More stories

  • in

    Prebiotic effects of yeast mannan, which selectively promotes Bacteroides thetaiotaomicron and Bacteroides ovatus in a human colonic microbiota model

    1.
    Liu, H. Z., Liu, L., Hui, H. & Wang, Q. Structural characterization and antineoplastic activity of Saccharomyces cerevisiae mannoprotein. Int. J. Food Prop. 18, 359–371 (2015).
    CAS  Google Scholar 
    2.
    Kocourek, J. & Ballou, C. E. Method for fingerprinting yeast cell wall mannans. J. Bacteriol. 100, 1175–1181 (1969).
    CAS  PubMed  PubMed Central  Google Scholar 

    3.
    Scheller, H. V. & Ulvskov, P. Hemicelluloses. Annu. Rev. Plant Biol. 61, 263–289 (2010).
    CAS  PubMed  Google Scholar 

    4.
    Jin, X., Zhang, M., Cao, G. F. & Yang, Y. F. Saccharomyces cerevisiae mannan induces sheep beta-defensin-1 expression via Dectin-2-Syk-p38 pathways in ovine ruminal epithelial cells. Vet. Res. (Faisalabad) 50, 8 (2019).
    Google Scholar 

    5.
    Michael, C. F. et al. Airway epithelial repair by a prebiotic mannan derived from Saccharomyces cerevisiae. J. Immunol. Res. 2017, 8903982 (2017).
    PubMed  PubMed Central  Google Scholar 

    6.
    Lew, D. B. et al. Beneficial effects of prebiotic Saccharomyces cerevisiae mannan on allergic asthma mouse models. J. Immunol. Res. 2017, 3432701 (2017).
    PubMed  PubMed Central  Google Scholar 

    7.
    Cuskin, F. et al. Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism. Nature 517, 165–169 (2015).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    8.
    Flint, H. J., Scott, K. P., Louis, P. & Duncan, S. H. The role of the gut microbiota in nutrition and health. Nat. Rev. Gastroenterol. Hepatol. 9, 577–589 (2012).
    CAS  PubMed  Google Scholar 

    9.
    Cani, P. D. et al. Microbial regulation of organismal energy homeostasis. Nat. Metab. 1, 34–46 (2019).
    CAS  PubMed  Google Scholar 

    10.
    Hooper, L. V. & Macpherson, A. J. Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat. Rev. Immunol. 10, 159–169 (2010).
    CAS  PubMed  Google Scholar 

    11.
    Pickard, J. M., Zeng, M. Y., Caruso, R. & Núñez, G. Gut microbiota: Role in pathogen colonization, immune responses, and inflammatory disease. Immunol. Rev. 279, 70–89 (2017).
    CAS  PubMed  PubMed Central  Google Scholar 

    12.
    Arora, T. & Bäckhed, F. The gut microbiota and metabolic disease: Current understanding and future perspectives. J. Intern. Med. 280, 339–349 (2016).
    CAS  PubMed  Google Scholar 

    13.
    Wang, Z. et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 472, 57–63 (2011).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    14.
    Wong, S. H. & Yu, J. Gut microbiota in colorectal cancer: Mechanisms of action and clinical applications. Nat. Rev. Gastroenterol. Hepatol. 16, 690–704 (2019).
    CAS  PubMed  PubMed Central  Google Scholar 

    15.
    Vogt, N. M. et al. Gut microbiome alterations in Alzheimer’s disease. Sci. Rep. 7, 13537 (2017).
    ADS  PubMed  PubMed Central  Google Scholar 

    16.
    The Human Microbiome Project Consortium. Structure, function, and diversity of the healthy human microbiome. Nature 486, 207–214 (2012).
    ADS  PubMed Central  Google Scholar 

    17.
    Bolam, D. N. & Koropatkin, N. M. Glycan recognition by the Bacteroidetes Sus-like systems. Curr. Opin. Struct. Biol. 22, 563–569 (2012).
    CAS  PubMed  Google Scholar 

    18.
    Foley, M. H., Cockburn, D. W. & Koropatkin, N. M. The Sus operon: A model system for starch uptake by the human gut Bacteroidetes. Cell. Mol. Life. Sci. 73, 2603–2617 (2016).
    CAS  PubMed  PubMed Central  Google Scholar 

    19.
    Bågenholm, V. et al. Galactomannan catabolism conferred by a polysaccharide utilization locus of Bacteroides ovatus. J. Biol. Chem. 292, 229–243 (2017).
    PubMed  Google Scholar 

    20.
    Martens, E. C., Koropatkin, N. M., Smith, T. J. & Gordon, J. I. Complex glycan catabolism by the human gut microbiota: The Bacteroidetes Sus-like paradigm. J. Biol. Chem. 284, 24673–24677 (2009).
    CAS  PubMed  PubMed Central  Google Scholar 

    21.
    Larsbrink, J. et al. A discrete genetic locus confers xyloglucan metabolism in select human gut Bacteroidetes. Nature 506, 498–502 (2014).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    22.
    Martens, E. C. et al. Recognition and degradation of plant cell wall polysaccharides by two human gut symbionts. PLoS Biol. 9, e1001221 (2011).
    CAS  PubMed  PubMed Central  Google Scholar 

