Final Report Summary - TROPICALCARBON (Tropical forest soil carbon storage and microbial diversity under climatic warming)
Tropical forests play a disproportionately large role in the global carbon (C) cycle, exchanging more carbon dioxide (CO2) with the atmosphere than any other ecosystem and containing over two-thirds of terrestrial plant biomass (Pan et al., 2011) and a third of global soil C (Jobbagy & Jackson, 2000). Soil microorganisms play a pivotal role in their C cycle, with 40% of tropical forest ecosystem respiration from soils (Malhi, 2012), approximately two-thirds of which is derived from microbial activity during the decomposition of organic matter (Sayer & Tanner, 2010). There is considerable concern regarding the potential for increased global temperatures to destabilize this flux and amplify climate warming (Crowther et al., 2016), yet – surprisingly - the magnitude and direction of these changes remain unknown because, until only very recently, no warming experiments have been performed in tropical forest (Cavaleri et al., 2015, Nottingham et al., 2015) and no closed-canopy tropical forest occurs today under the mean annual temperature predicted by the end of this century (Wright et al., 2009). The response of tropical forests to future climate change is the greatest source of uncertainty in global C cycle models (Friedlingstein et al., 2006, IPCC, 2013); and experiments are urgently required to address this uncertainty because they provide process-response information that purely-observational studies cannot (Cavaleri et al., 2015, Meir et al., 2015).
The long-term sensitivity of tropical forest soil carbon loss under elevated temperature, as measured in temperate ecosystem experiments (Kirschbaum 2006; Knorr et al. 2005; Melillo et al. 2011), remains controversial. Not only because no warming experiments have been implemented in tropical forests, but also because there is insufficient understanding of the factors that control soil carbon mineralization. Multiple factors have been shown to influence the long-term effect of warming on soil carbon, including the chemistry soil carbon fractions (Craine et al. 2010; Knorr et al. 2005), the availability of nutrients and labile carbon (Hartley et al. 2007; Kirschbaum 2013) and the extent of functional diversity and thermal-acclimation of microbial communities (Allison et al. 2010; Bradford 2013). The influence of these factors may differ strongly in tropical forests compared to other ecosystems, especially given differences in biotic diversity and nutrient availability. Evidence from controlled laboratory studies showing that aspects of microbial diversity regulate soil carbon storage (Fontaine & Barot 2005) is of high significance for tropical forests, which contain the highest -and most threatened- biodiversity of any terrestrial ecosystem. Only recently have techniques to quantify the diversity of soil organisms been developed (Fierer et al. 2007; Fierer et al. 2005), and emerging evidence indicates that the high-levels of diversity found aboveground in tropical forests are also found belowground (Barberán et al. 2015; Mangan et al. 2010). Soil microbial diversity has not yet been quantified at the continental scale in tropical forests, and the extent to which such diversity regulates its soil carbon storage under climatic change remains unexplored. The response of tropical forest soil carbon to temperature change is also likely to depend on nutrient limitations to microbial growth, given their strongly weathered soils and consequent scarcity of rock-derived nutrients such as phosphorus (Porder & Hilley 2010). The importance of substrate limitations in constraining the temperature-sensitivity of organic matter decomposition is often cited (Craine et al. 2010; Davidson & Janssens 2006) and the inter-dependency of microbial cycling of carbon and nutrients well documented (Melillo et al. 2011; Nottingham et al. 2012). Despite this, no study to date has asked to what extent nutrient limitation may constrain soil carbon losses under scenarios of soil warming. The response of tropical forest soil carbon to temperature change will likely be regulated by complex interactions among soil chemistry, nutrient availability, microbial activity and diversity.
