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    Increasing sensitivity of dryland vegetation greenness to precipitation due to rising atmospheric CO2

    Pascolini-Campbell, M., Reager, J. T., Chandanpurkar, H. A. & Rodell, M. A 10 per cent increase in global land evapotranspiration from 2003 to 2019. Nature 593, 543–547 (2021).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Yuan, W. et al. Increased atmospheric vapor pressure deficit reduces global vegetation growth. Sci. Adv. 5, eaax1396 (2019).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Zhang, Y., Parazoo, N. C., Williams, A. P., Zhou, S. & Gentine, P. Large and projected strengthening moisture limitation on end-of-season photosynthesis. Proc. Natl Acad. Sci. 117, 9216–9222 (2020).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Berg, A., Sheffield, J. & Milly, P. C. D. Divergent surface and total soil moisture projections under global warming. Geophys. Res. Lett. 44, 2016GL071921 (2017).
    Google Scholar 
    Williams, A. P. et al. Large contribution from anthropogenic warming to an emerging North American megadrought. Science 368, 314–318 (2020).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Liu, Y., Kumar, M., Katul, G. G., Feng, X. & Konings, A. G. Plant hydraulics accentuates the effect of atmospheric moisture stress on transpiration. Nat. Clim. Change 10, 691–695 (2020).ADS 
    CAS 
    Article 

    Google Scholar 
    Guan, K. et al. Photosynthetic seasonality of global tropical forests constrained by hydroclimate. Nat. Geosci. 8, 284–289 (2015).ADS 
    CAS 
    Article 

    Google Scholar 
    Dannenberg, M. P., Wise, E. K. & Smith, W. K. Reduced tree growth in the semiarid United States due to asymmetric responses to intensifying precipitation extremes. Sci. Adv. 5, eaaw0667 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Poulter, B. et al. Contribution of semi-arid ecosystems to interannual variability of the global carbon cycle. Nature 509, 600–603 (2014).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Zhou, L. et al. Widespread decline of Congo rainforest greenness in the past decade. Nature 509, 86–90 (2014).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Humphrey, V. et al. Sensitivity of atmospheric CO 2 growth rate to observed changes in terrestrial water storage. Nature 560, 628–631 (2018).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Wang, X. et al. A two-fold increase of carbon cycle sensitivity to tropical temperature variations. Nature 506, 212–215 (2014).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Huxman, T. E. et al. Convergence across biomes to a common rain-use efficiency. Nature 429, 651–654 (2004).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Maurer, G. E., Hallmark, A. J., Brown, R. F., Sala, O. E. & Collins, S. L. Sensitivity of primary production to precipitation across the United States. Ecol. Lett. 23, 527–536 (2020).PubMed 
    Article 

    Google Scholar 
    Hsu, J. S., Powell, J. & Adler, P. B. Sensitivity of mean annual primary production to precipitation. Glob. Change Biol. 18, 2246–2255 (2012).ADS 
    Article 

    Google Scholar 
    Zuidema, P. A. et al. Recent CO2 rise has modified the sensitivity of tropical tree growth to rainfall and temperature. Glob. Change Biol. 26, 4028–4041 (2020).ADS 
    Article 

    Google Scholar 
    Bansal, S., James, J. J. & Sheley, R. L. The effects of precipitation and soil type on three invasive annual grasses in the western United States. J. Arid Environ. 104, 38–42 (2014).ADS 
    Article 

    Google Scholar 
    Konings, A. G., Williams, A. P. & Gentine, P. Sensitivity of grassland productivity to aridity controlled by stomatal and xylem regulation. Nat. Geosci. 10, 284–288 (2017).ADS 
    CAS 
    Article 

    Google Scholar 
    O’Connor, J. C. et al. Forests buffer against variations in precipitation. Glob. Change Biol., 27, 4686–4696 (2021).Schuldt, B. et al. Change in hydraulic properties and leaf traits in a tall rainforest tree species subjected to long-term throughfall exclusion in the perhumid tropics. Biogeosciences 8, 2179–2194 (2011).ADS 
    Article 

    Google Scholar 
    Zhang, W. et al. Ecosystem structural changes controlled by altered rainfall climatology in tropical savannas. Nat. Commun. 10, 671 (2019).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Adams, M. A., Buckley, T. N., Binkley, D., Neumann, M. & Turnbull, T. L. CO2, nitrogen deposition and a discontinuous climate response drive water use efficiency in global forests. Nat. Commun. 12, 5194 (2021).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Abel, C. et al. The human–environment nexus and vegetation–rainfall sensitivity in tropical drylands. Nat. Sustain. 4, 25–32 (2021).Green, J. K. et al. Regionally strong feedbacks between the atmosphere and terrestrial biosphere. Nat. Geosci. 10, 410–414 (2017).ADS 
    MathSciNet 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Lian, X. et al. Multifaceted characteristics of dryland aridity changes in a warming world. Nat. Rev. Earth Environ. 2, 232–250 (2021).ADS 
    Article 

    Google Scholar 
    Zhang, W., Brandt, M., Guichard, F., Tian, Q. & Fensholt, R. Using long-term daily satellite based rainfall data (1983–2015) to analyze spatio-temporal changes in the sahelian rainfall regime. J. Hydrol. 550, 427–440 (2017).ADS 
    Article 

    Google Scholar 
    Martens, B. et al. GLEAM v3: satellite-based land evaporation and root-zone soil moisture. Geosci. Model Dev. 10, 1903–1925 (2017).ADS 
    Article 

    Google Scholar 
    Huntzinger, D. N. et al. The North American carbon program multi-scale synthesis and terrestrial model intercomparison project – part 1: overview and experimental design. Geosci. Model Dev. 6, 2121–2133 (2013).ADS 
    Article 

    Google Scholar 
    Porporato, A., Daly, E. & Rodriguez-Iturbe, I. Soil water balance and ecosystem response to climate change. Am. Naturalist 164, 625–632 (2004).Article 

    Google Scholar 
    Good, S. P., Moore, G. W. & Miralles, D. G. A mesic maximum in biological water use demarcates biome sensitivity to aridity shifts. Nat. Ecol. Evol. 1, 1883 (2017).PubMed 
    Article 

    Google Scholar 
    Donohue, R. J., Roderick, M. L., McVicar, T. R. & Yang, Y. A simple hypothesis of how leaf and canopy-level transpiration and assimilation respond to elevated CO 2 reveals distinct response patterns between disturbed and undisturbed vegetation: vegetation responses to elevated CO2. J. Geophys. Res. Biogeosci. 122, 168–184 (2017).CAS 
    Article 

    Google Scholar 
    Milly, P. C. D. & Dunne, K. A. Potential evapotranspiration and continental drying. Nat. Clim. Change 6, 946 (2016).ADS 
    Article 

    Google Scholar 
    Yang, Y., Roderick, M. L., Zhang, S., McVicar, T. R. & Donohue, R. J. Hydrologic implications of vegetation response to elevated CO 2 in climate projections. Nat. Clim. Change 9, 44–48 (2019).ADS 
    Article 
    CAS 

    Google Scholar 
    Wolf, A., Anderegg, W. R. L. & Pacala, S. W. Optimal stomatal behavior with competition for water and risk of hydraulic impairment. Proc. Natl Acad. Sci. 113, E7222–E7230 (2016).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Keenan, T. F. et al. Increase in forest water-use efficiency as atmospheric carbon dioxide concentrations rise. Nature 499, 324–327 (2013).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Guerrieri, R. et al. Disentangling the role of photosynthesis and stomatal conductance on rising forest water-use efficiency. Proc. Natl Acad. Sci. USA 116, 16909–16914 (2019).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Anderegg, W. R. L. et al. Hydraulic diversity of forests regulates ecosystem resilience during drought. Nature 561, 538–541 (2018).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    González de Andrés, E. et al. Tree-to-tree competition in mixed European beech-Scots pine forests has different impacts on growth and water-use efficiency depending on site conditions. J. Ecol. 106, 59–75 (2018).Article 
    CAS 

    Google Scholar 
    Donohue, R. J., Roderick, M. L., McVicar, T. R. & Farquhar, G. D. Impact of CO2 fertilization on maximum foliage cover across the globe’s warm, arid environments. Geophys. Res. Lett. 40, 3031–3035 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    Gonsamo, A. et al. Greening drylands despite warming consistent with carbon dioxide fertilization effect. Glob. Change Biol. 27, 3336–3349 (2021).Article 

    Google Scholar 
    Mankin, J. S., Smerdon, J. E., Cook, B. I., Williams, A. P. & Seager, R. The curious case of projected twenty-first-century drying but greening in the American West. J. Clim. 30, 8689–8710 (2017).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Fatichi, S. et al. Partitioning direct and indirect effects reveals the response of water-limited ecosystems to elevated CO2. Proc. Natl Acad. Sci. 113, 12757–12762 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ainsworth, E. A. & Rogers, A. The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions: Photosynthesis and stomatal conductance responses to rising [CO2]. Plant, Cell Environ. 30, 258–270 (2007).CAS 
    Article 

    Google Scholar 
    Morgan, J. A. et al. C4 grasses prosper as carbon dioxide eliminates desiccation in warmed semi-arid grassland. Nature 476, 202–205 (2011).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Duursma, R. A. et al. On the minimum leaf conductance: its role in models of plant water use, and ecological and environmental controls. N. Phytologist 221, 693–705 (2019).Article 

    Google Scholar 
    Ukkola, A. M. et al. Reduced streamflow in water-stressed climates consistent with CO2 effects on vegetation. Nat. Clim. Change 6, 75–78 (2015).ADS 
    Article 

    Google Scholar 
    Thompson, S. E., Harman, C. J., Heine, P. & Katul, G. G. Vegetation-infiltration relationships across climatic and soil type gradients: vegetation-infiltration relationships. J. Geophys. Res. 115, G02023 (2010).ADS 

    Google Scholar 
    Norby, R. J. & Zak, D. R. Ecological lessons from free-air CO2 enrichment (FACE) experiments. Annu. Rev. Ecol. Evol. Syst. 42, 181–203 (2011).Article 

    Google Scholar 
    Fatichi, S., Leuzinger, S. & Körner, C. Moving beyond photosynthesis: from carbon source to sink-driven vegetation modeling. N. Phytologist 201, 1086–1095 (2014).CAS 
    Article 

    Google Scholar 
    Cui, J. et al. Vegetation forcing modulates global land monsoon and water resources in a CO2-enriched climate. Nat. Commun. 11, 5184 (2020).Gedney, N. et al. Detection of a direct carbon dioxide effect in continental river runoff records. Nature 439, 835–838 (2006).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Cui, J. et al. Vegetation response to rising CO2 amplifies contrasts in water resources between global wet and dry land Areas. Geophys. Res. Lett. 48, e2021GL094293 (2021).Yang, Y. et al. Low and contrasting impacts of vegetation CO2 fertilization on global terrestrial runoff over 1982–2010: Accounting for aboveground and belowground vegetation-CO2 effects. Hydrol. Earth Syst. Sci. 25, 3411–3427 (2021).ADS 
    CAS 
    Article 

    Google Scholar 
    Keenan, T. F. et al. A constraint on historic growth in global photosynthesis due to increasing CO2. Nature 600, 253–258 (2022).ADS 
    Article 
    CAS 

    Google Scholar 
    Sang, Y. et al. Comment on “Recent global decline of CO 2 fertilization effects on vegetation photosynthesis”. Science 373, eabg4420 (2021).PubMed 
    Article 
    CAS 