    23.
    Rakoff-Nahoum, S., Foster, K. R. & Comstock, L. E. The evolution of cooperation within the gut microbiota. Nature 533, 255–259 (2016).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    24.
    Flint, H. J., Bayer, E. A., Rincon, M. T., Lamed, R. & White, B. A. Polysaccharide utilization by gut bacteria: Potential for new insights from genomic analysis. Nat. Rev. Microbiol. 6, 121–131 (2008).
    CAS  PubMed  Google Scholar 

    25.
    Koropatkin, N. M., Cameron, E. A. & Martens, E. C. How glycan metabolism shapes the human gut microbiota. Nat. Rev. Microbiol. 10, 323–335 (2012).
    CAS  PubMed  PubMed Central  Google Scholar 

    26.
    Varyukhina, S. et al. Glycan-modifying bacteria-derived soluble factors from Bacteroides thetaiotaomicron and Lactobacillus casei inhibit rotavirus infection in human intestinal cells. Microbes Infect. 14, 273–278 (2012).
    CAS  PubMed  Google Scholar 

    27.
    López-Boado, Y. S. et al. Bacterial exposure induces and activates matrilysin in mucosal epithelial cells. J. Cell Biol. 148, 1305–1315 (2000).
    PubMed  PubMed Central  Google Scholar 

    28.
    Delday, M., Mulder, I., Logan, E. T. & Grant, G. Bacteroides thetaiotaomicron ameliorates colon inflammation in preclinical models of Crohn’s disease. Inflamm. Bowel Dis. 25, 85–96 (2019).
    PubMed  Google Scholar 

    29.
    Hansen, R. et al. A phase I randomized, double-blind, placebo-controlled study to assess the safety and tolerability of (Thetanix) Bacteroides thetaiotaomicron in adolescents with stable Crohn’s disease. https://www.4dpharmaplc.com/application/files/1815/5824/8886/Thetanix_DDW_poster_2019.pdf. Accessed 15 July 2020 (2019).

    30.
    Salyers, A. A., Vercellotti, J. R., West, S. E. & Wilkins, T. D. Fermentation of mucin and plant polysaccharides by strains of Bacteroides from the human colon. Appl. Environ. Microbiol. 33, 319–322 (1977).
    CAS  PubMed  PubMed Central  Google Scholar 

    31.
    Rawi, M. H., Zaman, S. A., Pa’ee, K. F., Leong, S. S. & Sarbini, S. R. Prebiotics metabolism by gut-isolated probiotics. J. Food Sci. Technol. 57, 1–14 (2020).
    Google Scholar 

    32.
    Oba, S. et al. Yeast mannan increases Bacteroides thetaiotaomicron abundance and suppresses putrefactive compound production in in vitro fecal microbiota fermentation. Biosci. Biotechnol. Biochem. 84, 2174–2178 (2020).
    CAS  PubMed  Google Scholar 

    33.
    Sasaki, D. et al. Low amounts of dietary fibre increase in vitro production of short-chain fatty acids without changing human colonic microbiota structure. Sci. Rep. 8, 435 (2018).
    ADS  PubMed  PubMed Central  Google Scholar 

    34.
    Takagi, R. et al. A single-batch fermentation system to simulate human colonic microbiota for high-throughput evaluation of prebiotics. PLoS ONE 11, e0160533 (2016).
    PubMed  PubMed Central  Google Scholar 

    35.
    Sender, R., Fuchs, S. & Milo, R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol. 14, e1002533 (2016).
    PubMed  PubMed Central  Google Scholar 

    36.
    Wexler, H. M. Bacteroides: The good, the bad, and the nitty-gritty. Clin. Microbiol. Rev. 20, 593–621 (2007).
    CAS  PubMed  PubMed Central  Google Scholar 

    37.
    Tong, J., Liu, C., Summanen, P., Xu, H. & Finegold, S. M. Application of quantitative real-time PCR for rapid identification of Bacteroides fragilis group and related organisms in human wound samples. Anaerobe 17, 64–68 (2011).
    CAS  PubMed  Google Scholar 

    38.
    Slavin, J. Fiber and prebiotics: Mechanisms and health benefits. Nutrients 5, 1417–1435 (2013).
    CAS  PubMed  PubMed Central  Google Scholar 

    39.
    Koh, A., De Vadder, F., Kovatcheva-Datchary, P. & Bäckhed, F. From dietary fiber to host physiology: Short-chain fatty acids as key bacterial metabolites. Cell 165, 1332–1345 (2016).
    CAS  PubMed  Google Scholar 

    40.
    den Besten, G. et al. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J. Lipid Res. 54, 2325–2340 (2013).
    Google Scholar 

    41.
    Gibson, G. R. et al. The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat. Rev. Gastroenterol. Hepatol. 14, 491–502 (2017).
    PubMed  Google Scholar 

    42.
    Holscher, H. D. Dietary fiber and prebiotics and the gastrointestinal microbiota. Gut Microbes 8, 172–184 (2017).
    CAS  PubMed  PubMed Central  Google Scholar 

    43.
    Chang, C. J. et al. Next generation probiotics in disease amelioration. J. Food Drug Anal. 27, 615–622 (2019).
    CAS  PubMed  Google Scholar 

