More stories

  • in

    Radiolysis generates a complex organosynthetic chemical network

    1.
    Garrison, W. M., Morrison, D. C., Hamilton, J. G., Benson, A. A. & Calvin, M. Reduction of carbon dioxide in aqueous solutions by ionizing radiation. Science 114, 416–418 (1951).
    CAS  PubMed  Article  ADS  PubMed Central  Google Scholar 
    2.
    Draganić, Z. D., Draganić, I. G. & Borovičanin, M. The radiation chemistry of aqueous solutions of hydrogen cyanide in the megarad dose range. Radiat. Res. 66, 42–53 (1976).
    PubMed  Article  ADS  PubMed Central  Google Scholar 

    3.
    Bar-Nun, A. & Hartman, H. Synthesis of organic compounds from carbon monoxide and water by UV photolysis. Origins Life 9, 93–101 (1978).
    CAS  Article  ADS  Google Scholar 

    4.
    Miller, S. L. & Urey, H. C. Organic compound synthesis on the primitive earth. Science 130, 245–251 (1959).
    CAS  PubMed  Article  ADS  PubMed Central  Google Scholar 

    5.
    Pasek, M. A., Dworkin, J. P. & Lauretta, D. S. A radical pathway for organic phosphorylation during schreibersite corrosion with implications for the origin of life. Geochim. Cosmochim. Acta 71, 1721–1736 (2007).
    CAS  Article  ADS  Google Scholar 

    6.
    Lim, R. W. J. & Fahrenbach, A. C. Radicals in prebiotic chemistry. Pure Appl. Chem. 92, 1971–1986 (2020).
    CAS  Article  Google Scholar 

    7.
    Studer, A. & Curran, D. P. Catalysis of radical reactions: A radical chemistry perspective. Angew. Chem. Int. Ed. 55, 58–102 (2016).
    CAS  Article  Google Scholar 

    8.
    Shock, E. L. et al. Quantifying inorganic sources of geochemical energy in hydrothermal ecosystems, Yellowstone National Park, USA. Geochim. Cosmochim. Acta 74, 4005–4043 (2010).
    CAS  Article  ADS  Google Scholar 

    9.
    Bím, D., Maldonado-Domínguez, M., Rulíšek, L. & Srnec, M. Beyond the classical thermodynamic contributions to hydrogen atom abstraction reactivity. Proc. Natl. Acad. Sci. USA 115, E10287–E10294 (2018).
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    10.
    Mayer, J. M. Hydrogen atom abstraction by metal–oxo complexes: Understanding the analogy with organic radical reactions. Acc. Chem. Res. 31, 441–450 (1998).
    CAS  Article  Google Scholar 

    11.
    Gutowski, M. & Kowalczyk, S. A study of free radical chemistry: Their role and pathophysiological significance. Acta Biochim. Pol. 60, 1–16 (2013).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    12.
    Moran, J. & Rauscher, S. Energy and self-organization at the origin of metabolism. Commun. Chem. (in rev.).

    13.
    Nghe, P. et al. Prebiotic network evolution: Six key parameters. Mol. BioSyst. 11, 3206–3217 (2015).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    14.
    Jolley, C. & Douglas, T. Topological biosignatures: Large-scale structure of chemical networks from biology and astrochemistry. Astrobiology 12, 29–39 (2012).
    CAS  PubMed  Article  ADS  PubMed Central  Google Scholar 

    15.
    Solé, R. V. & Munteanu, A. The large-scale organization of chemical reaction networks in astrophysics. Europhys. Lett. 68, 170–176 (2004).
    Article  ADS  CAS  Google Scholar 

    16.
    Shenhav, B., Solomon, A., Lancet, D. & Kafri, R. in Transactions on Computational Systems Biology I (ed. Priami, C.) 14–27 (Springer, Berlin, 2005).
    Google Scholar 

    17.
    Brown, J. H. et al. The fractal nature of nature: Power laws, ecological complexity and biodiversity. Philos. Trans. R. Soc. Lond. B 357, 619–626 (2002).
    Article  Google Scholar 

    18.
    Walker, S. I. & Mathis, C. in Prebiotic Chemistry and Chemical Evolution of Nucleic Acids (ed. Menor-Salvár, C.) 263–291 (Springer, Berlin, 2018).
    Google Scholar 

    19.
    Hordijk, W., Hein, J. & Steel, M. Autocatalytic sets and the origin of life. Entropy 12, 1733–1742 (2010).
    CAS  Article  ADS  Google Scholar 

    20.
    Albert, R. Scale-free networks in cell biology. J. Cell. Sci. 118, 4947–4957 (2005).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    21.
    Liu, R., Mao, G. & Zhang, N. Research of chemical elements and chemical bonds from the view of complex network. Found. Chem. 21, 193–206 (2019).
    CAS  Article  Google Scholar 

    22.
    Estrada, E. The complex networks of earth minerals and chemical elements. MATCH Commun. Math. Comput. Chem. 59, 605–624 (2008).
    MathSciNet  CAS  MATH  Google Scholar 

    23.
    Fricker, M. D., Boddy, L., Nakagaki, T. & Bebber, D. P. In Adaptive Biological Networks (eds. Gross, T. & Sayama, H.) 51–70 (Springer, Berlin, 2009).
    Google Scholar 

    24.
    Nicolis, G. Chemical chaos and self-organization. J. Phys. Condens. Matter 2, SA47–SA62 (1990).
    CAS  Article  ADS  Google Scholar 

    25.
    Pérez-Mercader, J. In Astrobiology (eds. Horneck, G. & Baumstark-Khan, C.) 337–360 (Springer, Berlin, 2002).
    Google Scholar 

    26.
    Li, W. Expansion-modification systems: A model for spatial 1/f spectra. Phys. Rev. A 43, 5240–5260 (1991).
    MathSciNet  CAS  PubMed  Article  ADS  PubMed Central  Google Scholar 

    27.
    Albert, R. & Barabási, A.-L. Topology of evolving networks: Local events and universality. Phys. Rev. Lett. 85, 5234–5237 (2000).
    CAS  PubMed  Article  ADS  PubMed Central  Google Scholar 

    28.
    Barabási, A.-L. & Albert, R. Emergence of scaling in random networks. Science 286, 509–512 (1999).
    MathSciNet  PubMed  MATH  Article  ADS  PubMed Central  Google Scholar 

    29.
    Marković, D. & Gros, C. Power laws and self-organized criticality in theory and nature. Phys. Rep. 536, 41–74 (2014).
    MathSciNet  Article  ADS  Google Scholar 

    30.
    Adler, R., Feldman, R. & Taqqu, M. (eds.) A Practical Guide to Heavy Tails: Statistical Techniques and Applications (Springer, Berlin, 1998).
    Google Scholar 

    31.
    Patten, B. C. & Higashi, M. Modified cycling index for ecological applications. Ecol. Modell. 25, 69–83 (1984).
    Article  Google Scholar 

    32.
    Essington, T. E. & Carpenter, S. R. Nutrient cycling in lakes and streams: Insights from a comparative analysis. Ecosystems 3, 131–143 (2000).
    CAS  Article  Google Scholar 

    33.
    Christian, R. R. & Thomas, C. R. Network analysis of nitrogen inputs and cycling in the Neuse River estuary, North Carolina, USA. Estuaries 26, 815–828 (2003).
    CAS  Article  Google Scholar 

    34.
    Allesina, S. & Ulanowicz, R. E. Cycling in ecological networks: Finn’s index revisited. Comput. Biol. Chem. 28, 227–233 (2004).
    CAS  PubMed  MATH  Article  PubMed Central  Google Scholar 

    35.
    Loreau, M. Material cycling and the stability of ecosystems. Am. Nat. 143, 508–513 (1994).
    Article  Google Scholar 

    36.
    DeAngelis, D. L. et al. Nutrient dynamics and food-web stability. Annu. Rev. Ecol. Syst. 20, 71–95 (1989).
    Article  Google Scholar 

    37.
    Artzy-Randrup, Y. & Stone, L. Connectivity, cycles, and persistence thresholds in metapopulation networks. PLoS Comput. Biol. 6, e1000876 (2010).
    MathSciNet  PubMed  PubMed Central  Article  ADS  CAS  Google Scholar 

    38.
    Newsholme, E. A. & Crabtree, B. Substrate cycles in metabolic regulation and in heat generation. Biochem. Soc. Symp. 41, 61–109 (1976).
    CAS  Google Scholar 

    39.
    Kritz, M. V., dos Santos, M. T., Urrutia, S. & Schwartz, J.-M. Organising metabolic networks: Cycles in flux distributions. J. Theor. Biol. 265, 250–260 (2010).
    MathSciNet  PubMed  MATH  Article  PubMed Central  Google Scholar 

    40.
    Valentine, J. W. & May, C. L. Hierarchies in biology and paleontology. Paleobiology 22, 23–33 (1996).
    Article  Google Scholar 

    41.
    McShea, D. W. The hierarchical structure of organisms: A scale and documentation of a trend in the maximum. Paleobiology 27, 405–423 (2001).
    Article  Google Scholar 

    42.
    Trebilco, R., Baum, J. K., Salomon, A. K. & Dulvy, N. K. Ecosystem ecology: Size-based constraints on the pyramids of life. Trends Ecol. Evol. 28, 423–431 (2013).
    PubMed  Article  PubMed Central  Google Scholar 

    43.
    Lindeman, R. L. The trophic-dynamic aspect of ecology. Bull. Math. Biol. 53, 167–191 (1991).
    Article  Google Scholar 

    44.
    Kleidon, A. & Lorenz, R. D. (eds.) Non-equilibrium Thermodynamics and the Production of Entropy: Life, Earth, and Beyond (Springer, Berlin, 2005).
    Google Scholar 

    45.
    Goldenfeld, N. & Woese, C. Life is physics: Evolution as a collective phenomenon far from equilibrium. Annu. Rev. Condens. Matter Phys. 2, 375–399 (2011).
    CAS  Article  ADS  Google Scholar 

    46.
    Braakman, R. & Smith, E. The compositional and evolutionary logic of metabolism. Phys. Biol. 10, 011001 (2013).
    PubMed  Article  ADS  CAS  PubMed Central  Google Scholar 

    47.
    Ji, S. Molecular Theory of the Living Cell: Concepts, Molecular Mechanisms, and Biomedical Applications (Springer, Berlin, 2012).
    Google Scholar 

    48.
    Yi, R. et al. A continuous reaction network that produces RNA precursors. Proc. Natl. Acad. Sci. USA 117, 13267–13274 (2020).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    49.
    Yi, R., Hongo, Y., Yoda, I., Adam, Z. R. & Fahrenbach, A. C. Radiolytic synthesis of cyanogen chloride, cyanamide and simple sugar precursors. ChemistrySelect 3, 10169–10174 (2018).
    CAS  Article  Google Scholar 

    50.
    Ritson, D. & Sutherland, J. D. Prebiotic synthesis of simple sugars by photoredox systems chemistry. Nat. Chem. 4, 895–899 (2012).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    51.
    Ferus, M. et al. High energy radical chemistry formation of HCN-rich atmospheres on early Earth. Sci. Rep. 7, 6275 (2017).
    PubMed  PubMed Central  Article  ADS  CAS  Google Scholar 

    52.
    Getoff, N. Significance of solvated electrons (eaq−) as promoters of life on Earth. In Vivo 28, 61–66 (2014).
    CAS  PubMed  PubMed Central  Google Scholar 

    53.
    Negrón-Mendoza, A., Draganić, Z. D., Navarro-González, R. & Draganić, I. G. Aldehydes, ketones, and carboxylic acids formed radiolytically in aqueous solutions of cyanides and simple nitriles. Radiat. Res. 95, 248–261 (1983).
    Article  ADS  Google Scholar 

    54.
    Adam, Z. R. et al. Estimating the capacity for production of formamide by radioactive minerals on the prebiotic Earth. Sci. Rep. 8, 265 (2018).
    PubMed  PubMed Central  Article  ADS  CAS  Google Scholar 

    55.
    Bedau, M. A. et al. Open problems in artificial life. Artif. Life 6, 363–376 (2000).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    56.
    Grassberger, P. in Information Dynamics NATO ASI Series (Series B: Physics) (eds. Atmanspacher, H. & Scheingraber, H.) 15–33 (Springer, Berlin, 1991).
    Google Scholar 

    57.
    Kaneko, K. Chaos as a source of complexity and diversity in evolution. Artif. Life 1, 163–177 (1993).
    Article  Google Scholar 

    58.
    Buhl, D. & Ponnamperuma, C. Interstellar molecules and the origin of life. Sp. Life Sci. 3, 157–164 (1971).
    CAS  ADS  Google Scholar 

    59.
    Airapetian, V. S., Glocer, A., Gronoff, G., Hébrard, E. & Danchi, W. Prebiotic chemistry and atmospheric warming of early Earth by an active young Sun. Nat. Geosci. 9, 452–455 (2016).
    CAS  Article  ADS  Google Scholar 

    60.
    Paranicas, C., Cooper, J. F., Garrett, H. B., Johnson, R. E. & Sturner, S. J. in Europa (eds. Pappalardo, R. T. et al.) 529–544 (University of Arizona Press, Tucson, 2009).
    Google Scholar 

    61.
    Takano, Y., Masuda, H., Kaneko, T. & Kobayashi, K. Formation of amino acids from possible interstellar media by γ-rays and UV irradiation. Chem. Lett. 31, 986–987 (2002).
    Article  Google Scholar 

    62.
    Powner, M. W., Gerland, B. & Sutherland, J. D. Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible conditions. Nature 459, 239–242 (2009).
    CAS  PubMed  Article  ADS  PubMed Central  Google Scholar 

    63.
    Clauset, A., Shalizi, C. R. & Newman, M. E. J. Power-law distributions in empirical data. SIAM Rev. 51, 661–703 (2009).
    MathSciNet  MATH  Article  ADS  Google Scholar 

    64.
    Grohe, M. in Proceedings of the 39th ACM SIGMOD-SIGACT-SIGAI Symposium on Principles of Database Systems 1–16 (Portland, OR, USA, 2020).

    65.
    Grover, A. & Leskovec, J. in Proceedings of the 22nd ACM SIGKDD International Conference on Knowledge Discovery and Data Mining 855–864 (San Francisco, CA, USA, 2016).

    66.
    Palumbo, E. et al. in The Semantic Web: European Semantic Web Conference Vol. 11155, 117–120 (Springer, Crete, Greece, 2018).