    Google Scholar 
    Jump, A. S. et al. Structural overshoot of tree growth with climate variability and the global spectrum of drought‐induced forest dieback. Glob. Change Biol. 23, 3742–3757 (2017).ADS 
    Article 

    Google Scholar 
    Zhang, Y., Keenan, T. F. & Zhou, S. Exacerbated drought impacts on global ecosystems due to structural overshoot. Nat. Ecol. Evol. 5, 1490–1498 (2021).Ahlstrom, A. et al. The dominant role of semi-arid ecosystems in the trend and variability of the land CO2 sink. Science 348, 895–899 (2015).ADS 
    PubMed 
    Article 
    CAS 

    Google Scholar 
    Pinzon, J. E. & Tucker, C. J. A non-stationary 1981–2012 AVHRR NDVI3g time series. Remote Sens. 6, 6929–6960 (2014).ADS 
    Article 

    Google Scholar 
    Tian, F. et al. Evaluating temporal consistency of long-term global NDVI datasets for trend analysis. Remote Sens. Environ. 163, 326–340 (2015).ADS 
    Article 

    Google Scholar 
    Zhu, Z. et al. Greening of the Earth and its drivers. Nat. Clim. Change 6, 791–795 (2016).ADS 
    CAS 
    Article 

    Google Scholar 
    Zhu, Z. et al. Global data sets of vegetation leaf area index (LAI)3g and fraction of photosynthetically active radiation (FPAR)3g derived from global inventory modeling and mapping studies (GIMMS) normalized difference vegetation index (NDVI3g) for the period 1981 to 2011. Remote Sens. 5, 927–948 (2013).ADS 
    Article 

    Google Scholar 
    Harris, I., Osborn, T. J., Jones, P. & Lister, D. Version 4 of the CRU TS monthly high-resolution gridded multivariate climate dataset. Sci. Data 7, 109 (2020).Schneider, U. et al. GPCC’s new land surface precipitation climatology based on quality-controlled in situ data and its role in quantifying the global water cycle. Theor. Appl Climatol. 115, 15–40 (2014).ADS 
    Article 

    Google Scholar 
    Prado, R. & West, M. Time series: modeling, computation, and inference (CRC Press, 2010).West, M. & Harrison, J. Bayesian forecasting and dynamic models (Springer, 1997).Liu, Y., Kumar, M., Katul, G. G. & Porporato, A. Reduced resilience as an early warning signal of forest mortality. Nat. Clim. Chang. 9, 880–885 (2019).ADS 
    Article 

    Google Scholar 
    Medlyn, B. E. et al. Reconciling the optimal and empirical approaches to modelling stomatal conductance. Glob. Change Biol. 17, 2134–2144 (2011).ADS 
    Article 

    Google Scholar  More

  • in

    Effects of vegetation spatial pattern on erosion and sediment particle sorting in the loess convex hillslope

    Zhao, B. H. et al. Spatial distribution of soil organic carbon and its influencing factors under the condition of ecological construction in a hilly-gully watershed of the Loess Plateau China. Geoderma 296, 10–17 (2017).ADS 
    CAS 
    Article 

    Google Scholar 
    Shi, P. et al. Soil respiration and response of carbon source changes to vegetation restoration in the Loess Plateau China. Sci. Total Environ. 707, 135507 (2019).ADS 
    PubMed 
    Article 
    CAS 

    Google Scholar 
    Zhang, Y. et al. Effects of farmland conversion on the stoichiometry of carbon, nitrogen, and phosphorus in soil aggregates on the Loess Plateau of China. Geoderma 351, 188–196 (2019).ADS 
    CAS 
    Article 

    Google Scholar 
    Chang, E. H. et al. Using water isotopes to analyze water uptake during vegetation succession on abandoned cropland on the Loess Plateau China. CATENA 181, 104095 (2019).Article 

    Google Scholar 
    Chang, E. H. et al. The impact of vegetation successional status on slope runoff erosion in the Loess Plateau of China. Water 11, 2614 (2019).CAS 
    Article 

    Google Scholar 
    Sun, L. Y., Zhou, J. L., Cai, Q. G., Liu, S. X. & Xiao, J. G. Comparing surface erosion processes in four soils from the Loess Plateau under extreme rainfall events. Int. Soil Water Conse. 9, 520–531 (2021).Article 

    Google Scholar 
    Wang, R. et al. Effects of gully head height and soil texture on gully headcut erosion in the Loess Plateau of China. CATENA 207, 105674 (2021).Article 

    Google Scholar 
    Wei, H., Zhao, W. W. & Wang, H. Effects of vegetation restoration on soil erosion on the Loess Plateau: A case study in the Ansai watershed. Int. J. Environ. Res. Pub He. 18, 6266 (2021).Article 

    Google Scholar 
    Zhang, X., Li, P., Li, Z. B., Yu, G. Q. & Li, C. Effects of precipitation and different distributions of grass strips on runoff and sediment in the loess convex hillslope. CATENA 162, 130–140 (2018).Article 

    Google Scholar 
    Foster, G. R., Huggins, L. F. & Meyer, L. D. A laboratory study of rill hydraulics: II Shear Stress Relationships. T Asabe. 27, 797–804 (1984).Article 

    Google Scholar 
    Zhu, B. B., Zhou, Z. C. & Li, Z. B. Soil erosion and controls in the slope-gully system of the Loess Plateau of China: A review. Front. Environ. Sci. 9, 657030 (2021).Article 

    Google Scholar 
    Wang, H., Wang, J. & Zhang, G. H. Impact of landscape positions on soil erodibility indices in typical vegetation-restored slope-gully systems on the Loess Plateau of China. CATENA 201, 105235 (2021).Article 

    Google Scholar 
    Chang, X. G. et al. Determining the contributions of vegetation and climate change to ecosystem WUE variation over the last two decades on the Loess Plateau China. Forests 12, 1442 (2021).Article 

    Google Scholar 
    Li, B. B. et al. Deep soil moisture limits the sustainable vegetation restoration in arid and semi-arid Loess Plateau. Geoderma 399, 115122 (2021).ADS 
    Article 

    Google Scholar 
    Dong, L. B. et al. Effects of vegetation restoration types on soil nutrients and soil erodibility regulated by slope positions on the Loess Plateau. J. Environ. Manage. 302, 113985 (2022).CAS 
    PubMed 
    Article 

    Google Scholar 
    Shi, P. et al. Effects of grass vegetation coverage and position on runoff and sediment yields on the slope of Loess Plateau China. Agric. Water Manage. 259, 107231 (2022).Article 

    Google Scholar 
    Xia, L. et al. Soil moisture response to land use and topography across a semi-arid watershed: Implications for vegetation restoration on the Chinese Loess Plateau. J. Mt Sci. 19, 103–120 (2022).Article 

    Google Scholar 
    Chen, Y. X. et al. Soil enzyme activities of typical plant communities after vegetation restoration on the Loess Plateau China. Appl. Soil Ecol. 170, 104292 (2022).Article 

    Google Scholar 
    Qiu, L. J. et al. Quantifying spatiotemporal variations in soil moisture driven by vegetation restoration on the Loess Plateau of China. J. Hydrol. 600, 126580 (2021).Article 

    Google Scholar 
    Fang, H. Y., Li, Q. Y. & Cai, Q. G. A study on the vegetation recovery and crop pattern adjustment on the Loess Plateau of China. Afr. J. Microbiol. Res. 5, 1414–1419 (2011).Article 

    Google Scholar 
    Hu, C. J., Fu, B. J., Liu, G. H., Jin, T. T. & Guo, L. Vegetation patterns influence on soil microbial biomass and functional diversity in a hilly area of the Loess Plateau China. J. Soil Sedim. 10, 1082–1091 (2010).CAS 
    Article 

    Google Scholar 
    Sun, C. L., Chai, Z. Z., Liu, G. B. & Xue, S. Changes in species diversity patterns and spatial heterogeneity during the secondary succession of grassland vegetation on the Loess Plateau China. Front. Plant Sci. 8, 1465 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Xu, J. X. Threholds in vegetation-precipitation relationship and the implications in restoration of vegetation on the Loesee Plateau China. Acta Ecol. Sin. 25, 1233–1239 (2005).
    Google Scholar 
    Yang, X., Shao, M. A., Li, T. C. G, M. & Chen, M. Y. Community characteristics and distribution patterns of soil fauna after vegetation restoration in the northern Loess Plateau. Ecol. Indic. 122, 107236 (2021).Bullock, M. S., Nelson, S. D. & Kemper, W. D. Soil cohesion as affected by freezing, water content, time and tillage. Soil Sci. Soc. Am. J. 52, 70–776 (1988).Article 

    Google Scholar 
    Wang, T. et al. Effects of freeze-thaw on soil erosion processes and sediment selectivity under simulated rainfall. J. Arid Land. 9, 34–243 (2017).
    Google Scholar 
    Su, Y. Y., Li, P., Ren, Z. P., Xiao, L. & Zhang, H. Freeze–thaw effects on erosion process in loess slope under simulated rainfall. J. Arid Land. 12, 937–949 (2020).Article 

    Google Scholar 
    Slattery, M. C. & Burt, T, P. Particle size characteristics of suspended sediment in hillslope runoff and stream flow. Earth Surf. Proc. Land. 22, 705–719 (1997).Wu, F. Z., Shi, Z. H., Yue, B. J. & Wang, L. Particle characteristics of sediment in erosion on hillslope. Acta Pedol. Sin. 49, 1235–1240 (2012).
    Google Scholar 
    Issa, O. M., Bissonnais, Y. L. & Planchon, O. Soil detachment and transport on field-and laboratory-scale interrill areas: Erosion processes and the size-selectivity of eroded sediment. Earth Surf. Proc. Land. 31, 929–939 (2006).ADS 
    Article 

    Google Scholar 
    Shi, Z. H. et al. Soil erosion processes and sediment sorting associated with transport mechanisms on steep slopes. J. Hydrol. 454–455, 123–130 (2012).Article 

    Google Scholar 
    Koiter, A. J., Owens, P. N. & Petticrew, E. L. The behavioural characteristics of sediment properties and their implications for sediment fingerprinting as an approach for identifying sediment sources in river basins. Earth Sci. Rev. 125, 24–42 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    Pan, C. Z. & Shang, G. Z. P. Runoff hydraulic characteristics and sediment generation in sloped grassplots under simulated rainfall conditions. J. Hydrol. 331, 178–185 (2006).ADS 
    Article 

    Google Scholar 
    Pan, C. Z. & Shang, G. Z. P. The effects of ryegrass roots and shoots on loess erosion under simulated rainfall. CATENA 2007(70), 350–355 (2007).
    Google Scholar 
    Zheng, M. G., Cai, Q. G., Wang, C. F. & Liu, J. G. Effect of vegetation and other measures for soil and water conservation on runoff-sediment relationship in watershed scale. J. Hydraul. Eng. 38, 47–53 (2007).
    Google Scholar 
    Wei, X. et al. Flow characteristics of convex composite slopes of loess under vegetation cover. Trans. Chin. Soc. Agric. Eng. 30, 147–154 (2014).CAS 

    Google Scholar 
    Wang, L. et al. Rainfall kinetic energy controlling erosion processes and sediment sorting on steep hillslopes: A case study of clay loam soil from the Loess Plateau China. J. Hydrol. 512, 168–176 (2014).ADS 
    Article 

