photosynthetic tissue mass and N-fixing nodule production to support growth (39). Strontium is only an indirect tracer of P (14, 40), but can directly trace Ca (14, 18 ⇓⇓–21). Ecosystem supplies of both P and Ca can limit nonfixer tree growth where N is abundant (12, 41), including in our forests (13). Alder-enhanced uptake of rock-derived Ca and its subsequent redistribution via litterfall may especially benefit bigleaf maple and western redcedar, two nonfixers with consistently high Ca demands (42) that have limited direct access to rock-derived nutrients.

Over long-term soil development, high rates of mineral weathering and solute mobilization can accelerate the pace at which forest ecosystems move through soil process domains. Work along climate gradients has elucidated clear thresholds of soil chemical change, wherein rainfall amount defines distinct domains of relatively stable soil properties (27, 43). Forest soils across our region display a similar nonlinear threshold of base cation depletion as a function of soil N, spanning a well-buffered domain of base-rich soil under low N conditions that changes sharply in N-rich sites to an acidified and poorly buffered domain depleted of weatherable base cations (20, 21). These changes due to soil N are caused ultimately by long-term N inputs from red alder. This N-fixing tree belongs to a widespread genus (Alnus spp) that spans boreal, temperate, and montane tropical regions, and consistently hosts symbiotic bacteria that carry out biological N fixation (44). High soil N in the region that we studied is maintained over millennia by wildfire disturbances that permit alder colonization and N fixation, even when N is not a limiting nutrient (28, 45). The result is sustained soil N saturation that continues to acidify soil and leach base cations even when N-fixing alder is no longer present (22), eventually leading to irreversible depletion of parent rock Ca from soil (20). Such long-term shifts in soil process domains due to excess N further implicate nitric acid generation as a key driver of enhanced mineral weathering in the rooting zone. Where persistent and irreversible depletion of rock-derived nutrients occurs, forests must shift to depend on atmospheric nutrient inputs to sustain primary productivity (14, 20).

Our finding that an N-fixing tree species can directly access rock-derived nutrients has implications for nutrient supplies that regulate tree growth and C uptake in forests. Inputs of fixed N can increase tree growth in N-limited forests (9 ⇓–11), and could be further stimulated by access to rock-derived nutrients (5, 12, 28, 39). Where N is already abundant and other nutrients are limiting, supplies of rock-derived nutrients can be even more important to forest growth and C uptake (5, 12 ⇓–14, 41). It is presently unknown whether high rates of N fixation by trees are geographically widespread (10 ⇓–12), and whether N fixers other than red alder can similarly access rock-derived nutrients. Our suggestion that excess N fixation and nitric acid production can release rock-derived nutrients in forests is analogous to high rates of N fertilization that cause nitric acid-driven weathering in agricultural systems (31, 32). Resolving these interactions more broadly in forests requires new understanding to distinguish N fixers like red alder that routinely fix excess N, from species that down-regulate N fixation when soil N is abundant (11).

Methods

Field Site and Sample Collection.

We studied a mixed-species temperate rainforest in the Tillamook State Forest of the north central Oregon Coast Range (45°38′38.46″N, 123°47′51.51″W). The climate has cool wet winters and warm dry summers, with mean annual temperature of 9.4 °C and mean annual precipitation of 352 cm (46). The site is in the low-elevation Sitka spruce forest zone, which is among the most productive forest types worldwide, with exceptionally high plant and soil C storage potential (47). Soils developed from the Tillamook formation of basalt bedrock and are classified as Typic Fulvudands. The soils have high concentrations of total N and low exchangeable Ca (Table 2), which is typical of the broader study area (9, 13, 20 ⇓–22) reflecting long-term legacies of N fixation (45).

We sampled a forest ∼80 y of age, in which trees established naturally after stand-replacing wildfire in 1933. Inspection of the field site and records from the Oregon Department of Forestry indicate that the site has been undisturbed since establishment. The forest has a closed canopy structure and well-integrated mixture of six tree species that codominate in the region. This codominance reflects a diverse availability of seed sources after disturbance, although differences in shade tolerance and longevity will filter species through succession (47). The species we examined include the evergreen conifers Sitka spruce (Picea sitchensis), Douglas-fir (Pseudotsuga menziesii), western hemlock (Tsuga heterophylla), and western redcedar (Thuja plicata) and the deciduous broadleaf trees bigleaf maple (Acer macrophyllum) and symbiotic N-fixing red alder (Alnus rubra).