    67.
    Kim, M., Baek, S. H. & Song, M. Relation extraction for biological pathway construction using node2vec. BMC Bioinform. 19, 206 (2018).
    Article  CAS  Google Scholar 

    68.
    Shen, Z., Chen, F., Yang, L. & Wu, J. Node2vec representation for clustering journals and as a possible measure of diversity. J. Data Inf. Sci. 4, 79–92 (2019).
    Google Scholar 

    69.
    Barabási, A.-L. & Oltvai, Z. N. Network biology: Understanding the cell’s functional organization. Nat. Rev. Genet. 5, 101–113 (2004).
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    70.
    Jeong, H., Tombor, B., Albert, R., Oltvai, Z. N. & Barabási, A.-L. The large-scale organization of metabolic networks. Nature 407, 651–654 (2000).
    CAS  PubMed  Article  ADS  PubMed Central  Google Scholar 

    71.
    Ritson, D. J. & Sutherland, J. D. Synthesis of aldehydic ribonucleotide and amino acid precursors by photoredox chemistry. Angew. Chem. Int. Ed. 52, 5845–5847 (2013).
    CAS  Article  Google Scholar 

    72.
    Fahrenbach, A. C. et al. Common and potentially prebiotic origin for precursors of nucleotide synthesis and activation. J. Am. Chem. Soc. 139, 8780–8783 (2017).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    73.
    Muñoz, M. A. Colloquium: Criticality and dynamical scaling in living systems. Rev. Mod. Phys. 90, 031001 (2018).
    MathSciNet  Article  ADS  Google Scholar 

    74.
    Langton, C. G. Computation at the edge of chaos: Phase transitions and emergent computation. Phys. D Nonlinear Phenom. 42, 12–37 (1990).
    MathSciNet  Article  ADS  Google Scholar 

    75.
    Bak, P., Tang, C. & Wiesenfeld, K. Self-organized criticality: An explanation of the 1/f noise. Phys. Rev. Lett. 59, 381–384 (1987).
    CAS  PubMed  Article  ADS  PubMed Central  Google Scholar 

    76.
    Gaveau, B., Moreau, M. & Toth, J. Scenarios for self-organized criticality in dynamical systems. Open Syst. Inf. Dyn. 7, 297–308 (2000).
    MathSciNet  MATH  Article  Google Scholar 

    77.
    Bak, P. & Paczuski, M. Complexity, contingency, and criticality. Proc. Natl. Acad. Sci. USA 92, 6689–6696 (1995).
    CAS  PubMed  Article  ADS  PubMed Central  Google Scholar 

    78.
    Hoffmann, H. & Payton, D. W. Optimization by self-organized criticality. Sci. Rep. 8, 2358 (2018).
    PubMed  PubMed Central  Article  ADS  CAS  Google Scholar 

    79.
    Lovecchio, E., Allegrini, P., Geneston, E., West, B. J. & Grigolini, P. From self-organized to extended criticality. Front. Physiol. 3, 98 (2012).
    PubMed  PubMed Central  Article  Google Scholar 

    80.
    Lima-Mendez, G. & van Helden, J. The powerful law of the power law and other myths in network biology. Mol. BioSyst. 5, 1482–1493 (2009).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    81.
    Broido, A. D. & Clauset, A. Scale-free networks are rare. Nat. Commun. 10, 1017 (2019).
    Article  ADS  CAS  Google Scholar 

    82.
    Stumpf, M. P. H. & Porter, M. A. Critical truths about power laws. Science 335, 665–666 (2012).
    MathSciNet  CAS  PubMed  MATH  Article  ADS  PubMed Central  Google Scholar 

    83.
    Mitzenmacher, M. A brief history of generative models for power law and lognormal distributions. Internet Math. 1, 226–251 (2003).
    MathSciNet  MATH  Article  Google Scholar 

    84.
    Glassman, I., Yetter, R. A. & Glumac, N. G. Combustion 41–69 (Elsevier, New York, 2015).
    Google Scholar 

    85.
    Gleiss, P. M., Stadler, P. F., Wagner, A. & Fell, D. A. Relevant cycles in chemical reaction networks. Adv. Complex Syst. 4, 207–226 (2001).
    MathSciNet  MATH  Article  Google Scholar 

    86.
    Dančík, V., Basu, A. & Clemons, P. in Systems Biology (eds. Prokop, A. & Csukas, B.) 129–178 (Springer, Berlin, 2013).
    Google Scholar 

    87.
    Patten, B. C., Higashi, M. & Burns, T. P. Trophic dynamics in ecosystem networks: Significance of cycles and storage. Ecol. Modell. 51, 1–28 (1990).
    Article  Google Scholar 

    88.
    Orgel, L. E. The implausibility of metabolic cycles on the prebiotic Earth. PLoS Biol. 6, e18 (2008).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    89.
    Monks, P. S. Gas-phase radical chemistry in the troposphere. Chem. Soc. Rev. 34, 376–395 (2005).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    90.
    Platt, U. et al. in Tropospheric Chemistry: Results of the German Tropospheric Chemistry Programme (eds. Seiler, W. et al.) 359–394 (Springer, Berlin, 2002).
    Google Scholar 

    91.
    Vasas, V., Fernando, C., Santos, M., Kauffman, S. & Szathmáry, E. Evolution before genes. Biol. Direct 7, 1 (2012).
    PubMed  PubMed Central  Article  Google Scholar 

    92.
    Robertson, M. P. & Joyce, G. F. The origins of the RNA world. Cold Spring Harb. Perspect. Biol. 4, a003608 (2012).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    93.
    Damer, B. & Deamer, D. The hot spring hypothesis for an origin of life. Astrobiology 20, 429–452 (2020).
    PubMed  PubMed Central  Article  ADS  Google Scholar 

    94.
    Martin, W., Baross, J., Kelley, D. & Russell, M. J. Hydrothermal vents and the origin of life. Nat. Rev. Microbiol. 6, 805–814 (2008).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    95.
    Soloveichik, D., Cook, M., Winfree, E. & Bruck, J. Computation with finite stochastic chemical reaction networks. Nat. Comput. 7, 615–633 (2008).
    MathSciNet  MATH  Article  Google Scholar 

    96.
    Bastian, M., Heymann, S. & Jacomy, M. in Proceedings of the Third International AAAI Conference on Weblogs and Social Media 361–362 (2009).

    97.
    Alstott, J., Bullmore, E. & Plenz, D. powerlaw: A Python package for analysis of heavy-tailed distributions. PLoS One 9, e85777 (2014).
    PubMed  PubMed Central  Article  ADS  CAS  Google Scholar  More

  • in

    Mobilizing the past to shape a better Anthropocene

    1.
    Steffen, W. et al. Trajectories of the Earth System in the Anthropocene. Proc. Natl Acad. Sci. USA 115, 8252–8259 (2018).
    CAS  PubMed  Article  Google Scholar 
    2.
    Crutzen, P. J. Geology of mankind. Nature 415, 23 (2002).
    CAS  PubMed  Article  Google Scholar 

    3.
    Foley, J. A. et al. Global consequences of land use. Science 309, 570–574 (2005).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    4.
    Kopp, R. E., Kirschvink, J. L., Hilburn, I. A. & Nash, C. Z. The Paleoproterozoic snowball Earth: a climate disaster triggered by the evolution of oxygenic photosynthesis. Proc. Natl Acad. Sci. USA 102, 11131–11136 (2005).
    CAS  PubMed  Article  Google Scholar 

    5.
    Schirrmeister, B. E., de Vos, J. M., Antonelli, A. & Bagheri, H. C. Evolution of multicellularity coincided with increased diversification of cyanobacteria and the Great Oxidation Event. Proc. Natl Acad. Sci. USA 110, 1791–1796 (2013).
    CAS  PubMed  Article  Google Scholar 

    6.
    Bennett, E. M. et al. Bright spots: seeds of a good Anthropocene. Front. Ecol. Environ. 14, 441–448 (2016).
    Article  Google Scholar 

    7.
    Braje, T. J. Earth systems, human agency, and the Anthropocene: Planet Earth in the human age. J. Archaeol. Res. 23, 369–396 (2015).
    Article  Google Scholar 

    8.
    Rick, T. C. & Sandweiss, D. H. Archaeology, climate, and global change in the age of humans. Proc. Natl Acad. Sci. USA 117, 8250–8253 (2020).
    CAS  PubMed  Article  Google Scholar 

    9.
    Sabloff, J. A. Archaeology Matters: Action Archaeology in the Modern World (Routledge, 2008).

    10.
    Guttmann-Bond, E. Sustainability out of the past: how archaeology can save the planet. World Archaeol. 42, 355–366 (2010).
    Article  Google Scholar 

    11.
    Reed, K. & Ryan, P. Lessons from the past and the future of food. World Archaeol. 51, 1–16 (2019).
    Article  Google Scholar 

    12.
    Isendahl, C. & Stump, D. (eds) The Oxford Handbook of Historical Ecology and Applied Archaeology (Oxford Univ. Press, 2019).

    13.
    Fisher, C. Archaeology for sustainable agriculture. J. Archaeol. Res. 28, 393–441 (2019).
    Article  Google Scholar 

    14.
    Wolverton, S. & Lyman, R. L. (eds) Conservation Biology and Applied Zooarchaeology (Univ. Arizona Press, 2012).

    15.
    Folke, C. Resilience: the emergence of a perspective for social-ecological systems analyses. Glob. Environ. Change 16, 253–267 (2006).
    Article  Google Scholar 

    16.
    Raymond, H. The ecologically noble savage debate. Annu. Rev. Anthropol. 36, 177–190 (2007).
    Article  Google Scholar 

    17.
    Steffen, W., Grinevald, J., Crutzen, P. J. & McNeill, J. R. The Anthropocene: conceptual and historical perspectives. Philos. Trans. R. Soc. Lond. A 369, 842–867 (2011).
    Google Scholar 

    18.
    Ellis, E., Maslin, M., Boivin, N. & Bauer, A. A. Involve social scientists in defining the Anthropocene. Nature 540, 192–193 (2016).
    Article  Google Scholar 

    19.
    Smith, B. D. & Zeder, M. A. The onset of the Anthropocene. Anthropocene 4, 8–13 (2013).
    Article  Google Scholar 

    20.
    Lewis, S. L. & Maslin, M. Defining the Anthropocene. Nature 519, 171–180 (2015).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    21.
    Boivin, N. et al. Ecological consequences of human niche construction: examining long-term anthropogenic shaping of global species distributions. Proc. Natl Acad. Sci. USA 113, 6388–6396 (2016).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    22.
    Butchart, S. H. M. et al. Global biodiversity: indicators of recent declines. Science 328, 1164–1168 (2010).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    23.
    Newbold, T. et al. Global effects of land use on local terrestrial biodiversity. Nature 520, 45–50 (2015).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    24.
    Barnosky, A. D. et al. Has the Earth’s sixth mass extinction already arrived? Nature 471, 51–57 (2011).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    25.
    Braje, T. J. & Erlandson, J. M. Human acceleration of animal and plant extinctions: a Late Pleistocene, Holocene, and Anthropocene continuum. Anthropocene 4, 14–23 (2013).
    Article  Google Scholar 

    26.
    Haines-Young, R. & Potschin, M. in Ecosystem Ecology: A New Synthesis (eds Raffaelli, D. G. & Frid, C. L. J.) 110–139 (Cambridge Univ. Press, 2010).

    27.
    Foster, D. et al. The importance of land-use legacies to ecology and conservation. BioScience 53, 77–88 (2003).
    Article  Google Scholar 

    28.
    Willis, K. J. & Birks, H. J. B. What is natural? The need for a long-term perspective in biodiversity conservation. Science 314, 1261–1265 (2006).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    29.
    Dietl, G. P. & Flessa, K. W. Conservation paleobiology: putting the dead to work. Trends Ecol. Evol. 26, 30–37 (2011).
    PubMed  Article  PubMed Central  Google Scholar 

    30.
    Szabó, P. & Hédl, R. Advancing the integration of history and ecology for conservation. Conserv. Biol. 25, 680–687 (2011).
    PubMed  Article  PubMed Central  Google Scholar 

    31.
    Scharf, E. A. Deep time: the emerging role of archaeology in landscape ecology. Landsc. Ecol. 29, 563–569 (2014).
    Article  Google Scholar 

    32.
    Dietl, G. P. et al. Conservation paleobiology: leveraging knowledge of the past to inform conservation and restoration. Annu. Rev. Earth Planet. Sci. 43, 79–103 (2015).
    CAS  Article  Google Scholar 

    33.
    Whitlock, C., Colombaroli, D., Conedera, M. & Tinner, W. Land‐use history as a guide for forest conservation and management. Conserv. Biol. 32, 84–97 (2018).
    PubMed  Article  PubMed Central  Google Scholar 

    34.
    Frazier, J. Sustainable use of wildlife: the view from archaeozoology. Nat. Conserv. 15, 163–173 (2007).
    Article  Google Scholar 

    35.
    Lyman, R. L. A warrant for applied palaeozoology. Biol. Rev. 87, 513–525 (2012).
    PubMed  Article  PubMed Central  Google Scholar 

    36.
    Braje, T. & Rick, T. C. From forest fires to fisheries management: anthropology, conservation biology, and historical ecology. Evol. Anthropol. 22, 303–311 (2013).
    PubMed  Article  PubMed Central  Google Scholar 

    37.
    Rick, T. C. & Lockwood, R. Integrating paleobiology, archeology, and history to inform biological conservation. Conserv. Biol. 27, 45–54 (2013).
    PubMed  Article  PubMed Central  Google Scholar 

    38.
    Barak, R. S. et al. Taking the long view: integrating recorded, archeological, paleoecological, and evolutionary data into ecological restoration. Int. J. Plant Sci. 177, 90–102 (2016).
    Article  Google Scholar 

    39.
    Lambrides, A. B. & Weisler, M. I. Pacific Islands ichthyoarchaeology: implications for the development of prehistoric fishing studies and global sustainability. J. Archaeol. Res. 24, 275–324 (2016).
    Article  Google Scholar 

    40.
    Foster, T., Olsen, L., Dale, V. & Cohen, A. Studying the past for the future: managing modern biodiversity from historic and prehistoric data. Hum. Organ. 69, 149–157 (2010).
    Article  Google Scholar 

    41.
    Wilmshurst, J. M. et al. Use of pollen and ancient DNA as conservation baselines for offshore islands in New Zealand. Conserv. Biol. 28, 202–212 (2014).
    PubMed  Article  PubMed Central  Google Scholar 

    42.
    Nogué, S. et al. Island biodiversity conservation needs palaeoecology. Nat. Ecol. Evol. 1, 0181 (2017).
    Article  Google Scholar 

    43.
    Willis, K. J., Bailey, R. M., Bhagwat, S. A. & Birks, H. J. B. Biodiversity baselines, thresholds and resilience: testing predictions and assumptions using palaeoecological data. Trends Ecol. Evol. 25, 583–591 (2010).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    44.
    Newsome, S. D. et al. The shifting baseline of northern fur seal ecology in the northeast Pacific Ocean. Proc. Natl Acad. Sci. USA 104, 9709–9714 (2007).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    45.
    Szpak, P., Orchard, T., McKechnie, I. & Gröcke, D. Historical ecology of late Holocene sea otters (Enhydra lutris) from northern British Columbia: isotopic and zooarchaeological perspectives. J. Archaeol. Sci. 39, 1553–1571 (2012).
    Article  Google Scholar 

    46.
    McCune, J. L., Pellatt, M. G. & Vellend, M. Multidisciplinary synthesis of long-term human–ecosystem interactions: a perspective from the Garry oak ecosystem of British Columbia. Biol. Conserv. 166, 293–300 (2013).
    Article  Google Scholar 

    47.
    Jackson, S. T. & Hobbs, R. J. Ecological restoration in the light of ecological history. Science 325, 567–569 (2009).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    48.
    Corlett, R. T. The shifted baseline: prehistoric defaunation in the tropics and its consequences for biodiversity conservation. Biol. Conserv. 163, 13–21 (2013).
    Article  Google Scholar 

    49.
    Hofman, C. A. & Rick, T. C. Ancient biological invasions and island ecosystems: tracking translocations of wild plants and animals. J. Archaeol. Res. 26, 65–115 (2018).
    Article  Google Scholar 

    50.
    Speller, C. F. et al. High potential for using DNA from ancient herring bones to inform modern fisheries management and conservation. PLoS ONE 7, e51122 (2012).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    51.
    Hofman, C. A., Rick, T. C., Fleischer, R. C. & Maldonado, J. E. Conservation archaeogenomics: ancient DNA and biodiversity in the Anthropocene. Trends Ecol. Evol. 30, 540–549 (2015).
    PubMed  Article  PubMed Central  Google Scholar 

    52.
    Waters, J. M. & Grosser, S. Managing shifting species: ancient DNA reveals conservation conundrums in a dynamic world. BioEssays 38, 1177–1184 (2016).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    53.
    Valentine, K. et al. Ancient DNA reveals genotypic relationships among Oregon populations of the sea otter (Enhydra lutris). Conserv. Genet. 9, 933–938 (2008).
    Article  Google Scholar 

    54.
    Newsome, S. D. et al. Pleistocene to historic shifts in bald eagle diets on the Channel Islands, California. Proc. Natl Acad. Sci. USA 107, 9246–9251 (2010).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    55.
    Guiry, E. J. et al. Lake Ontario salmon (Salmo salar) were not migratory: a long-standing historical debate solved through stable isotope analysis. Sci. Rep. 6, 36249 (2016).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    56.
    Jackson, J. B. et al. Historical overfishing and the recent collapse of coastal ecosystems. Science 293, 629–637 (2001).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    57.
    Brewington, S. et al. Islands of change vs. islands of disaster: managing pigs and birds in the Anthropocene of the North Atlantic. Holocene 25, 1676–1684 (2015).
    Article  Google Scholar 

    58.
    Hicks, M. et al. in The Oxford Handbook of Historical Ecology and Applied Archaeology (eds Isendahl, C. & Stump, D.) Ch. 12 (Oxford Univ. Press, 2019).