    Google Scholar 
    Li, M., Yao, W. Y., Ding, W. F., Yang, J. F. & Chen, J. N. Effect of grass coverage on sediment yield in the hillslope-gully side erosion system. J. Geogr. Sci. 19, 321–330 (2009).Article 

    Google Scholar 
    Benito, E., Santiago, J. L., Blas, E. D. & Varela, M. E. Deforestation of water-repellent soils in Galicia (NW Spain): Effects on surface runoff and erosion under simulated rainfall. Earth Surf. Proc. Land. 28, 145–155 (2003).ADS 
    Article 

    Google Scholar 
    Han, P. & Li, X. X. Study on soil erosion and vegetation effect on soil conservation in the Yellow River Basin. J. Basic Sci. Eng. 16, 181–190 (2008).
    Google Scholar 
    Bissonnais, Y. L. Aggregate stability and assessment of soil crustability and erodibility: I. Theory and methodology. Eur. J. Soil Sci. 47, 425–437 (1996).Zhang, X., Yu, G. Q., Li, Z. B. & Li, P. Experimental study on slope runoff, erosion and sediment under different vegetation types. Water Resour. Manag. 28, 2415–2433 (2014).Article 

    Google Scholar 
    Xu, G. C. et al. Temporal and spatial characteristics of soil water content in diverse soil layers on land terraces of the Loess Plateau China. CATENA 158, 20–29 (2017).Article 

    Google Scholar 
    Yu, Y. et al. Land preparation and vegetation type jointly determine soil conditions after long-term land stabilization measures in a typical hilly catchment, Loess Plateau of China. J. Soil Sedim. 17, 144–156 (2017).CAS 
    Article 

    Google Scholar 
    Dou, Y. X., Yang, Y., An, S. S. & Zhu, Z. L. Effects of different vegetation restoration measures on soil aggregate stability and erodibility on the Loess Plateau China. CATENA 185, 104294 (2020).CAS 
    Article 

    Google Scholar 
    He, J., Shi, X. Y. & Fu, Y. J. Identifying vegetation restoration effectiveness and driving factors on different micro-topographic types of hilly Loess Plateau: From the perspective of ecological resilience. J. Environ. Manage. 289, 112562 (2021).PubMed 
    Article 

    Google Scholar 
    Qiu, D. X., Gao, P., Mu, X. M. & Zhao, B. L. Vertical variations and transport mechanism of soil moisture in response to vegetation restoration on the Loess Plateau of China. Hydrol. Process. 35, e14397 (2021).
    Google Scholar 
    Zhang, G. H., Liu, G. B., Wang, G. L. & Wang, Y. X. Effects of Vegetation cover and rainfall intensity on sediment-bound nutrient loss, size composition and volume fractal dimension of sediment particles. Pedosphere 21, 676–684 (2011).CAS 
    Article 

    Google Scholar 
    Gu, Z. J. et al. Estimating the effect of Pinus massoniana Lamb plots on soil and water conservation during rainfall events using vegetation fractional coverage. CATENA 109, 225–233 (2013).Article 

    Google Scholar 
    Comprehensive analysis of relationship between vegetation attributes and soil erosion on hillslopes in the Loess Plateau of China. Environ Earth Sci. 72, 1721–1731 (2014).Zhao, G. J., Mu, X. M., Wen, Z. M., Wang, F. & Gao, P. Soil erosion, conservation, and eco-environment changes in the loess plateau of China. Land Degrad. Dev. 24, 499–510 (2013).Article 

    Google Scholar 
    Zhang, L., Wang, J. M., Bai, Z. K. & Lv, C. J. Effects of vegetation on runoff and soil erosion on reclaimed land in an opencast coal-mine dump in a loess area. CATENA 128, 44–53 (2015).Article 

    Google Scholar 
    Wei, W., Pan, D. L. & Feng, J. Tradeoffs between soil conservation and soil-water retention: The role of vegetation pattern and density. Land Degrad. Dev. 33, 18–27 (2021).Article 

    Google Scholar 
    Asadi, H., Ghadiri, H., Rose, C. W., Yu, B. & Hussein, J. An investigation of flow-driven soil erosion processes at low streampowers. J. Hydrol. 342, 134–142 (2007).ADS 
    Article 

    Google Scholar 
    Shi, Z. H., Yan, F. L., Li, L., Li, Z. X. & Cai, C. F. Interrill erosion from disturbed and undisturbed samples in relation to topsoil aggregate stability in red soils from subtropical China. CATENA 81, 240–248 (2010).Article 

    Google Scholar 
    Zhou, J. et al. Effects of precipitation and restoration vegetation on soil erosion in a semi-arid environment in the Loess Plateau China. CATENA 137, 1–11 (2016).Article 

    Google Scholar 
    Han, Z. M. et al. Effects of vegetation restoration on groundwater drought in the Loess Plateau China. J. Hydrol. 591, 125566 (2020).Article 

    Google Scholar 
    Liang, Y., Jiao, J. Y., Tang, B. Z., Cao, B. T. & Li, H. Response of runoff and soil erosion to erosive rainstorm events and vegetation restoration on abandoned slope farmland in the Loess Plateau region China. J. Hydrol. 584, 124694 (2020).Article 

    Google Scholar  More

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    Predicting the potential for zoonotic transmission and host associations for novel viruses

