Toward a Coordinated Understanding of Hydro-Biogeochemical Root Functions in Tropical Forests for Application in Vegetation Models

Tropical forest root characteristics and resource acquisition strategies are underrepresented in vegetation and global models, hampering the prediction of forest–climate feedbacks for these carbon-rich ecosystems. Lowland tropical forests often have globally unique combinations of high taxonomic and functional biodiversity, rainfall seasonality, and strongly weathered infertile soils, giving rise to distinct patterns in root traits and functions compared with higher latitude ecosystems. We provide a roadmap for integrating recent advances in our understanding of tropical forest belowground function into vegetation models, focusing on water and nutrient acquisition. We offer comparisons of recent advances in empirical and model understanding of root characteristics that represent important functional processes in tropical forests. We focus on: (1) fine-root strategies for soil resource exploration, (2) coupling and trade-offs in fine-root water vs nutrient acquisition, and (3) aboveground–belowground linkages in plant resource acquisition and use. We suggest avenues for representing these extremely diverse plant communities in computationally manageable and ecologically meaningful groups in models for linked aboveground–belowground hydro-nutrient functions. Tropical forests are undergoing warming, shifting rainfall regimes, and exacerbation of soil nutrient scarcity caused by elevated atmospheric CO2. The accurate model representation of tropical forest functions is crucial for understanding the interactions of this biome with the climate

Representation of phosphorus cycle in Joint UK Land Environment Simulator (vn5.5_JULES-CNP)

Most land surface models (LSMs), the land components of Earth system models (ESMs), include representation of N limitation on ecosystem productivity. However only few of these models have incorporated phosphorus (P) cycling. In tropical ecosystems, this is likely to be particularly important as N tends to be abundant but the availability of rock-derived elements, such as P, can be very low. Thus, without a representation of P cycling, tropical forest response in areas such as Amazonia to rising atmospheric CO2 conditions remains highly uncertain. In this study, we introduced P dynamics and its interactions with the N and carbon (C) cycles into the Joint UK Land Environment Simulator (JULES). The new model (JULES-CNP) includes the representation of P stocks in vegetation and soil pools, as well as key processes controlling fluxes between these pools. We evaluate JULES-CNP at the Amazon nutrient fertilization experiment (AFEX), a low fertility site, representative of about 60 % of Amazon soils. We apply the model under ambient CO2 and elevated CO2. The model is able to reproduce the observed plant and soil P pools and fluxes under ambient CO2. We estimate P to limit net primary productivity (NPP) by 24 % under current CO2 and by 46 % under elevated CO2. Under elevated CO2, biomass in simulations accounting for CNP increase by 10 % relative to at contemporary CO2, although it is 5 % lower compared with CN and C-only simulations. Our results highlight the potential for high P limitation and therefore lower CO2 fertilization capacity in the Amazon forest with low fertility soils

Direct evidence for phosphorus limitation on Amazon forest productivity

The productivity of rainforests growing on highly weathered tropical soils is expected to be limited by phosphorus availability1. Yet, controlled fertilization experiments have been unable to demonstrate a dominant role for phosphorus in controlling tropical forest net primary productivity. Recent syntheses have demonstrated that responses to nitrogen addition are as large as to phosphorus2, and adaptations to low phosphorus availability appear to enable net primary productivity to be maintained across major soil phosphorus gradients3. Thus, the extent to which phosphorus availability limits tropical forest productivity is highly uncertain. The majority of the Amazonia, however, is characterized by soils that are more depleted in phosphorus than those in which most tropical fertilization experiments have taken place2. Thus, we established a phosphorus, nitrogen and base cation addition experiment in an old growth Amazon rainforest, with a low soil phosphorus content that is representative of approximately 60% of the Amazon basin. Here we show that net primary productivity increased exclusively with phosphorus addition. After 2 years, strong responses were observed in fine root (+29%) and canopy productivity (+19%), but not stem growth. The direct evidence of phosphorus limitation of net primary productivity suggests that phosphorus availability may restrict Amazon forest responses to CO2 fertilization4, with major implications for future carbon sequestration and forest resilience to climate change.The authors acknowledge funding from the UK Natural Environment Research Council (NERC), grant number NE/L007223/1. This is publication 850 in the technical series of the BDFFP. C.A.Q. acknowledges the grants from Brazilian National Council for Scientific and Technological Development (CNPq) CNPq/LBA 68/2013, CNPq/MCTI/FNDCT no. 18/2021 and his productivity grant. C.A.Q., H.F.V.C., F.D.S., I.A., L.F.L., E.O.M. and S.G. acknowledge the AmazonFACE programme for financial support in cooperation with Coordination for the Improvement of Higher Education Personnel (CAPES) and the National Institute of Amazonian Research as part of the grants CAPES-INPA/88887.154643/2017-00 and 88881.154644/2017-01. T.F.D. acknowledges funds from FundacAo de Amparo a Pesquisa do Estado de SAo Paulo (FAPESP), grant 2015/50488-5, and the Partnership for Enhanced Engagement in Research (PEER) programme grant AID-OAA-A-11-00012. L.E.O.C.A. thanks CNPq (314416/2020-0)