Large-scale and long-term field studies are required in tropical forests to demonstrate how the variability in soil chemistry and biology will impact on the temperature response of soil carbon storage (Cavaleri et al. 2015). A combination of experimental manipulation and observation over natural temperature gradients (e.g. elevation gradients; Nottingham et al. 2015b) is likely to provide the richest insights. This project - TropicalCarbon - directly addressed the uncertainty in the response of tropical forest soil carbon cycling to future temperature change by using different experimental approaches (the study of natural temperature gradients, soil translocation and soil warming) in tropical forest in Peru and Panama to investigate how soil chemistry and biology (functional microbial diversity) regulate soil carbon storage under climatic warming. The key questions posed by the project were: 1) What is the fate of carbon in tropical forest soils (in Peru and Panama) under experimental warming? 2) To what extent is carbon storage in tropical forest soils regulated by adaptive responses of soil microbes to temperature and/or nutrient limitation? 3) By drawing on findings from the different experimental systems, and our understanding of the wider biogeography of tropical soils, can we infer the long-term fate of soil carbon in tropical forests, globally?
To address these questions in the first phase of TropicalCarbon, the researcher (Dr A. Nottingham) investigated the role of temperature in constraining soil microbial carbon cycling along a 3.4 km elevation gradient of tropical forest in the Peruvian Andes. Working with collaborating co-authors, he initially demonstrated how temperature effects on the nitrogen cycle are closely linked to soil microbial metabolism, by measuring changes in investment into extracellular enzymes along the elevation gradient (Nottingham et al. 2015a), and by using laboratory experiments to measure the growth responses and substrate use of microorganisms (Nottingham et al. 2017a, Hicks et al 2017). Although it is widely understood that nitrogen cycling responds positively to temperature because of increased rates of nitrogen fixation and decomposition, this enzymatic response of soil microorganisms had not previously been demonstrated. We went further in another study, by showing certain carbon-degrading extracellular enzymes being produced by the microbial communities along this elevation gradient showed different temperature responses at different elevations (Nottingham et al. 2016). Such ‘temperature-adaptive’ responses of enzymes, as we found here, lend support to the notion that microbial communities can adapt to temperature change, regulating their metabolic rates (or enzymatic rates) with consequences for carbon storage (Bradford 2013). These findings from the Peru elevation gradient study were supported in a collaborative global soil study where our data led the entire tropical component of this study and in which we found that ‘adaptive’ responses of microbial respiration rates where greater in soil from colder sites and in soils with high carbon-to-nitrogen ratios (Karhu et al. 2014). Therefore, we built multiple lines of evidence indicating a direct role of thermal adaptation and an indirect role through nitrogen cycling on constraining the soil carbon cycle. Lastly, we found intriguing evidence that temperature was directly driving both the diversity and the community composition and plants and soil microbial communities along this gradient (Nottingham et al., 2016). Not only does this suggest a critical direct role of future temperature change in altering these seemingly coupled communities, it is also an exciting and novel biogeographical observation in its own right and extends for the first time to microbes the subject-defining 19th century biogeographical observations of plant and animal communities on tropical mountains by Alexander von Humbolt (e.g. von Humboldt & Bonpland 1805). These findings were summarized in a review paper, where the researcher drew on findings from the Peru elevation gradient to synthesise the broader potential climatic feedbacks in lowland and montane tropical forest (Nottingham et al. 2015b). In parallel with these ‘observational’ studies along the elevation gradient in Peru, we used soil translocation experiments, whereby we reciprocally transplanted 50 cm deep soil monoliths between 4 sites along the gradient. We sampled from a pre-existing experiment (5 years of incubation) and set up a new experiment to increase the elevation range (2 years of incubation). Recent findings from this translocation study (Nottingham et al, 2017b), have demonstrated a fundamental role of carbon chemistry in determining its rate of decomposition under warming, consistent with predictions from kinetic theory (Davidson & Janssens, 2006). The work also demonstrated hitherto-unrecognized plasticity in the temperature-adaptive responses of specific microbial phyla, suggesting that temperature-adaptive soil C cycling responses (Bradford 2013) occur through (species) compositional changes. The major outcome of this study (Nottingham et al, 2017b) was that tropical montane forest carbon stores, which are large and abundant and present in relatively labile chemical forms (Zimmermann et al., 2010), are extremely vulnerable to warming.
