Soils store at least twice as much carbon (C) as plant biomass 1 , and, each year, soil microbial respiration releases ~60 Pg of C to the atmosphere as carbon dioxide (CO 2 ) 2 .In the short term, soil microbial respiration increases exponentially with temperature 3 , and thus models predict that warming-induced increases in CO 2 release from soils could represent an important positive feedback to 21 st century climate change 4 . However, the magnitude of this feedback remains uncertain, not least because the adaptation of soil microbial communities to changing temperatures has the potential to either substantially decrease ('compensatory adaptation' 5-7 ) or substantially increase ('enhancing adaptation' 8,9 ) warming-induced C losses. By collecting contrasting soils along a climatic gradient from the Arctic to the Amazon, we undertook the first global analysis of the role microbial thermal adaptation plays in controlling rates of CO 2 release from soils. Here we show that, enhancing adaptation was between three and ten times more common than compensatory adaptation. Furthermore, the strongest enhancing responses were observed in soils with high C contents and from cold climates; enhancing thermal adaptation increased the temperature sensitivity of respiration in these soils by a factor of 1.4. This suggests that the substantial stores of C present in organic and high-latitude soils may be more vulnerable to climate warming than currently predicted. Text:Short-term experiments have demonstrated that the rate of microbial respiration in soil increases exponentially with temperature, and this general relationship has been used in parameterising soil C and Earth system models 4,10 . However, plant physiologists have demonstrated that short-term measurements are inadequate for representing the dynamic response of plant respiration to changes in temperature. In plants, thermal acclimation, defined as the "subsequent adjustment in the rate of respiration to compensate for an initial change in temperature" 11 greatly reduces the impact of temperature change on plant respiration in the medium-to long-term, with major consequences for modelling C-cycle feedbacks to climate change 12 . In soil there is growing evidence of the potential for a similar compensatory effect through microbial adaptation to temperature 13 ('compensatory adaptation': defined here to include the potential for physiological acclimation, adaptation within populations, and changes in microbial community size and structure). However, it is unclear if microbial community-level responses should always be compensatory. In fact, responses that enhance the direct and instantaneous effect of temperature changes on soil respiration ('enhancing adaptation') have also been observed 8,9,14 . To date there has been no large-scale evaluation of the role of microbial adaptation in controlling the temperature sensitivity of soil respiration. This lack of understanding adds considerable uncertainty to predictions of the magnitude and direction of carbon-cycle feedb...
Tropical soils contain a third of global soil carbon 1 , so destabilization of soil organic matter caused by the approximate 4°C warming predicted for tropical regions this century could accelerate climate change by releasing additional carbon dioxide (CO2) to the atmosphere 2-5 . Theory predicts that warming should cause only modest carbon loss in tropical soils relative to those at higher latitudes 4,6 , but there have been no warming experiments in tropical forests to test this prediction 7 . Here we show that in situ experimental warming of a lowland tropical forest soil on Barro Colorado Island, Panama, caused an unexpectedly large increase in soil CO2 emissions. Two years of warming of the whole soil profile by 4 o C increased CO2 emission by 55% compared to soils at ambient temperature. The additional CO2 originated from heterotrophic rather than autotrophic sources and equated to a loss of 8.2 ± 4.2 (± 1 SE) Mg C ha -1 yr -1 from the breakdown of soil organic matter. During this time, we detected no acclimation of respiration rates, no thermal compensation or change in temperature sensitivity of enzyme activities, and no change in microbial carbon-use efficiency. These results demonstrate a high sensitivity of soil carbon in tropical forests to warming, which represents a potentially substantial positive feedback to climate change.
More than 200 years ago, Alexander von Humboldt reported that tropical plant species richness decreased with increasing elevation and decreasing temperature. Surprisingly, coordinated patterns in plant, bacterial, and fungal diversity on tropical mountains have not yet been observed, despite the central role of soil microorganisms in terrestrial biogeochemistry and ecology. We studied an Andean transect traversing 3.5 km in elevation to test whether the species diversity and composition of tropical forest plants, soil bacteria, and fungi follow similar biogeographical patterns with shared environmental drivers. We found coordinated changes with elevation in all three groups: species richness declined as elevation increased, and the compositional dissimilarity among communities increased with increased separation in elevation, although changes in plant diversity were larger than in bacteria and fungi. Temperature was the dominant driver of these diversity gradients, with weak influences of edaphic properties, including soil pH. The gradients in microbial diversity were strongly correlated with the activities of enzymes involved in organic matter cycling, and were accompanied by a transition in microbial traits towards slower-growing, oligotrophic taxa at higher elevations. We provide the first evidence of coordinated temperature-driven patterns in the diversity and distribution of three major biotic groups in tropical ecosystems: soil bacteria, fungi, and plants. These findings suggest that interrelated and fundamental patterns of plant and microbial communities with shared environmental drivers occur across landscape scales. These patterns are revealed where soil pH is relatively constant, and have implications for tropical forest communities under future climate change.