Rapid responses of root traits and productivity to phosphorus and cation additions in a tropical lowland forest in Amazonia

• Soil nutrient availability can strongly affect root traits. In tropical forests, phosphorus (P) is often considered the main limiting nutrient for plants. However, support for the P paradigm is limited, and N and cations might also control tropical forests functioning. • We used a large‐scale experiment to determine how the factorial addition of nitrogen (N), P and cations affected root productivity and traits related to nutrient acquisition strategies (morphological traits, phosphatase activity, arbuscular mycorrhizal colonisation and nutrient contents) in a primary rainforest growing on low‐fertility soils in Central Amazonia after one year of fertilisation. • Multiple root traits and productivity were affected. Phosphorus additions increased annual root productivity and root diameter, but decreased root phosphatase activity. Cation additions increased root productivity at certain times of year, also increasing root diameter and mycorrhizal colonisation. P and cation additions increased their element concentrations in root tissues. No responses were detected with N addition. • Here we show that rock‐derived nutrients determine root functioning in low‐fertility Amazonian soils, demonstrating not only the hypothesised importance of P, but also highlighting the role of cations. The changes in fine root traits and productivity indicate that even slow‐growing tropical rainforests can respond rapidly to changes in resource availability

Direct evidence for phosphorus limitation on Amazon forest productivity

The productivity of rainforests growing on highly weathered tropical soils is expected to be limited by phosphorus availability1. Yet, controlled fertilization experiments have been unable to demonstrate a dominant role for phosphorus in controlling tropical forest net primary productivity. Recent syntheses have demonstrated that responses to nitrogen addition are as large as to phosphorus2, and adaptations to low phosphorus availability appear to enable net primary productivity to be maintained across major soil phosphorus gradients3. Thus, the extent to which phosphorus availability limits tropical forest productivity is highly uncertain. The majority of the Amazonia, however, is characterized by soils that are more depleted in phosphorus than those in which most tropical fertilization experiments have taken place2. Thus, we established a phosphorus, nitrogen and base cation addition experiment in an old growth Amazon rainforest, with a low soil phosphorus content that is representative of approximately 60% of the Amazon basin. Here we show that net primary productivity increased exclusively with phosphorus addition. After 2 years, strong responses were observed in fine root (+29%) and canopy productivity (+19%), but not stem growth. The direct evidence of phosphorus limitation of net primary productivity suggests that phosphorus availability may restrict Amazon forest responses to CO2 fertilization4, with major implications for future carbon sequestration and forest resilience to climate change

Modeling the carbon costs of plant phosphorus acquisition in Amazonian forests

Plants growing in low phosphorus (P) soils, such as in the predominant soils of Amazonia, are believed to devote more energy to acquiring P through absorptive root production, symbionts, and root exudates than plants in more fertile soils. Accounting for these energy costs in vegetation models is essential, as underestimating carbon (C) allocation to nutrient acquisition may lead to overestimating plant biomass growth. We developed a quantitative model to test a theoretical framework of C costs of P acquisition across soil P gradients. The model considers four strategies: P foraging via absorptive roots and arbuscular mycorrhizal fungi and P mining via root exudation of phosphatases and organic acids. We used field observations (i.e., soil data, plant biomass production, and stoichiometry of different organs) from ten sites across Amazonia to calibrate the model and explore different scenarios of (i) experimental soil P addition and (ii) elevated atmospheric CO2 concentrations (eCO2). Our model reproduced expected trends in P-acquisition strategies, with plants increasingly investing in foraging strategies as soil soluble inorganic P (Pi) increases and increasingly investing in mining strategies as total P and less available P forms decrease. Relative investment in P acquisition was within observed ranges. Plants, on average and across all sites, invested the equivalent of 20.5% of their estimated total net primary production (NPP) in P acquisition. On average, plants allocated 15.3% of their NPP to P acquisition in the three most fertile sites, compared to 29.0% in the least fertile sites. C allocation to arbuscular mycorrhizas, phosphatases, and organic acids, which are not commonly measured components of total NPP, was up to 25.8% (16.9% on average) of the total NPP. We highlight the need for quantitative data on plant C allocation to P acquisition from the soil to strengthen further model development and future model projections.</p