    59.
    Grayson, D. K. & Delpech, F. Pleistocene reindeer and global warming. Conserv. Biol. 19, 557–562 (2005).
    Google Scholar 

    60.
    Enghoff, I. B., MacKenzie, B. R. & Nielson, E. E. The Danish fish fauna during the warm Atlantic period (ca. 7000–3900 BC): forerunner of future changes? Fish. Res. 87, 167–180 (2007).
    Article  Google Scholar 

    61.
    Tengberg, A. et al. Cultural ecosystem services provided by landscapes: assessment of heritage values and identity. Ecosyst. Serv. 2, 14–26 (2012).
    Article  Google Scholar 

    62.
    Walter, R. K. & Hamilton, R. J. A cultural landscape approach to community-based conservation in Solomon Islands. Ecol. Soc. 19, 41 (2014).
    Article  Google Scholar 

    63.
    Ekblom, A., Shoemaker, A., Gillson, L., Lane, P. & Lindholm, K. J. Conservation through biocultural heritage—examples from sub-Saharan Africa. Land 8, 5 (2019).
    Article  Google Scholar 

    64.
    Bliege Bird, R., Bird, D. W., Codding, B. F., Parker, C. H. & Jones, J. H. The “fire stick farming” hypothesis: Australian Aboriginal foraging strategies, biodiversity, and anthropogenic fire mosaics. Proc. Natl Acad. Sci. USA 105, 14796–14801 (2008).
    CAS  PubMed  Article  Google Scholar 

    65.
    Bowman, D. M. et al. Fire in the Earth system. Science 324, 481–484 (2009).
    CAS  Article  Google Scholar 

    66.
    Bowman, D. M. et al. Pyrodiversity is the coupling of biodiversity and fire regimes in food webs. Philos. Trans. R. Soc. Lond. B 371, 20150169 (2016).
    Article  Google Scholar 

    67.
    Kelly, L. T. & Brotons, L. Using fire to promote biodiversity. Science 355, 1264–1265 (2017).
    CAS  PubMed  Article  Google Scholar 

    68.
    Beale, C. M. et al. Pyrodiversity interacts with rainfall to increase bird and mammal richness in African savannas. Ecol. Lett. 21, 557–567 (2018).
    PubMed  PubMed Central  Article  Google Scholar 

    69.
    Gillson, L., Whitlock, C. & Humphrey, G. Resilience and fire management in the Anthropocene. Ecol. Soc. 24, 14 (2019).
    Article  Google Scholar 

    70.
    Berna, F. et al. Microstratigraphic evidence of in situ fire in the Acheulean strata of Wonderwerk Cave, Northern Cape province, South Africa. Proc. Natl Acad. Sci. USA 109, E1215–E1220 (2012).
    CAS  PubMed  Article  Google Scholar 

    71.
    Hlubik, S., Berna, F., Feibel, C., Braun, D. & Harris, J. W. K. Researching the nature of fire at 1.5 Mya on the site of FxJj20 AB, Koobi Fora, Kenya, using high-resolution spatial analysis and FTIR spectrometry. Curr. Anthropol. 58, S243–S257 (2017).
    Article  Google Scholar 

    72.
    Yibarbuk, D. et al. Fire ecology and Aboriginal land management in central Arnhem Land, northern Australia: a tradition of ecosystem management. J. Biogeogr. 28, 325–343 (2001).
    Article  Google Scholar 

    73.
    Black, B. A., Ruffner, C. M. & Abrams, M. D. Native American influences on the forest composition of the Allegheny Plateau, northwest Pennsylvania. Can. J. For. Res. 36, 1266–1275 (2006).
    Article  Google Scholar 

    74.
    Marlon, J. R. et al. Climate and human influences on global biomass burning over the past two millennia. Nat. Geosci. 1, 697–702 (2008).
    CAS  Article  Google Scholar 

    75.
    Bowman, D. M., O’Brien, J. A. & Goldammer, J. G. Pyrogeography and the global quest for sustainable fire management. Annu. Rev. Env. Res. 38, 57–80 (2013).
    Article  Google Scholar 

    76.
    Trauernicht, C., Brook, B. W., Murphy, B. P., Williamson, G. J. & Bowman, D. M. J. S. Local and global pyrogeographic evidence that indigenous fire management creates pyrodiversity. Ecol. Evol. 5, 1908–1918 (2015).
    PubMed  PubMed Central  Article  Google Scholar 

    77.
    Maezumi, S. Y. et al. New insights from pre-Columbian land use and fire management in Amazonian Dark Earth forests. Front. Ecol. Evol. 6, 111 (2018).
    Article  Google Scholar 

    78.
    Bowman, D. M. et al. The human dimension of fire regimes on Earth. J. Biogeogr. 38, 2223–2236 (2011).
    PubMed  PubMed Central  Article  Google Scholar 

    79.
    Nowacki, G. J. & Abrams, M. D. The demise of fire and “mesophication” of forests in the eastern United States. BioScience 58, 123–138 (2008).
    Article  Google Scholar 

    80.
    Russell-Smith, J. et al. Managing fire regimes in north Australian savannas: applying Aboriginal approaches to contemporary global problems. Front. Ecol. Env. 11, e55–e63 (2013).
    Google Scholar 

    81.
    Archibald, S. Managing the human component of fire regimes: lessons from Africa. Philos. Trans. R. Soc. Lond. B 371, 20150346 (2016).
    Article  CAS  Google Scholar 

    82.
    Roos, C. I. et al. Living on a flammable planet: interdisciplinary, cross-scalar and varied cultural lessons, prospects and challenges. Philos. Trans. R. Soc. Lond. B 371, 20150469 (2016).
    Article  Google Scholar 

    83.
    North, M. P. et al. Reform forest fire management. Science 349, 1280–1281 (2015).
    CAS  PubMed  Article  Google Scholar 

    84.
    Lawes, M. J. et al. Small mammals decline with increasing fire extent in northern Australia: evidence from long-term monitoring in Kakadu National Park. Int. J. Wildland Fire 23, 712–722 (2015).
    Article  Google Scholar 

    85.
    Edwards, A., Russell-Smith, J. & Meyer, M. Contemporary fire regime risks to key ecological assets and processes in north Australian savannas. Int. J. Wildland Fire 24, 857–870 (2015).
    Article  Google Scholar 

    86.
    Bliege Bird, R., Codding, B. F., Kauhanen, P. G. & Bird, D. W. Aboriginal hunting buffers climate-driven fire-size variability in Australia’s spinifex grasslands. Proc. Natl Acad. Sci. USA 109, 10287–10292 (2012).
    PubMed  Article  Google Scholar 

    87.
    Whitehead, P. J., Bowman, D. M., Preece, N., Fraser, F. & Cooke, P. Customary use of fire by indigenous peoples in northern Australia: its contemporary role in savanna management. Int. J. Wildland Fire 12, 415–425 (2003).
    Article  Google Scholar 

    88.
    Mitchell, R. J. et al. Future climate and fire interactions in the southeastern region of the United States. For. Ecol. Manag. 327, 316–326 (2014).
    Article  Google Scholar 

    89.
    Pechony, O. & Shindell, D. T. Driving forces of global wildfires over the past millennium and the forthcoming century. Proc. Natl. Acad. Sci. USA 107, 19167–19170 (2010).
    CAS  PubMed  Article  Google Scholar 

    90.
    Whitehead, P. J., Purdon, P., Russell-Smith, J., Cooke, P. M. & Sutton, S. The management of climate change through prescribed savanna burning: emerging contributions of indigenous people in northern Australia. Public Admin. Dev. 28, 374–385 (2008).
    Article  Google Scholar 

    91.
    Mistry, J., Bilbao, B. A. & Berardi, A. Community owned solutions for fire management in tropical ecosystems: case studies from Indigenous communities of South America. Philos. Trans. R. Soc. Lond. B 371, 20150174 (2016).
    Article  CAS  Google Scholar 

    92.
    Gillson, L. & Willis, K. J. ‘As Earth’s testimonies tell’: wilderness conservation in a changing world. Ecol. Lett. 7, 990–998 (2004).
    Article  Google Scholar 

    93.
    Vitousek, P. M., Ehrlich, P. R., Ehrlich, A. H. & Matson, P. A. Human appropriation of the products of photosynthesis. BioScience 36, 368–373 (1986).
    Article  Google Scholar 

    94.
    Haberl, H. et al. Quantifying and mapping the human appropriation of net primary production in earth’s terrestrial ecosystems. Proc. Natl Acad. Sci. USA 104, 12942–12947 (2007).
    CAS  PubMed  Article  Google Scholar 

    95.
    Khush, G. S. Green revolution: the way forward. Nat. Rev. Genet. 2, 815–822 (2001).
    CAS  PubMed  Article  Google Scholar 

    96.
    Foley, J. A. et al. Solutions for a cultivated planet. Nature 478, 337–342 (2011).
    CAS  PubMed  Article  Google Scholar 

    97.
    Tilman, D., Cassman, K. G., Matson, P. A., Naylor, R. & Polasky, S. Agricultural sustainability and intensive production practices. Nature 418, 671–677 (2002).
    CAS  PubMed  Article  Google Scholar 

    98.
    Renard, D. et al. Ecological engineers ahead of their time: the functioning of pre-Columbian raised-field agriculture and its potential contributions to sustainability today. Ecol. Eng. 45, 30–44 (2012).
    Article  Google Scholar 

    99.
    Kunen, J. L. Ancient Maya agricultural installations and the development of intensive agriculture in NW Belize. J. Field. Archaeol. 28, 325–346 (2001).
    Article  Google Scholar 

    100.
    Erickson, C. L. in Managing Change: Sustainable Approaches to the Conservation of the Built Environment (eds Erickson, C. L. et al.) 181–204 (Getty Conservation Institute, 2003).

    101.
    Sandor, J. A. & Eash, N. S. Significance of ancient agricultural soils for long‐term agronomic studies and sustainable agriculture research. Agron. J. 83, 29–37 (1991).
    Article  Google Scholar 

    102.
    Marston, J. M. Modeling resilience and sustainability in ancient agricultural systems. J. Ethnobiol. 35, 585–605 (2015).
    Article  Google Scholar 

    103.
    Logan, A. L., Stump, D., Goldstein, S. T., Orijemie, E. A. & Schoeman, M. H. Usable pasts forum: critically engaging food security. Afr. Archaeol. Rev. 36, 419–438 (2019).
    Article  Google Scholar 

    104.
    Stump, D. “Ancient and backward or long-lived and sustainable?” The role of the past in debates concerning rural livelihoods and resource conservation in eastern Africa. World Dev. 38, 1251–1122 (2010).
    Article  Google Scholar 

    105.
    Spriggs, M. in The Oxford Handbook of Historical Ecology and Applied Archaeology (eds Isendahl, C. & Stump, D.) 395–411 (Oxford Univ. Press, 2019).

    106.
    Herath, S., Mishra, B., Wong, P. & Weerakoon, S. B. in Resilient Asia: Fusion of Traditional and Modern Systems for a Sustainable Future (eds Takeuchi, K. et al.) 151–187 (Springer, 2018).

    107.
    Lang, C. & Stump, D. Geoarchaeological evidence for the construction, irrigation, cultivation, and resilience of 15th–18th century AD terraced landscape at Engaruka, Tanzania. Quat. Res. 88, 382–399 (2017).
    Article  Google Scholar 

    108.
    Abeywardana, N., Schütt, B., Wagalawatta, T. & Bebermeier, W. Indigenous agricultural systems in the Dry Zone of Sri Lanka: management transformation assessment and sustainability. Sustainability 11, 910 (2019).
    Article  Google Scholar 

    109.
    Kendall, A. & Drew, D. in The Oxford Handbook of Historical Ecology and Applied Archaeology (eds Isendahl, C. & Stump, D.) 423–440 (Oxford Univ. Press, 2019).

    110.
    Erickson, C. L. & Candler, K. L. in Fragile Lands of Latin America: Strategies For Sustainable Development (ed. Browder, J. O.) 230–248 (Westview Press, 1989).

    111.
    Erickson, C. L. Raised field agriculture in the Lake Titicaca Basin: putting ancient agriculture back to work. Expedition 30, 8–16 (1988).
    Google Scholar 

    112.
    McKey, D. et al. Pre-Columbian agricultural landscapes, ecosystem engineers, and self-organized patchiness in Amazonia. Proc. Natl Acad. Sci. USA 107, 7823–7828 (2010).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    113.
    Lombardo, U., Canal-Beeby, E., Fehr, S. & Veit, H. Raised fields in the Bolivian Amazonia: a prehistoric green revolution or a flood risk mitigation strategy? J. Archaeol. Sci. 38, 502–512 (2011).
    Article  Google Scholar 

    114.
    Kurashima, N., Fortini, L. & Ticktin, T. The potential of indigenous agricultural food production under climate change in Hawaiʻi. Nat. Sustain. 2, 191–199 (2019).
    Article  Google Scholar 

    115.
    Marshall, K. et al. Restoring people and productivity to Puanui: challenges and opportunities in the restoration of an intensive rain-fed Hawaiian field system. Ecol. Soc. 22, 23 (2017).
    Article  Google Scholar 

    116.
    Lincoln, N. K. et al. Restoration of ‘Āina Malo’o on Hawai’i Island: expanding biocultural relationships. Sustainability 10, 3985 (2018).
    Article  Google Scholar 

    117.
    Atlas, W. I. et al. Ancient fish weir technology for modern stewardship: lessons from community-based salmon monitoring. Ecosyst. Health Sustain. 3, 1341284 (2017).
    Article  Google Scholar 

    118.
    Rodrigues, L., Lombardo, U., Beeby, E. C. & Veit, H. Linking soil properties and pre-Columbian agricultural strategies in the Bolivian lowlands: the case of raised fields in Exaltación. Quat. Int. 437, 143–155 (2017).
    Article  Google Scholar 

    119.
    Iriarte, J. et al. Fire-free land use in pre-1492 Amazonian savannas. Proc. Natl Acad. Sci. USA 109, 6473–6478 (2012).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    120.
    Herrera, A. in The Oxford Handbook of Historical Ecology and Applied Archaeology (eds Isendahl, C. & Stump, D.) 459–479 (Oxford Univ. Press, 2019).