Lastly, the researcher accomplished a major feat by setting up the first soil warming experiment in lowland tropical forest, in Panama (‘SWELTR’ – Soil Warming Experiment in Lowland Tropical Forest). This kind of manipulative experiment is urgently needed to understand the warming responses of lowland tropical forests, and to fill in the gaps in understanding that gradient and translocation studies cannot (Cavaleri et al., 2015, Sundqvist et al., 2013). This task was a very large logistical and engineering challenge. Installation of the experiment was finally completed at the start of 2016, and with a delay to resolve various technical problems, was switched on in November 2016. With the help of on-site technical support through collaboration with the Smithsonian Tropical Research Institute (STRI), we will analyse short-term warming responses of soil microbial respiration and physiology, with expected publication in 2017 and 2018. Several early studies are already completed, where the researcher outlines mechanisms for climate warming feedbacks in tropical forests (Nottingham et al., 2017c), and uses laboratory experiments to demonstrate how phosphorus may be fundamentally important in regulating the stability of deep (> 50 cm) stores of soil carbon in tropical forest (Nottingham et al., 2017d).
The SWELTR experiment is expected to continue running for 5-10 years and will therefore have a long-lasting scientific legacy, with STRI offering long-term support of the infrastructure. The researcher intends to apply to the ERC in the coming year to extend and expand this major scientific project, to understand the long-term effect of warming on plants and soils in tropical forests, as the core research of a future possible professorship and to continue to develop this research through EU partner organizations.
Attachment: A promotional poster for the experiment 'SWELTR', illustrating the project logo and the background and rationale for the experiment.
Allison SD, Wallenstein MD, Bradford MA (2010) Soil-carbon response to warming dependent on microbial physiology. Nat Geosci 3: 336-340
Barberán A, McGuire KL, Wolf JA, Jones FA, Wright SJ, Turner BL, Essene A, Hubbell SP, Faircloth BC, Fierer N (2015) Relating belowground microbial composition to the taxonomic, phylogenetic, and functional trait distributions of trees in a tropical forest. Ecol Lett 18: 1397-1405
Bradford MA (2013) Thermal adaptation of decomposer communities in warming soils. Front Microbiol 4
Cavaleri MA, Reed SC, Smith WK, Wood TE (2015) Urgent need for warming experiments in tropical forests. Global Change Biol: DOI: 10.1111/gcb.12860
Craine JM, Fierer N, McLauchlan KK (2010) Widespread coupling between the rate and temperature sensitivity of organic matter decay. Nat Geosci 3: 854-857
Crowther TW, Todd-Brown KEO, Rowe CW et al. (2016) Quantifying global soil carbon losses in response to warming.
Nature, 540, 104-108.
Crowther TW, Todd-Brown KEO, Rowe CW et al. (2016) Quantifying global soil carbon losses in response to warming. Nature, 540, 104-108.
Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440: 165-173
Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88: 1354-1364
Fierer N, Jackson JA, Vilgalys R, Jackson RB (2005) Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microb 71: 4117-4120
Fontaine S, Barot S (2005) Size and functional diversity of microbe populations control plant persistence and long-term soil carbon accumulation. Ecol Lett 8: 1075-1087
Friedlingstein P, Cox P, Betts R, Bopp L, Von Bloh W, Brovkin V, Cadule P, Doney S, Eby M, Fung I, Bala G, John J, Jones C, Joos F, Kato T, Kawamiya M, Knorr W, Lindsay K, Matthews HD, Raddatz T, Rayner P, Reick C, Roeckner E, Schnitzler KG, Schnur R, Strassmann K, Weaver AJ, Yoshikawa C, Zeng N (2006) Climate-carbon cycle feedback analysis: Results from the (CMIP)-M-4 model intercomparison. J Climate 19: 3337-3353 Hartley IP, Heinemeyer A, Ineson P (2007) Effects of three years of soil warming and shading on the rate of soil respiration: substrate availability and not thermal acclimation mediates observed response. Global Change Biol 13: 1761-1770
Hicks L, Whitaker J, Nottingham AT, Reay DS, Stott AW, Meir P (2017) Nitrogen availability as a determinant of organic matter cycling in tropical upper montane forest and grassland soils, Frontiers in Microbiology, In Review
IPCC (2013) Climate Change 2013: The Physical Science Basis. Cambridge, Cambridge University Press.