Impact of nutrient additions on free-living nitrogen fixation in litter and soil of two French-Guianese lowland tropical forests

In tropical forests, free-living Biological nitrogen (N) fixation (BNF) in soil and litter tends to decrease when substrate N concentrations increase, whereas increasing phosphorus (P) and molybdenum (Mo) soil and litter concentrations have been shown to stimulate free-living BNF rates. Yet, very few studies explored the effects of adding N, P, and Mo together in a single large-scale fertilization experiment, which would teach us which of these elements constrain or limit BNF activities. At two distinct forest sites in French Guiana, we performed a 3-year in situ nutrient addition study to explore the effects of N, P, and Mo additions on leaf litter and soil BNF. Additionally, we conducted a short-term laboratory study with the same nutrient addition treatments (+N, +N+P, +P, +Mo, and +P+Mo). We found that N additions alone suppressed litter free-living BNF in the field, but not in the short-term laboratory study, while litter free-living BNF remained unchanged in response to N+P additions. Additionally, we found that P and P+Mo additions stimulated BNF in leaf litter, both in the field and in the lab, while Mo alone yielded no changes. Soil BNF increased with P and P+Mo additions in only one of the field sites, while in the other site soil BNF increased with Mo and P+Mo additions. We concluded that increased substrate N concentrations suppress BNF. Moreover, both P and Mo have the potential to limit free-living BNF in these tropical forests, but the balance between P versus Mo limitation is determined by site-specific characteristics of nutrient supply and demand

Impact of nutrient additions on free-living nitrogen fixation in litter and soil of two french-guianese lowland tropical forests

In tropical forests, free-living Biological nitrogen (N) fixation (BNF) in soil and litter tends to decrease when substrate N concentrations increase, whereas increasing phosphorus (P) and molybdenum (Mo) soil and litter concentrations have been shown to stimulate free-living BNF rates. Yet, very few studies explored the effects of adding N, P, and Mo together in a single large-scale fertilization experiment, which would teach us which of these elements constrain or limit BNF activities. At two distinct forest sites in French Guiana, we performed a 3-year in situ nutrient addition study to explore the effects of N, P, and Mo additions on leaf litter and soil BNF. Additionally, we conducted a short-term laboratory study with the same nutrient addition treatments (+N, +N+P, +P, +Mo, and +P+Mo). We found that N additions alone suppressed litter free-living BNF in the field, but not in the short-term laboratory study, while litter free-living BNF remained unchanged in response to N+P additions. Additionally, we found that P and P+Mo additions stimulated BNF in leaf litter, both in the field and in the lab, while Mo alone yielded no changes. Soil BNF increased with P and P+Mo additions in only one of the field sites, while in the other site soil BNF increased with Mo and P+Mo additions. We concluded that increased substrate N concentrations suppress BNF. Moreover, both P and Mo have the potential to limit free-living BNF in these tropical forests, but the balance between P versus Mo limitation is determined by site-specific characteristics of nutrient supply and demand

Phosphorus scarcity contributes to nitrogen limitation in lowland tropical rainforests

International audienceAbstract There is increasing evidence to suggest that soil nutrient availability can limit the carbon sink capacity of forests, a particularly relevant issue considering today's changing climate. This question is especially important in the tropics, where most part of the Earth's plant biomass is stored. To assess whether tropical forest growth is limited by soil nutrients and to explore N and P limitations, we analyzed stem growth and foliar elemental composition of the five stem widest trees per plot at two sites in French Guiana after 3 years of nitrogen (N), phosphorus (P), and N + P addition. We also compared the results between potential N‐fixer and non‐N‐fixer species. We found a positive effect of N fertilization on stem growth and foliar N, as well as a positive effect of P fertilization on stem growth, foliar N, and foliar P. Potential N‐fixing species had greater stem growth, greater foliar N, and greater foliar P concentrations than non‐N‐fixers. In terms of growth, there was a negative interaction between N‐fixer status, N + P, and P fertilization, but no interaction with N fertilization. Because N‐fixing plants do not show to be completely N saturated, we do not anticipate N providing from N‐fixing plants would supply non‐N‐fixers. Although the soil‐age hypothesis only anticipates P limitation in highly weathered systems, our results for stem growth and foliar elemental composition indicate the existence of considerable N and P co‐limitation, which is alleviated in N‐fixing plants. The evidence suggests that certain mechanisms invest in N to obtain the scarce P through soil phosphatases, which potentially contributes to the N limitation detected by this study