    44.
    Tan, H. et al. Pilot safety evaluation of a novel strain of Bacteroides ovatus. Front. Genet. 9, 539 (2018).
    CAS  PubMed  PubMed Central  Google Scholar 

    45.
    Tzianabos, A. O., Onderdonk, A. B., Rosner, B., Cisneros, R. L. & Kasper, D. L. Structural features of polysaccharides that induce intra-abdominal abscesses. Science 262, 416–419 (1993).
    ADS  CAS  PubMed  Google Scholar 

    46.
    Bamba, T., Matsuda, H., Endo, M. & Fujiyama, Y. The pathogenic role of Bacteroides vulgatus in patients with ulcerative colitis. J Gastroenterol. 30(Suppl 8), 45–47 (1995).
    PubMed  Google Scholar 

    47.
    Ulsemer, P. et al. Specific humoral immune response to the Thomsen-Friedenreich tumor antigen (CD176) in mice after vaccination with the commensal bacterium Bacteroides ovatus D-6. Cancer Immunol. Immunother. 62, 875–887 (2013).
    CAS  PubMed  Google Scholar 

    48.
    Tan, H., Zhao, J., Zhang, H., Zhai, Q. & Chen, W. Novel strains of Bacteroides fragilis and Bacteroides ovatus alleviate the LPS-induced inflammation in mice. Appl. Microbiol. Biotechnol. 103, 2353–2365 (2019).
    CAS  PubMed  Google Scholar 

    49.
    Luis, A. S. et al. Dietary pectic glycans are degraded by coordinated enzyme pathways in human colonic Bacteroides. Nat. Microbiol. 3, 210–219 (2018).
    CAS  PubMed  Google Scholar 

    50.
    Rakoff-Nahoum, S., Coyne, M. J. & Comstock, L. E. An ecological network of polysaccharide utilization among human intestinal symbionts. Curr. Biol. 24, 40–49 (2014).
    CAS  PubMed  Google Scholar 

    51.
    Rogowski, A. et al. Glycan complexity dictates microbial resource allocation in the large intestine. Nat. Commun. 6, 7481 (2015).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    52.
    Le Poul, E. et al. Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation. J. Biol. Chem. 278, 25481–25489 (2003).
    PubMed  Google Scholar 

    53.
    Okubo, T. et al. Effects of partially hydrolyzed guar gum intake on human intestinal microflora and its metabolism. Biosci. Biotechnol. Biochem. 58, 1364–1369 (1994).
    CAS  Google Scholar 

    54.
    Klindworth, A. et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 41, e1 (2013).
    CAS  PubMed  Google Scholar 

    55.
    Magoč, T. & Salzberg, S. L. FLASH: Fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957–2963 (2011).
    PubMed  PubMed Central  Google Scholar 

    56.
    Li, W., Fu, L., Niu, B., Wu, S. & Wooley, J. Ultrafast clustering algorithms for metagenomic sequence analysis. Brief. Bioinform. 13, 656–668 (2012).
    PubMed  PubMed Central  Google Scholar 

    57.
    Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010).
    CAS  Google Scholar 

    58.
    Maidak, B. L. et al. The RDP-II (ribosomal database project). Nucleic Acids Res. 29, 173–174 (2001).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    59.
    Lozupone, C. & Knight, R. UniFrac: A new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71, 8228–8235 (2005).
    CAS  PubMed  PubMed Central  Google Scholar 

    60.
    Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336 (2010).
    CAS  PubMed  PubMed Central  Google Scholar 

    61.
    Furet, J. P. et al. Comparative assessment of human and farm animal faecal microbiota using real-time quantitative PCR. FEMS Microbiol. Ecol. 68, 351–362 (2009).
    CAS  PubMed  Google Scholar 

    62.
    Goubet, F., Jackson, P., Deery, M. J. & Dupree, P. Polysaccharide analysis using carbohydrate gel electrophoresis: A method to study plant cell wall polysaccharides and polysaccharide hydrolases. Anal. Biochem. 300, 53–68 (2002).
    CAS  PubMed  Google Scholar 

    63.
    Terrapon, N. et al. PULDB: The expanded database of polysaccharide utilization loci. Nucleic Acids Res. 46, D677–D683 (2018).
    CAS  PubMed  Google Scholar  More

  • in

    Experimentally-validated correlation analysis reveals new anaerobic methane oxidation partnerships with consortium-level heterogeneity in diazotrophy

    1.
    Knittel K, Boetius A. Anaerobic oxidation of methane: progress with an unknown process. Annu Rev Microbiol. 2009;63:311–34.
    CAS  PubMed  Article  Google Scholar 
    2.
    Reeburgh WS. Oceanic Methane Biogeochemistry. Chem Rev. 2007;107:486–513.
    CAS  PubMed  Article  Google Scholar 

    3.
    Orphan VJ, House CH, Hinrichs K-U, McKeegan KD, DeLong EF. Methane-consuming archaea revealed by directly coupled isotopic and phylogenetic analysis. Science. 2001;293:484–7.
    CAS  PubMed  Article  Google Scholar 

    4.
    Boetius A, Ravenschlag K, Schubert CJ, Rickert D, Widdel F, Gieseke A, et al. A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature. 2000;407:623.
    CAS  PubMed  Article  Google Scholar 

