The Carbon Science Group uses both observational data and models to improve understanding of carbon sinks and predict the impact of climate change on the carbon cycle. The PI’s of the Science Group are Steve Pacala and Lars Hedin of the Department of Ecology and Evolutionary Biology, and Michael Bender, David Medvigy, Francois Morel and Jorge Sarmiento from the Department of Geosciences.
New insights into the CO2 fertilization sink
Research indicates that, despite water and nutrient limitation, forest carbon uptake will likely keep pace with CO2 increases in the atmosphere, maintaining a large sink for anthropogenic carbon.
Cutting-edge modeling tools
CMI’s innovative land and ocean inputs to GFDL’s Earth System Model are helping to provide state-of-the-art predictions of future climate and ecosystem responses.
Groundbreaking observationsNew field-based observational efforts:
- have dramatically improved our ability to measure ocean carbon uptake;
- suggest that high-latitude ecosystems are at risk from climate change; and
- show that the climate-CO2 connection extends back at least 1 million years.
Forests have taken up a large fraction of CO2 emitted by humans, substantially slowing the rise of atmospheric CO2 levels. The Pacala, Hedin, and Medvigy research groups are investigating how future forest storage of carbon will be impacted by increasing CO2 levels and climate change. Their insights are leading to new tools that will be incorporated into LM3, the land model component of GFDL’s Earth System Model, to improve its representation of forest processes and predictions of future climate.
The impact of increased CO2 on forest carbon storage, or “CO2 fertilization,” remains controversial. Estimates of terrestrial carbon uptake made over a decade ago commonly ignored nutrient limitation and predicted large carbon sinks in response to increasing atmospheric CO2. Coupled carbon-nutrient models were subsequently developed and predicted far smaller carbon sinks, but are inconsistent with field-based CO2 fertilization experiments that seem to affirm the original larger estimates. To address this inconsistency, Caroline Farrior, Ray Dybzinski, and Steve Pacala are using models of allocation and carbon storage in forests to investigate how plants’ competitive responses impact carbon sinks in nutrient and water-limited environments.
The group found two main impacts of increasing atmospheric CO2 on forest carbon storage. First, plants will shift allocation patterns in such a way that they will use all additional carbon provided. Because wood has a low nitrogen-to-carbon ratio and is always beneficial to plants in competition for light, nitrogen-limited plants under high CO2 increase their investment in wood, sacrificing a small amount of nitrogen in leaves or fine roots in order to make use of extra carbon in wood.
If plants are also water-limited, enhanced CO2 benefits carbon sinks further. Increased water-use efficiency resulting from increased CO2 frees plants from water-limitation and intense competition for water belowground. As a result, plants decrease investment in fine roots, allowing even greater storage of carbon as woody biomass. Taken together, the team finds that nitrogen limitation does not work to decrease carbon storage in forests, and, if water is scarce, that belowground limitation is actually a driver of increases in carbon storage.
As these competitive allocation patterns are critical to carbon allocation, the team has built the machinery to include them into the Earth System Model at GFDL (in collaboration with Ensheng Weng, Elena Shevliakova, and Sergey Malyshev).
In tropical forests, legume trees that fix nitrogen can play a large role in combating nutrient limitation and enhancing carbon storage. The Hedin and Medvigy groups are investigating this phenomenon using both field observations and numerical models.
In a recent paper published in Nature, lead author and postdoctoral scholar Sarah Batterman reported that nitrogen-fixing species can help overcome ecosystem-scale deficiencies in nitrogen that emerge during periods of rapid biomass accumulation in tropical forests, and they consequently have a strong impact on the ability of tropical forests to sequester CO2. Over a 300-year period in Panama, such nitrogen-fixing tree species accumulated carbon up to nine times faster per individual than their non-fixing neighbors.
Postdoctoral scholar Jennifer Levy has been using measurements to develop a regional-scale model relating tropical forest carbon accumulation to nitrogen, land use, and climate change that distinguishes between nitrogen-fixing and non-fixing trees. The model has been used to realistically predict forest carbon accumulation, nitrogen fixation, and the proportion of trees that are capable of nitrogen fixation. This property allows researchers, for the first time, to isolate the control of nitrogen-fixing trees on carbon accumulation in re-growing tropical forests. As next steps, they plan to use the regional-scale model to inform the development of the nitrogen cycle in GFDL’s global-scale land model, LM3. Using LM3, they will be able to understand how their results scale up from particular regions to the entire globe.