    Data collectionVirus-host data was collated from various sources. Major sources for the association databases included data shared by Olival et al4., Pandit et al.3, and Johnson et al.13. In data provided by Olival et al (assessed September 2019), host-virus associations have been assigned a score, based on detection methods and tests that are specific and more reliable. We used associations that have been identified as the most reliable (stringent data) from Olival et al4. In addition, a query in GenBank was run to parse out hosts reported for each GenBank submission for viruses presented in each of these three databases. Initially, for each virus name, taxonomic ID was identified using entrez.esearch function in biopython package. The taxonomic ID helped linked to the GenBank databases, identify the ICTV lineage and associated data in PubMed20,21. NCBI TaxID closely follows the ICTV database, but some recent changes in ICTV might not always be reflected in NCBI, so we manually checked names to ensure matching. This included virus genus and family information along with a standard virus name. Host data were aggregated based on the taxonomic ID and associated standard name. Finally, for each virus, a search was completed in PubMed to compile the number of hits related to the virus and their vertebrate hosts using the search terms below. The number of PubMed hits (PMH1) were used as a proxy for sampling bias3,13. The virus-host association data source is presented in supplementary code and data files (https://zenodo.org/record/5899054).$$ searchterm= (+virus_name+,[Title/Abstract])\ ANDleft(host,OR,hosts,OR,reservoir,OR,reservoirs,OR right.\ wild,OR,wildlife,OR,domestic,OR,animal,OR,animals,OR\ mammal,OR,bird,OR,birds,OR,aves,OR,avian,OR,avians\ left. OR,vertebrate,OR,vertebrates,OR,surveillance,OR,sylvaticright)$$Along with the PubMed terms we also queried the nucleotide database on PubMed using the taxonomic ID to find the number of GenBank entries for these viruses (PMH2). A correlation analysis between the PMH1 and PMH2 of well-recognized known viruses showed a high correlation with each other for us to safely use GenBank hits for novel viruses during the prediction stage of the model (Fig. S32).Development of ({{{{{{boldsymbol{G}}}}}}}_{{{{{{boldsymbol{c}}}}}}})
    a. Centrality measures of observed network (({{{{{{boldsymbol{G}}}}}}}_{{{{{{boldsymbol{c}}}}}}}))To test if centrality measures (degree centrality, betweenness centrality, eigenvector centrality, clustering coefficient) for viral nodes in the observed network (({G}_{c})) vary significantly between viral families, we firstly used the Kolmogorov-Smirnov (KS) test. KS test is routinely used to identify distances between cumulative distribution functions of two probability distributions and is largely used to compare degree distributions of networks22,23. For each viral family, distributions of centrality measures (degree centrality, betweenness centrality, and eigenvector centrality) and clustering coefficient within the observed network (({G}_{c})) were compared with the distribution of all nodes in the network using the two-tailed KS test. Secondly, a linear regression model with virus family as a categorical variable and the number of PubMed hits as a covariate to adjust for sampling bias were fitted to understand associations of viral families with centrality measures.$${centrality},{measure}={beta }_{0}{intercept}+{{beta }_{1}{Viral}{family}}_{{categorical}}+{beta }_{2}{PubMed},{hits}$$After fitting the model, node-level permutations were implemented. For each random permutation, the output variable was randomly assigned to covariate values and the model was re-fitted. Finally, a p-value was calculated by comparing the distribution of coefficients from permutations with the original model coefficient.Network topology feature selectionUsing the observed network (({{{{{{boldsymbol{G}}}}}}}_{{{{{{boldsymbol{c}}}}}}})), multiple network topological features for all node (virus) pairs were calculated. The following are topological network features calculated. Features data type, definition and methods to calculate these features are presented in Table S3.1. The Jaccard coefficient: a commonly used similarity metric between nodes in information retrieval, is also called an intersection of over the union for two nodes in the network. In the unipartite network generated here, it represents the proportion of common neighbor viruses from the union of neighbor viruses for two nodes. Neighbor viruses are defined as viruses with which the virus shares at least a single host.2. Adamic/Adar (Frequency-Weighted Common Neighbors): Is the sum of inverse logarithmic degree centrality of the neighbors shared by two nodes in the network24. The concept of Adamic Adar index is a weighted common neighbors for viruses in the network. Within network prediction, the index assumes that viruses with large neighborhoods have a less significant impact while predicting a connection between two viruses compared with smaller neighborhoods.Both Jaccard and Adamic Adar coefficients have been routinely used for generalized network prediction and have shown high accuracy in predicting missing links in networks, specifically bipartite networks25, the information flowing through neighborhoods formed by two nodes might not always be enough to have similar predictive power in an unipartite network. This warrants use of other topology features along with neighborhood-based features.3. Resource allocation: Similarity score of two nodes defined by the weights of common neighbors of two nodes. Resource allocation is another measure to quantify the closeness of two nodes in the network and hence to understand the similarity of hosts they infect.4. Preferential attachment coefficients: The mechanism of preferential attachment can be used to generate evolving scale-free networks, where the probability that a new link is connected to node x is proportional to k26.5. Betweenness centrality: For a node in the network betweenness centrality is the sum of the fraction of all-pairs shortest paths that pass through it. The feature that we used for training the supervised learning model was the absolute difference between of betweenness centralities of two nodes. The difference between the betweenness centrality represents the difference in the sharing observed by two viruses in the pair.6. Degree centrality: The degree centrality for a node v is the fraction of nodes it is connected to. The feature that we used for training the supervised learning model was the absolute difference between degree centralities of two nodes. Unlike the difference in the betweenness centrality, the difference in degree centrality only looks at the difference in the number of observed host sharing.7. Network clustering: All nodes were classified into community clusters using Louvain methods27. A binary feature variable was generated to describe if both the nodes in the pair were part of the same cluster or not. If both viruses are from the same cluster, it represents a similar host predilection than when both viruses are not from the same cluster hence accounting for the evolutionary predilection of viruses (or virus families) to infect a certain type of host.These topological network characteristics come with certain limitations when it comes to the unipartite network of viruses with links formed due to shared hosts and might not truly represent the flow of information between nodes as compared to a bipartite network. Therefore, to account for these limitations, we use multiple network features as weak learners in our model building characteristics summarizing the network through the use of several quantitative metrics. In addition to this, we estimated the feature importance of these metrics in predicting missing links between viruses to quantify the information pasting through these links.Pearson’s correlation coefficients were calculated to identify highly correlated features and for choosing features for model training (Fig. S33). Virological features included in model training were categorical variables describing the virus family of both the nodes in the pair, followed by a binary variable if both the viruses belong to the same virus family. During the model development, PubMed hits generated three predictive features for each pair of viruses on which model training and predictions were conducted. These included two features representing PubMed hits for the two viruses in the pair (PubMedV1, PubMedV2) and the absolute difference between PubMedV1 and PubMedV2 to account for differences in sampling bias between the two viruses.Cross-validation and fitting generalized boosting machine (GBMs) modelsA nested-cross-validation was implemented for the binary model while simple cross-validation was implemented for the multiclass model (multiple output categories). The parameters of the binary model were first hyper-tuned using a cross-validated grid-search method. Values were tested using a grid search to find the best-performing model parameters that showed the highest sensitivity (recall). The parameters tested for hypertuning and their performance are provided in the supplementary material (supplementary results and Table S5). For further cross-validation of the overall binary model, all the viruses were randomly assigned to five groups. For each fold, the viruses assigned to a group were dropped from the data, and a temporary training network (({{{{{{boldsymbol{G}}}}}}}_{{{{{{boldsymbol{t}}}}}}}{{{{{boldsymbol{)}}}}}}) was constructed, assuming that this represented the current observed status of the virus-host community. For all possible pairs in ({{{{{{boldsymbol{G}}}}}}}_{{{{{{boldsymbol{t}}}}}}}) (both that sharing and not sharing any hosts) ten topological and viral characteristics were calculated as training features (Table S4). Categorical features were one-hot-encoded and numeric features were scaled. An XGBClassifier model with binary: logistic family was trained using the feature dataset to predict if virus pairs share hosts (1,0 encoded output). The cross-validation was also used to determine the optimum decision threshold for determining binary classification (Fig. S6) and a precision-recall curve was used to identify positive predictive value and sensitivity at the optimum threshold (Fig. S8).The multiclass model was implemented in the same way, creating an observed network (({G}_{c})) based on species-level sharing of hosts and randomly dropping viruses to generate a training network (({G}_{t})) to train the XGboost model. The output variables were generated based on the taxonomical orders of shared hosts. A pair of viruses can share multiple hosts, hence we trained a multioutput-multiclass model. Humans were considered an independent category of taxonomical order (label) and were given a separate label from primates. For fine-tuning the multiclass model, we started with the best performing parameters of the binary model and manually tested 5 combinations of model parameters by adjusting values of the learning rate, number of estimators, maximum depth, and minimum child weight (Supplementary code and results).We used three methods to estimate the importance of features for our binary model. Specifically, improvement in accuracy brought by branching based on the feature (gain), the percentage of times the feature appears in the XGboost tree model (weight), and the relative number of observations related to the specific feature (cover). Results for feature importance are shown in supplementary results (Fig. S10).Missing links for novel viruses, binary and multiclass predictionThe wildlife surveillance data represented a sampling of 99,379 animals (94,723 wildlife, 4656 domesticated animals) conducted in 34 countries around the world between 2009–2019 (Table S6)1. Specimens were tested using conventional Rt-PCR, Quantitative PCR, Sanger sequencing, and Next Generation Sequencing protocols to detect viruses from 28 virus families or taxonomic groups (Table S7). Testing resulted in 951 novel monophyletic clusters of virus sequences (referred to as novel viruses henceforth). Within 951 novel viruses, 944 novel viruses had vertebrate hosts that were identified with certainty based on barcoding methods and field identification. Host species identification was confirmed by cytochrome b (cytb) DNA barcoding using DNA extracted from the samples28. We predicted the shared host links between novel viruses and known viruses using binary and multiclass models in the following steps. Out of 944 novel viruses discovered in the last ten years, we were able to generate predictions for 531 novel viruses that were detected in species already classified as hosts within the network. The remaining 413 viruses were the first detection of any virus in that species and thus host associations could not be informed by the observed network (({{{{{{boldsymbol{G}}}}}}}_{{{{{{boldsymbol{C}}}}}}})) data.1. A new node representing the novel virus was inserted in the observed network (({{{{{{boldsymbol{G}}}}}}}_{{{{{{boldsymbol{c}}}}}}})). Using the list of species in which the novel virus was detected, new edges were created with known viruses that are also known to be found in those hosts. This generated a temporary network for the novel virus (({{{{{{boldsymbol{G}}}}}}}_{{temp}})). If the novel virus was not able to generate any edges with known viruses, meaning the host in which they have been found was never found positive for any known virus, predictions were not performed.2. Using ({{{{{{boldsymbol{G}}}}}}}_{{temp}}) feature values were calculated for the novel virus (betweenness centrality, clustering, and degree). For all possible pairs of the novel virus with known viruses that are not yet connected with each other through an edge in ({{{{{{boldsymbol{G}}}}}}}_{{temp}}) a feature dataset was generated (Jaccard coefficient(novel virus, known virus), the difference in betweenness centrality of the novel virus and known virus, if the novel virus and known virus were in the same cluster, the difference in degree centrality(novel virus, known virus), if the novel virus and known virus were from same virus family, the difference in PubMed hits(novel virus, known virus), PubMed hits for the novel virus, PubMed hits for the known virus). Studies and nucleotide sequences for novel viruses are expected to be published and shared on PubMed’s Nucleotide database and in various peer-reviewed publications. Data associated with GenBank accession numbers and nucleotide sequences for novel viruses are presented in Supplementary Data 3 and Supplementary Data 4 respectively. At the time of development of the model, data for all viruses was not shared in a format that would reflect on PubMed’s database, we decided to use the number of unique species the virus was detected in the last ten years of wildlife surveillance conducted by the USAID PREDICT project. These detections will be reflected in PubMed’s Nucleotide database and search term eventually, hence we considered them as a proxy for search terms conducted for known viruses. Currently, evaluation of the effects of this substitution of PubMed hits with the number of detections for novel viruses is not possible with limited data on novel viruses but needs to be reevaluated as more studies are published on these novel viruses. To further evaluate the association between PubMed hits through search term and Genbank hits, we ran a generalized linear regression model with PubMed hits as dependent variable and Genbank hits as intendent variable, accounting for virus families.$${{PubMed}}_{{Search}}left({log }right)={beta }_{0}{intercept}+{{beta }_{1}{Virus}{family}}_{{categorical}}+{beta }_{2}{Genbank},{hits},({log })$$The results indicated that Genbank hits had statistically significant predictive value in predicting PubMed hits (β = 0.72, p  More

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    Ecological analysis of Pavlovian fear conditioning in rats

    Watson, J. B. & Morgan, J. J. B. Emotional reactions and psychological experimentation. Am. J. Psychol. 28, 163–174 (1917).Article 

    Google Scholar 
    Watson, J. B. & Rayner, R. Conditioned emotional reactions. J. Exp. Psychol. 3, 1–14 (1920).Article 

    Google Scholar 
    LeDoux, J. Fear and the brain: where have we been, and where are we going. Biol. Psychiatry 44, 1229–1238 (1998).CAS 
    PubMed 
    Article 

    Google Scholar 
    Fendt, M. & Fanselow, M. S. The neuroanatomical and neurochemical basis of conditioned fear. Neurosci. Biobehav. Rev. 23, 743–760 (1999).CAS 
    PubMed 
    Article 

    Google Scholar 
    Maren, S. & Quirk, G. J. Neuronal signalling of fear memory. Nat. Rev. Neurosci. 5, 844–852 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    Bouton, M. E., Mineka, S. & Barlow, D. H. A modern learning theory perspective on the etiology of panic disorder. Psychol. Rev. 108, 4–32 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    Kim, J. J. & Jung, M. W. Neural circuits and mechanisms involved in Pavlovian fear conditioning: a critical review. Neurosci. Biobehav. Rev. 30, 188–202 (2006).PubMed 
    Article 

    Google Scholar 
    Watson, J. B. Psychology as the behaviorist views it. Psychological Rev. 20, 158–177 (1913).Article 

    Google Scholar 
    Pavlov, I. P. Conditioned Reflexes: An Investigation of the Physiological Activity of the Cerebral Cortex (Oxford University Press, 1927).Guthrie, E. R. Conditioning as a principle of learning. Psychological Rev. 37, 412–428 (1930).Article 

    Google Scholar 
    Kamin, L. J. in Miami Symposium on the Prediction of Behavior (ed. Jones, M. R.) 9–33 (University of Miami Press, 1968).Rescorla, R. A. Probability of shock in the presence and absence of CS in fear conditioning. J. Comp. Physiol. Psychol. 66, 1–5 (1968).CAS 
    PubMed 
    Article 

    Google Scholar 
    Wagner, A. R., Logan, F. A., Haberlandt, K. & Price, T. Stimulus selection in animal discrimination learning. J. Exp. Psychol. 76, 171–180 (1968).CAS 
    PubMed 
    Article 

    Google Scholar 
    Rescorla, R. A. & Wagner, A. R. A Theory of Pavlovian Conditioning: Variations in the Effectiveness of Reinforcement and Nonreinforcement 64–99 (Appleton-Century-Crofts, 1972).Josselyn, S. A. & Tonegawa, S. Memory engrams: recalling the past and imagining the future. Science 367, https://doi.org/10.1126/science.aaw4325 (2020).Tovote, P., Fadok, J. P. & Luthi, A. Neuronal circuits for fear and anxiety. Nat. Rev. Neurosci. 16, 317–331 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Haubensak, W. et al. Genetic dissection of an amygdala microcircuit that gates conditioned fear. Nature 468, 270–276 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Foa, E. B. & Rothbaum, B. O. Treating the Trauma of Rape: Cognitive Behavioral Therapy for PTSD (Guilford Press, 1998).Butler, A. C., Chapman, J. E., Forman, E. M. & Beck, A. T. The empirical status of cognitive-behavioral therapy: a review of meta-analyses. Clin. Psychol. Rev. 26, 17–31 (2006).PubMed 
    Article 

    Google Scholar 
    Delgado, M. R., Olsson, A. & Phelps, E. A. Extending animal models of fear conditioning to humans. Biol. Psychol. 73, 39–48 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    Mahan, A. L. & Ressler, K. J. Fear conditioning, synaptic plasticity and the amygdala: implications for posttraumatic stress disorder. Trends Neurosci. 35, 24–35 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Craske, M. G. et al. What is an anxiety disorder? Focus 9, 20 (2011).
    Google Scholar 
    LeDoux, J. E. The Emotional Brain: the Mysterious Underpinnings of Emotional Life (Simon & Schuster, 1996).Fanselow, M. S. From contextual fear to a dynamic view of memory systems. Trends Cogn. Sci. 14, 7–15 (2010).PubMed 
    Article 

    Google Scholar 
    Lima, S. L. & Dill, L. M. Behavioral decisions made under the risk of predation—a review and prospectus. Can. J. Zool. 68, 619–640 (1990).Article 

    Google Scholar 
    Bednekoff, P. A. Foraging in the Face of Danger 305–329 (University of Chicago Press, 2007).Stephens, D. W. Decision ecology: foraging and the ecology of animal decision making. Cogn. Affect Behav. Neurosci. 8, 475–484 (2008).PubMed 
    Article 