We established six replicate study plots spanning midslope to upslope across a 15-ha area. Each plot contained a mixture of all six codominant tree species within a 0.1-ha area. We sampled sun foliage using a shotgun from three positions around the canopy of each tree, and composited these into one sample per species per plot. We sampled surface mineral soil (0 cm to 10 cm) using a 6.8-cm-diameter corer in eight locations on a transect bisecting the site.

Sample Processing and Analysis.

Field moist soil pH was determined in a 2:1 mixture of soil and deionized water after 30 min equilibration. Field moist soil was extracted for exchangeable Ca, Sr, Mg, K, and Na using 5 g of soil shaken for 30 min with 25 mL of unbuffered 1M NH₄OAc, then filtered through a 0.45-µm Aerodisk PES membrane. Soil moisture was determined by drying at 105 °C for 48 h. Subsamples of foliage and soil were dried at 65 °C for 48 h and ground to fine powder using an agate ball mill before analysis.

Foliage and soil were analyzed for total C and N on a Costech ECS-4010 combustion analyzer at the USGS Forest and Rangeland Ecosystem Science Center, and, for δ¹³C and δ¹⁵N, on a PDZ Europa 20-20 isotope ratio mass spectrometer at the University of California, Davis Stable Isotope Facility. Foliage Ca, Sr, Mg, K, and P was processed with nitric acid microwave digestion. Foliage digests and soil exchangeable nutrients were analyzed using inductively coupled plasma optical emission spectrometry at the W. M. Keck Collaboratory at Oregon State University. Based on repeat analyses of standard reference materials, uncertainty for C was 1.5%, for N was 2.7%, for δ¹³C was 0.2‰, for δ¹⁵N was 0.3‰, and for Ca, Sr, Mg, K, and P was less than 5%.

Strontium isotopes (⁸⁷Sr/⁸⁶Sr) in foliage and soil exchangeable fractions were determined by purifying 30 ng of Sr using 1.8 mL of Eichrom AG50W-X8 (H⁺ form) cation resin followed by 50 µL of Eichrom Sr-Spec resin. Isotopic measurements were made on a Nu Plasma multicollector inductively coupled plasma mass spectrometer at the W. M. Keck Collaboratory at Oregon State University. Masses 83 to 88 were monitored in static collection mode. Masses 83 and 85 were monitored for Kr (blank only) and Rb (standards and samples) interferences. Sr isotope ratios were measured 40 times per sample and have analytical uncertainties of <0.000020. Reported values are corrected to ⁸⁶Sr/⁸⁸Sr = 0.1194 and Sr standard NBS-987 ⁸⁷Sr/⁸⁶Sr = 0.710245. This instrument measured an average value of 0.70818 and a 2σ = 0.000045 for an in-house standard (EMD Millipore) (n = 205) over the duration that samples were run.

Strontium Isotope Mixing Calculations.

An extensive study of 22 forests across the region found, previously, that ecosystem inputs of Sr and Ca were dominated by two distinct sources: atmospheric inputs from sea salt aerosols in rainwater and mineral weathering inputs from bedrock (20). That study measured end-member values of atmospheric inputs for ⁸⁷Sr/⁸⁶Sr of 0.70916 and Ca/Sr_(molar) of 138.87, and of mineral weathering of Tillamook Formation basalt from 1 M HNO₃ leaches of fresh bedrock for ⁸⁷Sr/⁸⁶Sr of 0.70374 and Ca/Sr_(molar) of 236.30 (20). This well-constrained, two-component system permits the use of standard equations to partition Sr and Ca in foliage and soil exchangeable pools into contributions from atmospheric versus rock-derived sources (19). We calculated the fractional contribution of rock-derived Sr to foliage and soil exchangeable pools usingfrock,Sr=(S87rS86r)mix−(S87rS86r)atm(S87rS86r)rock−(S87rS86r)atm,[1]

where (⁸⁷Sr/⁸⁶Sr)_mix is the Sr isotope ratio of foliage or soil exchangeable pools, (⁸⁷Sr/⁸⁶Sr)_rock is the Sr isotope ratio of 1 M HNO₃ bedrock leachate, and (⁸⁷Sr/⁸⁶Sr)_atm is the Sr isotope ratio of rainfall. Our primary inferences regarding tree species access to rock-derived nutrients rely on Eq. 1. Tracing Ca dynamics with Sr isotopes requires modification of Eq. 1 to include molar Sr/Ca ratios of end-members (19), yielding the mass fraction of rock-derived Ca in foliage or soil exchangeable pools, as infrock,Ca=[(S87rS86r)mix−(S87rS86r)atm]∗(SrCa)atm[(S87rS86r)mix−(S87rS86r)atm]∗(SrCa)atm−[(S87rS86r)rock−(S87rS86r)mix]∗(SrCa)rock.[2]