The global impact of drought on the carbon cycle is also a critical unknown that the Earth System Model at GFDL is uniquely poised to address, because of its unique treatment of species diversity and competition in forests. Adam Wolf of the Pacala group is working on multiple fronts to improve understanding of the diverse strategies plants use to deal with water limitation.
Water is the pre-eminent scarce resource for plants, and they compete desperately to attain it. Wolf is working to understand the extent of water “theft” belowground in a combination of field experiment, lab investigation, and modeling work (Figure 2). The field experiment takes place in the Silas Little Experimental Forest in central New Jersey. In this experiment, shelters are built around focal trees to divert rain water, and isotopically labeled water is applied instead. This labeled water can be traced to the different trees that take it up, allowing a quantification of the degree to which plants can “hoard” water in private fiefdoms, or instead compete in an open access commons. Wolf is using this work to recast models of plant responses to low humidity as plant responses to water status, which should be a better indicator of soil water availability.
The benefit for this understanding will be an improved understanding for how plants, especially forests, deal with water limitation, particularly to avoid drought-induced mortality. This work directly leads to improvements to the LM3 land surface model in its treatment of water limitation and forest mortality.
Biomass burning contributes large amounts of greenhouse gases and aerosols to the atmosphere every year. Wildfires are not the only source of this burning, however. People also use fire to manage land, in ways that can differ significantly from burning patterns in less-managed areas. Sam Rabin has helped develop a method that estimates the fraction of observed fire occurring on different landuse types, which has resulted in the first regional and global estimates of pasture burning extent and seasonality (Figure 3). Using these estimates, he is building a model that will simulate burning in croplands and pastures, as well as undisturbed and secondary lands, that will be incorporated in the GFDL Earth System Model. When development is complete, Rabin will be able to: answer questions about how fire has influenced the distribution of biomes around the world, explore how changing climate and land use will affect fire and therefore vegetation in the future, and assess the consequences of these changes for global climate.
The ocean also serves as a natural sink for anthropogenic carbon, taking up roughly as much as the terrestrial sink. The Bender group of CMI uses innovative observational techniques to determine current rates of carbon uptake by the ocean, while the Sarmiento group develops cutting-edge models to understand the controls on this uptake and to help predict its response to future climate change.
Over the course of the CMI grant, the Bender group has developed an instrument to make highprecision measurements of the concentration of dissolved inorganic carbon (DIC) by measuring isotope ratios, which can be done very accurately and rather easily. Through implementation of a new “double-spike” technique, this year the researchers have achieved a measurement precision which is at least 2 times better than the state of the art (0.03% vs. 0.06%). The instrument also has an analysis time of about only 2-8 minutes (up to 10 times shorter than the competition) and requires much less operator attention, making it a very attractive instrument for use in oceanographic cruises. This instrument has 3 applications. The first is measuring the seasonal cycle of dissolved inorganic carbon in a region to constrain the fertility of the waters. The second involves measuring the rate of increase in the surface water DIC concentration, along a cruise track, over a period of years. The rate of increase is the rate at which the surface ocean is taking up fossil fuel CO2. The third involves measuring DIC in deep sea waters at selected locations to determine the rate at which fossil fuel CO2 is mixed, very slowly, into this vast reservoir.
The Sarmiento group, in collaboration with scientists at GFDL, has developed a new high-resolution global earth system model for studying the dynamics of air-sea carbon fluxes and interior ocean carbon transport in the Southern Ocean. At present, the Southern Ocean accounts for up to half of the oceanic uptake of anthropogenic CO2 from the atmosphere. However, it is unknown how today’s uptake rate will respond to changing atmospheric forcing in the region. The uncertainty arises from a scarcity of observations over the Southern Ocean and the difficulty of modeling the small-scale eddy features, which play a pivotal role in the response of the ocean circulation. The old model had a resolution of 1°, whereas the new CM2.6 model has a resolution of 1/10°, which enables it to resolve eddies (~10 km across) and their impact on the response of the carbon uptake in the Southern Ocean to climate change (Figure 4). The model will be used to investigate the dynamical processes controlling the air-sea CO2 flux and to identify if localized carbon transport pathways exist within the ocean.