    Google Scholar 
    Beckers, T., Krypotos, A. M., Boddez, Y., Effting, M. & Kindt, M. What’s wrong with fear conditioning? Biol. Psychol. 92, 90–96 (2013).PubMed 
    Article 

    Google Scholar 
    Mobbs, D. & Kim, J. J. Neuroethological studies of fear, anxiety, and risky decision-making in rodents and humans. Curr. Opin. Behav. Sci. 5, 8–15 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Pellman, B. A. & Kim, J. J. What can ethobehavioral studies tell us about the Brain’s fear system. Trends Neurosci. 39, 420–431 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Thorndike, E. Biological Lectures from the Marine Laboratory at Woods’ Holl, USA, for 1899. Nature 62, 411 (1900).Bolles, R. C. Species-specific defense reactions and avoidance learning. Psychol. Rev. 77, 32–48 (1970).Choi, J. S. & Kim, J. J. Amygdala regulates risk of predation in rats foraging in a dynamic fear environment. Proc. Natl Acad. Sci. USA 107, 21773–21777 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Zambetti, P. R., Schuessler, B. P. & Kim, J. J. Sex differences in foraging rats to naturalistic aerial predator stimuli. iScience 16, 442–452 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Yilmaz, M. & Meister, M. Rapid innate defensive responses of mice to looming visual stimuli. Curr. Biol. 23, 2011–2015 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Papes, F., Logan, D. W. & Stowers, L. The vomeronasal organ mediates interspecies defensive behaviors through detection of protein pheromone homologs. Cell 141, 692–703 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Tolman, E. C. Cognitive maps in rats and men. Psychol. Rev. 55, 189–208 (1948).CAS 
    PubMed 
    Article 

    Google Scholar 
    Wilensky, A. E., Schafe, G. E. & LeDoux, J. E. The amygdala modulates memory consolidation of fear-motivated inhibitory avoidance learning but not classical fear conditioning. J. Neurosci. 20, 7059–7066 (2000).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Lee, T. & Kim, J. J. Differential effects of cerebellar, amygdalar, and hippocampal lesions on classical eyeblink conditioning in rats. J. Neurosci. 24, 3242–3250 (2004).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Stiedl, O. & Spiess, J. Effect of tone-dependent fear conditioning on heart rate and behavior of C57BL/6N mice. Behav. Neurosci. 111, 703–711 (1997).CAS 
    PubMed 
    Article 

    Google Scholar 
    Guimaraes, F. S., Hellewell, J., Hensman, R., Wang, M. & Deakin, J. F. Characterization of a psychophysiological model of classical fear conditioning in healthy volunteers: influence of gender, instruction, personality and placebo. Psychopharmacology 104, 231–236 (1991).CAS 
    PubMed 
    Article 

    Google Scholar 
    Mackintosh, N. J. The Psychology of Animal Learning (Academic Press, 1974).Bouton, M. E. Learning and Behavior (Sinauer Associates 2007).Sheafor, P. J. “Pseudoconditioned” jaw movements of the rabbit reflect associations conditioned to contextual background cues. J. Exp. Psychol. Anim. Behav. Process 1, 245–260 (1975).CAS 
    PubMed 
    Article 

    Google Scholar 
    Rescorla, R. A. Behavioral studies of Pavlovian conditioning. Annu. Rev. Neurosci. 11, 329–352 (1988).CAS 
    PubMed 
    Article 

    Google Scholar 
    Thompson, R. F. & Krupa, D. J. Organization of memory traces in the mammalian brain. Annu. Rev. Neurosci. 17, 519–549 (1994).CAS 
    PubMed 
    Article 

    Google Scholar 
    Fanselow, M. S. & Wassum, K. M. The origins and organization of vertebrate pavlovian conditioning. Cold Spring Harb. Perspect. Biol. 8, a021717 (2015).PubMed 
    Article 

    Google Scholar 
    Lee, H. J., Berger, S. Y., Stiedl, O., Spiess, J. & Kim, J. J. Post-training injections of catecholaminergic drugs do not modulate fear conditioning in rats and mice. Neurosci. Lett. 303, 123–126 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    Palgi, Y., Gelkopf, M. & Berger, R. The inoculating role of previous exposure to potentially traumatic life events on coping with prolonged exposure to rocket attacks: a lifespan perspective. Psychiatry Res. 227, 296–301 (2015).PubMed 
    Article 

    Google Scholar 
    Somer, E. et al. Israeli civilians under heavy bombardment: prediction of the severity of post-traumatic symptoms. Prehosp. Disaster Med. 24, 389–394 (2009).PubMed 
    Article 

    Google Scholar 
    Alexander, B. K., Beyerstein, B. L., Hadaway, P. F. & Coambs, R. B. Effect of early and later colony housing on oral ingestion of morphine in rats. Pharm. Biochem. Behav. 15, 571–576 (1981).CAS 
    Article 

    Google Scholar 
    Gage, S. H. & Sumnall, H. R. Rat Park: how a rat paradise changed the narrative of addiction. Addiction 114, 917–922 (2019).PubMed 
    Article 

    Google Scholar 
    Fanselow, M. S. & Lester, L. S. A Functional Behavioristic Approach to Aversively Motivated Behavior: Predatory Imminence as a Determinant of the Topography of Defensive Behavior 185–212 (Lawrence Erlbaum Associates Inc, 1988).Cain, C. & LeDoux, J. Brain mechanisms of Pavlovian and instrumental aversive conditioning. Handb. Behav. Neurosci. 17, 103–124 (2008).Article 

    Google Scholar 
    Choi, J. S., Cain, C. K. & LeDoux, J. E. The role of amygdala nuclei in the expression of auditory signaled two-way active avoidance in rats. Learn Mem. 17, 139–147 (2014).Article 

    Google Scholar 
    Steimer, T. The biology of fear- and anxiety-related behaviors. Dialogues Clin. Neurosci. 4, 231–249 (2002).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Fanselow, M. S. The role of learning in threat imminence and defensive behaviors. Curr. Opin. Behav. Sci. 24, 44–49 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Fanselow, M. S. Associative vs topographical accounts of the immediate shock freezing deficit in rats—implications for the response selection-rules governing species-specific defensive reactions. Learn. Motiv. 17, 16–39 (1986).Article 

    Google Scholar 
    Landeira-Fernandez, J., DeCola, J. P., Kim, J. J. & Fanselow, M. S. Immediate shock deficit in fear conditioning: effects of shock manipulations. Behav. Neurosci. 120, 873–879 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hull, C. L. A functional interpretation of the conditioned reflex. Psychol. Rev. 36, 498–511 (1929).Article 

    Google Scholar 
    Lazarus, A. A. Behavior Therapy and Beyond (McGraw-Hill Companies, 1971).Öhman, A. & Mineka, S. Fears, phobias, and preparedness: toward an evolved module of fear and fear learning. Psychol. Rev. 108, 483–522 (2001).PubMed 
    Article 

    Google Scholar 
    Lee, H. & Kim, J. J. Amygdalar NMDA receptors are critical for new fear learning in previously fear-conditioned rats. J. Neurosci. 18, 8444–8454 (1998).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Mathis, A. et al. DeepLabCut: markerless pose estimation of user-defined body parts with deep learning. Nat. Neurosci. 21, 1281–1289 (2018).CAS 
    PubMed 
    Article 

    Google Scholar  More

  • in

    Cell death responses to acute high light mediated by non-photochemical quenching in the dinoflagellate Karenia brevis

    Brand, L. E., Campbell, L. & Bresnan, E. Karenia: The biology and ecology of a toxic genus. Harmful Algae 14, 156–178 (2012).
    Google Scholar 
    Hetland, R. D. & Campbell, L. Convergent blooms of Karenia brevis along the Texas coast. Geophys. Res. Lett. 34, 1–5 (2007).
    Google Scholar 
    Liu, G., Janowitz, G. S. & Kamykowski, D. A biophysical model of population dynamics of the autotrophic dinoflagellate Gymnodinium breve. Mar. Ecol. Prog. Ser. 210, 101–124 (2001).ADS 
    CAS 

    Google Scholar 
    Walsh, J. J. et al. Red tides in the Gulf of Mexico: Where, when, and why?. J. Geophys. Res. 111, C11003 (2006).ADS 

    Google Scholar 
    Bidle, K. D. The molecular ecophysiology of programmed cell death in marine phytoplankton. Ann. Rev. Mar. Sci. 7, 341–375 (2015).PubMed 

    Google Scholar 
    Bidle, K. D. & Bender, S. J. Iron starvation and culture age activate metacaspases and programmed cell death in the marine diatom Thalassiosira pseudonana. Eukaryot. Cell 7, 223–236 (2008).CAS 
    PubMed 

    Google Scholar 
    Bidle, K. D., Haramaty, L., Barcelos, R. J. & Falkowski, P. Viral activation and recruitment of metacaspases in the unicellular coccolithophore, Emiliania huxleyi. Proc. Natl. Acad. Sci. 104, 6049–6054 (2007).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Vardi, A. et al. Programmed cell death of the dinoflagellate Peridinium gatunense is mediated by CO2 limitation and oxidative stress. Curr. Biol. 9, 1061–1064 (1999).CAS 
    PubMed 

    Google Scholar 
    Zuppini, A., Andreoli, C. & Baldan, B. Heat stress: An inducer of programmed cell death in Chlorella saccharophila. Plant Cell Physiol. 48, 1000–1009 (2007).CAS 
    PubMed 

    Google Scholar 
    Britt, A. B. DNA damage and repair in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 75–100 (1996).CAS 
    PubMed 

    Google Scholar 
    Jimenez, C. et al. Different ways to die: Cell death modes of the unicellular chlorophyte Dunaliella viridis exposed to various environmental stresses are mediated by the caspase-like activity DEVDase. J. Exp. Bot. 60, 815–828 (2009).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Moharikar, S., D’Souza, J. S., Kulkarni, A. B. & Rao, B. J. Apoptotic-like cell death pathway is induced in unicellular chlorophyte chlamydomonas reinhardtii (Chlorophyceae) cells following UV irradiation: Detection and functional analyses. J. Phycol. 42, 423–433 (2006).CAS 

    Google Scholar 
    Li, Z., Wakao, S., Fischer, B. B. & Niyogi, K. K. Sensing and responding to excess light. Annu. Rev. Plant Biol. 60, 239–260 (2009).CAS 
    PubMed 

    Google Scholar 
    Niyogi, K. K. Photoprotection revisited: Genetic and molecular approaches. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 333–359 (1999).CAS 
    PubMed 

    Google Scholar 
    Apel, K. & Hirt, H. Reactive oxygen species: Metabolism, Oxidative Stress, and Signal Transduction. Annu. Rev. Plant Biol. 55, 373–399 (2004).CAS 
    PubMed 

    Google Scholar 
    Müller, P., Li, X. & Niyogi, K. K. Non-photochemical quenching. A response to excess light energy. Plant Physiol. 125, 1558–1566 (2001).PubMed 
    PubMed Central 

    Google Scholar 
    Bidle, K. D. Programmed cell death in unicellular phytoplankton. Curr. Biol. 26, R594–R607 (2016).CAS 
    PubMed 

    Google Scholar 
    McKay, L., Kamykowski, D., Milligan, E., Schaeffer, B. & Sinclair, G. Comparison of swimming speed and photophysiological responses to different external conditions among three Karenia brevis strains. Harmful Algae 5, 623–636 (2006).CAS 