This calculation of % rock-derived Ca uses Sr/Ca ratios of atmospheric deposition and weathering, but does not use Sr/Ca ratios of the mixture (i.e., foliage or soil exchangeable pool). This calculation is therefore unaffected by biological processes that discriminate between Ca and Sr (19). Biological processes do not discriminate appreciably between ⁸⁷Sr and ⁸⁶Sr, and what little fractionation may occur is corrected during the mass spectrometer bias correction. Substitution of ⁸⁷Sr/⁸⁶Sr and Sr/Ca values from whole-rock digests instead of nitric acid leaches of bedrock in Eqs. 1 and 2 yields roughly 2% more rock-derived Sr and Ca, with no change in patterns among species.

We calculated weathering rates under N-fixing and nonfixing species usingInputweathering=((S87rS86ratm−S87rS86rfoliage)Inputatm)(S87rS86rfoliage−S87rS86rrock),[3]

where Inputatm is the Sr flux of atmospheric inputs, estimated at 0.33 mol⋅ha⁻¹⋅y⁻¹ Sr based on 350 cm⋅y⁻¹ mean annual precipitation and measured precipitation chemistry (20, 46, 48). The average ⁸⁷Sr/⁸⁶Sr of atmospheric inputs is 0.70916 (SE = 0.00005, n = 3; compare with seawater = 0.70917), and the average ⁸⁷Sr/⁸⁶Sr of 1 M HNO₃ leachates of fresh Tillamook formation rocks is 0.70374 (SE = 0.00007, n = 5) (20). This yields an average weathering rate for our five nonfixing species of 0.397 mol Sr⋅ha⁻¹⋅y⁻¹ and, for N-fixing red alder, of 0.650 mol Sr⋅ha⁻¹⋅y⁻¹, leading to 64% higher weathering rates under alder. These Sr isotope-based weathering rates represent the input of Sr from basalt minerals to the biologically cycled pool of Sr, consisting of soil exchangeable cations in the rooting zone plus plant biomass. This calculated weathering flux represents a supply from weathering to the trees, and is limited to the rooting zone ∼1 m deep at our site. Consequently, this rooting zone weathering input flux is not directly comparable to a landscape-scale weathering output flux. Sr isotopes do not fractionate during weathering, and, in basalt, ions such as Sr²⁺, Ca²⁺, and HCO₃⁻ are released congruently with the dissolution of major phases such as olivine, plagioclase, pyroxene, and volcanic glass. The differences in both ⁸⁷Sr/⁸⁶Sr signatures and weathering rates among major mineral phases in basalt are negligible in the context of the range of values observed in most ecosystem studies (19). This well‐constrained behavior of Sr isotopes during basalt weathering permits insights not possible in more heterogeneous types of bedrock.

Statistical Analyses.

We tested for differences among tree species in foliar chemistry, isotopes, and % rock-derived Sr and Ca using ANOVA blocked by plot, with Tukey B post hoc comparisons. Community-level tracking in % rock-derived Sr among tree species was evaluated using least-squares linear regression. Significance was set at P ≤ 0.05. Analyses were performed using SYSTAT v13.

Acknowledgments

We thank April Strid, Kecia Jones, Haley Casebier, Chris Catricala, Valerie Maule, George Pope, Collin Ruark, and Brian Haley for field and laboratory assistance; Stephen Porder and Jana Compton for manuscript comments; and the Oregon Department of Forestry for site access. Support was provided by National Science Foundation Grants DEB-1457650 (to S.S.P.) and EAR-1053470 (to J.C.P.-R.). Any use of trade names does not imply endorsement by the US government.

Footnotes

↵¹To whom correspondence should be addressed. Email: sperakis{at}usgs.gov.

Author contributions: S.S.P. and J.C.P.-R. designed research, performed research, analyzed data, and wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1814782116/-/DCSupplemental.

Published under the PNAS license.