Adding biogeochemistry to ocean models is critical to predicting the future of the ocean carbon sink, but the extra calculations required can make models prohibitively time-consuming to run. The Sarmiento group is testing the sensitivity of carbon uptake modeled to the complexity of the ocean biogeochemical model, evaluating whether the three tracer configuration (the MINIBLING model) used within the 1/10 degree ocean configuration of GFDL’s coupled model CM2.6 is consistent with the more complex published BLING (Biology Light Iron Nutrient and Gas) model. This project will validate the biogeochemistry for the aforementioned project titled “Modeling the Southern Ocean CO2 sink at unprecedented resolution.”
Organic carbon in particles sinking from the sunlit surface is a food source for heterotrophic bacteria living in the deep ocean. Using a water column model, the Sarmiento group has found that bacterial colonization rates and activities on particles impact the depth at which organic carbon is transformed to CO2 via bacterial respiration, which can exert significant influence on the residence time and concentration of CO2 in the atmosphere and ocean. This means that as the climate warms, increasing ocean temperatures may alter bacterial activity and growth, with consequent feedbacks on the carbon cycle.
Because bacteria use oxygen and produce CO2 when they respire, changes in ocean oxygen concentrations would also be expected as ocean temperatures warm. In large regions of the ocean, oxygen is depleted to almost zero between 100 and 1000 m depth by respiration as bacteria consume organic carbon. In the future, the Sarmiento group plans to incorporate its water column model into a 3-dimensional ocean model to simulate the effects of bacterial activity on particulate carbon flux and oxygen utilization in the global ocean, and to help assess the impacts of oxygen depletion on marine species (see “Compression of marine habitats” under “Climate change impacts on ecosystems” below).
The Pacala, Sarmiento, Morel, and Bender groups are using models and laboratory experiments to understand how climate change will impact the terrestrial and marine biospheres.
In the past year, Anping Chen’s research focused on how terrestrial ecosystems respond to climate change. With remote sensing techniques and modeling, Chen and colleagues have found:
- vegetation growth responses to asymmetric daytime and night-time warming cause important variations in carbon uptake currently not captured in most models;
- the sensitivity of atmospheric CO2 growth rate to variations in tropical temperature has doubled over the last 50 years, but is not reproduced in model simulations; and
- under the Intergovernmental Panel on Climate Change (IPCC)-projected future climate scenarios, General Circulation Models (GCMs) used in the IPCC’s latest assessment report predict decreases of 1-15% in the extents of tropical forests by 2100.
In addition, the researchers evaluated the potential impact of future climate change on global biodiversity conservation priority areas. The research highlights a heterogeneous but highly sensitive ecosystem and carbon cycle response to climate change.
Because of experimental challenges, the rate of photosynthesis has never been measured directly in plants. Plants, like humans, respire to make energy, but this rate has never been measured in the daytime (in the light). Postdoctoral fellow Paul Gauthier, working with Michael Bender, has built an apparatus for making these measurements (Figure 5). Air is passed through a chamber containing a leaf which water has been “labeled” with the heavy oxygen isotope 18O. The rate of photosynthesis, and respiration in the light, are determined by analyzing the change in the concentration of O2, and its isotopic composition, as air passes through the chamber.
Gauthier has conducted preliminary experiments documenting a linear increase of photosynthesis with light, as indicated by theory, and increased rates of respiration as illumination falls. In the coming year, experiments are planned to investigate the influence of atmospheric CO2 concentration on the energetics of plant growth.
The vertical range (thickness) of the habitat that can be used by organisms living in pelagic marine ecosystems is limited by the availability of oxygen. Recently, shallowing of oxygen depleted waters has been observed in many locations throughout the ocean, compressing the vertical habitat structure of marine ecosystems.
In an ongoing project, the Sarmiento group is developing new approaches to predict the extent of compression for many different species, as well as evaluating what impact additional environmental stressors such as ocean warming will have on oxygen acquisition in pelagic habitats. In particular, they will identify which physiologies will be most susceptible to changes in oxygen and other environmental stressors, with commercially fished species being of particular concern.