    Google Scholar 
    Miller-Morey, J. S. & Van Dolah, F. M. Differential responses of stress proteins, antioxidant enzymes, and photosynthetic efficiency to physiological stresses in the Florida red tide dinoflagellate, Karenia brevis. Comp. Biochem. Physiol. Part C Toxicol. Pharmacol. 138, 493–505 (2004).
    Google Scholar 
    Tilney, C. L., Shankar, S., Hubbard, K. A. & Corcoran, A. A. Is Karenia brevis really a low-light-adapted species?. Harmful Algae 90, 101709 (2019).CAS 
    PubMed 

    Google Scholar 
    Yuasa, K., Shikata, T., Kuwahara, Y. & Nishiyama, Y. Adverse effects of strong light and nitrogen deficiency on cell viability, photosynthesis, and motility of the red-tide dinoflagellate Karenia mikimotoi. Phycologia 57, 525–533 (2018).CAS 

    Google Scholar 
    Krause, G. H. & Jahns, P. Non-photochemical energy dissipation determined by chlorophyll fluorescence quenching: Characterization and function. In Chlorophyll a Fluorescence 463–495 (Springer, Netherlands, Cham, 2004).
    Google Scholar 
    Evens, T. J. Photophysiological responses of the toxic red-tide dinoflagellate Gymnodinium breve (Dinophyceae) under natural sunlight. J. Plankton Res. 23, 1177–1194 (2001).CAS 

    Google Scholar 
    Heil, C. A. et al. Influence of daylight surface aggregation behavior on nutrient cycling during a Karenia brevis (Davis) G. Hansen & Ø Moestrup bloom: Migration to the surface as a nutrient acquisition strategy. Harmful Algae 38, 86–94 (2014).CAS 

    Google Scholar 
    Errera, R. Response of the Toxic Dinoflagellate Karenia Brevis to Current and Projected Environmental Conditions. (Texas A&M University, PhD dissertation, 2013).Guillard, R. R. L. & Hargraves, P. E. Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia 32, 234–236 (1993).
    Google Scholar 
    Dingman, J. E. & Lawrence, J. E. Heat-stress-induced programmed cell death in Heterosigma akashiwo (Raphidophyceae). Harmful Algae 16, 108–116 (2012).
    Google Scholar 
    Lin, Q. et al. Differential cellular responses associated with oxidative stress and cell fate decision under nitrate and phosphate limitations in Thalassiosira pseudonana: Comparative proteomics. PLoS ONE 12(9), e0184849 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    Choi, C. J., Brosnahan, M. L., Sehein, T. R., Anderson, D. M. & Erdner, D. L. Insights into the loss factors of phytoplankton blooms: The role of cell mortality in the decline of two inshore Alexandrium blooms. Limnol. Oceanogr. 62, 1742–1753 (2017).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Johnson, J. G., Janech, M. G. & Van Dolah, F. M. Caspase-like activity during aging and cell death in the toxic dinoflagellate Karenia brevis. Harmful Algae 31, 41–53 (2014).CAS 
    PubMed 

    Google Scholar 
    Jauzein, C. & Erdner, D. L. Stress-related responses in Alexandrium tamarense cells exposed to environmental Changes. J. Eukaryot. Microbiol. 60, 526–538 (2013).CAS 
    PubMed 

    Google Scholar 
    Severin, T. & Erdner, D. L. The phytoplankton taxon-dependent oil response and its microbiome: Correlation but not causation. Front. Microbiol. 10, 1–14 (2019).
    Google Scholar 
    Ralph, P. J. & Gademann, R. Rapid light curves: A powerful tool to assess photosynthetic activity. Aquat. Bot. 82, 222–237 (2005).CAS 

    Google Scholar 
    Suzuki, N. & Mittler, R. Reactive oxygen species and temperature stresses: A delicate balance between signaling and destruction. Physiol. Plant. 126, 45–51 (2006).CAS 

    Google Scholar 
    Krause, G. H. & Weis, E. Chlorophyll fluorescence and photosynthesis: The basics. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42, 313–349 (1991).CAS 

    Google Scholar 
    Gechev, T. S. & Hille, J. Hydrogen peroxide as a signal controlling plant programmed cell death. J. Cell Biol. 168, 17–20 (2005).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Miller, G., Suzuki, N., Ciftci-Yilmaz, S. & Mittler, R. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant. Cell Environ. 33, 453–467 (2010).CAS 
    PubMed 

    Google Scholar 
    Purvis, A. C. Role of the alternative oxidase in limiting superoxide production by plant mitochondria. Physiol. Plant. 100, 165–170 (1997).CAS 

    Google Scholar 
    Demmig-Adams, B. & Adams Iii, W. W. Photoprotection and other responses of plants to high light stress. Annu. Rev. Plant Biol. 43, 599–626 (1992).CAS 

    Google Scholar 
    Cui, Y., Zhang, H. & Lin, S. Enhancement of non-photochemical quenching as an adaptive strategy under phosphorus deprivation in the Dinoflagellate Karlodinium veneficum. Front. Microbiol. 8, 1–14 (2017).
    Google Scholar 
    Cassell, R. T., Chen, W., Thomas, S., Liu, L. & Rein, K. S. Brevetoxin, the dinoflagellate neurotoxin, localizes to thylakoid membranes and interacts with the light-harvesting complex II (LHCII) of photosystem II. ChemBioChem 16, 1060–1067 (2015).CAS 
    PubMed 

    Google Scholar 
    Milne, A., Davey, M. S., Worsfold, P. J., Achterberg, E. P. & Taylor, A. R. Real-time detection of reactive oxygen species generation by marine phytoplankton using flow injection-chemiluminescence. Limnol. Oceanogr. Methods 7, 706–715 (2009).CAS 

    Google Scholar 
    Berman-Frank, I. et al. Segregation of nitrogen fixation and oxygenic photosynthesis in the marine cyanobacterium trichodesmium. Science (80-) 294, 1534–1537 (2001).ADS 
    CAS 

    Google Scholar 
    Triantaphylidès, C. et al. Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiol. 148, 960–968 (2008).PubMed 
    PubMed Central 

    Google Scholar 
    Gao, Y. & Erdner, D. L. Dynamics of cell death across growth stages and the diel cycle in the dinoflagellate Karenia brevis. J. Eukaryot. Microbiol. https://doi.org/10.1111/jeu.12874 (2021).Article 
    PubMed 

    Google Scholar 
    Xu, K., Jiang, H., Juneau, P. & Qiu, B. Comparative studies on the photosynthetic responses of three freshwater phytoplankton species to temperature and light regimes. J. Appl. Phycol. 24, 1113–1122 (2012).CAS 

    Google Scholar 
    Yamori, W., Makino, A. & Shikanai, T. A physiological role of cyclic electron transport around photosystem I in sustaining photosynthesis under fluctuating light in rice. Sci. Rep. 6, 20147 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Berman-Frank, I., Bidle, K. D., Haramaty, L. & Falkowski, P. G. The demise of the marine cyanobacterium, Trichodesmium spp., via an autocatalyzed cell death pathway. Limnol. Oceanogr. 49, 997–1005 (2004).ADS 

    Google Scholar  More

  • in

    Adaptive phenotypic plasticity is under stabilizing selection in Daphnia

    Scheiner, S. M. Genetics and evolution of phenotypic plasticity. Annu. Rev. Ecol. Syst. 24, 35–68 (1993).Article 

    Google Scholar 
    Via, S. et al. Adaptive phenotypic plasticity: consensus and controversy. Trends Ecol. Evol. 10, 212–217 (1995).CAS 
    PubMed 
    Article 

    Google Scholar 
    Ghalambor, C. K. et al. Adaptive versus non‐adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct. Ecol. 21, 394–407 (2007).Article 

    Google Scholar 
    King, J. G. & Hadfield, J. D. The evolution of phenotypic plasticity when environments fluctuate in time and space. Evol. Lett. 3, 15–27 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Newman, R. A. Genetic variation for phenotypic plasticity in the larval life history of spadefoot toads (Scaphiopus couchii). Evolution 48, 1773–1785 (1994).PubMed 

    Google Scholar 
    Nussey, D. H. et al. Selection on heritable phenotypic plasticity in a wild bird population. Science 310, 304–306 (2005).CAS 
    PubMed 
    Article 

    Google Scholar 
    Scheiner, S. Selection experiments and the study of phenotypic plasticity 1. J. Evol. Biol. 15, 889–898 (2002).Article 

    Google Scholar 
    Ghalambor, C. K. et al. Non-adaptive plasticity potentiates rapid adaptive evolution of gene expression in nature. Nature 525, 372–375 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Reger, J. et al. Predation drives local adaptation of phenotypic plasticity. Nat. Ecol. Evol. 2, 100–107 (2018).PubMed 
    Article 

    Google Scholar 
    Sommer, R. J. Phenotypic plasticity: from theory and genetics to current and future challenges. Genetics 215, 1–13 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Brakefield, P. M. & Reitsma, N. Phenotypic plasticity, seasonal climate and the population biology of Bicyclus butterflies (Satyridae) in Malawi. Ecol. Entomol. 16, 291–303 (1991).Article 

    Google Scholar 
    Rountree, D. & Nijhout, H. Hormonal control of a seasonal polyphenism in Precis coenia (Lepidoptera: Nymphalidae). J. Insect Physiol. 41, 987–992 (1995).CAS 
    Article 

    Google Scholar 
    Scheiner, S. M. & Holt, R. D. The genetics of phenotypic plasticity. X. Variation versus uncertainty. Ecol. Evol. 2, 751–767 (2012).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bonamour, S. et al. Phenotypic plasticity in response to climate change: the importance of cue variation. Philos. Trans. R. Soc. B 374, 20180178 (2019).Article 

    Google Scholar 
    Fox, R.J., Donelson, J. M., Schunter, C., Ravasi, T. & Gaitán-Espitia, J. D. Beyond buying time: the role of plasticity in phenotypic adaptation to rapid environmental change. Philos. Trans. R. Soc. B https://doi.org/10.1098/rstb.2018.0174 (2019).Auld, J. R., Agrawal, A. A. & Relyea, R. A. Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proc. R. Soc. B 277, 503–511 (2010).PubMed 
    Article 

    Google Scholar 
    Murren, C. J. et al. Constraints on the evolution of phenotypic plasticity: limits and costs of phenotype and plasticity. Heredity 115, 293–301 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Yampolsky, L. Y., Schaer, T. M. & Ebert, D. Adaptive phenotypic plasticity and local adaptation for temperature tolerance in freshwater zooplankton. Proc. R. Soc. B 281, 20132744 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Schmid, M. & Guillaume, F. The role of phenotypic plasticity on population differentiation. Heredity 119, 214–225 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Charlesworth, B., Lande, R. & Slatkin, M. A neo-Darwinian commentary on macroevolution. Evolution 36, 474–498 (1982).PubMed 

    Google Scholar 
    Lynch, M. The rate of morphological evolution in mammals from the standpoint of the neutral expectation. Am. Nat. 136, 727–741 (1990).Article 

    Google Scholar 
    Kingsolver, J. G. & Pfennig, D. W. Patterns and power of phenotypic selection in nature. Bioscience 57, 561–572 (2007).Article 