Terrestrial biogeochemical feedbacks to the climate are strongly modulated by the temperature response of soil microorganisms. Tropical forests, in particular, exert a major influence on global climate because they are the most productive terrestrial ecosystem. We used an elevation gradient across tropical forest in the Andes (a gradient of 20°C mean annual temperature, MAT), to test whether soil bacterial and fungal community growth responses are adapted to long‐term temperature differences. We evaluated the temperature dependency of soil bacterial and fungal growth using the leucine‐ and acetate‐incorporation methods, respectively, and determined indices for the temperature response of growth: Q 10 (temperature sensitivity over a given 10oC range) and T min (the minimum temperature for growth). For both bacterial and fungal communities, increased MAT (decreased elevation) resulted in increases in Q 10 and T min of growth. Across a MAT range from 6°C to 26°C, the Q 10 and T min varied for bacterial growth ( Q 10–20 = 2.4 to 3.5; T min = −8°C to −1.5°C) and fungal growth ( Q 10–20 = 2.6 to 3.6; T min = −6°C to −1°C). Thus, bacteria and fungi did not differ significantly in their growth temperature responses with changes in MAT. Our findings indicate that across natural temperature gradients, each increase in MAT by 1°C results in increases in T min of microbial growth by approximately 0.3°C and Q 10–20 by 0.05, consistent with long‐term temperature adaptation of soil microbial communities. A 2°C warming would increase microbial activity across a MAT gradient of 6°C to 26°C by 28% to 15%, respectively, and temperature adaptation of microbial communities would further increase activity by 1.2% to 0.3%. The impact of warming on microbial activity, and the related impact on soil carbon cycling, is thus greater in regions with lower MAT. These results can be used to predict future changes in the temperature response of microbial activity over different levels of warming and over large temperature ranges, extending to tropical regions.
1. The Andes are predicted to warm by 3–5 °C this century with the potential to alter the processes regulating carbon (C) cycling in these tropical forest soils. This rapid warming is expected to stimulate soil microbial respiration and change plant species distributions, thereby affecting the quantity and quality of C inputs to the soil and influencing the quantity of soil-derived CO2 released to the atmosphere.2. We studied tropical lowland, premontane and montane forest soils taken from along a 3200-m elevation gradient located in south-east Andean Peru. We determined how soil microbial communities and abiotic soil properties differed with elevation. We then examined how these differences in microbial composition and soil abiotic properties affected soil C-cycling processes, by amending soils with C substrates varying in complexity and measuring soil heterotrophic respiration (RH).3. Our results show that there were consistent patterns of change in soil biotic and abiotic properties with elevation. Microbial biomass and the abundance of fungi relative to bacteria increased significantly with elevation, and these differences in microbial community composition were strongly correlated with greater soil C content and C:N (nitrogen) ratios. We also found that RH increased with added C substrate quality and quantity and was positively related to microbial biomass and fungal abundance.4. Statistical modelling revealed that RH responses to changing C inputs were best predicted by soil pH and microbial community composition, with the abundance of fungi relative to bacteria, and abundance of gram-positive relative to gram-negative bacteria explaining much of the model variance.5. Synthesis. Our results show that the relative abundance of microbial functional groups is an important determinant of RH responses to changing C inputs along an extensive tropical elevation gradient in Andean Peru. Although we do not make an experimental test of the effects of climate change on soil, these results challenge the assumption that different soil microbial communities will be ‘functionally equivalent’ as climate change progresses, and they emphasize the need for better ecological metrics of soil microbial communities to help predict C cycle responses to climate change in tropical biomes.
Summary• Arbuscular mycorrhizal fungi (AMF) are widespread in tropical forests and represent a major sink of photosynthate, yet their contribution to soil respiration in such ecosystems remains unknown.• Using in-growth mesocosms we measured AMF mycelial respiration in two separate experiments: (1) an experiment in a semi-evergreen moist tropical forest, and (2) an experiment with 6-m-tall Pseudobombax septenatum in 4.5-m 3 containers, for which we also determined the dependence of AMF mycelial respiration on the supply of carbon from the plant using girdling and root-cutting treatments.• In the forest, AMF mycelia respired carbon at a rate of 1.4 t ha )1 yr )1 , which accounted for 14 ± 6% of total soil respiration and 26 ± 12% of root-derived respiration. For P. septenatum, 40 ± 6% of root-derived respiration originated from AMF mycelia and carbon was respired < 4 h after its supply from roots.• We conclude that arbuscular mycorrhizal mycelial respiration can be substantial in lowland tropical forests. As it is highly dependent on the recent supply of carbon from roots, a function of aboveground fixation, AMF mycelial respiration is therefore an important pathway of carbon flux from tropical forest trees to the atmosphere.
While lignin geochemistry has been extensively investigated in the Amazon River, little is known about lignin distribution and dynamics within deep, stratified river channels or its transformations within soils prior to delivery to rivers. We characterized lignin phenols in soils, river particulate organic matter (POM), and dissolved organic matter (DOM) across a 4 km elevation gradient in the Madre de Dios River system, Peru, as well as in marine sediments to investigate the source‐to‐sink evolution of lignin. In soils, we found more oxidized lignin in organic horizons relative to mineral horizons. The oxidized lignin signature was maintained during transfer into rivers, and lignin was a relatively constant fraction of bulk organic carbon in soils and riverine POM. Lignin in DOM became increasingly oxidized downstream, indicating active transformation of dissolved lignin during transport, especially in the dry season. In contrast, POM accumulated undegraded lignin downstream during the wet season, suggesting that terrestrial input exceeded in‐river degradation. We discovered high concentrations of relatively undegraded lignin in POM at depth in the lower Madre de Dios River in both seasons, revealing a woody undercurrent for its transfer within these deep rivers. Our study of lignin evolution in the soil‐river‐ocean continuum highlights important seasonal and depth variations of river carbon components and their connection to soil carbon pools, providing new insights into fluvial carbon dynamics associated with the transfer of lignin biomarkers from source to sink.
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