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(2010) Terrestrial phosphorus limitation: Mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20:5–15.
OpenUrl
↵
1. Mainwaring DB,
2. Maguire DA,
3. Perakis SS
(2014) Three-year growth response of young Douglas-fir to nitrogen, calcium, phosphorus, and blended fertilizers in Oregon and Washington. For Ecol Manage 327:178–188.
OpenUrl CrossRef
↵
1. Chadwick OA,
2. Derry LA,
3. Vitousek PM,
4. Huebert BJ,
5. Hedin LO
(1999) Changing sources of nutrients during four million years of ecosystem development. Nature 397:491–497.
OpenUrl CrossRef
↵
1. Uroz S,
2. Calvaruso C,
3. Turpault MP,
4. Frey-Klett P
(2009) Mineral weathering by bacteria: Ecology, actors and mechanisms. Trends Microbiol 17:378–387.
OpenUrl CrossRef PubMed
↵
1. Hoffland E, et al.
(2004) The role of fungi in weathering. Front Ecol Environ 5:258–264.
OpenUrl
↵
1. Quirk J, et al.
(2012) Evolution of trees and mycorrhizal fungi intensifies silicate mineral weathering. Biol Lett 8:1006–1011.
OpenUrl CrossRef PubMed
↵
1. Blum JD, et al.
(2002) Mycorrhizal weathering of apatite as an important calcium source in base-poor forest ecosystems. Nature 417:729–731.
OpenUrl CrossRef PubMed
↵
1. Capo RC,
2. Stewart BW,
3. Chadwick OA
(1998) Strontium isotopes as tracers of ecosystem processes: Theory and methods. Geoderma 82:197–225.
OpenUrl CrossRef
↵
1. Hynicka JD,
2. Pett-Ridge JC,
3. Perakis SS
(2016) Nitrogen enrichment regulates calcium sources in forests. Glob Change Biol 22:4067–4079.
OpenUrl
↵
1. Perakis SS, et al.
(2006) Coupled nitrogen and calcium cycles in forests of the Oregon Coast Range. Ecosystems 9:63–74.
OpenUrl CrossRef
↵
1. Perakis SS,
2. Sinkhorn ER
(2011) Biogeochemistry of a temperate forest nitrogen gradient. Ecology 92:1481–1491.
OpenUrl PubMed
↵
1. Waring BG, et al.
(2015) Pervasive and strong effects of plants on soil chemistry: A meta-analysis of individual plant ‘Zinke’ effects. Proc Biol Sci 282:20151001.
OpenUrl CrossRef PubMed
↵
1. Meek K,
2. Derry L,
3. Sparks J,
4. Cathles L
(2016) ⁸⁷Sr/⁸⁶Sr, Ca/Sr, and Ge/Si ratios as tracers of solute sources and biogeochemical cycling at a temperate forested shale catchment, central Pennsylvania, USA. Chem Geol 445:84–102.
OpenUrl
↵
1. Bormann FH,
2. Likens GE
(1967) Nutrient cycling. Science 155:424–429.
OpenUrl Abstract/FREE Full Text
↵
1. Hartmann J, et al.
(2013) Enhanced chemical weathering as a geoengineering strategy to reduce atmospheric carbon dioxide, supply nutrients, and mitigate ocean acidification. Rev Geophys 51:113–149.
OpenUrl
↵
1. Vitousek PM,
2. Chadwick OA
(2013) Pedogenic thresholds and soil process domains in basalt-derived soils. Ecosystems 16:1379–1395.
OpenUrl CrossRef
↵
1. Hibbs DE,
2. DeBell DS,
3. Tarrant RF
1. Binkley D,
2. Cromack K Jr,
3. Baker DD
(1994) Nitrogen fixation by red alder: Biology, rates, and controls. The Biology and Management of Red Alder, eds Hibbs DE, DeBell DS, Tarrant RF (Oregon State Univ Press, Corvallis, OR), pp 57–72.
↵
1. Homann PS,
2. Van Miegroet H,
3. Cole DW,
4. Wolfe GV
(1992) Cation distribution, cycling, and removal from mineral soil in Douglas-fir and red alder forests. Biogeochemistry 16:121–150.
OpenUrl
↵
1. Compton JE,
2. Church MR,
3. Larned ST,
4. Hogsett WE
(2003) Nitrogen export from forested watersheds in the Oregon Coast Range: The role of N₂-fixing red alder. Ecosystems 6:773–785.
OpenUrl CrossRef
↵
1. Pierson-Wickmann AC, et al.
(2009) High chemical weathering rates in first-order granitic catchments induced by agricultural stress. Chem Geol 265:369–380.
OpenUrl CrossRef
↵
1. Perrin AS,
2. Probst A,
3. Probst JL
(2008) Impact of nitrogenous fertilizers on carbonate dissolution in small agricultural catchments: Implications for weathering CO₂ uptake at regional and global scales. Geochim Cosmochim Acta 72:3105–3123.
OpenUrl
↵
1. Watmough SA, et al.
(2005) Sulphate, nitrogen and base cation budgets at 21 forested catchments in Canada, the United States and Europe. Environ Monit Assess 109:1–36.
OpenUrl CrossRef PubMed
↵
1. Smith JHG
(1964) Root spread can be estimated from crown width of Douglas fir, lodgepole pine, and other British Columbia tree species. For Chron 40:456–473.
OpenUrl
↵
1. Burns RM,
2. Honkala BH
(1990) Silvics of North America. Agriculture Handbook (USDA Forest Serv, Washington, DC), Vol 654.
↵
1. Eis S
(1974) Root system morphology of western hemlock, western red cedar, and Douglas-fir. Can J Res 4:28–38.
OpenUrl
↵
1. Yamanaka T,
2. Li CY,
3. Bormann BT,
4. Okabe H
(2003) Tripartite associations in an alder: Effects of Frankia and Alpova diplophloeus on the growth, nitrogen fixation and mineral acquisition of Alnus tenuifolia. Plant Soil 254:179–186.
OpenUrl CrossRef
↵
1. Turner DP,
2. Franz EH
(1985) The influence of western hemlock and western redcedar on microbial numbers, nitrogen, and nitrification. Plant Soil 88:259–267.
OpenUrl
↵
1. Uliassi DD,
2. Ruess RW
(2002) Limitations to symbiotic nitrogen fixation in primary succession on the Tanana River floodplain. Ecology 83:88–103.
OpenUrl CrossRef
↵
1. Pett-Ridge JC
(2009) Contributions of dust to phosphorus cycling in tropical forests of the Luquillo Mountains, Puerto Rico. Biogeochemistry 94:63–80.
OpenUrl
↵
1. Vadeboncoeur MA
(2010) Meta-analysis of fertilization experiments indicates multiple limiting nutrients in northeastern deciduous forests. Can J Res 40:1766–1780.
OpenUrl
↵
1. Cross A,
2. Perakis SS
(2010) Tree species and soil nutrient profiles in old-growth forests of the Oregon Coast Range. Can J Res 41:195–210.
OpenUrl
↵
1. Dixon JL,
2. Chadwick OA,
3. Vitousek PM
(2016) Climate‐driven thresholds for chemical weathering in postglacial soils of New Zealand. J Geophys Res Earth Surf 121:1619–1634.
OpenUrl
↵
1. Põlme S,
2. Bahram M,
3. Kõljalg U,
4. Tedersoo L
(2014) Global biogeography of Alnus-associated Frankia actinobacteria. New Phytol 204:979–988.
OpenUrl CrossRef
↵
1. Perakis SS,
2. Sinkhorn ER,
3. Compton JE
(2011) δ¹⁵N constraints on long-term nitrogen balances in temperate forests. Oecologia 167:793–807.
OpenUrl CrossRef PubMed
↵
1. Wang T,
2. Hamann A,
3. Spittlehouse D,
4. Carroll C
(2016) Locally downscaled and spatially customizable climate data for historical and future periods for North America. PLoS One 11:e0156720.
OpenUrl CrossRef
↵
1. Franklin JF,
2. Dyrness CT
(1988) Natural Vegetation of Oregon and Washington (Oregon State Univ Press, Corvallis, OR).
↵
1. National Atmospheric Deposition Program
(2014) National Atmospheric Deposition Program (NRSP-3). Available at nadp.slh.wisc.edu/data/sites/siteDetails.aspx?net=NTN&id=OR02. Accessed June 27, 2013.