Jobbagy EG, Jackson RB (2000) The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl 10: 423-436
Karhu K, Auffret MD, Dungait JAJ, Hopkins DW, Prosser JI, Singh BK, Subke JA, Wookey PA, Agren GI, Sebastia MT, Gouriveau F, Bergkvist G, Meir P, Nottingham AT, Salinas N, Hartley (2014) Temperature sensitivity of soil respiration rates enhanced by microbial community response. Nature 513: 81
Kirschbaum M (2006) The temperature dependence of organic-matter decomposition—still a topic of debate. Soil Biology and Biochemistry 38: 2510-2518
Kirschbaum MUF (2013) Seasonal variations in the availability of labile substrate confound the temperature dependence of organic matter decomposition. Soil Biol Biochem 57: 568-576 Knorr W, Prentice IC, House JI, Holland EA (2005) Long-term sensitivity of soil carbon turnover to warming. Nature 433: 298-301
Malhi Y, Aragao LEOC, Galbraith D et al. (2009) Exploring the likelihood and mechanism of a climate-change-induce dieback of the Amazon rainforest.
Proceedings of the National Academy of Sciences of the United States of America, 106,20610-20615.
Malhi Y (2012) The productivity, metabolism and carbon cycle of tropical forest vegetation. Journal of Ecology, 100, 65-75.
Mangan SA, Schnitzer SA, Herre EA, Mack KM, Valencia MC, Sanchez EI, Bever JD (2010) Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466: 752-755
Meir P, Wood TE, Galbraith DR, Brando PM, Da Costa ACL, Rowland L, Ferreira LV (2015) Threshold Responses to Soil Moisture Deficit by Trees and Soil in
Tropical Rain Forests: Insights from Field Experiments. Bioscience, 65, 882-892.
Melillo JM, Butler S, Johnson J, Mohan J, Steudler P, Lux H, Burrows E, Bowles F, Smith R, Scott L, Vario C, Hill T, Burton A, Zhou YM, Tang J (2011) Soil warming, carbon-nitrogen interactions, and forest carbon budgets. P Natl Acad Sci USA 108: 9508-9512
Nottingham AT, Turner BL, Chamberlain PM, Stott AW, Tanner EVJ (2012) Priming and microbial nutrient limitation in lowland tropical forest soils of contrasting fertility. Biogeochemistry 111: 219-237
Nottingham AT, Turner BL, Whitaker J, Ostle N, Bardgett RD, McNamara NP, Salinas N, Meir P (2016) Temperature sensitivity of soil enzymes along an elevation gradient in the Peruvian Andes. Biogeochemistry 127: 217-230
Nottingham AT, Turner BL, Whitaker J, Ostle N, McNamara NP, Bardgett RD, Salinas N, Meir P (2015a) Soil microbial nutrient constraints along a tropical forest elevation gradient: a belowground test of a biogeochemical paradigm. Biogeosciences 12: 6489-6523
Nottingham AT, Whitaker J, Turner BL, Salinas N, Zimmermann M, Malhi Y, Meir P (2015b) Climate Warming and Soil Carbon in Tropical Forests: Insights from an Elevation Gradient in the Peruvian Andes. Bioscience 65: 906-921
Nottingham A, Fierer N, Turner B et al. (2016) Temperature drives plant and soil microbial diversity patterns across an elevation gradient from the Andes to the
Amazon. bioRxiv.
Nottingham AT, Whitaker J, Turner BL, Salinas N, Zimmermann M, Malhi Y, Meir P (2015) Climate Warming and Soil Carbon in Tropical Forests: Insights from
an Elevation Gradient in the Peruvian Andes. Bioscience, 65, 906-921.
Nottingham AT, Hicks L, Baath E, Meir P (2017a) Nutrient constraints to bacterial and fungal growth during cellulose decomposition in tropical forest soils. Biology and Fertility of Soils, In Review
Nottingham AT, Turner BL, Whitaker J, Ostle N, Bardgett RD, McNamara NP, Salinas N, Meir P (2017b) Tropical montane soil carbon is highly vulnerable climate warming: labile carbon and temperature adaptive phyla. Global Change Biology, to be submitted
Nottingham AT, Turner BT, Meir P (2017c) Climate warming and nitrogen feedbacks in lowland tropical forest soils. Trends in Ecology and Evolution, In Review
Nottingham AT, Turner BT, Meir P (2017d) Phosphorus deficiency stabilizes deep soil organic carbon in tropical forest soils. Soil Biology and Biochemistry, to be submitted
Pan Y, Birdsey RA, Fang J et al. (2011) A large and persistent carbon sink in the world's forests. Science, 333, 988-993.