    121.
    Barthel, S. & Isendahl, C. Urban gardens, agriculture, and water management: sources of resilience for long-term food security in cities. Ecol. Econ. 86, 224–234 (2013).
    Article  Google Scholar 

    122.
    Barthel, S., Crumley, C. & Svedin, U. Bio-cultural refugia: combating the erosion of diversity in landscapes of food production. Ecol. Soc. 18, 71 (2013).
    Article  Google Scholar 

    123.
    Maezumi, S. The legacy of 4,500 years of polyculture agroforestry in the eastern Amazon. Nat. Plants 4, 540–547 (2018).
    PubMed  PubMed Central  Article  Google Scholar 

    124.
    Barthel, S., Crumley, C. & Svedin, U. Bio-cultural refugia—safeguarding diversity of practices for food security and biodiversity. Glob. Environ. Change 23, 1142–1152 (2013).
    Article  Google Scholar 

    125.
    Poschlod, P. & Braun-Reichert, R. Small natural features with large ecological roles in ancient agricultural landscapes of Central Europe-history, value, status, and conservation. Biol. Conserv. 211, 60–68 (2017).
    Article  Google Scholar 

    126.
    Smýkal, P., Nelson, M. N., Berger, J. D. & Von Wettberg, E. J. The impact of genetic changes during crop domestication. Agronomy 8, 119 (2018).
    Article  Google Scholar 

    127.
    Massawe, F., Mayes, S. & Cheng, A. Crop diversity: an unexploited treasure trove for food security. Trends Plant Sci. 21, 365–368 (2016).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    128.
    Cheng, A. Shaping a sustainable food future by rediscovering long-forgotten ancient grains. Plant Sci. 269, 136–142 (2018).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    129.
    Mueller, N. G., Fritz, G. J., Patton, P., Carmody, S. & Horton, E. T. Growing the lost crops of eastern North America’s original agricultural system. Nat. Plants 3, 17092 (2017).
    PubMed  Article  PubMed Central  Google Scholar 

    130.
    Logan, A. L. “Why Can’t People Feed Themselves?”: archaeology as alternative archive of food security in Banda, Ghana. Am. Anthropol. 118, 508–524 (2016).
    Article  Google Scholar 

    131.
    Mueller, N. G., White, A. & Szilagyi, P. Experimental cultivation of eastern North America’s lost crops: insights into agricultural practice and yield potential. J. Ethnobiol. 39, 549–566 (2019).
    Article  Google Scholar 

    132.
    Palmer, S. A., Smith, O. & Allaby, R. G. The blossoming of plant archaeogenetics. Ann. Anat. 194, 146–156 (2012).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    133.
    Østerberg, J. T. et al. Accelerating the domestication of new crops: feasibility and approaches. Trends Plant Sci. 22, 373–384 (2017).
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    134.
    McNeill, J. R. & Winiwarter, V. Breaking the sod: humankind, history, and soil. Science 304, 1627–1629 (2004).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    135.
    Brown, A. G. & Walsh, K. Societal stability and environmental change: examining the archaeology‐soil erosion paradox. Geoarchaeology 32, 23–35 (2017).
    Article  Google Scholar 

    136.
    Sandor, J. A. & Homburg, J. A. Anthropogenic soil change in ancient and traditional agricultural fields in arid to semiarid regions of the Americas. J. Ethnobiol. 37, 196–217 (2017).
    Article  Google Scholar 

    137.
    Glaser, B., Haumaier, L., Guggenberger, G. & Zech, W. The ‘Terra Preta’ phenomenon: a model for sustainable agriculture in the humid tropics. Naturwissenschaften 88, 37–41 (2001).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    138.
    Lehmann, J., Kern, D. C., Glaser, B. & Woods, W. I. (eds) Amazonian Dark Earths: Origin, Properties, Management (Springer, 2007).

    139.
    Blume, H. P. & Leinweber, P. Plaggen soils: landscape history, properties, and classification. J. Plant Nutr. Soil Sci. 16, 319–327 (2004).
    Article  Google Scholar 

    140.
    Davidson, D. A., Dercon, G., Stewart, M. & Watson, F. The legacy of past urban waste disposal on local soils. J. Archaeol. Sci. 33, 778–783 (2006).
    Article  Google Scholar 

    141.
    Sandor, J. A. & Eash, N. S. Ancient agricultural soils in the Andes of southern Peru. Soil Sci. Soc. Am. J. 59, 170–179 (1995).
    CAS  Article  Google Scholar 

    142.
    Fairhead, J. & Leach, M. in Amazonian Dark Earths: Wim Sombroek’s Vision (eds Woods, W. I. et al.) 265–278 (Springer, 2009).

    143.
    McFadgen, B. G. Maori plaggen soils in New Zealand, their origin and properties. J. R. Soc. N. Z. 10, 3–18 (1980).
    Article  Google Scholar 

    144.
    Calvelo Pereira, R. et al. Detailed carbon chemistry in charcoals from pre‐European Māori gardens of New Zealand as a tool for understanding biochar stability in soils. Eur. J. Soil Sci. 65, 83–95 (2014).
    CAS  Article  Google Scholar 

    145.
    Downie, A. E., Van Zwieten, L., Smernik, R. J., Morris, S. & Munroe, P. R. Terra Preta Australis: reassessing the carbon storage capacity of temperate soils. Agric. Ecosyst. Environ. 140, 137–147 (2011).
    Article  Google Scholar 

    146.
    Kern, J., Giani, L., Teixeira, W., Lanza, G. & Glaser, B. What can we learn from ancient fertile anthropic soil (Amazonian Dark Earths, shell mounds, Plaggen soil) for soil carbon sequestration? CATENA 172, 104–112 (2019).
    CAS  Article  Google Scholar 

    147.
    Woolf, D., Amonette, J. E., Street-Perrott, F. A., Lehmann, J. & Joseph, S. Sustainable biochar to mitigate global climate change. Nat. Commun. 1, 56 (2010).
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    148.
    Bezerra, J., Turnhout, E., Rittl, T. F., Arts, B. & Kuyper, T. W. The promises of the Amazonian soil: shifts in discourses of Terra Preta and biochar. J Environ. Policy Plan. 21, 623–635 (2019).
    Article  Google Scholar 

    149.
    Novotny, E. H. et al. Lessons from the Terra Preta de Índios of the Amazon region for the utilisation of charcoal for soil amendment. J. Braz. Chem. Soc. 20, 1003–1010 (2009).
    CAS  Article  Google Scholar 

    150.
    Lehmann, J. & Joseph, S. in Biochar for Environmental Management (eds Lehmann, J. & Joseph, S.) 1–14 (Routledge, 2015).

    151.
    Kim, J. S., Sparovek, G., Longo, R. M., De Melo, W. J. & Crowley, D. Bacterial diversity of terra preta and pristine forest soil from the Western Amazon. Soil Biol. Biochem. 39, 684–690 (2007).
    CAS  Article  Google Scholar 

    152.
    Glaser, B. & Birk, J. J. State of the scientific knowledge on properties and genesis of anthropogenic dark earths in Central Amazonia (terra preta de Índio). Geochim. Cosmochim. Acta 82, 39–51 (2012).
    CAS  Article  Google Scholar 

    153.
    Jorio, A. et al. Microscopy and spectroscopy analysis of carbon nanostructures in highly fertile Amazonian anthrosoils. Soil Tillage Res. 122, 61–66 (2012).
    Article  Google Scholar 

    154.
    More, A. F. et al. Next-generation ice core technology reveals true minimum natural levels of lead (Pb) in the atmosphere: insights from the Black Death. GeoHealth 1, 211–219 (2017).
    PubMed  PubMed Central  Article  Google Scholar 

    155.
    Factura, H. et al. Terra Preta sanitation: re-discovered from an ancient Amazonian civilisation – integrating sanitation, bio-waste management and agriculture. Water Sci. Technol. 61, 2673–2679 (2010).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    156.
    Glaser, B. Prehistorically modified soils of central Amazonia: a model for sustainable agriculture in the twenty-first century. Philos. Trans. R. Soc. Lond. B 362, 187–196 (2007).
    CAS  Article  Google Scholar 

    157.
    Fedick, S. L. & Morrison, B. A. Ancient use and manipulation of landscape in the Yalahau region of the northern Maya lowlands. Agric. Hum. Values 21, 207–219 (2004).
    Article  Google Scholar 

    158.
    Sedov, S. et al. Soil genesis in relation to landscape evolution and ancient sustainable land use in the northeastern Yucatan Peninsula, Mexico. Atti Soc. Tosc. Sci. Nat. Mem. A 112, 115–126 (2007).
    Google Scholar 

    159.
    Acksel, A., Kapenberg, A., Kühn, P. & Leinweber, P. Human activity formed deep, dark topsoils around the Baltic Sea. Geoderma Region. 10, 93–101 (2017).
    Article  Google Scholar 

    160.
    Marshall, F. et al. Ancient herders enriched and restructured African grasslands. Nature 561, 387–390 (2018).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    161.
    Muchiru, A. N., Western, D. & Reid, R. S. The impact of abandoned pastoral settlements on plant and nutrient succession in an African savanna ecosystem. J. Arid Environ. 73, 322–331 (2009).
    Article  Google Scholar 

    162.
    Bogaard, A. et al. Crop manuring and intensive land management by Europe’s first farmers. Proc. Natl Acad. Sci. USA 110, 12589–12594 (2013).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    163.
    Beach, T., Luzzadder-Beach, S., Dunning, N., Hageman, J. & Lohse, J. Upland agriculture in the Maya Lowlands: ancient Maya soil conservation in northwestern Belize. Geogr. Rev. 92, 372–397 (2002).
    Article  Google Scholar 

    164.
    Akimoto, H. Global air quality and pollution. Science 302, 1716–1719 (2003).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    165.
    Hong, S., Candelone, J. P., Patterson, C. & Boutron, C. F. History of ancient copper smelting pollution during Roman and medieval times recorded in Greenland ice. Science 272, 246–249 (1996).
    CAS  Article  Google Scholar 

    166.
    Hong, S., Candelone, J. P., Patterson, C. C. & Boutron, C. F. Greenland ice evidence of hemispheric lead pollution two millennia ago by Greek and Roman civilizations. Science 265, 1841–1843 (1994).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    167.
    Shotyk, W. et al. History of atmospheric lead deposition since 12,370 14C yr BP from a peat bog, Jura Mountains, Switzerland. Science 281, 1635–1640 (1998).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    168.
    Borsos, E., Makra, L., Béczi, R., Vitányi, B. & Szentpéteri, M. Anthropogenic air pollution in the ancient times. Acta Climatol. Chorolog. 36–37, 5–15 (2003).
    Google Scholar 

    169.
    Pyatt, F. B. & Grattan, J. P. Some consequences of ancient mining activities on the health of ancient and modern human populations. J. Public Health 23, 235–236 (2001).
    CAS  Article  Google Scholar 

    170.
    Pyatt, F. B., Pyatt, A. J., Walker, C., Sheen, T. & Grattan, J. P. The heavy metal content of skeletons from an ancient metalliferous polluted area in southern Jordan with particular reference to bioaccumulation and human health. Ecotoxicol. Environ. Saf. 60, 295–300 (2005).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    171.
    Longman, J., Veres, D., Finsinger, W. & Ersek, V. Exceptionally high levels of lead pollution in the Balkans from the Early Bronze Age to the Industrial Revolution. Proc. Natl Acad. Sci. USA 115, E5661–E5668 (2018).
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    172.
    Renberg, I. et al. Environmental history: a piece in the puzzle for establishing plans for environmental management. J. Environ. Manag. 90, 2794–2800 (2009).
    CAS  Article  Google Scholar 

    173.
    Bennion, H., Battarbee, R. W., Sayer, C. D., Simpson, G. L. & Davidson, T. A. Defining reference conditions and restoration targets for lake ecosystems using palaeolimnology: a synthesis. J. Paleolimnol. 45, 533–544 (2011).
    Article  Google Scholar 

    174.
    Bindler, R., Rydberg, J. & Renberg, I. Establishing natural sediment reference conditions for metals and the legacy of long-range and local pollution on lakes in Europe. J. Paleolimnol. 45, 519–531 (2011).
    Article  Google Scholar 

    175.
    Fuller, D. Q. et al. The contribution of rice agriculture and livestock pastoralism to prehistoric methane levels: an archaeological assessment. Holocene 21, 743–759 (2011).
    Article  Google Scholar 

    176.
    Ruddiman, W. F. et al. Late Holocene climate: natural or anthropogenic? Rev. Geophys. 54, 93–118 (2016).
    Article  Google Scholar 

    177.
    Ruddiman, W. F. The Anthropocene. Annu. Rev. Earth Planet. Sci. 41, 45–68 (2013).
    CAS  Article  Google Scholar 

    178.
    Pyatt, F. B. Copper and lead bioaccumulation by Acacia retinoides and Eucalyptus torquata in sites contaminated as a consequence of extensive ancient mining activities in Cyprus. Ecotoxicol. Environ. Saf. 50, 60–64 (2001).
    CAS  PubMed  Article  Google Scholar 

    179.
    Pyatt, F. B., Gilmore, G., Grattan, J. P., Hunt, C. O. & McLaren, S. An imperial legacy? An exploration of the environmental impact of ancient metal mining and smelting in southern Jordan. J. Archaeol. Sci. 27, 771–778 (2000).
    Article  Google Scholar 

    180.
    Bindler, R., Renberg, I. & Klaminder, J. Bridging the gap between ancient metal pollution and contemporary biogeochemistry. J. Paleolimnol. 40, 755–770 (2008).
    Article  Google Scholar 

    181.
    Farmer, J. G. et al. Historical accumulation rates of mercury in four Scottish ombrotrophic peat bogs over the past 2000 years. Sci. Total Environ. 407, 5578–5588 (2009).
    CAS  PubMed  Article  Google Scholar 

    182.
    Knabb, K. A. et al. Environmental impacts of ancient copper mining and metallurgy: multi-proxy investigation of human-landscape dynamics in the Faynan valley, southern Jordan. J. Archaeol. Sci. 74, 85–101 (2016).
    CAS  Article  Google Scholar 

    183.
    Grattan, J. P., Gilbertson, D. D. & Hunt, C. O. The local and global dimensions of metalliferous pollution derived from a reconstruction of an eight thousand year record of copper smelting and mining at a desert-mountain frontier in southern Jordan. J. Archaeol. Sci. 34, 83–110 (2007).
    Article  Google Scholar 

    184.
    Wilson, B. & Pyatt, F. B. Heavy metal bioaccumulation by the important food plant, Olea europaea L., in an ancient metalliferous polluted area of Cyprus. Bull. Environ. Contam. Toxicol. 78, 390–394 (2007).
    CAS  PubMed  Article  Google Scholar 

    185.
    Seto, K. C. & Shepherd, J. M. Global urban land-use trends and climate impacts. Curr. Opin. Environ. Sustain. 1, 89–95 (2009).
    Article  Google Scholar 

    186.
    Simon, D. & Adam-Bradford, A. in Balanced Urban Development: Options and Strategies for Liveable Cities (eds Maheshwari, B. et al.) 57–83 (Springer, 2016).

    187.
    Isendahl, C. & Smith, M. E. Sustainable agrarian urbanism: the low-density cities of the Mayas and Aztecs. Cities 31, 132–143 (2013).
    Article  Google Scholar 

    188.
    Lucero, L. J., Fletcher, R. & Coningham, R. From ‘collapse’ to urban diaspora: the transformation of low-density, dispersed agrarian urbanism. Antiquity 89, 1139–1154 (2015).
    Article  Google Scholar 

    189.
    Fletcher, R. in The Comparative Archaeology of Complex Societies (ed. Smith, M. E.) 285–320 (Cambridge Univ. Press, 2011).