    Google Scholar 
    West-Eberhard, M. J. Developmental plasticity and the origin of species differences. Proc. Natl Acad. Sci. USA 102, 6543–6549 (2005).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Turelli, M. & Barton, N. Polygenic variation maintained by balancing selection: pleiotropy, sex-dependent allelic effects and G × E interactions. Genetics 166, 1053–1079 (2004).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Charlesworth, B. Causes of natural variation in fitness: evidence from studies of Drosophila populations. Proc. Natl Acad. Sci. USA 112, 1662–1669 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Noble, D. W., Radersma, R. & Uller, T. Plastic responses to novel environments are biased towards phenotype dimensions with high additive genetic variation. Proc. Natl Acad. Sci. USA 116, 13452–13461 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Draghi, J. A. & Whitlock, M. C. Phenotypic plasticity facilitates mutational variance, genetic variance, and evolvability along the major axis of environmental variation. Evolution 66-9, 2891–2902 (2012).Article 

    Google Scholar 
    Houle, D. How should we explain variation in the genetic variance of traits? Genetica 102, 241–253 (1998).PubMed 
    Article 

    Google Scholar 
    Tollrian, R. Predator‐induced morphological defenses: costs, life history shifts, and maternal effects in Daphnia pulex. Ecology 76, 1691–1705 (1995).Article 

    Google Scholar 
    Agrawal, A. A., Laforsch, C. & Tollrian, R. Transgenerational induction of defences in animals and plants. Nature 401, 60–63 (1999).CAS 
    Article 

    Google Scholar 
    Tollrian, R. Neckteeth formation in Daphnia pulex as an example of continuous phenotypic plasticity: morphological effects of Chaoborus kairomone concentration and their quantification. J. Plankton Res. 15, 1309–1318 (1993).Article 

    Google Scholar 
    Dennis, S. et al. Phenotypic convergence along a gradient of predation risk. Proc. R. Soc. B 278, 1687–1696 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hammill, E. & Beckerman, A. P. Reciprocity in predator–prey interactions: exposure to defended prey and predation risk affects intermediate predator life history and morphology. Oecologia 163, 193–202 (2010).PubMed 
    Article 

    Google Scholar 
    Hammill, E., Rogers, A. & Beckerman, A. P. Costs, benefits and the evolution of inducible defences: a case study with Daphnia pulex. J. Evol. Biol. 21, 705–715 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    Barnard-Kubow, K. et al. Polygenic variation in sexual investment across an ephemerality gradient in Daphnia pulex. Mol. Bio. Evol. 39, msac121 (2022).Article 

    Google Scholar 
    Deng, H.-W. & Lynch, M. Inbreeding depression and inferred deleterious-mutation parameters in Daphnia. Genetics 147, 147–155 (1997).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Seyfert, A. L. et al. The rate and spectrum of microsatellite mutation in Caenorhabditis elegans and Daphnia pulex. Genetics 178, 2113–2121 (2008).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Xu, S. et al. High mutation rates in the mitochondrial genomes of Daphnia pulex. Mol. Biol. Evol. 29, 763–769 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Collyer, M. L. & Adams, D. C. Phenotypic trajectory analysis: comparison of shape change patterns in evolution and ecology. Hystrix 24, 75 (2013).
    Google Scholar 
    Adams, D.C., Collyer, M., Kaliontzopoulou, A. & Sherratt, E. et al. Geomorph: software for geometric morphometric analyses (University of New England, 2016); https://hdl.handle.net/1959.11/21330Adams, D. C. & Collyer, M. L. Comparing the strength of modular signal, and evaluating alternative modular hypotheses, using covariance ratio effect sizes with morphometric data. Evolution 73, 2352–2367 (2019).PubMed 
    Article 

    Google Scholar 
    Richards, C. L., Bossdorf, O. & Pigliucci, M. What role does heritable epigenetic variation play in phenotypic evolution? BioScience 60, 232–237 (2010).Article 

    Google Scholar 
    Latta, L. C. IV et al. The phenotypic effects of spontaneous mutations in different environments. Am. Nat. 185, 243–252 (2015).PubMed 
    Article 

    Google Scholar 
    Lind, M. I. et al. The alignment between phenotypic plasticity, the major axis of genetic variation and the response to selection. Proc. R. Soc. B 282, 20151651 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Laforsch, C. & Tollrian, R. Inducible defenses in multipredator environments: cyclomorphosis in Daphnia cucullata. Ecology 85, 2302–2311 (2004).Article 

    Google Scholar 
    Weiss, L. C., Leimann, J. & Tollrian, R. Predator-induced defences in Daphnia longicephala: location of kairomone receptors and timeline of sensitive phases to trait formation. J. Exp. Biol. 218, 2918–2926 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Tollrian, R. & Harvell, C.D. The Ecology and Evolution of Inducible Defenses (Princeton Univ. Press, 1999).Lande, R. Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. J. Evol. Biol. 22, 1435–1446 (2009).PubMed 
    Article 
    CAS 

    Google Scholar 
    Via, S. & Lande, R. Genotype–environment interaction and the evolution of phenotypic plasticity. Evolution 39, 505–522 (1985).PubMed 
    Article 

    Google Scholar 
    Kvist, J. et al. Temperature treatments during larval development reveal extensive heritable and plastic variation in gene expression and life history traits. Mol. Ecol. 22, 602–619 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Siepielski, A. M. et al. Differences in the temporal dynamics of phenotypic selection among fitness components in the wild. Proc. R. Soc. B 278, 1572–1580 (2011).PubMed 
    Article 

    Google Scholar 
    Muschick, M. et al. Adaptive phenotypic plasticity in the Midas cichlid fish pharyngeal jaw and its relevance in adaptive radiation. BMC Evol. Biol. 11, 116 (2011).Salzburger, W. Understanding explosive diversification through cichlid fish genomics. Nat. Rev. Genet. 19, 705–717 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Halligan, D. L. & Keightley, P. D. Spontaneous mutation accumulation studies in evolutionary genetics. Annu. Rev. Ecol. Evol. Syst. 40, 151–172 (2009).Article 

    Google Scholar 
    Houle, D., Morikawa, B. & Lynch, M. Comparing mutational variabilities. Genetics 143, 1467–1483 (1996).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Eberle, S. et al. Hierarchical assessment of mutation properties in Daphnia magna. G3 Genes Genomes Genetics 8, 3481–3487 (2018).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Stenseth, N. C. et al. Ecological effects of climate fluctuations. Science 297, 1292–1296 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    Burgmer, T., Hillebrand, H. & Pfenninger, M. Effects of climate-driven temperature changes on the diversity of freshwater macroinvertebrates. Oecologia 151, 93–103 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    Yan, N. D. et al. Long-term trends in zooplankton of Dorset, Ontario, lakes: the probable interactive effects of changes in pH, total phosphorus, dissolved organic carbon, and predators. Can. J. Fish. Aquat. Sci. 65, 862–877 (2008).CAS 
    Article 

    Google Scholar 
    Reed, T. E., Schindler, D. E. & Waples, R. S. Interacting effects of phenotypic plasticity and evolution on population persistence in a changing climate. Conserv. Biol. 25, 56–63 (2011).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    ASTM, Standard Guide for Conducting Acute Toxicity Tests with Fishes, Macroinvertebrates, and Amphibians (American Society for Testing and Materials, 1988).Baym, M. et al. Inexpensive multiplexed library preparation for megabase-sized genomes. PLoS ONE 10, e0128036 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Zhang, J. et al. PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics 30, 614–620 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Preprint at https://arxiv.org/abs/1303.3997 (2013).MarkDuplicates v.2.20 (Broad Institute, 2019); http://broadinstitute.github.io/picardMcKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Poplin, R. et al. Scaling accurate genetic variant discovery to tens of thousands of samples. Preprint at bioRxiv https://doi.org/10.1101/201178 (2018).Zheng, X. et al. A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics 28, 3326–3328 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Manichaikul, A. et al. Robust relationship inference in genome-wide association studies. Bioinformatics 26, 2867–2873 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Beckerman, A. P., Rodgers, G. M. & Dennis, S. R. The reaction norm of size and age at maturity under multiple predator risk. J. Anim. Ecol. 79, 1069–1076 (2010).PubMed 
    Article 

    Google Scholar 
    Naraki, Y., Hiruta, C. & Tochinai, S. Identification of the precise kairomone-sensitive period and histological characterization of necktooth formation in predator-induced polyphenism in Daphnia pulex. Zool. Sci. 30, 619–625 (2013).Article 

    Google Scholar 
    Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Scrucca, L. et al. mclust 5: clustering, classification and density estimation using Gaussian finite mixture models. R J. 8, 289 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Fox, J. & Weisberg, S. An R Companion to Applied Regression (Sage, 2018).Ben-Shachar, M. S., Lüdecke, D. & Makowski, D. effectsize: estimation of effect size indices and standardized parameters. J. Open Source Softw. 5, 2815 (2020).Article 

    Google Scholar 
    Collyer, M. L. & Adams, D. C. RRPP: an r package for fitting linear models to high‐dimensional data using residual randomization. Methods Ecol. Evol. 9, 1772–1779 (2018).Article 

    Google Scholar 
    Collyer, M., Adams, D. & and Collyer, M.M. RRPP: linear model evaluation with randomized residuals in a permutation procedure. R package version 1.3 https://CRAN.R-project.org/package=RRPP (2021).Smirnov, P. robcor: Robust correlations. R package version 0.1-6.1 https://CRAN.R-project.org/package=ropcor (2014).Hadfield, J. D. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1–22 (2010).Article 

    Google Scholar 
    Yang, J. et al. GCTA: a tool for genome-wide complex trait analysis. Am. J. Hum. Genet. 88, 76–82 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2017).Villanueva, R., Chen, Z. & Wickham, H. ggplot2: Elegant Graphics for Data Analysis Using the Grammar of Graphics (Springer-Verlag, 2016).Wilke, C. cowplot: Streamlined plot theme and plot annotations for ‘ggplot2’. R package version 0.9. 2 https://CRAN.R-project.org/package=cowplot (2020).Dowle, M. et al. data.table: Extension of ‘data.frame‘. R package version 1.14.0 https://CRAN.R-project.org/package=data.table (2021).Daniel, M. foreach: Provides foreach looping construct. R package version 1.5.1 https://CRAN.R-project.org/package=foreach (2020).Weston, S. doMC: Foreach parallel adaptor for ‘parallel’. R package version 1.3.7 https://CRAN.R-project.org/package=doMC (2020).Clarke, E. & Sherrill-Mix, S. Ggbeeswarm: Categorical scatter (violin point) plots. R package version 0.6. 0 https://CRAN.R-project.org (2017).Garnier, S. et al. viridis: Default color maps from ‘matplotlib’. R package version 0.5.1 (2018). More

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    Ecoenzymatic stoichiometry reveals widespread soil phosphorus limitation to microbial metabolism across Chinese forests

    Bastin, J. F. et al. The global tree restoration potential. Science 364, 76–79 (2019).Article 
    CAS 

    Google Scholar 
    Lewis, S. L., Wheeler, C. E., Mitchard, E. T. A. & Koch, A. Restoring natural forests is the best way to remove atmospheric carbon. Nature 568, 25–28 (2019).CAS 
    Article 

    Google Scholar 
    Bonan, G. B. Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science 320, 1444–1449 (2008).CAS 
    Article 

    Google Scholar 
    Beer, C. et al. Terrestrial gross carbon dioxide uptake: global distribution and covariation with climate. Science 329, 834–838 (2010).CAS 
    Article 