Porder S, Hilley GE (2010) Linking chronosequences with the rest of the world: predicting soil phosphorus content in denuding landscapes. Biogeochemistry 102: 153-166
Rustad LE, Campbell JL, Marion GM, Norby RJ, Mitchell MJ, Hartley AE, Cornelissen JHC, Gurevitch J, Gcte-News (2001) A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126: 543-562
Sayer EJ, Tanner EVJ (2010) A new approach to trenching experiments for measuring root–rhizosphere respiration in a lowland tropical forest. Soil Biology and
Biochemistry, 42, 347-352.
Schlesinger WH (1997) Biogeochemistry, an Analysis of Global Change. Academic Press, London, UK
Singh BK, Bardgett RD, Smith P, Reay DS (2010) Microorganisms and climate change: terrestrial feedbacks and mitigation options. Nature reviews. Microbiology 8: 779-790 Tilman D, Knops J, Wedin D, Reich P, Ritchie M, Siemann E (1997) The influence of functional diversity and composition on ecosystem processes. Science 277: 1300-1302
Sundqvist MK, Sanders NJ, Wardle DA (2013) Community and Ecosystem Responses to Elevational Gradients: Processes, Mechanisms, and Insights for Global
Change. Annual Review of Ecology, Evolution, and Systematics, 44, 261-280.
von Humboldt A, Bonpland A (1805) Essai sur la ge´ographie des plantes. Chez Levrault, Scoell et Campagnie, Librarie, Paris
Wright SJ, Muller-Landau HC, Schipper J (2009) The Future of Tropical Species on a Warmer Planet. Conservation Biology, 23, 1418-1426.
Zimmermann M, Meir P, Silman MR et al. (2010) No Differences in Soil Carbon Stocks Across the Tree Line in the Peruvian Andes. Ecosystems, 13, 62-74.
The long-term sensitivity of tropical forest soil carbon loss under elevated temperature, as measured in temperate ecosystem experiments (Kirschbaum 2006; Knorr et al. 2005; Melillo et al. 2011), remains controversial. Not only because no warming experiments have been implemented in tropical forests, but also because there is insufficient understanding of the factors that control soil carbon mineralization. Multiple factors have been shown to influence the long-term effect of warming on soil carbon, including the chemistry soil carbon fractions (Craine et al. 2010; Knorr et al. 2005), the availability of nutrients and labile carbon (Hartley et al. 2007; Kirschbaum 2013) and the extent of functional diversity and thermal-acclimation of microbial communities (Allison et al. 2010; Bradford 2013). The influence of these factors may differ strongly in tropical forests compared to other ecosystems, especially given differences in biotic diversity and nutrient availability. Evidence from controlled laboratory studies showing that aspects of microbial diversity regulate soil carbon storage (Fontaine & Barot 2005) is of high significance for tropical forests, which contain the highest -and most threatened- biodiversity of any terrestrial ecosystem. Only recently have techniques to quantify the diversity of soil organisms been developed (Fierer et al. 2007; Fierer et al. 2005), and emerging evidence indicates that the high-levels of diversity found aboveground in tropical forests are also found belowground (Barberán et al. 2015; Mangan et al. 2010). Soil microbial diversity has not yet been quantified at the continental scale in tropical forests, and the extent to which such diversity regulates its soil carbon storage under climatic change remains unexplored. The response of tropical forest soil carbon to temperature change is also likely to depend on nutrient limitations to microbial growth, given their strongly weathered soils and consequent scarcity of rock-derived nutrients such as phosphorus (Porder & Hilley 2010). The importance of substrate limitations in constraining the temperature-sensitivity of organic matter decomposition is often cited (Craine et al. 2010; Davidson & Janssens 2006) and the inter-dependency of microbial cycling of carbon and nutrients well documented (Melillo et al. 2011; Nottingham et al. 2012). Despite this, no study to date has asked to what extent nutrient limitation may constrain soil carbon losses under scenarios of soil warming. The response of tropical forest soil carbon to temperature change will likely be regulated by complex interactions among soil chemistry, nutrient availability, microbial activity and diversity.