    5.
    McGlynn SE, Chadwick GL, Kempes CP, Orphan VJ. Single cell activity reveals direct electron transfer in methanotrophic consortia. Nature. 2015;526:531–5.
    CAS  PubMed  Article  Google Scholar 

    6.
    Scheller S, Yu H, Chadwick GL, McGlynn SE, Orphan VJ. Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction. Science. 2016;351:703–7.
    CAS  PubMed  Article  Google Scholar 

    7.
    Wegener G, Krukenberg V, Riedel D, Tegetmeyer HE, Boetius A. Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria. Nature. 2015;526:587–90.
    CAS  PubMed  Article  Google Scholar 

    8.
    Dekas AE, Connon SA, Chadwick GL, Trembath-Reichert E, Orphan VJ. Activity and interactions of methane seep microorganisms assessed by parallel transcription and FISH-NanoSIMS analyses. ISME J. 2016;10:678–92.
    CAS  PubMed  Article  Google Scholar 

    9.
    Dekas AE, Poretsky RS, Orphan VJ. Deep-sea archaea fix and share nitrogen in methane-consuming microbial consortia. Science. 2009;326:422–6.
    CAS  PubMed  Article  Google Scholar 

    10.
    Dekas AE, Chadwick GL, Bowles MW, Joye SB, Orphan VJ. Spatial distribution of nitrogen fixation in methane seep sediment and the role of the ANME archaea. Environ Microbiol. 2014;16:3012–29.
    CAS  PubMed  Article  Google Scholar 

    11.
    Orphan VJ, Turk KA, Green AM, House CH. Patterns of 15N assimilation and growth of methanotrophic ANME-2 archaea and sulfate-reducing bacteria within structured syntrophic consortia revealed by FISH-SIMS. Environ Microbiol. 2009;11:1777–91.
    CAS  PubMed  Article  Google Scholar 

    12.
    Evans PN, Boyd JA, Leu AO, Woodcroft BJ, Parks DH, Hugenholtz P, et al. An evolving view of methane metabolism in the Archaea. Nat Rev Microbiol. 2019;17:219–32.
    CAS  PubMed  Article  Google Scholar 

    13.
    Krukenberg V, Riedel D, Gruber‐Vodicka HR, Buttigieg PL, Tegetmeyer HE, Boetius A, et al. Gene expression and ultrastructure of meso- and thermophilic methanotrophic consortia. Environ Microbiol. 2018;20:1651–66.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    14.
    Skennerton CT, Chourey K, Iyer R, Hettich RL, Tyson GW, Orphan VJ. Methane-fueled syntrophy through extracellular electron transfer: uncovering the genomic traits conserved within diverse bacterial partners of anaerobic methanotrophic archaea. mBio. 2017;8:e00530–17.
    PubMed  PubMed Central  Google Scholar 

    15.
    Schreiber L, Holler T, Knittel K, Meyerdierks A, Amann R. Identification of the dominant sulfate-reducing bacterial partner of anaerobic methanotrophs of the ANME-2 clade. Environ Microbiol. 2010;12:2327–40.
    CAS  PubMed  Google Scholar 

    16.
    Green-Saxena A, Dekas AE, Dalleska NF, Orphan VJ. Nitrate-based niche differentiation by distinct sulfate-reducing bacteria involved in the anaerobic oxidation of methane. ISME J. 2014;8:150–63.
    CAS  PubMed  Article  Google Scholar 

    17.
    Hinrichs K-U, Hayes JM, Sylva SP, Brewer PG, DeLong EF. Methane-consuming archaebacteria in marine sediments. Nature. 1999;398:802.
    CAS  PubMed  Article  Google Scholar 

    18.
    Hallam SJ, Girguis PR, Preston CM, Richardson PM, DeLong EF. Identification of methyl coenzyme M Reductase A (mcrA) genes associated with methane-oxidizing archaea. Appl Environ Microbiol. 2003;69:5483–91.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    19.
    Michaelis W, Seifert R, Nauhaus K, Treude T, Thiel V, Blumenberg M, et al. Microbial reefs in the black sea fueled by anaerobic oxidation of methane. Science. 2002;297:1013–5.
    CAS  PubMed  Article  Google Scholar 

    20.
    Knittel K, Lösekann T, Boetius A, Kort R, Amann R. Diversity and distribution of methanotrophic archaea at cold seeps. Appl Environ Microbiol. 2005;71:467–79.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    21.
    Orphan VJ, Hinrichs K-U, Ussler W, Paull CK, Taylor LT, Sylva SP, et al. Comparative analysis of methane-oxidizing archaea and sulfate-reducing bacteria in anoxic marine sediments. Appl Environ Microbiol. 2001;67:1922–34.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    22.
    Orphan VJ, House CH, Hinrichs K-U, McKeegan KD, DeLong EF. Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments. Proc Natl Acad Sci. 2002;99:7663–8.
    CAS  PubMed  Article  Google Scholar 

    23.
    Raghoebarsing AA, Pol A, Pas-Schoonen KT, van de, Smolders AJP, Ettwig KF, Rijpstra WIC, et al. A microbial consortium couples anaerobic methane oxidation to denitrification. Nature. 2006;440:918.
    CAS  PubMed  Article  Google Scholar 