    Google Scholar 
    Vitousek, P. M., Porder, S., Houlton, B. Z. & Chadwick, O. A. Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecol. Appl. 20, 5–15 (2010).Article 

    Google Scholar 
    Camenzind, T., Httenschwiler, S., Treseder, K. K., Lehmann, A. & Rillig, M. C. Nutrient limitation of soil microbial processes in tropical forests. Ecol. Monogr. 88, 4–21 (2018).Article 

    Google Scholar 
    Hou, E., Luo, Y., Kuang, Y., Chen, C. & Wen, D. Global meta-analysis shows pervasive phosphorus limitation of aboveground plant production in natural terrestrial ecosystems. Nat. Commun. 11, 1–9 (2020).Article 
    CAS 

    Google Scholar 
    Du, E. et al. Global patterns of terrestrial nitrogen and phosphorus limitation. Nat. Geosci. 13, 221–226 (2020).CAS 
    Article 

    Google Scholar 
    Sinsabaugh, R. L. & Follstad Shah, J. J. Ecoenzymatic stoichiometry and ecological theory. Annu. Rev. Ecol. Evol. Syst. 43, 313–343 (2012).Article 

    Google Scholar 
    Houghton, R. A. Balancing the global carbon budget. Annu. Rev. Earth Planet. Sci. 35, 313–347 (2007).CAS 
    Article 

    Google Scholar 
    Chen, J. et al. Differential responses of carbon-degrading enzyme activities to warming: implications for soil respiration. Global Change Biol. 24, 4816–4826 (2018).Article 

    Google Scholar 
    Waring, B. G., Weintraub, S. R. & Sinsabaugh, R. L. Ecoenzymatic stoichiometry of microbial nutrient acquisition in tropical soils. Biogeochemistry 117, 101–113 (2014).CAS 
    Article 

    Google Scholar 
    Mori, T., Lu, X., Aoyagi, R. & Mo, J. Reconsidering the phosphorus limitation of soil microbial activity in tropical forests. Funct. Ecol. 32, 1145–1154 (2018).Article 

    Google Scholar 
    Gallardo, A. & Schlesinger, W. H. Factors limiting microbial biomass in the mineral soil and forest floor of a warm-temperate forest. Soil Biol. Biochem. 26, 1409–1415 (1994).Article 

    Google Scholar 
    Feng, J. et al. Coupling and decoupling of soil carbon and nutrient cycles across an aridity gradient in the drylands of northern China: Evidence from ecoenzymatic stoichiometry. Global Biogeochem. Cycles. 33, 559–569 (2019).CAS 

    Google Scholar 
    Cui, Y. et al. Patterns of soil microbial nutrient limitations and their roles in the variation of soil organic carbon across a precipitation gradient in an arid and semi-arid region. Sci. Total Environ. 658, 1440–1451 (2019).CAS 
    Article 

    Google Scholar 
    Jing, X. et al. Soil microbial carbon and nutrient constraints are driven more by climate and soil physicochemical properties than by nutrient addition in forest ecosystems. Soil Biol. Biochem. 141, 107657 (2020).CAS 
    Article 

    Google Scholar 
    Fernández-Martínez, M. et al. Nutrient availability as the key regulator of global forest carbon balance. Nat. Clim. Change 4, 471–476 (2014).Article 
    CAS 

    Google Scholar 
    Zhou, L. et al. Soil extracellular enzyme activity and stoichiometry in China’s forests. Funct. Ecol. 34, 1461–1471 (2020).Article 

    Google Scholar 
    Fang, J., Chen, A., Peng, C., Zhao, S. & Ci, L. Changes in forest biomass carbon storage in China between 1949 and 1998. Science 292, 2320–2322 (2001).CAS 
    Article 

    Google Scholar 
    Zhu, J. et al. Carbon stocks and changes of dead organic matter in China’s forests. Nat. Commun. 8, 1–10 (2017).Article 
    CAS 

    Google Scholar 
    Fang, J., Yu, G., Liu, L., Hu, S. & Chapin, F. S. Climate change, human impacts, and carbon sequestration in China. Proc. Natl. Acad. Sci. USA 115, 4015–4020 (2018).CAS 
    Article 

    Google Scholar 
    Sinsabaugh, R. L. et al. Stoichiometry of soil enzyme activity at global scale. Ecol. Lett. 11, 1252–1264 (2008).Article 

    Google Scholar 
    Sinsabaugh, R. L., Hill, B. H. & Follstad Shah, J. J. Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462, 795–798 (2009).CAS 
    Article 

    Google Scholar 
    Moorhead, D. L., Sinsabaugh, R. L., Hill, B. H. & Weintraub, M. N. Vector analysis of ecoenzyme activities reveal constraints on coupled C, N and P dynamics. Soil Biol. Biochem. 93, 1–7 (2016).CAS 
    Article 

    Google Scholar 
    Cui, Y. et al. Stoichiometric models of microbial metabolic limitation in soil systems. Global Ecol. Biogeogr. 30, 2297–2311 (2021).Article 

    Google Scholar 
    Elser, J. J. et al. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine, and terrestrial ecosystems. Ecol. Lett. 10, 1135–1142 (2007).Article 

    Google Scholar 
    Schulte-Uebbing, L. & Vries, W. D. Global-scale impacts of nitrogen deposition on tree carbon sequestration in tropical, temperate, and boreal forests: a meta-analysis. Global Change Biol. 24, 416–431 (2017).Article 

    Google Scholar 
    Richardson, S. J., Peltzer, D. A., Allen, R. B. & Parfitt, M. G. L. Rapid development of phosphorus limitation in temperate rainforest along the Franz josef soil chronosequence. Oecologia 139, 267–276 (2004).Article 

    Google Scholar 
    Augusto, L., Achat, D. L., Jonard, M., Vidal, D. & Ringeval, B. Soil parent material-a major driver of plant nutrient limitations in terrestrial ecosystems. Global Change Biol. 23, 3808–3824 (2017).Article 

    Google Scholar 
    Yao, Q. et al. Community proteogenomics reveals the systemic impact of phosphorus availability on microbial functions in tropical soil. Nat. Ecol. Evol. 2, 499–509 (2018).Article 

    Google Scholar 
    Philippot, L., Raaijmakers, J. M., Lemanceau, P. & Putten, W. H. Going back to the roots: the microbial ecology of the rhizosphere. Nat. Rev. Microbiol. 11, 789–799 (2013).CAS 
    Article 

    Google Scholar 
    Kuzyakov, Y. & Xu, X. Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytol. 198, 656–669 (2013).CAS 
    Article 

    Google Scholar 
    Cui, Y. et al. Ecoenzymatic stoichiometry and microbial nutrient limitation in rhizosphere soil in the arid area of the northern Loess Plateau, China. Soil Biol. Biochem. 116, 11–21 (2018).CAS 
    Article 

    Google Scholar 
    Cui, Y. et al. Soil moisture mediates microbial carbon and phosphorus metabolism during vegetation succession in a semiarid region. Soil Biol. Biochem. 147, 107814 (2020).CAS 
    Article 

    Google Scholar 
    Johnson, J. et al. The response of soil solution chemistry in european forests to decreasing acid deposition. Global Change Biol. 24, 3603–3619 (2018).Article 

    Google Scholar 
    Janssens, I. A. et al. Reduction of forest soil respiration in response to nitrogen deposition. Nat. Geosci. 3, 315–322 (2010).CAS 
    Article 

    Google Scholar 
    Penuelas, J. et al. Human-induced nitrogen-phosphorus imbalances alter natural and managed ecosystems across the globe. Nat. Commun. 4, 1–10 (2013).
    Google Scholar 
    Yu, G. et al. Stabilization of atmospheric nitrogen deposition in china over the past decade. Nat. Geosci. 12, 424–429 (2019).CAS 
    Article 

    Google Scholar 
    Cui, Y. et al. Decreasing microbial phosphorus limitation increases soil carbon release. Geoderma 419, 115868 (2022).CAS 
    Article 

    Google Scholar 
    Sinsabaugh, R. L., Moorhead, D. L., Xu, X. & Litvak, M. E. Plant, microbial and ecosystem carbon use efficiencies interact to stabilize microbial growth as a fraction of gross primary production. New Phytol. 214, 1518–1526 (2017).CAS 
    Article 

    Google Scholar 
    Craig, M. E., Mayes, M. A., Sulman, B. N. & Walker, A. P. Biological mechanisms may contribute to soil carbon saturation patterns. Global Change Biol. 27, 2633–2644 (2021).CAS 
    Article 

    Google Scholar 
    Friggens, N. L., Hester, A. J., Mitchell, R. J., Parker, T. C. & Wookey, P. A. Tree planting in organic soils does not result in net carbon sequestration on decadal timescales. Global Change Biol. 26, 5178–5188 (2020).Article 

    Google Scholar 
    Jiang, M. et al. The fate of carbon in a mature forest under carbon dioxide enrichment. Nature 580, 227–231 (2020).CAS 
    Article 

    Google Scholar 
    Rosinger, C., Rousk, J. & Sandén, H. Can enzymatic stoichiometry be used to determine growth-limiting nutrients for microorganisms?-A critical assessment in two subtropical soils. Soil Biol. Biochem. 128, 115–126 (2019).CAS 
    Article 

    Google Scholar 
    Mori, T. Does ecoenzymatic stoichiometry really determine microbial nutrient limitations? Soil Biol. Biochem. 146, 107816 (2020).CAS 
    Article 

    Google Scholar 
    Allison, S. D., Wallenstein, M. D. & Bradford, M. A. Soil-carbon response to warming dependent on microbial physiology. Nat. Geosci. 3, 336–340 (2010).CAS 
    Article 

    Google Scholar 
    Saiya-Cork, K. R., Sinsabaugh, R. L. & Zak, D. R. The effects of long term nitrogen deposition on extracellular enzyme activity in an acer saccharum, forest soil. Soil Biol. Biochem. 34, 1309–1315 (2002).CAS 
    Article 

    Google Scholar 
    German, D. P. et al. Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol. Biochem. 43, 1387–1397 (2011).CAS 
    Article 

    Google Scholar 
    Lindstrom, M. J. & Bates, D. M. Newton-Raphson and EM Algorithms for Linear Mixed-Effects Models for Repeated-Measures Data. J. Am. Stat. Assoc. 83, 1014–1022 (1988).
    Google Scholar 
    Legendre, P. & Legendre, L. Numerical ecology, 2nd English edition. Elsevier Science BV, Amsterdam (1998).Muggeo, V. M. R. Segmented: an R package to fit regression models with broken-line relationships. R News 8/1, 20–25 (2008).
    Google Scholar 
    Toms, J. D. & Lesperance, M. Piecewise regression: a tool for identifying ecological thresholds. Ecology 84, 2034–2041 (2003).Article 

    Google Scholar 
    Borcard, D., Legendre, P. & Drapeau, P. Partialling out the spatial component of ecological variation. Ecology 73, 1045–1055 (1992).Article 

    Google Scholar 
    Breiman, L. Random forests. Machine Learning 45, 5–32 (2001).Article 

    Google Scholar 
    Sanchez, G., Trinchera, L. & Russolillo, G. plspm: Tools for Partial Least Squares Path Modeling (PLS-PM). R package version 0.4.7 edn (2016).Development Core Team R. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria (2016). More