    190.
    Heckenberger, M. J. et al. Pre-Columbian urbanism, anthropogenic landscapes, and the future of the Amazon. Science 321, 1214–1217 (2008).
    CAS  PubMed  Article  Google Scholar 

    191.
    Barthel, S. et al. Global urbanization and food production in direct competition for land: leverage places to mitigate impacts on SDG2 and on the Earth System. Anthropocene Rev. 6, 71–97 (2019).
    Article  Google Scholar 

    192.
    Wilkinson, A. The Garden in Ancient Egypt (Rubicon Press, 1998).

    193.
    Edmondson, J. L. et al. The hidden potental of urban horticulture. Nat. Food 1, 155–159 (2020).
    Article  Google Scholar 

    194.
    Scarborough, V. L. et al. Water and sustainable land use at the ancient tropical city of Tikal, Guatemala. Proc. Natl Acad. Sci. USA 109, 12408–12413 (2012).
    CAS  PubMed  Article  Google Scholar 

    195.
    Angelakis, A. N. & Spyridakis, S. V. Major urban water and wastewater systems in Minoan Crete, Greece. Water Sci. Technol. Water Supply 13, 564–573 (2013).
    Article  Google Scholar 

    196.
    Mays, L., Antoniou, G. P. & Angelakis, A. N. History of water cisterns: legacies and lesson. Water 5, 1916–1940 (2013).
    Article  Google Scholar 

    197.
    French, K. D. & Duffy, C. J. Understanding ancient Maya water resources and the implications for a more sustainable future. Wiley Interdiscip. Rev. Water 1, 305–313 (2014).
    Article  Google Scholar 

    198.
    Chase, A. S. Beyond elite control: residential reservoirs at Caracol, Belize. Wiley Interdiscip. Rev. Water 3, 885–897 (2016).
    Article  Google Scholar 

    199.
    Rosenzweig, C. et al. Attributing physical and biological impacts to anthropogenic climate change. Nature 453, 353–357 (2008).
    CAS  PubMed  Article  Google Scholar 

    200.
    Van de Noort, R. Conceptualising climate change archaeology. Antiquity 85, 1039–1048 (2011).
    Article  Google Scholar 

    201.
    Hudson, M. J., Aoyama, M., Hoover, K. C. & Uchiyama, J. Prospects and challenges for an archaeology of global climate change. Wiley Interdiscip. Rev. Clim. Change 3, 313–328 (2012).
    Article  Google Scholar 

    202.
    Sandweiss, D. H. & Kelley, A. R. Archaeological contributions to climate change research: the archaeological record as a paleoclimatic and paleoenvironmental archive. Annu. Rev. Anthropol. 41, 371–391 (2012).
    Article  Google Scholar 

    203.
    Rockman, M. & Hritz, C. Expanding use of archaeology in climate change response by changing its social environment. Proc. Natl Acad. Sci. USA 117, 8295–8302 (2020).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    204.
    Douglass, K. & Cooper, J. Archaeology, environmental justice, and climate change on islands of the Caribbean and southwestern Indian Ocean. Proc. Natl Acad. Sci. USA 117, 8254–8262 (2020).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    205.
    Nelson, M. C. et al. Climate challenges, vulnerabilities, and food security. Proc. Natl Acad. Sci. USA 113, 298–303 (2016).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    206.
    Mitchell, P. Practising archaeology at a time of climatic catastrophe. Antiquity 82, 1093–1103 (2008).
    Article  Google Scholar 

    207.
    Weiss, H. & Bradley, R. S. What drives societal collapse? Science 291, 609–610 (2001).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    208.
    Haug, G. H. et al. Climate and the collapse of Maya civilization. Science 299, 1731–1735 (2003).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    209.
    Weninger, B. et al. The impact of rapid climate change on prehistoric societies during the Holocene in the eastern Mediterranean. Doc. Praehistorica 36, 7–59 (2009).
    Article  Google Scholar 

    210.
    Kennett, D. J. et al. Development and disintegration of Maya political systems in response to climate change. Science 338, 788–791 (2012).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    211.
    Anderson, D. G., Maasch, K. A., Sandweiss, D. H. & Mayewski, P. A. in Climate Change and Cultural Dynamics: A Global Perspective on Mid-Holocene Transitions (eds Anderson, D. G. et al.) 1–23 (Academic Press, 2007).

    212.
    Kintigh, K. W. & Ingram, S. E. Was the drought really responsible? Assessing statistical relationships between climate extremes and cultural transitions. J. Archaeol. Sci. 89, 25–31 (2018).
    Article  Google Scholar 

    213.
    Amand, F. S. et al. Leveraging legacy archaeological collections as proxies for climate and environmental research. Proc. Natl Acad. Sci. USA 117, 8287–8294 (2020).
    Article  CAS  Google Scholar 

    214.
    Jones, T. L. et al. Environmental imperatives reconsidered: demographic crises in western North America during the Medieval climatic anomaly. Curr. Anthropol. 40, 137–170 (1999).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    215.
    Mann, M. E. in Encyclopedia of Global Environmental Change (ed. MacCracken, M. C.) 504–509 (John Wiley & Sons, Ltd, 2002).

    216.
    Flohr, P., Fleitmann, D., Matthews, R., Matthews, W. & Black, S. Evidence of resilience to past climate change in Southwest Asia: early farming communities and the 9.2 and 8.2 ka events. Quat. Sci. Rev. 136, 23–39 (2016).
    Article  Google Scholar 

    217.
    Buckley, B. M. et al. Climate as a contributing factor in the demise of Angkor, Cambodia. Proc. Natl Acad. Sci. USA 107, 6748–6752 (2010).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    218.
    Roscoe, P. A changing climate for anthropological and archaeological research? Improving the climate‐change models. Am. Anthropol. 116, 535–548 (2014).
    Google Scholar 

    219.
    Büntgen, U. et al. 2500 years of European climate variability and human susceptibility. Science 331, 578–582 (2011).
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    220.
    Petraglia, M. D., Groucutt, H., Guagnin, M., Breeze, P. S. & Boivin, N. Human responses to climate and ecosystem change in ancient Arabia. Proc. Natl Acad. Sci. USA 117, 8263–8270 (2020).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    221.
    Manuel, M., Lightfoot, D. & Fattahi, M. The sustainability of ancient water control techniques in Iran: an overview. Water Hist. 10, 13–30 (2018).
    Article  Google Scholar 

    222.
    Avriel-Avni, N., Avni, Y., Babad, A. & Meroz, A. Wisdom dwells in places: what can modern farmers learn from ancient agricultural systems in the desert of the Southern Levant? J. Arid Environ. 163, 86–98 (2019).
    Article  Google Scholar 

    223.
    Lasaponara, R., Rojas, J. L. & Masini, N. in The Ancient Nasca World (eds Lasaponara, R. et al.) 279–327 (Springer, 2016).

    224.
    Bebermeier, W., Meister, J., Withanachchi, C. R., Middelhaufe, I. & Schütt, B. Tank cascade systems as a sustainable measure of watershed management in South Asia. Water 9, 231 (2017).
    Article  Google Scholar 

    225.
    Altschul, J. H. et al. Opinion: Fostering synthesis in archaeology to advance science and benefit society. Proc. Natl Acad. Sci. USA 114, 10999–11002 (2017).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    226.
    Tainter, J. The Collapse of Complex Societies (Cambridge Univ. Press, 1988).

    227.
    Redman, C. L. Human Impact on Ancient Environments (Univ. Arizona, 1999).

    228.
    Redman, C. L. Resilience theory in archaeology. Am. Anthropol. 107, 70–77 (2005).
    Article  Google Scholar 

    229.
    Jenny, J.-P. et al. Human and climate global-scale imprint on sediment transfer during the Holocene. Proc. Natl Acad. Sci. USA 116, 22972–22976 (2019).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    230.
    Kaplan, J. O., Krumhardt, K. M. & Zimmermann, N. The prehistoric and preindustrial deforestation of Europe. Quat. Sci. Rev. 28, 3016–3034 (2009).
    Article  Google Scholar 

    231.
    Lane, P. Archaeology in the age of the Anthropocene: a critical assessment of its scope and societal contributions. J. Field Archaeol. 40, 485–498 (2015).
    Article  Google Scholar 

    232.
    Catlin, K. A. Archaeology for the Anthropocene: scale, soil, and the settlement of Iceland. Anthropocene 15, 13–21 (2016).
    Article  Google Scholar 

    233.
    Kintigh, K. W. et al. Grand challenges for archaeology. Proc. Natl Acad. Sci. USA 111, 879–880 (2014).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    234.
    Smith, M. E. Sprawl, squatters and sustainable cities: can archaeological data shed light on modern urban issues? Camb. Archaeol. J. 20, 229–253 (2010).
    Article  Google Scholar 

    235.
    Dave, R. Archaeology must open up to become more diverse. The Guardian (23 May 2016); https://go.nature.com/36mbRRl

    236.
    White, W. & Draycott, C. Why the whiteness of archaeology is a problem. Sapiens (7 July 2020); https://go.nature.com/3lhgS3T

    237.
    Smith, C. & Wobst, H. M. Indigenous Archaeologies: Decolonising Theory and Practice (Routledge, 2004).

    238.
    Hamilakis, Y. Decolonial archaeology as social justice. Antiquity 92, 518–520 (2018).
    Article  Google Scholar 

    239.
    Mustaphi, C. J. C. et al. Integrating evidence of land use and land cover change for land management policy formulation along the Kenya-Tanzania borderlands. Anthropocene 28, 100228 (2019).
    Article  Google Scholar 

    240.
    Widgren, M. in Rethinking Environmental History World-System History and Global Environmental Change (eds Hornberg, A. et al.) 61–77 (Rowman Altamira, 2007).

    241.
    Matthews, D. German humanities scholars’ unusual role. Inside Higher Ed (24 April 2020); https://go.nature.com/3nbVCNi

    242.
    Agnoletti, M. (ed.) The Conservation of Cultural Landscapes (CABI, 2006).

    243.
    Lowenthal, D. The Past is a Foreign Country – Revisited (Cambridge Univ. Press, 2015). More

  • in

    Author Correction: Clustered versus catastrophic global vertebrate declines

    Affiliations

    Department of Biology, McGill University, Montreal, Quebec, Canada
    Brian Leung & Anna L. Hargreaves

    Bieler School of Environment, McGill University, Montreal, Quebec, Canada
    Brian Leung

    Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, Canada
    Dan A. Greenberg

    School of Biology and Ecology, University of Maine, Orono, ME, USA
    Brian McGill

    Mitchell Center for Sustainability Solutions, University of Maine, Orono, ME, USA
    Brian McGill

    Centre for Biological Diversity, University of St Andrews, St Andrews, UK
    Maria Dornelas

    Indicators and Assessments Unit, Institute of Zoology, Zoological Society of London, London, UK
    Robin Freeman

    Authors
    Brian Leung

    Anna L. Hargreaves

    Dan A. Greenberg

    Brian McGill

    Maria Dornelas

    Robin Freeman

    Corresponding author
    Correspondence to Brian Leung. More

  • in

    Genome analysis of the monoclonal marbled crayfish reveals genetic separation over a short evolutionary timescale

    1.
    Suomalainen, E., Saura, A. & Lokki, J. Cytology and Evolution in Parthenogenesis (CRC Press, 1987).
    2.
    Astaurov, B. L. Experimental alterations of the developmental cytogenetic mechanisms in mulberry silkworms: artificial parthenogenesis, polyploidy, gynogenesis, and androgenesis. Adv. Morphog. 6, 199–257 (1967).
    CAS  PubMed  Article  Google Scholar 

    3.
    Innes, D. J. & Hebert, P. D. N. The origin and genetic basis of obligate parthenogenesis in daphnia pulex. Evolution 42, 1024–1035 (1988).
    PubMed  Article  Google Scholar 

    4.
    Saura, A., Lokki, J. & Suomalainen, E. Origin of polyploidy in parthenogenetic weevils. J. Theor. Biol. 163, 449–456 (1993).
    Article  Google Scholar 

    5.
    Schwander, T., Henry, L. & Crespi, B. J. Molecular evidence for ancient asexuality in timema stick insects. Curr. Biol. 21, 1129–1134 (2011).
    CAS  PubMed  Article  Google Scholar 

    6.
    Birky, C. W. Jr. Heterozygosity, heteromorphy, and phylogenetic trees in asexual eukaryotes. Genetics 144, 427–437 (1996).
    PubMed  Google Scholar 

    7.
    Mark Welch, D. & Meselson, M. Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange. Science 288, 1211–1215 (2000).
    CAS  PubMed  Article  Google Scholar 

    8.
    Jaron, K. S. et al. Genomic features of parthenogenetic animals. J. Hered. https://doi.org/10.1093/jhered/esaa031 (2020).

    9.
    Scholtz, G. et al. Ecology: parthenogenesis in an outsider crayfish. Nature 421, 806 (2003).
    CAS  PubMed  Article  Google Scholar 

    10.
    Lyko, F. The marbled crayfish (Decapoda: Cambaridae) represents an independent new species. Zootaxa 4363, 544–552 (2017).
    PubMed  Article  Google Scholar 

    11.
    Martin, P., Dorn, N. J., Kawai, T., van der Heiden, C. & Scholtz, G. The enigmatic Marmorkrebs (marbled crayfish) is the parthenogenetic form of Procambarus fallax (Hagen, 1870). Contrib. Zool. 79, 107–118 (2010).
    Article  Google Scholar 

    12.
    Vogt, G. et al. The marbled crayfish as a paradigm for saltational speciation by autopolyploidy and parthenogenesis in animals. Biol. Open 4, 1583–1594 (2015).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    13.
    Schön, I., Martens, K. & van, Dijk P. Lost Sex. The Evolutionary Biology of Parthenogenesis (Springer, 2009).

    14.
    Martin, P., Kohlmann, K. & Scholtz, G. The parthenogenetic Marmorkrebs (marbled crayfish) produces genetically uniform offspring. Naturwissenschaften 94, 843–846 (2007).
    CAS  PubMed  Article  Google Scholar 

    15.
    Vogt, G. et al. Production of different phenotypes from the same genotype in the same environment by developmental variation. J. Exp. Biol. 211, 510–523 (2008).
    CAS  PubMed  Article  Google Scholar 

    16.
    Vogt, G., Tolley, L. & Scholtz, G. Life stages and reproductive components of the Marmorkrebs (marbled crayfish), the first parthenogenetic decapod crustacean. J. Morphol. 261, 286–311 (2004).
    PubMed  Article  Google Scholar 

    17.
    Kato, M., Hiruta, C. & Tochinai, S. The behavior of chromosomes during parthenogenetic oogenesis in Marmorkrebs Procambarus fallax f. virginalis. Zool. Sci. 33, 426–430 (2016).
    Article  Google Scholar 

    18.
    Gutekunst, J. et al. Clonal genome evolution and rapid invasive spread of the marbled crayfish. Nat. Ecol. Evol. 2, 567–573 (2018).
    PubMed  Article  Google Scholar 

    19.
    Chucholl, C. Marbled crayfish gaining ground in Europe: the role of the pet trade as invasion pathway. in Freshwater Crayfish: Global Overview (eds Kawai, T. et al.) 83–114 (CRC Press, 2015).

