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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.

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