Marine phytoplankton are responsible for nearly half of Earth’s primary production but we have little understanding of how they will respond to global change. The most rapid changes are occurring in the highly productive waters of the Antarctic. François Morel and colleagues are using recent data from a six-month deployment at Palmer station in the Western Antarctic Peninsula (Figure 6), complemented with laboratory experiments with model species, to provide new insights into the adaptations responsible for the high productivity of phytoplankton in cold waters (< 0°C). This information will provide a basis for predicting the likely responses of the Antarctic flora to changing environmental parameters, such as increases in temperature and CO2 concentration. In early December, continuous recording of gas concentrations quantified a massive diatom bloom that drove the ambient CO2 concentration to nearly zero. Physiological and biochemical data showed that the organisms had a very high protein content to compensate for slow enzyme kinetics, and that particularities of their photosynthetic apparatus resulted in very low respiration rates. The net result is a much higher ratio of net/gross production compared to more temperate marine ecosystems. However, as high latitude temperatures warm, an increase in respiration is likely to more than offset the increasing rate of photosynthesis (gross production), lowering the net production in high latitude oceans. If confirmed, this result could have large implications for higher trophic levels, including krill and the large animals that feed on it.
The Bender group examines atmospheric gases trapped in ice cores to understand the history of CO2 and climate. The group is extending the CO2 record back in time by looking for ever-older ice in Antarctica.
The deepest ice cores yet drilled, targeted to encompass the longest possible continuous records, end at ice 800,000 years old. To extend this record, Michael Bender and colleagues have been searching Antarctic sites where, because of complex glacier flows influenced by the Transantarctic Mountains, older ice may be present near the surface. Working with John Higgins (Princeton) and collaborators from the University of Maine, Bender’s group drilled a 126-meter long ice core in the Allan Hills region of Antarctica and dated it to be 1,000,000 years old in the bottom 10 m. This age is 200,000 years older than the previous oldest ice. It takes us back to a time when glacial cycles lasted 40,000 years instead of the 100,000 year period characterizing the past 800,000 years.
Working with Ed Brook (Oregon State), the researchers have begun measuring greenhouse gases in this ice. Previous work has shown that there is a very strong link between atmospheric CO2 and global temperature over the past 800,000 years. The new data show that this link persisted in the earlier world of 40,000 year climate cycles. They also show that interglacials, known to be warmer between 0-400,000 years than between 400,000 and 800,000 years, were once again warmer prior to 800,000 years ago. The work also suggests that glacial periods in the 40,000 year world were not as cold as more recent glacial periods. The team is exploring the implications of these results for the dynamics of climate change. Already their results strengthen the empirical link between CO2 and global temperature.
Batterman S.A., L.O. Hedin, M .van Breugel, J. Ransijn, D.J. Craven, J.S. Hall, 2013. Key role of symbiotic dinitrogen fixation in tropical forest secondary succession. Nature 502: 224- 227. doi:10.1038/nature12525.
Beaulieu, C., S. A. Henson, J. L. Sarmiento, J. P. Dunne, S. C. Doney, R. R. Rykaczewski, and L. Bopp, 2013. Factors challenging our ability to detect long-term trends in ocean chlorophyll. Biogeosciences 10: 2711–2724. doi:10.5194/bg-10-2711-2013.
Bernardello, R., I. Marinov, J. B. Palter, J. L. Sarmiento, E. D. Galbraith, and R. D. Slater, 2013. Response of the ocean natural carbon storage to projected 21st century climate change. J. Climate, 131127131524002. doi:10.1175/JCLI-D-13-00343.1.
Berry, J.A., Wolf, A., Campbell, J.E., Baker, B.,Blake, N., Blake, D., Denning, A.S., Kawa, S.R., Montzka, S.A., Seibt, U., Stimler, K., Yakir, D., Zhu, Z., 2013. A coupled model of the global cycles of carbonyl sulfide and CO2: a possible new window on the carbon cycle. JGR-Biogeosciences 118: 1c11. doi:10.1002/ jgrg.20068.
Bianchi, D., Galbraith, E. D., Carozza, D. A., Mislan, K. A. S., and Stock, C. , 2013. Intensification of open-ocean oxygen depletion by vertically migrating animals. Nature Geosci., 6:545-548. doi:10.1038/ ngeo1837.
Bianchi, D., C. Stock, E. D. Galbraith, and J. L. Sarmiento, 2013. Diel vertical migration: Ecological controls and impacts on the biological pump in a one-dimensional ocean model. Global Biogeochem. Cycles 27: 1-14. doi:10.1002/gbc.20031.