Large-scale and long-term field studies are required in tropical forests to demonstrate how the variability in soil chemistry and biology will impact on the temperature response of soil carbon storage (Cavaleri et al. 2015). A combination of experimental manipulation and observation over natural temperature gradients (e.g. elevation gradients; Nottingham et al. 2015b) is likely to provide the richest insights. This project - TropicalCarbon - directly addressed the uncertainty in the response of tropical forest soil carbon cycling to future temperature change by using different experimental approaches (the study of natural temperature gradients, soil translocation and soil warming) in tropical forest in Peru and Panama to investigate how soil chemistry and biology (functional microbial diversity) regulate soil carbon storage under climatic warming. The key questions posed by the project were: 1) What is the fate of carbon in tropical forest soils (in Peru and Panama) under experimental warming? 2) To what extent is carbon storage in tropical forest soils regulated by adaptive responses of soil microbes to temperature and/or nutrient limitation? 3) By drawing on findings from the different experimental systems, and our understanding of the wider biogeography of tropical soils, can we infer the long-term fate of soil carbon in tropical forests, globally?
To address these questions in the first phase of TropicalCarbon, the researcher (Dr A. Nottingham) investigated the role of temperature in constraining soil microbial carbon cycling along a 3.4 km elevation gradient of tropical forest in the Peruvian Andes. Working with collaborating co-authors, he initially demonstrated how temperature effects on the nitrogen cycle are closely linked to soil microbial metabolism, by measuring changes in investment into extracellular enzymes along the elevation gradient (Nottingham et al. 2015a), and by using laboratory experiments to measure the growth responses and substrate use of microorganisms (Nottingham et al. 2017a, Hicks et al 2017). Although it is widely understood that nitrogen cycling responds positively to temperature because of increased rates of nitrogen fixation and decomposition, this enzymatic response of soil microorganisms had not previously been demonstrated. We went further in another study, by showing certain carbon-degrading extracellular enzymes being produced by the microbial communities along this elevation gradient showed different temperature responses at different elevations (Nottingham et al. 2016). Such ‘temperature-adaptive’ responses of enzymes, as we found here, lend support to the notion that microbial communities can adapt to temperature change, regulating their metabolic rates (or enzymatic rates) with consequences for carbon storage (Bradford 2013). These findings from the Peru elevation gradient study were supported in a collaborative global soil study where our data led the entire tropical component of this study and in which we found that ‘adaptive’ responses of microbial respiration rates where greater in soil from colder sites and in soils with high carbon-to-nitrogen ratios (Karhu et al. 2014). Therefore, we built multiple lines of evidence indicating a direct role of thermal adaptation and an indirect role through nitrogen cycling on constraining the soil carbon cycle. Lastly, we found intriguing evidence that temperature was directly driving both the diversity and the community composition and plants and soil microbial communities along this gradient (Nottingham et al., 2016). Not only does this suggest a critical direct role of future temperature change in altering these seemingly coupled communities, it is also an exciting and novel biogeographical observation in its own right and extends for the first time to microbes the subject-defining 19th century biogeographical observations of plant and animal communities on tropical mountains by Alexander von Humbolt (e.g. von Humboldt & Bonpland 1805). These findings were summarized in a review paper, where the researcher drew on findings from the Peru elevation gradient to synthesise the broader potential climatic feedbacks in lowland and montane tropical forest (Nottingham et al. 2015b). In parallel with these ‘observational’ studies along the elevation gradient in Peru, we used soil translocation experiments, whereby we reciprocally transplanted 50 cm deep soil monoliths between 4 sites along the gradient. We sampled from a pre-existing experiment (5 years of incubation) and set up a new experiment to increase the elevation range (2 years of incubation). Recent findings from this translocation study (Nottingham et al, 2017b), have demonstrated a fundamental role of carbon chemistry in determining its rate of decomposition under warming, consistent with predictions from kinetic theory (Davidson & Janssens, 2006). The work also demonstrated hitherto-unrecognized plasticity in the temperature-adaptive responses of specific microbial phyla, suggesting that temperature-adaptive soil C cycling responses (Bradford 2013) occur through (species) compositional changes. The major outcome of this study (Nottingham et al, 2017b) was that tropical montane forest carbon stores, which are large and abundant and present in relatively labile chemical forms (Zimmermann et al., 2010), are extremely vulnerable to warming.