    20.
    Jones, J. P. G. et al. The perfect invader: a parthenogenic crayfish poses a new threat to Madagascar’s freshwater biodiversity. Biol. Invasions 11, 1475–1482 (2009).
    Article  Google Scholar 

    21.
    Kawai, T. et al. Parthenogenetic alien crayfish (Decapoda: Cambaridae) spreading in Madagascar. J. Crust. Biol. 29, 562–567 (2009).
    Article  Google Scholar 

    22.
    Andriantsoa, R. et al. Ecological plasticity and commercial impact of invasive marbled crayfish populations in Madagascar. BMC Ecol. 19, 8 (2019).
    PubMed  PubMed Central  Article  Google Scholar 

    23.
    Chucholl, C. & Pfeiffer, M. First evidence for an established Marmorkrebs (Decapoda, Astacida, Cambaridae) population in Southwestern Germany, in syntopic occurrence with Orconectes limosus (Rafinesque, 1817). Aquat. Invasions 5, 405–412 (2010).
    Article  Google Scholar 

    24.
    Lipták, B. et al. Expansion of the marbled crayfish in Slovakia: beginning of an invasion in the Danube catchment? J. Limnol. 75, 305–312 (2016).
    Google Scholar 

    25.
    Novitsky, R. A. & Son, M. O. The first records of Marmorkrebs [Procambarus fallax (Hagen, 1870) f. virginalis] (Crustacea, Decapoda, Cambaridae) in Ukraine. Ecol. Montenegrina 5, 44–46 (2016).
    Article  Google Scholar 

    26.
    Patoka, J. et al. Predictions of marbled crayfish establishment in conurbations fulfilled: evidences from the Czech Republic. Biologia 71, 1380–1385 (2016).
    CAS  Article  Google Scholar 

    27.
    Pârvulescu, L. et al. First established population of marbled crayfish Procambarus fallax (Hagen, 1870) f. virginalis (Decapoda, Cambaridae) in Romania. Bioinvasions Rec. 6, 357–362 (2017).
    Article  Google Scholar 

    28.
    Deidun, A. et al. Invasion by non-indigenous freshwater decapods of Malta and Sicily, central Mediterranean Sea. J. Crust. Biol. 38, 748–753 (2018).
    Google Scholar 

    29.
    Ercoli, F., Kaldre, K., Paaver, T. & Gross, R. First record of an established marbled crayfish Procambarus virginalis (Lyko, 2017) population in Estonia. Bioinvasions Rec. 8, 675–683 (2019).
    Article  Google Scholar 

    30.
    Charlesworth, B. Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation. Nat. Rev. Genet. 10, 195–205 (2009).
    CAS  PubMed  Article  Google Scholar 

    31.
    Ellegren, H. & Galtier, N. Determinants of genetic diversity. Nat. Rev. Genet. 17, 422–433 (2016).
    CAS  PubMed  Article  Google Scholar 

    32.
    Munoz, J., Chaturvedi, A., De Meester, L. & Weider, L. J. Characterization of genome-wide SNPs for the water flea Daphnia pulicaria generated by genotyping-by-sequencing (GBS). Sci. Rep. 6, 28569 (2016).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    33.
    Flynn, J. M., Chain, F. J., Schoen, D. J. & Cristescu, M. E. Spontaneous mutation accumulation in Daphnia pulex in selection-free vs. competitive environments. Mol. Biol. Evol. 34, 160–173 (2017).
    CAS  PubMed  Article  Google Scholar 

    34.
    Fazalova, V. & Nevado, B. Low spontaneous mutation rate and pleistocene radiation of pea aphids. Mol. Biol. Evol. 37, 2045–2051 (2020).
    CAS  PubMed  Article  Google Scholar 

    35.
    Krebs, C. J. Estimating abundance in animal and plant populations. in Ecological Methodology https://www.zoology.ubc.ca/~krebs/downloads/krebs_chapter_02_2020.pdf (2014).

    36.
    van der Heiden, C. A. & Dorn, N. J. Benefits of adjacent habitat patches to the distribution of a crayfish population in a hydro-dynamic wetland landscape. Aquat. Ecol. 51, 219–233 (2017).
    Article  Google Scholar 

    37.
    Liu, H. et al. Direct determination of the mutation rate in the bumblebee reveals evidence for weak recombination-associated mutation and an approximate rate constancy in insects. Mol. Biol. Evol. 34, 119–130 (2017).
    CAS  PubMed  Article  Google Scholar 

    38.
    Vandel, A. La parthénogenèse géographique. Contribution à l’étude biologique et cytologique de la parthénogenèse naturelle. Bull. Biol. Fr. Belg. 62, 164–281 (1928).
    Google Scholar 

    39.
    Baker, H. G. Characteristics and modes of origin of weeds. in The Genetics of Colonising Species (eds Baker, H. G. & Stebbins, G. L.) 147–172 (Academic Press, 1965).

    40.
    Tilquin, A. & Kokko, H. What does the geography of parthenogenesis teach us about sex? Philos. Trans. R. Soc. Lond. B Biol. Sci. 371, 20150538 (2016).
    PubMed  PubMed Central  Article  Google Scholar 

    41.
    Van Doninck, K., Schon, I., De Bruyn, L. & Martens, K. A general purpose genotype in an ancient asexual. Oecologia 132, 205–212 (2002).
    PubMed  Article  Google Scholar 

    42.
    Van Doninck, K., Schon, I., Martens, K. & Backeljau, T. Clonal diversity in the ancient asexual ostracod Darwinula stevensoni assessed by RAPD-PCR. Heredity 93, 154–160 (2004).
    PubMed  Article  CAS  Google Scholar 

    43.
    Gatzmann, F. et al. The methylome of the marbled crayfish links gene body methylation to stable expression of poorly accessible genes. Epigenetics Chromatin 11, 57 (2018).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    44.
    Carneiro, V. C. & Lyko, F. Rapid epigenetic adaptation in animals and its role in invasiveness. Integr. Comp. Biol. 60, 267–274 (2020).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    45.
    Mauvisseau, Q., Tönges, S., Andriantsoa, R., Lyko, F. & Sweet, M. Early detection of an emerging invasive species: eDNA monitoring of a parthenogenetic crayfish in freshwater systems. Manag. Biol. Invasions 10, 461–472 (2019).
    Article  Google Scholar 

    46.
    Andriantsoa, R. et al. Perceived socio-economic impacts of the marbled crayfish invasion in Madagascar. PLoS ONE 15, e0231773 (2020).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    47.
    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 

    48.
    Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    49.
    Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    50.
    McKenna, 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 

    51.
    Cingolani, P. et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 6, 80–92 (2012).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    52.
    Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).
    CAS  Article  Google Scholar 

    53.
    Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).
    Article  Google Scholar 

    54.
    Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321 (2010).
    CAS  PubMed  Article  Google Scholar 

    55.
    Stacklies, W., Redestig, H., Scholz, M., Walther, D. & Selbig, J. pcaMethods–a bioconductor package providing PCA methods for incomplete data. Bioinformatics 23, 1164–1167 (2007).
    CAS  PubMed  Article  Google Scholar 

    56.
    Johnson, K. E. et al. Cancer cell population growth kinetics at low densities deviate from the exponential growth model and suggest an Allee effect. PLoS Biol. 17, e3000399 (2019).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    57.
    Maiakovska, O. & Legrand, C. OlenaMaiakovska/Population_Analysis_MC. Zenodo, https://doi.org/10.5281/zenodo.4110932 (2020). More

  • in

    The effectiveness of national biodiversity investments to protect the wealth of nature

    1.
    Huwyler, F., Kappeli, J., Serafimova, K., Swanson, E. & Tobin, J. Conservation Finance: Moving Beyond Donor Funding Toward an Investor-driven Approach (WWF, Credit Suisse and McKinsey & Company, 2014); http://go.nature.com/2Ka5Y2u
    2.
    Deutz, A. et al. Financing Nature: Closing the Global Biodiversity Financing Gap: Full Report (Paulson Institute, Nature Conservancy and Cornell Atkinson Center for Sustainability, 2020).

    3.
    Halpern, B. et al. Gaps and mismatches between global conservation priorities and spending. Conserv. Biol. 20, 56–64 (2006).
    Article  Google Scholar 

    4.
    James, A., Gaston, K. J. & BalmfordA. Can we afford to conserve biodiversity? BioScience 51, 43–52 (2001).
    Article  Google Scholar 

    5.
    McCarthy, D. et al. Financial costs of meeting global biodiversity conservation targets: current spending and unmet needs. Science 338, 946–949 (2012).
    CAS  Article  Google Scholar 

    6.
    Nature’s Dangerous Decline ‘Unprecedented’; Species Extinction Rates ‘Accelerating’ (IPBES, 2019); http://go.nature.com/2V4ZBN9

    7.
    The Global Risks Report 2020 (WEF, 2020); https://go.nature.com/3ahNfg8

    8.
    IUCN Views on the Preparation, Scope and Content of the Post-2020 Global Biodiversity Framework (IUCN, 2018); https://go.nature.com/2WlW3ti

    9.
    Biodiversity: Finance and the Economic and Business Case for Action (OECD, 2019); https://go.nature.com/3h0F9Kc

    10.
    Parker, C. & Cranford, M. The Little Biodiversity Finance Book. A Guide to Proactive Investment in Natural Capital (Global Canopy Program, 2010); https://go.nature.com/3mwyxUJ

    11.
    Coad, L. et al. Widespread shortfalls in protected area resourcing undermine efforts to conserve biodiversity. Front. Ecol. Environ. 17, 259–264 (2019).
    Article  Google Scholar 

    12.
    Kearney, S. G. et al. Estimating the benefit of well-managed protected areas for threatened species conservation. ORYX 54, 276–284 (2020).
    Article  Google Scholar 

    13.
    Waldron, A. et al. Protecting 30% of the Planet for Nature: Costs, Benefits and Economic Implications (IIASA, 2020); https://go.nature.com/387GkDq

    14.
    Stepping, K. M. K. & Meijer, K. S. The challenges of assessing the effectiveness of biodiversity-related development aid. Trop. Conserv. Sci. https://doi.org/10.1177/1940082918770995 (2018).

    15.
    Waldron, A. et al. Targeting global conservation funding to limit immediate biodiversity declines. Proc. Natl Acad. Sci. USA 110, 12144–12148 (2018).
    Article  Google Scholar 

    16.
    Gallo-Cajiao, E. et al. Crowdfunding biodiversity conservation. Conserv. Biol. 32, 1426–1435 (2018).
    Article  Google Scholar 

    17.
    Parker, C., Cranford, M., Oakes, N. & Leggett, M. The Little Biodiversity Finance Book 3rd edn (Global Canopy Programme, 2012).

    18.
    Arlaud, M. et al. in Towards a Sustainable Bioeconomy: Principles, Challenges and Perspectives (eds Filho, W. L. et al.) Ch. 5 (Springer, 2018); https://doi.org/10.1007/978-3-319-73028-8_5

    19.
    Rawat, U. S. & Agarwal, N. K. Biodiversity: concept, threats and conservation. Environ. Conserv. J. 16, 19–28 (2015).
    Article  Google Scholar 

    20.
    Gorobets, A. Wild fauna conservation: IUCN-CITES match is required. Ecol. Indic. 112, 106091 (2020).
    Article  Google Scholar 

    21.
    Rodrigues, A. S. L. et al. The value of the IUCN Red List for conservation. Trends Ecol. Evol. 21, 71–76 (2006).
    Article  Google Scholar 

    22.
    Rao, M., Naro-Maciel, E. & Sterling, E. Protected Areas and Biodiversity Conservation II: Management and Effectiveness (Network of Conservation Educators and Practitioners, 2009).

    23.
    Adams, V. M., Iacona, G. D. & Possingham, H. P. Weighing the benefits of expanding protected areas versus managing existing ones. Nat. Sustain. 2, 404–411 (2019).
    Article  Google Scholar 

    24.
    BIOFIN The Biodiversity Finance Initiative Workbook 2018 (United Nations Development Programme, 2018).

    25.
    Costanza, R. et al. The value of the world’s ecosystem services and natural capital. Nature 387, 253–260 (1997).
    CAS  Article  Google Scholar 

    26.
    Costanza, R. et al. Changes in the global value of ecosystem services. Glob. Environ. Change 26, 152–158 (2014).
    Article  Google Scholar 

    27.
    Naidoo, R. et al. Global mapping of ecosystem services and conservation priorities. Proc. Natl Acad. Sci. USA 105, 9495–9500 (2008).
    CAS  Article  Google Scholar 

    28.
    Turner, W. et al. Global conservation of biodiversity and ecosystem services. BioScience 57, 868–873 (2007).
    Article  Google Scholar 

    29.
    Balmford, A. et al. Economic reasons for conserving wild nature. Science 297, 950–953 (2002).
    CAS  Article  Google Scholar 

    30.
    Hily, E. et al. Assessing the cost-effectiveness of a biodiversity conservation policy: a bio-econometric analysis of Natura 2000 contracts in forests. Ecol. Econ. 119, 197-208 (2015).

    31.
    Ferraro, P. J., McIntosh, C. & Ospina, M. The effectiveness of the US endangered special act: an econometric analysis using matching methods. J. Environ. Econ. Manag. 54, 245–261 (2007).
    Article  Google Scholar 

    32.
    Waldron, A. et al. Targeting global conservation funding to limit immediate biodiversity declines. Proc. Natl Acad. Sci. USA 110, 12144–12148 (2013).
    CAS  Article  Google Scholar 

    33.
    Waldron, A. et al. Reductions in global biodiversity loss predicted from conservation spending. Nature 551, 364–367 (2017).
    CAS  Article  Google Scholar 

    34.
    Richerzhagen, C. et al. Why We Need More and Better Biodiversity Aid Briefing Paper 13 (German Development Institute, 2016); https://go.nature.com/2K0S9Dz

    35.
    Myers, N., Mittermeier, R. A., Mittermeier, C. G., Da Fonseca, G. A. & Kent, J. Biodiversity hotspots for conservation priorities. Nature 403, 853–858 (2000).

    36.
    Karousakis, K. Evaluating the Effectiveness of Policy Instruments for Biodiversity: Impact Evaluation, Cost-effectiveness Analysis and Other Approaches Environment Working Paper No.141 (OECD, 2018).

    37.
    Isaza, C., Bofill, W. & Cabrera, H. Cost-effective species conservation: an application to Huemul (Hippocamelus bisulcus) in Chile. Environ. Dev. Econ. 12, 535–551 (2007).
    Article  Google Scholar 

    38.
    Alix-Garcia, J. M., Shapiro, E. N. & Sims, K. R. Forest conservation and slippage: evidence from Mexico’s national payments for ecosystem services program. Land Econ. 88, 613–638 (2012).
    Article  Google Scholar 

    39.
    Bare, M. Assessing the impact of international conservation aid on deforestation in sub-Saharan Africa. Environ. Res. Lett. 10, 125010 (2015).
    Article  Google Scholar 

    40.
    Ferraro, P. J. et al. More strictly protected areas are not necessarily more protective: evidence from Bolivia, Costa Rica, Indonesia, and Thailand. Environ. Res. Lett. 8, 025011 (2013).
    Article  Google Scholar 

    41.
    Lindsey, P. A. et al. More than $1 billion needed annually to secure Africa’s protected areas with lions. Proc. Natl Acad. Sci. USA 115, E10788–E10796 (2018).
    CAS  Article  Google Scholar 

    42.
    Bonham, C. et al. Conservation trust funds, protected area management effectiveness and conservation outcomes: lessons from the global conservation fund. Parks 20, 89–100 (2014).
    Article  Google Scholar 

    43.
    Hein, Lars et al. Progress in natural capital accounting for ecosystems. Science 367, 514–515 (2020).
    CAS  Article  Google Scholar 

    44.
    Natural Capital Accounting and Valuing Ecosystem Services Project (UN, 2019); http://go.nature.com/2K2jsxn

    45.
    Ecosystem Valuation and Natural Capital Accounting (Gaborone Declaration for Sustainability in Africa, 2012); http://www.gaboronedeclaration.com/nca

    46.
    Climate Public Expenditure and Institutional Review (CPEIR) (UNDP, 2015); https://go.nature.com/2K0C7tp

    47.
    BIOFIN Workbook: Mobilising Resources for Biodiversity and Sustainable Development (UND, 2016); https://go.nature.com/3p1PDMb

    48.
    Shieh, G. Effect size, statistical power, and sample size for assessing interactions between categorical and continuous variables. Br. J. Math. Stat. Psychol. 72, 136–154 (2019).
    Article  Google Scholar 

    49.
    Leon, A. C. & Heo, M. Sample sizes required to detect interactions between two binary fixed-effects in a mixed-effects linear regression model. Comput. Stat. Data Anal. 53, 603–608 (2009).
    Article  Google Scholar 

    50.
    Marques, A. et al. Increasing impacts of land use on biodiversity and carbon sequestration driven by population and economic growth. Nat. Ecol. Evol. 3, 628–637 (2019).
    Article  Google Scholar 

    51.
    Tilman, D. et al. Future threats to biodiversity and pathways to their prevention. Nature 546, 73–81 (2017).
    CAS  Article  Google Scholar 

    52.
    Luther, D. A. et al. Determinants of bird conservation—action implementation and associated population trends of threatened species. Conserv. Biol. 30, 1338–1346 (2016).
    Article  Google Scholar 