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Proceedings of the National Academy of Sciences: 116 (11)

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Article Classifications

Biological Sciences
Ecology

[1] ↵
Kelly EF,
Chadwick OA,
Hilinski TE
(1998) The effect of plants on mineral weathering. Biogeochemistry 42:21–53.
OpenUrl CrossRef

[2] Kelly EF,

[3] Chadwick OA,

[4] Hilinski TE

[5] ↵
Moulton KL,
West J,
Berner RA
(2000) Solute flux and mineral mass balance approaches to the quantification of plant effects on silicate weathering. Am J Sci 300:539–570.
OpenUrl Abstract/FREE Full Text

[6] Moulton KL,

[7] West J,

[8] Berner RA

[9] ↵
Pawlik Ł,
Phillips JD,
Šamonil P
(2016) Roots, rock, and regolith: Biomechanical and biochemical weathering by trees and its impact on hillslopes—A critical literature review. Earth Sci Rev 159:142–159.
OpenUrl

[10] Pawlik Ł,

[11] Phillips JD,

[12] Šamonil P

[13] ↵
Houlton BZ,
Morford SL,
Dahlgren RA
(2018) Convergent evidence for widespread rock nitrogen sources in Earth’s surface environment. Science 360:58–62.
OpenUrl Abstract/FREE Full Text