    24.
    Haroon MF, Hu S, Shi Y, Imelfort M, Keller J, Hugenholtz P, et al. Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature. 2013;500:567–70.
    CAS  PubMed  Article  Google Scholar 

    25.
    Niemann H, Lösekann T, Beer D, de, Elvert M, Nadalig T, Knittel K, et al. Novel microbial communities of the Haakon Mosby mud volcano and their role as a methane sink. Nature. 2006;443:854.
    CAS  PubMed  Article  Google Scholar 

    26.
    Lösekann T, Knittel K, Nadalig T, Fuchs B, Niemann H, Boetius A, et al. Diversity and abundance of aerobic and anaerobic methane oxidizers at the Haakon Mosby Mud Volcano, Barents Sea. Appl Environ Microbiol. 2007;73:3348–62.
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    27.
    Manz W, Eisenbrecher M, Neu TR, Szewzyk U. Abundance and spatial organization of gram-negative sulfate-reducing bacteria in activated sludge investigated by in situ probing with specific 16S rRNA targeted oligonucleotides. FEMS Microbiol Ecol. 1998;25:43–61.
    CAS  Article  Google Scholar 

    28.
    Nauhaus K, Albrecht M, Elvert M, Boetius A, Widdel F. In vitro cell growth of marine archaeal-bacterial consortia during anaerobic oxidation of methane with sulfate. Environ Microbiol. 2007;9:187–96.
    CAS  PubMed  Article  Google Scholar 

    29.
    Pernthaler A, Dekas AE, Brown CT, Goffredi SK, Embaye T, Orphan VJ. Diverse syntrophic partnerships from deep-sea methane vents revealed by direct cell capture and metagenomics. Proc Natl Acad Sci USA. 2008;105:7052–7.
    CAS  PubMed  Article  Google Scholar 

    30.
    Vigneron A, Cruaud P, Pignet P, Caprais J-C, Cambon-Bonavita M-A, Godfroy A, et al. Archaeal and anaerobic methane oxidizer communities in the Sonora Margin cold seeps, Guaymas Basin (Gulf of California). ISME J. 2013;7:1595–608.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    31.
    McGlynn SE, Chadwick GL, O’Neill A, Mackey M, Thor A, Deerinck TJ, et al. Subgroup characteristics of marine methane-oxidizing ANME-2 archaea and their syntrophic partners as revealed by integrated multimodal analytical microscopy. Appl Environ Microbiol. 2018;84:e00399–18.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    32.
    Treude T, Krüger M, Boetius A, Jørgensen BB. Environmental control on anaerobic oxidation of methane in the gassy sediments of Eckernförde Bay (German Baltic). Limnol Oceanogr. 2005;50:1771–86.
    CAS  Article  Google Scholar 

    33.
    Girguis PR, Orphan VJ, Hallam SJ, DeLong EF. Growth and methane oxidation rates of anaerobic methanotrophic archaea in a continuous-flow bioreactor. Appl Environ Microbiol. 2003;69:5472–82.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    34.
    Kleindienst S, Ramette A, Amann R, Knittel K. Distribution and in situ abundance of sulfate-reducing bacteria in diverse marine hydrocarbon seep sediments. Environ Microbiol. 2012;14:2689–710.
    CAS  PubMed  Article  Google Scholar 

    35.
    Holler T, Widdel F, Knittel K, Amann R, Kellermann MY, Hinrichs K-U, et al. Thermophilic anaerobic oxidation of methane by marine microbial consortia. ISME J. 2011;5:1946–56.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    36.
    Loy A, Lehner A, Lee N, Adamczyk J, Meier H, Ernst J, et al. Oligonucleotide Microarray for 16S rRNA Gene-Based Detection of All Recognized Lineages of Sulfate-Reducing Prokaryotes in the Environment. Appl Environ Microbiol. 2002;68:5064–81.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    37.
    Trembath-Reichert E, Case DH, Orphan VJ. Characterization of microbial associations with methanotrophic archaea and sulfate-reducing bacteria through statistical comparison of nested Magneto-FISH enrichments. PeerJ. 2016;4:e1913.
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    38.
    Trembath-Reichert E, Green-Saxena A, Orphan VJ. Chapter Two—whole cell immunomagnetic enrichment of environmental microbial consortia using rRNA-targeted magneto-FISH. In: DeLong EF (eds). Methods in Enzymology. (Academic Press, San Diego, 2013) pp 21–44.

    39.
    Hatzenpichler R, Connon SA, Goudeau D, Malmstrom RR, Woyke T, Orphan VJ. Visualizing in situ translational activity for identifying and sorting slow-growing archaeal−bacterial consortia. Proc Natl Acad Sci. 2016;113:E4069–78.
    CAS  PubMed  Article  Google Scholar 

    40.
    Degnan PH, Ochman H. Illumina-based analysis of microbial community diversity. ISME J. 2012;6:183–94.
    CAS  PubMed  Article  Google Scholar 