Chen A.P., J.W. Lichstein, J.L.D. Osnas, S.W. Pacala, 2014. Species-independent down-regulation of leaf photosynthesis and respiration in response to shading: evidence from six temperate forest tree species. PLoS ONE, accepted.
Doughty, C.E., A. Wolf, Y. Malhi, 2013. The impact of large animal extinctions on nutrient fluxes in early river valley civilizations. Ecosphere 4(12):148. doi:10.1890/ES13- 00221.1.
Doughty, C.E., A. Wolf, Y. Malhi, 2013. The legacy of the Pleistocene megafauna extinctions on nutrient availability in Amazonia. Nature Geosciences. doi: 10.1038/ ngeo1895.
Frölicher, T. L., F. Joos, C. C. Raible, and J. L. Sarmiento, 2013. Atmospheric CO2 response to volcanic eruptions: The role of ENSO, season, and variability. Global Biogeochem. Cycles, 27: 239-251. doi:10.1002/gbc.20028. Frölicher, T. L., M. Winton, and J. L. Sarmiento, 2013. Continued global warming after CO2 emissions stoppage. Nature Climate Change, 3: 1–5. doi:10.1038/nclimate2060.
Guan, K., M. Pan, A,Wolf, H. Li, K.K. Caylor, D. Medvigy, J. Sheffield, E.F. Wood, N. Aloysius, 2014. Contrasting photosynthesis cycles reveal geographical differences in global tropical evergreen forests. In review.
Huang, K., N. Cassar, R. Wanninhkof, and M. Bender, 2014. An isotope dilution method for high-frequency measurements of dissolved inorganic carbon concentration in the surface ocean, Limnology and Oceanography: Methods, 11: 572-583. doi: 10.4319/lom.2013.11.572.
Jonssen, B., S. Doney, J. Dunne, and M. Bender, 2013. Evaluation of Southern Ocean O2/ Ar–based measurements of net community production in a model framework, Journal of Geophysical Research: Biogeosciences, 118. doi: 10.1002/jgrg.20032.
Kearney, K. A., C. Stock, and J. L. Sarmiento, 2013. Amplification and attenuation of increased primary production in a marine food web. Mar Ecol Prog Ser, 491: 1–14. doi:10.3354/meps10484.
Levy J, D. Medvigy, L. Hedin, S.A. Batterman, X. Xu, 2013. Tropical forest carbon sink depends on tree functional diversity and competition. American Geophysical Union Fall 2013 Meeting, San Francisco, CA.
Lichstein, J. W., N.-Z. Golaz, S. Malyshev, E. Shevliakova, T. Zhang, J. Sheffield, R. A. Birdsey, J. L. Sarmiento, and S. W. Pacala, in press, Sep 2013. Confronting the functional response of terrestrial biosphere models with forest inventory data. Ecological Applications. doi:10.1890/13-0600.1.
Li J., X. Lin, A. Chen, T. Peterson, K. Ma et al., 2013. Global priority conservation areas in the face of 21st century climate change. PLoS ONE 8: e54839. doi:10.1371/journal. pone.0054839.
Majkut, J., B. Carter, C. O. Dufour, T. L. Frölicher, K. Rodgers, and J. Sarmiento, 2014. An observing system simulation for Southern Ocean CO2 uptake. Proc. R. Soc. B, submitted.
Majkut, J. D., J. L. Sarmiento, and K. B. Rodgers, revised, Aug 2013. A growing oceanic carbon uptake: results from an inversion study of surface pCO2 data. Global Biogeochem. Cycles, submitted.
Medvigy D, J. Levy, X. Xu, S.A. Batterman, L. Hedin, 2013. Simulating changes in ecosystem structure and composition in response to climate change: a case study focused on tropical nitrogen-fixing trees. American Geophysical Union Fall 2013 Meeting, San Francisco, CA.
Mislan, K. A. S., C. A. Stock, J. P. Dunne, and J. L. Sarmiento, 2014. Group behavior among model bacteria influences particulate carbon remineralization depths. ISME Journal, submitted.