    53.
    Hoffmann, M. et al. The impact of conservation on the status of the world’s vertebrates. Science 330, 1503–1509 (2010).
    CAS  Article  Google Scholar 

    54.
    Brooks, T. M. et al. Analysing biodiversity and conservation knowledge products to support regional environmental assessments. Sci. Data 3, I60007 (2016).
    Article  Google Scholar 

    55.
    Keith, D. A. et al. Scientific foundations for an IUCN Red List of ecosystems. PLoS ONE 8, e62111 (2013).
    CAS  Article  Google Scholar 

    56.
    Kaufmann, D., Kraay, A. & Mastruzzi, M. The worldwide governance indicators: methodology and analytical issues. Hague J. Rule Law 3, 220–246 (2011).
    Article  Google Scholar 

    57.
    Akaike, H. Information Theory and an Extension of the Maximum Likelihood Principle (Academiai Kiado, 1973).

    58.
    Bozdogan, H. Model selection and Akaike’s Information Criterion (AIC): the general theory and its analytical extensions. Psychometrika 52, 345–370 (1987).
    Article  Google Scholar 

    59.
    Angrist, J. D. & Pischke, J.-S. Mostly Harmless Econometrics: An Empiricist’s Companion (Princeton Univ. Press, 2009); http://go.nature.com/3r5t6zA

    60.
    Wooldridge, J. M. Econometric Analysis of Cross Section and Panel Data 2nd edn (MIT Press, 2010). More

  • in

    Simulated atmospheric nitrogen deposition inhibited the leaf litter decomposition of Cinnamomum migao H. W. Li in Southwest China

    1.
    Galloway, J. N. et al. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320, 889–892 (2008).
    ADS  CAS  PubMed  Article  Google Scholar 
    2.
    Zhou, X., Zhang, Y. & Downing, A. Non-linear response of microbial activity across a gradient of nitrogen addition to a soil from the gurbantunggut desert, northwestern China. Soil Biol. Biochem. 47, 67–77 (2012).
    CAS  Article  Google Scholar 

    3.
    Liu, X. et al. Enhanced nitrogen deposition over China. Nature 494, 459–462 (2013).
    ADS  CAS  PubMed  Article  Google Scholar 

    4.
    Fang, Y. T., Gundersen, P., Mo, J. M. & Zhu, W. X. Input and output of dissolved organic and inorganic nitrogen in subtropical forests of south China under high air pollution. Biogeosciences 5, 339–352 (2008).
    ADS  CAS  Article  Google Scholar 

    5.
    Hoorens, B., Aerts, R. & Stroetenga, M. Does initial litter chemistry explain litter mixture effects on decomposition?. Oecologia 137, 578–586 (2003).
    ADS  PubMed  Article  Google Scholar 

    6.
    Passarinho, J. A. P., Lamosa, P., Baeta, J. P., Santos, H. & Ricardo, C. P. P. Annual changes in the concentration of minerals and organic compounds of Quercus suber leaves. Physiol. Plantarum 127, 100–110 (2006).
    CAS  Article  Google Scholar 

    7.
    Shen, F. F. et al. Litterfall ecological stoichiometry and soil available nutrients under long-term nitrogen deposition in a Chinese fir plantation. Acta Ecol. Sin. 38, 7477–7487 (2018).
    Google Scholar 

    8.
    Huangfu, C. & Wei, Z. Nitrogen addition drives convergence of leaf litter decomposition rates between Flaveria bidentis and native plant. Plant Ecol. 219, 1355–1368 (2018).
    Article  Google Scholar 

    9.
    Vivanco, L. & Austin, A. Nitrogen addition stimulates forest litter decomposition and disrupts species interactions in Patagonia, Argentina. Global Change Biol. 17, 1963–1974 (2011).
    ADS  Article  Google Scholar 

    10.
    Li, H., Wei, Z., Huangfu, C., Chen, X. & Yang, D. Litter mixture dominated by leaf litter of the invasive species, Flaveria bidentis, accelerates decomposition and favors nitrogen release. J. Plant Res. 130, 167–180 (2017).
    CAS  PubMed  Article  Google Scholar 

    11.
    Aerts, R. D. C. H. Nutritional and plant-mediated controls on leaf litter decomposition of Carex species. Ecology 78, 244–260 (1997).
    Article  Google Scholar 

    12.
    Osono, T. & Takeda, H. Accumulation and release of nitrogen and phosphorus in relation to lignin decomposition in leaf litter of 14 tree species. Ecol. Res. 19, 593–602 (2004).
    Article  Google Scholar 

    13.
    Bradford, M. A., Berg, B., Maynard, D. S., Wieder, W. R. & Wood, S. A. Understanding the dominant controls on litter decomposition. J. Ecol. 104, 229–238 (2016).
    CAS  Article  Google Scholar 

    14.
    García-Palacios, P., Shaw, E. A., Wall, D. H. & Hättenschwiler, S. Temporal dynamics of biotic and abiotic drivers of litter decomposition. Ecol. Lett. 19, 554–563 (2016).
    PubMed  Article  Google Scholar 

    15.
    Song, C., Liu, D., Yang, G., Song, Y. & Mao, R. Effect of nitrogen addition on decomposition of Calamagrostis angustifolia litters from freshwater marshes of northeast China. Ecol. Eng. 37, 1578–1582 (2011).
    Article  Google Scholar 

    16.
    Zhang, D., Hui, D., Luo, Y. & Zhou, G. Rates of litter decomposition in terrestrial ecosystems: global patterns and controlling factors. J. Plant Ecol. 1, 85–93 (2008).
    Article  Google Scholar 

    17.
    Chen, F. et al. Nitrogen deposition effect on forest litter decomposition is interactively regulated by endogenous litter quality and exogenous resource supply. Plant Soil. 437, 413 (2019).
    CAS  Article  Google Scholar 

    18.
    Wang, Q., Kwak, J., Choi, W. & Chang, S. X. Long-term N and S addition and changed litter chemistry do not affect trembling aspen leaf litter decomposition, elemental composition and enzyme activity in a boreal forest. Environ. Pollut. 250, 143–154 (2019).
    CAS  PubMed  Article  Google Scholar 

    19.
    Hou, S. et al. Increasing rates of long-term nitrogen deposition consistently increased litter decomposition in a semi-arid grassland. New Phytol. 229, 296–307 (2020).
    PubMed  Article  Google Scholar 

    20.
    Yu, Z. et al. Nitrogen addition enhances home-field advantage during litter decomposition in subtropical forest plantations. Soil Biol. Biochem. 90, 188–196 (2015).
    CAS  Article  Google Scholar 

    21.
    Pichon, N. et al. Decomposition disentangled: A test of the multiple mechanisms by which nitrogen enrichment alters litter decomposition. Funct. Ecol. 34, 1485–1496 (2020).
    Article  Google Scholar 

    22.
    Hobbie, S. et al. Response of decomposing litter and its microbial community to multiple forms of nitrogen enrichment. Ecol. Monogr. 82, 389–405 (2012).
    Article  Google Scholar 

    23.
    Knops, J., Naeem, S. & Reich, P. The impact of elevated CO2, increased nitrogen availability and biodiversity on plant tissue quality and decomposition. Global Change Biol. 13, 1960–1971 (2007).
    ADS  Article  Google Scholar 

    24.
    Prescott, C. E. Does nitrogen availability control rates of litter decomposition in forests?. Plant Soil. 168, 83–88 (1995).
    Article  Google Scholar 

    25.
    Zhou, Y., Wang, L., Chen, Y., Zhang, J. & Liu, Y. Litter stoichiometric traits have stronger impact on humification than environment conditions in an alpine treeline ecotone. Plant Soil 453, 545–560 (2020).
    CAS  Article  Google Scholar 

    26.
    Mooshammer, M. et al. Stoichiometric controls of nitrogen and phosphorus cycling in decomposing beech litter. Ecology 93, 770–782 (2012).
    PubMed  Article  Google Scholar 

    27.
    Remy, E. et al. Driving factors behind litter decomposition and nutrient release at temperate forest edges. Ecosystems 24, 755–771 (2017).
    Google Scholar 

    28.
    Zhou, S. et al. Simulated nitrogen deposition significantly suppresses the decomposition of forest litter in a natural evergreen broad-leaved forest in the rainy area of western China. Plant Soil 420, 135–145 (2017).
    CAS  Article  Google Scholar 

    29.
    Cornwell, W. et al. Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecol. Lett. 11, 1065–1071 (2008).
    PubMed  Article  Google Scholar 

    30.
    Norris, M., Avis, P., Reich, P. & Hobbie, S. E. Positive feedbacks between decomposition and soil nitrogen availability along fertility gradients. Plant Soil 367, 347–361 (2013).
    CAS  Article  Google Scholar 

    31.
    Berg, B. & McClaugherty, C. Plant Litter: Decomposition, Humus Formation, Carbon Sequestration 2nd edn. (Springer, Berlin, 2008).
    Google Scholar 

    32.
    Cuchietti, A., Marcotti, E., Gurvich, D. E., Cingolani, A. M. & Harguindeguy, N. P. Leaf litter mixtures and neighbour effects: Low-nitrogen and high-lignin species increase decomposition rate of high-nitrogen and low-lignin neighbours. Appl. Soil Ecol. 82, 44–51 (2014).
    Article  Google Scholar 

    33.
    Jing, H. & Wang, G. Temporal dynamics of Pinus tabulaeformis litter decomposition under nitrogen addition on the loess plateau of China. For. Ecol. Manag. 476, 118465 (2020).
    Article  Google Scholar 

    34.
    Sun, T., Dong, L., Wang, Z., Lü, X. & Mao, Z. Effects of long-term nitrogen deposition on fine root decomposition and its extracellular enzyme activities in temperate forests. Soil Biol. Biochem. 93, 50–59 (2016).
    CAS  Article  Google Scholar 

    35.
    Carrera, A. L. & Bertiller, M. B. Combined effects of leaf litter and soil microsite on decomposition process in arid rangelands. J. Environ. Manag. 114, 505–511 (2013).
    CAS  Article  Google Scholar 

    36.
    Sun, Z. et al. The effect of nitrogen addition on soil respiration from a nitrogen-limited forest soil. Agr. For. Meteorol. 197, 103–110 (2014).
    Article  Google Scholar 

    37.
    He, X., Lin, Y., Han, G. & Ma, T. Litterfall interception by understorey vegetation delayed litter decomposition in Cinnamomum camphora plantation forest. Plant Soil 372, 207–219 (2013).
    CAS  Article  Google Scholar 

    38.
    Wang, Q. et al. Impact of 36 years of nitrogen fertilization on microbial community composition and soil carbon cycling-related enzyme activities in rhizospheres and bulk soils in northeast China. Appl. Soil Ecol. 136, 148–157 (2019).
    Article  Google Scholar 

    39.
    Chen, J. et al. Co-stimulation of soil glycosidase activity and soil respiration by nitrogen addition. Global Change Biol. 23, 1328–1337 (2016).
    ADS  Article  Google Scholar 

    40.
    Wang, C. et al. Responses of soil microbial community to continuous experimental nitrogen additions for 13 years in a nitrogen-rich tropical forest. Soil Biol. Biochem. 121, 103–112 (2018).
    CAS  Article  Google Scholar 

    41.
    Jing, X. et al. Neutral effect of nitrogen addition and negative effect of phosphorus addition on topsoil extracellular enzymatic activities in an alpine grassland ecosystem. Appl. Soil Ecol. 107, 205–213 (2016).
    Article  Google Scholar 

    42.
    Jing, X. et al. Nitrogen deposition has minor effect on soil extracellular enzyme activities in six Chinese forests. Sci. Total Environ. 607–608, 806–815 (2017).
    ADS  PubMed  Article  CAS  Google Scholar 

    43.
    Wang, Q., Kwak, J., Choi, W. & Chang, S. X. Decomposition of trembling aspen leaf litter under long-term nitrogen and sulfur deposition: effects of litter chemistry and forest floor microbial properties. For. Ecol. Manag. 412, 53–61 (2018).
    Article  Google Scholar 

    44.
    Huang, X. et al. Autotoxicity hinders the natural regeneration of Cinnamomum migao H W. Li in southwest China. Forests 10, 919 (2019).
    Article  Google Scholar 

    45.
    Feng, H., Xue, L. & Chen, H. Responses of decomposition of green leaves and leaf litter to stand density, N and P additions in Acacia auriculaeformis stands. Eur. J. For. Res. 137, 819–830 (2018).
    Article  Google Scholar 

    46.
    Diepen, L. V. et al. Changes in litter quality caused by simulated nitrogen deposition reinforce the N-induced suppression of litter decay. Ecosphere 6, t205 (2015).
    Article  Google Scholar 

    47.
    Zechmeister-Boltenstern, S. et al. The application of ecological stoichiometry to plant–microbial–soil organic matter transformations. Ecol. Monogr. 85, 133–155 (2015).
    Article  Google Scholar 

    48.
    Hobbie, S. E. Nitrogen effects on decomposition: A five-year experiment in eight temperate sites. Ecology 89, 2633–2644 (2008).
    PubMed  Article  Google Scholar 

    49.
    Hobbie, S. Interactions between litter lignin and nitrogenitter lignin and soil nitrogen availability during leaf litter decomposition in a hawaiian montane forest. Ecosystems 3, 484–494 (2000).
    CAS  Article  Google Scholar 

    50.
    Zhang, J. et al. Effect of nitrogen and phosphorus addition on litter decomposition and nutrients release in a tropical forest. Plant Soil 454, 139–153 (2020).
    CAS  Article  Google Scholar 

    51.
    Apolinário, V. et al. Litter decomposition of signalgrass grazed with different stocking rates and nitrogen fertilizer levels. Agron. J. 106, 1–6 (2014).
    Article  Google Scholar 

    52.
    Takeda, H. Decomposition Processes of Litter Along a Latitudinal Gradient (Springer, Dordrecht, 1998).
    Google Scholar 

    53.
    Torreta, N. K. & Takeda, H. Carbon and nitrogen dynamics of decomposing leaf litter in a tropical hill evergreen forest. Eur. J. Soil Biol. 35, 57–63 (1999).
    CAS  Article  Google Scholar 

    54.
    Song, Y., Song, C., Ren, J., Zhang, X. & Jiang, L. Nitrogen input increases Deyeuxia angustifolia litter decomposition and enzyme activities in a marshland ecosystem in Sanjiang plain, northeast China. Wetlands. 39, 549–557 (2019).
    Article  Google Scholar 

    55.
    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).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    56.
    Xia, M. A. T. A. Long-term simulated atmospheric nitrogen deposition alters leaf and fine root decomposition. Ecosystems 21, 1–14 (2018).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    57.
    Chen, F., Feng, X. & Liang, C. Endogenous versus exogenous nutrient affects C, N, and P dynamics in decomposing litters in mid-subtropical forests of China. Ecol. Res. 27, 923–932 (2012).
    CAS  Article  Google Scholar 

    58.
    Zhou, Z., Wang, C., Zheng, M., Jiang, L. & Luo, Y. Patterns and mechanisms of responses by soil microbial communities to nitrogen addition. Soil Biol. Biochem. 115, 433–441 (2017).
    CAS  Article  Google Scholar 

    59.
    He, X. et al. Diversity and decomposition potential of endophytes in leaves of a Cinnamomum camphora plantation in China. Ecol. Res. 27, 273 (2011).
    ADS  Article  Google Scholar 

    60.
    Berg, B. R. & Laskowski, R. Litter Decomposition: A Guide to Carbon and Nutrient Turnover, Advances in Ecological Research Vol. 38 (Academic Press, Waltham, 2006).
    Google Scholar 

    61.
    Hall, S., Huang, W., Timokhin, V. & Hammel, K. Lignin lags, leads, or limits the decomposition of litter and soil organic carbon. Ecology 101, e03113 (2020).
    PubMed  Article  Google Scholar 