    41.
    Friedman J, Alm EJ. Inferring correlation networks from genomic survey data. PLOS Comput Biol. 2012;8:e1002687.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    42.
    Kurtz ZD, Müller CL, Miraldi ER, Littman DR, Blaser MJ, Bonneau RA. Sparse and compositionally robust inference of microbial ecological networks. PLOS Comput Biol. 2015;11:e1004226.
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    43.
    Schwager E, Mallick H, Ventz S, Huttenhower C. A Bayesian method for detecting pairwise associations in compositional data. PLOS Comput Biol. 2017;13:e1005852.
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    44.
    Lima-Mendez G, Faust K, Henry N, Decelle J, Colin S, Carcillo F, et al. Determinants of community structure in the global plankton interactome. Science. 2015;348:1–9.
    Article  CAS  Google Scholar 

    45.
    Bohrmann G, Heeschen K, Jung C, Weinrebe W, Baranov B, Cailleau B, et al. Widespread fluid expulsion along the seafloor of the Costa Rica convergent margin. Terra Nova. 2002;14:69–79.
    Article  Google Scholar 

    46.
    Mau S, Sahling H, Rehder G, Suess E, Linke P, Soeding E. Estimates of methane output from mud extrusions at the erosive convergent margin off Costa Rica. Mar Geol. 2006;225:129–44.
    CAS  Article  Google Scholar 

    47.
    Sahling H, Masson DG, Ranero CR, Hühnerbach V, Weinrebe W, Klaucke I, et al. Fluid seepage at the continental margin offshore Costa Rica and southern Nicaragua. Geochem Geophys Geosyst. 2008;9:1–22.
    Article  Google Scholar 

    48.
    Glass JB, Yu H, Steele JA, Dawson KS, Sun S, Chourey K, et al. Geochemical, metagenomic and metaproteomic insights into trace metal utilization by methane-oxidizing microbial consortia in sulphidic marine sediments. Environ Microbiol. 2014;16:1592–611.
    CAS  PubMed  Article  Google Scholar 

    49.
    Case DH, Pasulka AL, Marlow JJ, Grupe BM, Levin LA, Orphan VJ. Methane seep carbonates host distinct, diverse, and dynamic microbial assemblages. mBio. 2015;6:1–12.
    CAS  Article  Google Scholar 

    50.
    Parada AE, Needham DM, Fuhrman JA. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol. 2016;18:1403–14.
    CAS  PubMed  Article  Google Scholar 

    51.
    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    52.
    Mason OU, Case DH, Naehr TH, Lee RW, Thomas RB, Bailey JV, et al. Comparison of archaeal and bacterial diversity in methane seep carbonate nodules and host sediments, Eel River Basin and Hydrate Ridge, USA. Micro Ecol. 2015;70:766–84.
    CAS  Article  Google Scholar 

    53.
    Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460–1.
    CAS  Article  Google Scholar 

    54.
    Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–6.
    CAS  PubMed  Article  Google Scholar 

    55.
    Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–3.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    56.
    Towns J, Cockerill T, Dahan M, Foster I, Gaither K, Grimshaw A, et al. XSEDE: accelerating scientific discovery. Comput Sci Eng. 2014;16:62–74.
    Article  CAS  Google Scholar 

    57.
    Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the 2010 Gateway Computing Environments Workshop (GCE). (San Diego Supercomputing Center, San Diego, 2010) pp 1–8.

    58.
    Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–7.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    59.
    Eren AM, Esen ÖC, Quince C, Vineis JH, Morrison HG, Sogin ML, et al. Anvi’o: an advanced analysis and visualization platform for ‘omics data. PeerJ. 2015;3:e1319.
    PubMed  PubMed Central  Article  Google Scholar 

    60.
    Campbell BJ, Yu L, Heidelberg JF, Kirchman DL. Activity of abundant and rare bacteria in a coastal ocean. Proc Natl Acad Sci. 2011;108:12776–81.
    CAS  PubMed  Article  Google Scholar 

    61.
    Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 2019;47:W256–9.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    62.
    Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar, et al. ARB: a software environment for sequence data. Nucleic Acids Res. 2004;32:1363–71.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    63.
    Daims H, Stoecker K, Wagner M, Stoecker K, Wagner M. Fluorescence in situ hybridization for the detection of prokaryotes. Mol Microbial Ecol. https://www.taylorfrancis.com/. Accessed 15 Jul 2019.

    64.
    Glöckner FO, Fuchs BM, Amann R. Bacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Appl Environ Microbiol. 1999;65:3721–6.
    PubMed  PubMed Central  Article  Google Scholar 

    65.
    Dirks RM, Pierce NA. Triggered amplification by hybridization chain reaction. Proc Natl Acad Sci. 2004;101:15275–8.
    CAS  PubMed  Article  Google Scholar 

    66.
    Choi HMT, Beck VA, Pierce NA. Next-generation in situ hybridization chain reaction: higher gain, lower cost, greater durability. ACS Nano. 2014;8:4284–94.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    67.
    Yamaguchi T, Kawakami S, Hatamoto M, Imachi H, Takahashi M, Araki N, et al. In situ DNA-hybridization chain reaction (HCR): a facilitated in situ HCR system for the detection of environmental microorganisms. Environ Microbiol. 2015;17:2532–41.
    CAS  PubMed  Article  Google Scholar 

    68.
    Choi HMT, Schwarzkopf M, Fornace ME, Acharya A, Artavanis G, Stegmaier J, et al. Third-generation in situ hybridization chain reaction: multiplexed, quantitative, sensitive, versatile, robust. Development. 2018;145:1–10.
    Article  CAS  Google Scholar 