Peng S.S., S.L. Piao, P. Ciais, R.B. Myneni, A.P. Chen, F. Chevallier, A.J. Dolman, I.A. Janssens, J. Penuelas, G.X. Zhang, S. Vicca, S.Q. Wan, S.P. Wang, H. Zeng, 2013. Asymmetric effects of daytime and night-time warming on Northern Hemisphere vegetation. Nature 501: 88-92.
Peng S.S., S.L. Piao, Z.H. Shen, P. Ciais, Z.Z. Sun, S.P. Chen, C. Bacour, P. Peylin, A.P. Chen, 2013. Precipitation amount, seasonality and frequency regulate carbon cycling of a semiarid grassland ecosystem in Inner Mongolia, China: A modeling analysis. Agricultural and Forest Meteorology 178: 46-55.
Plancherel, Y., K. B. Rodgers, R. M. Key, A. R. Jacobson, and J. L. Sarmiento, 2013. Role of regression model selection and station distribution on the estimation of oceanic anthropogenic carbon change by eMLR. Biogeosciences 10: 4801-4831. doi:10.5194/bg- 10-4801-2013.
Rabin, S., S. Pacala, B. Magi, E. Shevliakova, 2013. Regional patterns of cropland and pasture burning: Statistical separation of signals from remote sensing products. American Geophysical Union Fall 2013 Meeting, San Francisco, CA.
Raupach, M. R., J. L. Sarmiento, J. G. Canadell, T. Gasser, M. Gloor, R. A. Houghton, C. Le Quéré, and C. M. Trudinger, 2014. Detection and attribution of trends in CO2 airborne fraction, cumulative airborne fraction and sink uptake rate. Biogeosciences, submitted.
Rubino, M., D. M. Etheridge, C. M. Trudinger, C. E. Allison, M. O. Battle, R. L. Langenfelds, L. P. Steele, M. Curran, M. Bender, J. W. C. White, T. M. Jenk, T. Blunier, and R. J. Francey, 2013. A revised 1000 year atmospheric δ13CCO2 record from Law Dome and South Pole, Antarctica. Journal of Geophysical Research- Atmospheres, 118: 8482-8400. doi:10.10002/ jgrd.50668.
Shen M.G., Z.Z. Sun, S.P. Wang, G.X. Zhang, W.D. Kong WD, A.P. Chen, S.L. Piao, 2013. No evidence of continuously advanced greenup dates in the Tibetan Plateau over the last decade. PNAS 110: E2329-E2329.
Tortell P.D., W.H. Dacey, H.W. Ducklow, J.J. Grzymski, J.N. Young, J.A.L. Goldman, S.A. Kranz, K.S. Bernard, and F.M.M. Morel, 2014. Metabolic balance of coastal Antarctic waters revealed by high frequency pCO2 and O2/Ar measurements. PNAS, in review.
Wang X.H., S.L. Piao, P. Ciais, P. Friedlingstein, R.B. Myneni, P. Cox, M. Heimann, J. Miller, S.S. Peng, T. Wang, H. Yang, A.P. Chen, 2014. A two-fold increase of carbon cycle sensitivity to tropical temperature variations. Nature. doi:10.1038/nature12915.
Wang S.P., A.P. Chen, J.Y., S.W. Pacala. 2013. Speciation rates decline through time in individual-based models of speciation and extinction. The Amer. Naturalist 182: E83– E93.
Wang S.P., A.P. Chen, J.Y., S.W. Pacala. 2013. Why Abundant Tropical Tree Species Are Phylogenetically Old. PNAS. doi: 10.1073/ pnas.1314992110.
Wolf, A., W.R.L. Anderegg, N.B. Zimmermann, P. Busby, J. Christensen, 2014. California’s endemic flora is disproportionately affected by 20th century warming. Revised; in re-review.
Wolf, A., C.E. Doughty, Y. Malhi, , 2013. Lateral diffusion of nutrients by mammalian herbivores in terrestrial ecosystems. Plos ONE 8(8): e71352. doi:10.1371/journal. pone.0071352.
Wolf, A., J.W. Lichstein, S.W. Pacala, J.A. Berry, 2014. J.A. Geometric optics of closed forest canopies. Remote Sensing of Environment, in revision.
Zeng Z.Z., S.L. Piao, A.P. Chen, X. Lin, H.J. Nan, J.S. Li, P. Ciais, 2013. Committed changes in tropical tree cover under the projected 21st century climate change. Sci. Rep., 3. doi:10.1038/srep01951.