[14] Houlton BZ,

[15] Morford SL,

[16] Dahlgren RA

[17] ↵
Vitousek PM,
Howarth RW
(1991) Nitrogen limitation on land and in the sea: How can it occur? Biogeochemistry 13:87–115.
OpenUrl CrossRef

[18] Vitousek PM,

[19] Howarth RW

[20] ↵
Gorham E,
Vitousek PM,
Reiners WA
(1979) The regulation of chemical budgets over the course of terrestrial ecosystem succession. Annu Rev Ecol Syst 10:53–84.
OpenUrl CrossRef

[21] Gorham E,

[22] Vitousek PM,

[23] Reiners WA

[24] ↵
Clark FE,
Roswall T
Reiners WA
(1981) Nitrogen cycling in relation to ecosystem succession. Terrestrial Nitrogen Cycles: Processes, Ecosystem Strategies, and Management Impacts, eds Clark FE, Roswall T (Ecol Bull, Stockholm), pp 507–528.

[25] Clark FE,

[26] Roswall T

[27] Reiners WA

[28] ↵
Beerling DJ, et al.
(2018) Farming with crops and rocks to address global climate, food and soil security. Nat Plants 4:138–147.
OpenUrl

[29] Beerling DJ, et al.

[30] ↵
Binkley D,
Sollins P,
Bell R,
Sachs D,
Myrold D
(1992) Biogeochemistry of adjacent conifer and alder‐conifer stands. Ecology 73:2022–2033.
OpenUrl CrossRef

[31] Binkley D,

[32] Sollins P,

[33] Bell R,

[34] Sachs D,

[35] Myrold D

[36] ↵
Wieder WR,
Cleveland CC,
Lawrence DM,
Bonan GB
(2015) Effects of model structural uncertainty on carbon cycle projections: Biological nitrogen fixation as a case study. Environ Res Lett 10:044016.
OpenUrl CrossRef

[37] Wieder WR,

[38] Cleveland CC,

[39] Lawrence DM,

[40] Bonan GB

[41] ↵
Menge DN,
Levin SA,
Hedin LO
(2009) Facultative versus obligate nitrogen fixation strategies and their ecosystem consequences. Am Nat 174:465–477.
OpenUrl CrossRef PubMed

[42] Menge DN,

[43] Levin SA,

[44] Hedin LO

[45] ↵
Vitousek PM,
Porder S,
Houlton BZ,
Chadwick OA
(2010) Terrestrial phosphorus limitation: Mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20:5–15.
OpenUrl

[46] Vitousek PM,

[47] Porder S,

[48] Houlton BZ,

[49] Chadwick OA

[50] ↵
Mainwaring DB,
Maguire DA,
Perakis SS
(2014) Three-year growth response of young Douglas-fir to nitrogen, calcium, phosphorus, and blended fertilizers in Oregon and Washington. For Ecol Manage 327:178–188.
OpenUrl CrossRef

[51] Mainwaring DB,

[52] Maguire DA,

[53] Perakis SS

[54] ↵
Chadwick OA,
Derry LA,
Vitousek PM,
Huebert BJ,
Hedin LO
(1999) Changing sources of nutrients during four million years of ecosystem development. Nature 397:491–497.
OpenUrl CrossRef

[55] Chadwick OA,

[56] Derry LA,

[57] Vitousek PM,

[58] Huebert BJ,

[59] Hedin LO

[60] ↵
Uroz S,
Calvaruso C,
Turpault MP,
Frey-Klett P
(2009) Mineral weathering by bacteria: Ecology, actors and mechanisms. Trends Microbiol 17:378–387.
OpenUrl CrossRef PubMed

[61] Uroz S,

[62] Calvaruso C,

[63] Turpault MP,

[64] Frey-Klett P

[65] ↵
Hoffland E, et al.
(2004) The role of fungi in weathering. Front Ecol Environ 5:258–264.
OpenUrl

[66] Hoffland E, et al.

[67] ↵
Quirk J, et al.
(2012) Evolution of trees and mycorrhizal fungi intensifies silicate mineral weathering. Biol Lett 8:1006–1011.
OpenUrl CrossRef PubMed

[68] Quirk J, et al.

[69] ↵
Blum JD, et al.
(2002) Mycorrhizal weathering of apatite as an important calcium source in base-poor forest ecosystems. Nature 417:729–731.
OpenUrl CrossRef PubMed

[70] Blum JD, et al.