    69.
    Bolte S, Cordelières FP. A guided tour into subcellular colocalization analysis in light microscopy. J Microsc. 2006;224:213–32.
    CAS  PubMed  Article  Google Scholar 

    70.
    Dabundo R, Lehmann MF, Treibergs L, Tobias CR, Altabet MA, Moisander PA, Granger J. The contamination of commercial 15N2 gas stocks with 15N-labeled nitrate and ammonium and consequences for nitrogen fixation measurements. PLoS ONE. 2014;9:e110335.
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    71.
    Cline JD. Spectrophotometric determination of hydrogen sulfide in natural waters1. Limnol Oceanogr. 1969;14:454–8.
    CAS  Article  Google Scholar 

    72.
    Dekas AE, Orphan VJ. Chapter Twelve—identification of diazotrophic microorganisms in marine sediment via fluorescence in situ hybridization coupled to nanoscale secondary ion mass spectrometry (FISH-NanoSIMS). In: Klotz MG, editor. Methods in enzymology. Academic Press; 2011. p 281–305.

    73.
    Polerecky L, Adam B, Milucka J, Musat N, Vagner T, Kuypers MMM. Look@NanoSIMS-a tool for the analysis of nanoSIMS data in environmental microbiology. Environ Microbiol. 2012;14:1009–23.
    CAS  PubMed  Article  Google Scholar 

    74.
    Berry D, Widder S. Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Front Microbiol. 2014;5:1–14.
    Article  Google Scholar 

    75.
    David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505:559–63.
    CAS  Article  Google Scholar 

    76.
    Leone V, Gibbons SM, Martinez K, Hutchison AL, Huang EY, Cham CM, et al. Effects of diurnal variation of gut microbes and high-fat feeding on host circadian clock function and metabolism. Cell Host Microbe. 2015;17:681–9.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    77.
    Ruff SE, Biddle JF, Teske AP, Knittel K, Boetius A, Ramette A. Global dispersion and local diversification of the methane seep microbiome. Proc Natl Acad Sci. 2015;112:4015–20.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    78.
    Fruchterman TMJ, Reingold EM. Graph drawing by force-directed placement. Softw Pr Exp. 1991;21:1129–64.
    Article  Google Scholar 

    79.
    Moody J, White DR. Structural cohesion and embeddedness: a hierarchical concept of social groups. Am Socio Rev. 2003;68:103–27.
    Article  Google Scholar 

    80.
    Gu Z, Gu L, Eils R, Schlesner M, Brors B. Circlize implements and enhances circular visualization in R. Bioinformatics. 2014;30:2811–2.
    CAS  PubMed  Article  Google Scholar 

    81.
    Nikolakakis K, Lehnert E, McFall-Ngai MJ, Ruby EG. Use of hybridization chain reaction-fluorescent in situ hybridization to track gene expression by both partners during initiation of symbiosis. Appl Environ Microbiol. 2015;81:4728–35.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    82.
    DePas WH, Starwalt-Lee R, Sambeek LV, Kumar SR, Gradinaru V, Newman DK. Exposing the three-dimensional biogeography and metabolic states of pathogens in cystic fibrosis sputum via hydrogel embedding, clearing, and rRNA Labeling. mBio. 2016;7:1–11.
    Article  Google Scholar 

    83.
    Imachi H, Nobu MK, Nakahara N, Morono Y, Ogawara M, Takaki Y, et al. Isolation of an archaeon at the prokaryote–eukaryote interface. Nature. 2020;577:519–25.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    84.
    Gloor GB, Macklaim JM, Pawlowsky-Glahn V, Egozcue JJ. Microbiome datasets are compositional: and this is not optional. Front Microbiol. 2017;8:1–6.
    Article  Google Scholar 

    85.
    Sampayo EM, Ridgway T, Bongaerts P, Hoegh-Guldberg O. Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proc Natl Acad Sci. 2008;105:10444–9.
    CAS  PubMed  Article  Google Scholar 

    86.
    Parkinson JE, Baumgarten S, Michell CT, Baums IB, LaJeunesse TC, Voolstra CR. Gene expression variation resolves species and individual strains among coral-associated dinoflagellates within the genus symbiodinium. Genome Biol Evol. 2016;8:665–80.
    PubMed  PubMed Central  Article  Google Scholar 

    87.
    Barshis DJ, Ladner JT, Oliver TA, Palumbi SR. Lineage-specific transcriptional profiles of Symbiodinium spp. unaltered by heat stress in a coral host. Mol Biol Evol. 2014;31:1343–52.
    CAS  PubMed  Article  Google Scholar 

    88.
    Kapili BJ, Barnett SE, Buckley DH, Dekas AE. Evidence for phylogenetically and catabolically diverse active diazotrophs in deep-sea sediment. ISME J. 2020;14:971–83.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    89.
    Klawonn I, Eichner MJ, Wilson ST, Moradi N, Thamdrup B, Kümmel S, et al. Distinct nitrogen cycling and steep chemical gradients in Trichodesmium colonies. ISME J. 2020;14:399–412.
    CAS  PubMed  Article  Google Scholar 