Lastly, the researcher accomplished a major feat by setting up the first soil warming experiment in lowland tropical forest, in Panama (‘SWELTR’ – Soil Warming Experiment in Lowland Tropical Forest). This kind of manipulative experiment is urgently needed to understand the warming responses of lowland tropical forests, and to fill in the gaps in understanding that gradient and translocation studies cannot (Cavaleri et al., 2015, Sundqvist et al., 2013). This task was a very large logistical and engineering challenge. Installation of the experiment was finally completed at the start of 2016, and with a delay to resolve various technical problems, was switched on in November 2016. With the help of on-site technical support through collaboration with the Smithsonian Tropical Research Institute (STRI), we will analyse short-term warming responses of soil microbial respiration and physiology, with expected publication in 2017 and 2018. Several early studies are already completed, where the researcher outlines mechanisms for climate warming feedbacks in tropical forests (Nottingham et al., 2017c), and uses laboratory experiments to demonstrate how phosphorus may be fundamentally important in regulating the stability of deep (> 50 cm) stores of soil carbon in tropical forest (Nottingham et al., 2017d).
The SWELTR experiment is expected to continue running for 5-10 years and will therefore have a long-lasting scientific legacy, with STRI offering long-term support of the infrastructure. The researcher intends to apply to the ERC in the coming year to extend and expand this major scientific project, to understand the long-term effect of warming on plants and soils in tropical forests, as the core research of a future possible professorship and to continue to develop this research through EU partner organizations.
Attachment: A promotional poster for the experiment 'SWELTR', illustrating the project logo and the background and rationale for the experiment.
Allison SD, Wallenstein MD, Bradford MA (2010) Soil-carbon response to warming dependent on microbial physiology. Nat Geosci 3: 336-340
Barberán A, McGuire KL, Wolf JA, Jones FA, Wright SJ, Turner BL, Essene A, Hubbell SP, Faircloth BC, Fierer N (2015) Relating belowground microbial composition to the taxonomic, phylogenetic, and functional trait distributions of trees in a tropical forest. Ecol Lett 18: 1397-1405
Bradford MA (2013) Thermal adaptation of decomposer communities in warming soils. Front Microbiol 4
Cavaleri MA, Reed SC, Smith WK, Wood TE (2015) Urgent need for warming experiments in tropical forests. Global Change Biol: DOI: 10.1111/gcb.12860
Craine JM, Fierer N, McLauchlan KK (2010) Widespread coupling between the rate and temperature sensitivity of organic matter decay. Nat Geosci 3: 854-857
Crowther TW, Todd-Brown KEO, Rowe CW et al. (2016) Quantifying global soil carbon losses in response to warming.
Nature, 540, 104-108.
Crowther TW, Todd-Brown KEO, Rowe CW et al. (2016) Quantifying global soil carbon losses in response to warming. Nature, 540, 104-108.
Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440: 165-173
Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88: 1354-1364
Fierer N, Jackson JA, Vilgalys R, Jackson RB (2005) Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microb 71: 4117-4120
Fontaine S, Barot S (2005) Size and functional diversity of microbe populations control plant persistence and long-term soil carbon accumulation. Ecol Lett 8: 1075-1087
Friedlingstein P, Cox P, Betts R, Bopp L, Von Bloh W, Brovkin V, Cadule P, Doney S, Eby M, Fung I, Bala G, John J, Jones C, Joos F, Kato T, Kawamiya M, Knorr W, Lindsay K, Matthews HD, Raddatz T, Rayner P, Reick C, Roeckner E, Schnitzler KG, Schnur R, Strassmann K, Weaver AJ, Yoshikawa C, Zeng N (2006) Climate-carbon cycle feedback analysis: Results from the (CMIP)-M-4 model intercomparison. J Climate 19: 3337-3353 Hartley IP, Heinemeyer A, Ineson P (2007) Effects of three years of soil warming and shading on the rate of soil respiration: substrate availability and not thermal acclimation mediates observed response. Global Change Biol 13: 1761-1770
Hicks L, Whitaker J, Nottingham AT, Reay DS, Stott AW, Meir P (2017) Nitrogen availability as a determinant of organic matter cycling in tropical upper montane forest and grassland soils, Frontiers in Microbiology, In Review
IPCC (2013) Climate Change 2013: The Physical Science Basis. Cambridge, Cambridge University Press.