[71] ↵
Capo RC,
Stewart BW,
Chadwick OA
(1998) Strontium isotopes as tracers of ecosystem processes: Theory and methods. Geoderma 82:197–225.
OpenUrl CrossRef

[72] Capo RC,

[73] Stewart BW,

[74] Chadwick OA

[75] ↵
Hynicka JD,
Pett-Ridge JC,
Perakis SS
(2016) Nitrogen enrichment regulates calcium sources in forests. Glob Change Biol 22:4067–4079.
OpenUrl

[76] Hynicka JD,

[77] Pett-Ridge JC,

[78] Perakis SS

[79] ↵
Perakis SS, et al.
(2006) Coupled nitrogen and calcium cycles in forests of the Oregon Coast Range. Ecosystems 9:63–74.
OpenUrl CrossRef

[80] Perakis SS, et al.

[81] ↵
Perakis SS,
Sinkhorn ER
(2011) Biogeochemistry of a temperate forest nitrogen gradient. Ecology 92:1481–1491.
OpenUrl PubMed

[82] Perakis SS,

[83] Sinkhorn ER

[84] ↵
Waring BG, et al.
(2015) Pervasive and strong effects of plants on soil chemistry: A meta-analysis of individual plant ‘Zinke’ effects. Proc Biol Sci 282:20151001.
OpenUrl CrossRef PubMed

[85] Waring BG, et al.

[86] ↵
Meek K,
Derry L,
Sparks J,
Cathles L
(2016) ⁸⁷Sr/⁸⁶Sr, Ca/Sr, and Ge/Si ratios as tracers of solute sources and biogeochemical cycling at a temperate forested shale catchment, central Pennsylvania, USA. Chem Geol 445:84–102.
OpenUrl

[87] Meek K,

[88] Derry L,

[89] Sparks J,

[90] Cathles L

[91] ↵
Bormann FH,
Likens GE
(1967) Nutrient cycling. Science 155:424–429.
OpenUrl Abstract/FREE Full Text

[92] Bormann FH,

[93] Likens GE

[94] ↵
Hartmann J, et al.
(2013) Enhanced chemical weathering as a geoengineering strategy to reduce atmospheric carbon dioxide, supply nutrients, and mitigate ocean acidification. Rev Geophys 51:113–149.
OpenUrl

[95] Hartmann J, et al.

[96] ↵
Vitousek PM,
Chadwick OA
(2013) Pedogenic thresholds and soil process domains in basalt-derived soils. Ecosystems 16:1379–1395.
OpenUrl CrossRef

[97] Vitousek PM,

[98] Chadwick OA

[99] ↵
Hibbs DE,
DeBell DS,
Tarrant RF
Binkley D,
Cromack K Jr,
Baker DD
(1994) Nitrogen fixation by red alder: Biology, rates, and controls. The Biology and Management of Red Alder, eds Hibbs DE, DeBell DS, Tarrant RF (Oregon State Univ Press, Corvallis, OR), pp 57–72.

[100] Hibbs DE,

[101] DeBell DS,

[102] Tarrant RF

[103] Binkley D,

[104] Cromack K Jr,

[105] Baker DD

[106] ↵
Homann PS,
Van Miegroet H,
Cole DW,
Wolfe GV
(1992) Cation distribution, cycling, and removal from mineral soil in Douglas-fir and red alder forests. Biogeochemistry 16:121–150.
OpenUrl

[107] Homann PS,

[108] Van Miegroet H,

[109] Cole DW,

[110] Wolfe GV

[111] ↵
Compton JE,
Church MR,
Larned ST,
Hogsett WE
(2003) Nitrogen export from forested watersheds in the Oregon Coast Range: The role of N₂-fixing red alder. Ecosystems 6:773–785.
OpenUrl CrossRef

[112] Compton JE,

[113] Church MR,

[114] Larned ST,

[115] Hogsett WE

[116] ↵
Pierson-Wickmann AC, et al.
(2009) High chemical weathering rates in first-order granitic catchments induced by agricultural stress. Chem Geol 265:369–380.
OpenUrl CrossRef

[117] Pierson-Wickmann AC, et al.

[118] ↵
Perrin AS,
Probst A,
Probst JL
(2008) Impact of nitrogenous fertilizers on carbonate dissolution in small agricultural catchments: Implications for weathering CO₂ uptake at regional and global scales. Geochim Cosmochim Acta 72:3105–3123.
OpenUrl

[119] Perrin AS,

[120] Probst A,

[121] Probst JL

[122] ↵
Watmough SA, et al.
(2005) Sulphate, nitrogen and base cation budgets at 21 forested catchments in Canada, the United States and Europe. Environ Monit Assess 109:1–36.
OpenUrl CrossRef PubMed

[123] Watmough SA, et al.