    62.
    Tu, L. et al. Nitrogen addition significantly affects forest litter decomposition under high levels of ambient nitrogen deposition. PLoS ONE 9, e88752 (2014).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    63.
    Zhou, X. & Zhang, Y. Temporal dynamics of soil oxidative enzyme activity across a simulated gradient of nitrogen deposition in the gurbantunggut desert, northwestern China. Geoderma 213, 261–267 (2014).
    ADS  CAS  Article  Google Scholar 

    64.
    Hao, C. et al. Effects of experimental nitrogen and phosphorus addition on litter decomposition in an old-growth tropical forest. PLoS ONE 8, e84101 (2013).
    ADS  Article  Google Scholar 

    65.
    Cameron, K. C., Di, H. J. & Moir, J. Nitrogen losses from the soil/plant system: a review. Ann. Appl. Biol. 162, 145–173 (2013).
    CAS  Article  Google Scholar 

    66.
    Waldrop, M. P., Zak, D. R., Sinsabaugh, R. L., Gallo, M. & Lauber, C. Nitrogen deposition modifies soil carbon storage through changes in microbial enzymatic activity. Ecol. Appl. 14, 1172–1177 (2004).
    Article  Google Scholar 

    67.
    Freedman, Z. B., Upchurch, R. A., Zak, D. R. & Cline, L. C. Anthropogenic N deposition slows decay by favoring bacterial metabolism: Insights from metagenomic analyses. Front. Microbiol. 7, 259 (2016).
    PubMed  PubMed Central  Article  Google Scholar 

    68.
    Marklein, A. R. & Houlton, B. Z. Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytol. 193, 696–704 (2012).
    CAS  PubMed  Article  Google Scholar 

    69.
    Weand, M. P., Arthur, M. A., Lovett, G. M., McCulley, R. L. & Weathers, K. C. Effects of tree species and N additions on forest floor microbial communities and extracellular enzyme activities. Soil Biol. Biochem. 42, 2161–2173 (2010).
    CAS  Article  Google Scholar 

    70.
    Wang, C. et al. Response of litter decomposition and related soil enzyme activities to different forms of nitrogen fertilization in a subtropical forest. Ecol. Res. 26, 505–513 (2011).
    CAS  Article  Google Scholar 

    71.
    Feng, H., Xue, L. & Chen, H. Responses of decomposition of green leaves and leaf litter to stand density, N and P additions in Acacia auriculaeformis stands. Eur. J. Forest Res. 137, 819 (2018).
    Article  Google Scholar 

    72.
    Frey, S. D., Knorr, M., Parrent, J. L. & Simpson, R. T. Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. For. Ecol. Manag. 196, 159–171 (2004).
    Article  Google Scholar 

    73.
    Zheng, Z. et al. Effects of nutrient additions on litter decomposition regulated by phosphorus-induced changes in litter chemistry in a subtropical forest, China. For. Ecol. Manag. 400, 123–128 (2017).
    Article  Google Scholar 

    74.
    Mo, J. et al. Nitrogen addition reduces soil respiration in a mature tropical forest in southern China. Glob. Change Biol. 14, 403–412 (2008).
    ADS  Article  Google Scholar 

    75.
    Liu, G., Jiang, N. & Zhang, L. D. Soil Physical and Chemical Analysis and Description of Soil Profiles (Standards Press of China, Beijing, 1996).
    Google Scholar 

    76.
    Bao, S. D. Soil and Agricultural Chemistry Analysis 3rd edn. (China Agricultural Press, Beijing, 2013).
    Google Scholar 

    77.
    Allen, S. E. Chemical analysis of Ecological Materials, 2nd edn, Vol. 13 (Blackwell Scientific Publications, Oxford, 1989).
    Google Scholar 

    78.
    Rowland, A. P. & Roberts, J. D. Lignin and cellulose fractionation in decomposition studies using acid-detergent fibre methods. Commun. Soil Sci. Plan. 25, 269–277 (1994).
    CAS  Article  Google Scholar 

    79.
    Olson, J. Energy storage and the balance of producers and decomposers in ecological systems. Ecology 44, 322–331 (1963).
    Article  Google Scholar 

    80.
    Bockheim, J., Jepsen, E. A. & Heisey, D. M. Nutrient dynamics in decomposing leaf litter of four tree species on a sandy soil in northwestern Wisconsin. Can. J. For. Res. 21, 803–812 (1991).
    CAS  Article  Google Scholar  More

  • in

    Analysis of global human gut metagenomes shows that metabolic resilience potential for short-chain fatty acid production is strongly influenced by lifestyle

    Our results are consistent with a non-industrial gut harboring a more resilient ecology with respect to SCFA production, while the industrial gut ecology would be vulnerable to disruption of such pathways, yet the pattern is complex and nuanced. The increased gene abundance in non-industrial populations and overall ratio of acetate:butyrate:propionate generally agrees with previous studies of SCFAs5,12. Similarly, the higher genus-level diversity of bacteria encoding acetate, compared to the other SCFAs, is expected and matches studies that have documented the taxa that encode different SCFAs13,17,19. The overall high richness, high diversity at Hill numbers 1 and 2, and high Gini-Simpson indices found in non-industrial populations at the genus level indicates a highly diverse and evenly distributed production of SCFAs. From an ecological perspective, uneven production of SCFA dominated by a few bacteria in industrial gut microbiomes means lower functional diversity and less redundancy, which ultimately leads to an expectation of decreased resilience. In other words, this study finds that industrial gut microbiomes are at a higher risk of reduced SCFA production because SCFA synthesis is dominated by only a few genera. Given the lower resilience, factors that disrupt the gut ecology are expected to have a more extreme consequence to those living an industrial lifestyle.
    While there is an overall trend of increased genus-level functional diversity and redundancy for SCFA production in non-industrial populations, variation exists when examining the SCFAs and populations individually. At the genus-level, the pastoral and rural agricultural populations have increased richness of genera encoding genes involved in acetate and butyrate synthesis, while there is similarity across the different lifestyles for genus richness for propionate encoding taxa. Although hunter-gatherers have similar, or lower, genus richness as industrial populations, they have significantly higher diversity at Hill number orders 1 and 2 and Gini-Simpson indices for butyrate and propionate. Additionally, the pastoralists have a generally similar profile to the industrial populations for acetate and propionate Hill number diversity, as well as similarity to the industrial populations in species PD, which may be linked to this pastoralist group having a diet similar to some industrial populations; namely, a diet high in dairy and red meat consumption, coupled with few dietary sources of plant-derived fibers23. This paints a complex picture. Non-industrial populations have a high diversity of genera encoding butyrate synthesis, and butyrate production is spread more evenly across genera in non-industrial populations than in industrial populations. Hunter-gatherers and rural agriculturalists have significantly greater evenness of propionate production, even though they have fewer number of total genera encoding this SCFA. Finally, the richness and evenness of genera encoding acetate is similar between industrial and non-industrial populations. Ecologically, we would expect the industrial populations to be less resilient for production of butyrate and propionate when faced with a shift in taxonomic composition, while non-industrial populations may be only marginally more resilient for acetate production compared to industrial populations. Intriguingly, SCFA relative abundance does not appear to correlate to resilience profile. Acetate and butyrate are significantly more abundant in non-industrial populations but only butyrate shows much stronger resilience profile for non-industrial populations. Additionally, propionate is slightly more abundant in industrial populations, although not significantly, yet our results indicate greater resilience in non-industrial groups for propionate production. This indicates that measuring only total gene, and/or molar, abundance is not enough to make statements about metabolic processes in the human microbiome; rather, ecological approaches are necessary to understand diversity in functional potential of the human microbiome.
    The increased species-level alpha diversity in industrial populations initially runs counter to the genus-level results but the genus and species level results ultimately yield similar interpretations after accounting for ecology and ascertainment bias, as discussed below. The substantially higher species richness in industrial populations is striking; however, the differences in PD between industrial and non-industrial populations are not nearly as extreme. This means that the high species richness in the industrial populations is driven by species that are closely phylogenetically related. Indeed, we observed SCFA producing genera found at high abundance in industrial populations (Bacteroides and Clostridium) to have up to nine species encoding SCFAs, while highly abundant non-industrial genera only have one or two species. Therefore, what first appears to indicate high species-level ecological resilience in SCFA production in the industrial populations is actually the result of closely related species performing the same function. It follows that closely related species may be prone to changes in abundance or even elimination after certain types of ecosystem shift events. For example, narrow-spectrum antibiotics33 and exposure to various xenobiotic compounds that lead to variable bacterial metabolic responses34 are events that can affect a limited range of bacteria and lead to shifts in microbial abundance and metabolic activity. While this result has ecological implications, it is also likely the result of historical trends of microbiology research. Bacterial taxa at high abundance in non-industrial gut microbiomes have not been a focus of microbiological isolation and species identification until recently; therefore, we expect more species to be identified from non-industrial gut microbiomes in the future35. Additionally, classification of bacteria into distinct genera and species is undergoing a revolution in the genomic era36 meaning that the high number of species classified to Bacteroides and Clostridium may ultimately be reclassified to different genera. Nevertheless, the fact that we observe a large jump in species richness, but only a minor increase in species PD, in the industrial gut microbiomes suggests that the high industrial species richness is driven by closely related species and therefore, results in the same interpretation as the genus richness results: diversity is high in non-industrial populations.
    Ascertainment bias extends to the databases used to identify taxa and genes: fewer genes were identified in non-industrial populations and a smaller proportion of these genes can be linked back to bacteria at every taxonomic level, in non-industrial gut microbiomes. In some cases, such as butyrate synthesis genes, less than 10% of genes are identified to species for non-industrial populations, while over 50% of such identifications were possible for industrial populations. A decreased ability to identify the genus and species encoding SCFA synthesis genes in non-industrial populations means that the ecological metrics underestimate the true ecological diversity of these genes. Moreover, the drop-off in classification from the genus to the species level was significantly greater in non-industrial populations compared to industrial populations. This drop-off means a much lesser ability to identify species compared to genera in non-industrial populations, which helps explain why species diversity was substantially lower in non-industrial populations. Nevertheless, the statistically significant differences observed at the genus-level send a strong signal of the high functional diversity, and potential resilience, of SCFA synthesis genes in non-industrial gut microbiomes.
    The metagenome-wide poor performance in terms of gene identification and classifying SCFA genes to genera and species indicates a bias in reference databases that underrepresents diversity in non-industrial gut microbiomes, which is unsurprising. Bias is expected because the vast majority of human gut microbiome studies have used samples from industrial populations. There is an immense challenge in including non-industrial communities in biomedical research, including recruiting research participants, sustaining longitudinal sampling, building culturally appropriate community relationships, and even securing transport of samples35. This has resulted in comparatively few metagenomic studies of human gut microbiomes from non-industrial settings35. Nevertheless, our data demonstrate the extent of this bias and how it can hinder more in-depth study of human gut microbiome health. Given this sizable ascertainment bias favored industrial populations, the non-industrial populations are likely even more diverse, more resilient, than our databases can sufficiently characterize, making our genus-level results even stronger. Without a serious investment to include such populations, the characterization of microbiomes will remain naive to the ecological breadth of the core, healthy, human gut. Imagine studying forest ecology, with only city parks at your disposal. This has been, overwhelmingly, the analogous practice of human microbiome research.
    The relative lack of microbiome studies with non-industrial populations means an underrepresentation of not only metagenomic data and genome annotation but also fewer opportunities for cultivation and validation of novel species of bacteria. This ultimately leads to an inequality in the depth to which researchers can describe microbiome samples from non-industrial communities, compared to industrial microbiomes, as diverse groups of novel taxa may be grouped into a single group of “unknown” or “unclassified” bacteria35. Similarly, an incomplete picture of microbial functional potential means that genes may be misidentified or even unannotated completely. Unknown taxa and misidentified genes may be playing key roles in ecological and metabolic processes but researchers are unable to confidently identify them, let alone make statements about their importance in a microbial ecology35. Recent human gut microbiome metagenome studies from diverse populations will undoubtedly improve database representation but the number of studies and metagenomic samples from non-industrial populations still pales in comparison to industrial gut microbiomes26,35,37,38.
    Limitations in annotating the full extent of microbial diversity impacts health research. Recently proposed ‘Microbiota Insufficiency Syndrome (MIS)’2 postulates that, while the microbiome has adapted to industrialization, these adaptations are maladaptive to human health. The decreased phylogenetic diversity and loss of specific taxa (e.g. Prevotellaceae, Succinivibrionaceae, and Spirochaetaceae) observed in industrial gut microbiomes may contribute to the increase in non-communicable chronic diseases found at higher prevalence in industrial populations. The root cause of MIS in industrial populations is undoubtedly multifactorial; however, diet is suggested to play a major role2. This syndrome is compelling and we postulate that this insufficiency precisely rests on the stability of functional capacity. Our findings of decreased resilience in industrial populations, as well as species-level diversity driven by a few closely related species, fits in well with MIS. Low resilience in SCFA production may ultimately manifest itself as altered colonocyte function and/or autoimmune disruptions (both symptoms of MIS) due to a decrease in SCFA bioavailability after a group SCFA-producing bacteria were wiped-out during an ecological shift, such as antibiotic or xenobiotic exposure. Similar to MIS, diet is likely to play an important role in SCFA resilience. The non-industrial populations studied in this paper consume much more fiber than industrial populations, on average3,5,14,25,26, and microbial fermentation of dietary fibers is a major source of SCFAs in the human digestive tract39. A diet poor in dietary fiber means less substrate for microbial fermentation and therefore less SCFA production and also higher competition for that fiber, potentially resulting in competitive exclusion and less microbial diversity. Nevertheless, if we are unable to fully characterize and annotate non-industrial gut microbiomes then we will be unable to paint a complete picture of MIS. Currently, we have confidence that there is a wealth of undiscovered resilience in non-industrial gut microbiomes. Once we describe the extent of this diversity/resilience, through increased sampling and focus on partnerships with research institutes in industrializing countries, we will have a more complete picture of MIS and possibly develop therapeutic approaches to combat non-communicable chronic diseases related to the human gut microbiome.
    Improved sampling, metabolic profiling, and annotation will not only improve our understanding of SCFA resilience, but it will also permit more detailed picture microbiome wide resilience. Our work shows the value of focusing on specific SCFA genes, due to their importance in human biology and previously reported variation in SCFA molar abundance between industrial and non-industrial populations31,32; however, future work will undoubtedly add to our findings. One avenue for future work is through analyzing SCFA molar concentrations in fecal samples in a longitudinal setting and comparing these results to predicted SCFA resilience from metagenome panels. Unlike genomic data, where we can infer about SCFA production potential via taxonomic diversity, one-time measures of fecal SCFA molar concentrations will not inform about future resilience because SCFA molar concentrations carry no information about which taxa produce each SCFA. Longitudinal SCFA concentration and metagenomic data from non-industrial populations, or animal models, is necessary to inform about SCFA resilience and production in diverse lifestyles. Another avenue for future work is to focus resilience analysis on other microbiome functions of interest, such as resilience of antibiotic resistance genes and amino acid biosynthetic pathways. These valuable studies would be valuable for comparing microbiome resilience dynamics for different functions, with the caveat that there is sufficient genomic annotation data to yield interpretable results.
    Lack of sample diversity is not unique to human microbiome research, as human genetics research has been grappling with this very issue for decades. In 2009, 96% of individuals included in human genome-wide association studies (GWAS) claimed European ancestry, as compared to 78% in 201940. Thus, while there have been improvements, GWAS clearly fail to reflect the breadth of human diversity. Incorporating diverse populations in human genome and microbiome research has the potential to greatly benefit the scientific community’s understanding of human biology and develop treatments that are based on human diversity rather than European-ancestry genetics and microbiomes. A key component of increasing representation in genetics and microbiome studies is that these studies are designed as partnerships with minority and/or indigenous communities in a manner that builds both trust between the community and researchers, as well as facilitates the ability for the sample donors to exercise their rights on how data are treated and shared41. More