Jobbagy EG, Jackson RB (2000) The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl 10: 423-436
Karhu K, Auffret MD, Dungait JAJ, Hopkins DW, Prosser JI, Singh BK, Subke JA, Wookey PA, Agren GI, Sebastia MT, Gouriveau F, Bergkvist G, Meir P, Nottingham AT, Salinas N, Hartley (2014) Temperature sensitivity of soil respiration rates enhanced by microbial community response. Nature 513: 81
Kirschbaum M (2006) The temperature dependence of organic-matter decomposition—still a topic of debate. Soil Biology and Biochemistry 38: 2510-2518
Kirschbaum MUF (2013) Seasonal variations in the availability of labile substrate confound the temperature dependence of organic matter decomposition. Soil Biol Biochem 57: 568-576 Knorr W, Prentice IC, House JI, Holland EA (2005) Long-term sensitivity of soil carbon turnover to warming. Nature 433: 298-301
Malhi Y, Aragao LEOC, Galbraith D et al. (2009) Exploring the likelihood and mechanism of a climate-change-induce dieback of the Amazon rainforest.
Proceedings of the National Academy of Sciences of the United States of America, 106,20610-20615.
Malhi Y (2012) The productivity, metabolism and carbon cycle of tropical forest vegetation. Journal of Ecology, 100, 65-75.
Mangan SA, Schnitzer SA, Herre EA, Mack KM, Valencia MC, Sanchez EI, Bever JD (2010) Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466: 752-755
Meir P, Wood TE, Galbraith DR, Brando PM, Da Costa ACL, Rowland L, Ferreira LV (2015) Threshold Responses to Soil Moisture Deficit by Trees and Soil in
Tropical Rain Forests: Insights from Field Experiments. Bioscience, 65, 882-892.
Melillo JM, Butler S, Johnson J, Mohan J, Steudler P, Lux H, Burrows E, Bowles F, Smith R, Scott L, Vario C, Hill T, Burton A, Zhou YM, Tang J (2011) Soil warming, carbon-nitrogen interactions, and forest carbon budgets. P Natl Acad Sci USA 108: 9508-9512
Nottingham AT, Turner BL, Chamberlain PM, Stott AW, Tanner EVJ (2012) Priming and microbial nutrient limitation in lowland tropical forest soils of contrasting fertility. Biogeochemistry 111: 219-237
Nottingham AT, Turner BL, Whitaker J, Ostle N, Bardgett RD, McNamara NP, Salinas N, Meir P (2016) Temperature sensitivity of soil enzymes along an elevation gradient in the Peruvian Andes. Biogeochemistry 127: 217-230
Nottingham AT, Turner BL, Whitaker J, Ostle N, McNamara NP, Bardgett RD, Salinas N, Meir P (2015a) Soil microbial nutrient constraints along a tropical forest elevation gradient: a belowground test of a biogeochemical paradigm. Biogeosciences 12: 6489-6523
Nottingham AT, Whitaker J, Turner BL, Salinas N, Zimmermann M, Malhi Y, Meir P (2015b) Climate Warming and Soil Carbon in Tropical Forests: Insights from an Elevation Gradient in the Peruvian Andes. Bioscience 65: 906-921
Nottingham A, Fierer N, Turner B et al. (2016) Temperature drives plant and soil microbial diversity patterns across an elevation gradient from the Andes to the
Amazon. bioRxiv.
Nottingham AT, Whitaker J, Turner BL, Salinas N, Zimmermann M, Malhi Y, Meir P (2015) Climate Warming and Soil Carbon in Tropical Forests: Insights from
an Elevation Gradient in the Peruvian Andes. Bioscience, 65, 906-921.
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