[124] ↵
Smith JHG
(1964) Root spread can be estimated from crown width of Douglas fir, lodgepole pine, and other British Columbia tree species. For Chron 40:456–473.
OpenUrl

[125] Smith JHG

[126] ↵
Burns RM,
Honkala BH
(1990) Silvics of North America. Agriculture Handbook (USDA Forest Serv, Washington, DC), Vol 654.

[127] Burns RM,

[128] Honkala BH

[129] ↵
Eis S
(1974) Root system morphology of western hemlock, western red cedar, and Douglas-fir. Can J Res 4:28–38.
OpenUrl

[130] Eis S

[131] ↵
Yamanaka T,
Li CY,
Bormann BT,
Okabe H
(2003) Tripartite associations in an alder: Effects of Frankia and Alpova diplophloeus on the growth, nitrogen fixation and mineral acquisition of Alnus tenuifolia. Plant Soil 254:179–186.
OpenUrl CrossRef

[132] Yamanaka T,

[133] Li CY,

[134] Bormann BT,

[135] Okabe H

[136] ↵
Turner DP,
Franz EH
(1985) The influence of western hemlock and western redcedar on microbial numbers, nitrogen, and nitrification. Plant Soil 88:259–267.
OpenUrl

[137] Turner DP,

[138] Franz EH

[139] ↵
Uliassi DD,
Ruess RW
(2002) Limitations to symbiotic nitrogen fixation in primary succession on the Tanana River floodplain. Ecology 83:88–103.
OpenUrl CrossRef

[140] Uliassi DD,

[141] Ruess RW

[142] ↵
Pett-Ridge JC
(2009) Contributions of dust to phosphorus cycling in tropical forests of the Luquillo Mountains, Puerto Rico. Biogeochemistry 94:63–80.
OpenUrl

[143] Pett-Ridge JC

[144] ↵
Vadeboncoeur MA
(2010) Meta-analysis of fertilization experiments indicates multiple limiting nutrients in northeastern deciduous forests. Can J Res 40:1766–1780.
OpenUrl

[145] Vadeboncoeur MA

[146] ↵
Cross A,
Perakis SS
(2010) Tree species and soil nutrient profiles in old-growth forests of the Oregon Coast Range. Can J Res 41:195–210.
OpenUrl

[147] Cross A,

[148] Perakis SS

[149] ↵
Dixon JL,
Chadwick OA,
Vitousek PM
(2016) Climate‐driven thresholds for chemical weathering in postglacial soils of New Zealand. J Geophys Res Earth Surf 121:1619–1634.
OpenUrl

[150] Dixon JL,

[151] Chadwick OA,

[152] Vitousek PM

[153] ↵
Põlme S,
Bahram M,
Kõljalg U,
Tedersoo L
(2014) Global biogeography of Alnus-associated Frankia actinobacteria. New Phytol 204:979–988.
OpenUrl CrossRef

[154] Põlme S,

[155] Bahram M,

[156] Kõljalg U,

[157] Tedersoo L

[158] ↵
Perakis SS,
Sinkhorn ER,
Compton JE
(2011) δ¹⁵N constraints on long-term nitrogen balances in temperate forests. Oecologia 167:793–807.
OpenUrl CrossRef PubMed

[159] Perakis SS,

[160] Sinkhorn ER,

[161] Compton JE

[162] ↵
Wang T,
Hamann A,
Spittlehouse D,
Carroll C
(2016) Locally downscaled and spatially customizable climate data for historical and future periods for North America. PLoS One 11:e0156720.
OpenUrl CrossRef

[163] Wang T,

[164] Hamann A,

[165] Spittlehouse D,

[166] Carroll C

[167] ↵
Franklin JF,
Dyrness CT
(1988) Natural Vegetation of Oregon and Washington (Oregon State Univ Press, Corvallis, OR).

[168] Franklin JF,

[169] Dyrness CT

[170] ↵
National Atmospheric Deposition Program
(2014) National Atmospheric Deposition Program (NRSP-3). Available at nadp.slh.wisc.edu/data/sites/siteDetails.aspx?net=NTN&id=OR02. Accessed June 27, 2013.

[171] National Atmospheric Deposition Program

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Nitrogen-fixing red alder trees tap rock-derived nutrients

This article has Letters. Please see:

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Abstract

Results and Discussion

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Sample Processing and Analysis.

Strontium Isotope Mixing Calculations.

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