    90.
    Petroff AP, Wu T-D, Liang B, Mui J, Guerquin-Kern J-L, Vali H, et al. Reaction–diffusion model of nutrient uptake in a biofilm: Theory and experiment. J Theor Biol. 2011;289:90–5.
    CAS  PubMed  Article  Google Scholar 

    91.
    Dekas AE, Fike DA, Chadwick GL, Green‐Saxena A, Fortney J, Connon SA, et al. Widespread nitrogen fixation in sediments from diverse deep-sea sites of elevated carbon loading. Environ Microbiol. 2018;20:4281–96.
    CAS  PubMed  Article  Google Scholar 

    92.
    Knapp AN. The sensitivity of marine N2 fixation to dissolved inorganic nitrogen. Front Microbiol. 2012;3:1–14.
    Google Scholar 

    93.
    Bertics VJ, Löscher CR, Salonen I, Dale AW, Gier J, Schmitz RA, et al. Occurrence of benthic microbial nitrogen fixation coupled to sulfate reduction in the seasonally hypoxic Eckernförde Bay, Baltic Sea. Biogeosciences. 2013;10:1243–58.
    CAS  Article  Google Scholar 

    94.
    Gier J, Sommer S, Löscher CR, Dale AW, Schmitz RA, Treude T. Nitrogen fixation in sediments along a depth transect through the Peruvian oxygen minimum zone. Biogeosciences. 2016;13:4065–80.
    CAS  Article  Google Scholar 

    95.
    Ackermann M. A functional perspective on phenotypic heterogeneity in microorganisms. Nat Rev Microbiol. 2015;13:497–508.
    CAS  PubMed  Article  Google Scholar 

    96.
    Schreiber F, Littmann S, Lavik G, Escrig S, Meibom A, Kuypers MMM, et al. Phenotypic heterogeneity driven by nutrient limitation promotes growth in fluctuating environments. Nat Microbiol. 2016;1:1–7.
    Article  CAS  Google Scholar 

    97.
    Masuda T, Inomura K, Takahata N, Shiozaki T, Yuji S. Heterogeneous nitrogen fixation rates confer energetic advantage and expanded ecological niche of unicellular diazotroph populations. Commun Biol. 2020;3:1–12.
    Article  CAS  Google Scholar 

    98.
    Raymond J, Siefert JL, Staples CR, Blankenship RE. The natural history of nitrogen fixation. Mol Biol Evol. 2004;21:541–54.
    CAS  PubMed  Article  Google Scholar  More

  • in

    Georgina Mace (1953–2020)

    OBITUARY
    15 October 2020

    Pioneer of biodiversity accounting who overhauled the Red List of threatened species.

    Nathalie Pettorelli

    Nathalie Pettorelli, a senior research fellow, started at the Institute of Zoology, London under Georgina’s directorship; they co-supervised a PhD student at Imperial College London.
    Contact

    Search for this author in:

    Credit: Jussi Puikkonen/KNAW

    Georgina Mace shaped two cornerstones of modern ecology and conservation. One was the global inventory of species threatened with extinction, the International Union for Conservation of Nature (IUCN) Red List. The second was the United Nations Millennium Ecosystem Assessment. One of the sharpest minds of her generation, she strove to document and stem biodiversity loss with analytical rigour and multidisciplinary approaches. She died on 19 September, aged 67.
    Throughout her career, Mace developed tools for evidence-based policymaking. Before her, the Red List was based on nominations from experts rather than data, undermining confidence in its accuracy. She devised criteria to standardize assessments. The Red List is now the most used and trusted source for assessing trends in global biodiversity.
    Mace was born in London in 1953. She studied zoology at the University of Liverpool, UK, before doing a PhD in the 1970s at the University of Sussex in Brighton, UK, where John Maynard Smith was pioneering mathematical approaches to evolutionary ecology. As a postdoc at the Smithsonian Institution in Washington DC, she studied the impacts of inbreeding on captive animals.
    In 1983, she joined the Institute of Zoology, the research arm of the Zoological Society of London, where she remained for 23 years, latterly as director from 2000 to 2006. There, Mace continued to work on the genetic management of zoological collections and small populations. Her findings informed the conservation status of several species, including the western lowland gorilla (Gorilla gorilla gorilla), and highlighted the value of reproductive technology in managing captive populations of endangered species, such as the Arabian oryx (Oryx leucoryx) and Przewalski’s horse (Equus przewalskii). She became increasingly interested in population viability, extinction risk and setting conservation priorities.
    In 1991, this led her, together with US population biologist Russell Lande, to question the IUCN categories of threats and the associated nomination process as being largely subjective. They suggested three categories: critical, endangered and vulnerable. These they defined in terms of the probability of a species becoming extinct within a specific period, such as five years or two generations. They drew up standardized criteria based on population-biology theory. These included, for example, total effective population size, the population trend over the past five years and observed or projected habitat loss. Mace later introduced, among other things, categories for species that are not currently under threat. This work ultimately defined the categories that the IUCN uses now.
    In 2006, Mace became director of the NERC Centre for Population Biology at Imperial College London. There, she worked on the definition of biodiversity targets and assessing species’ vulnerability to climate change. She also studied the link between biodiversity and ecosystem services — the benefits that humans draw from nature, such as carbon sequestration, medicines or waste decomposition.
    From 2012, as founding director of the Centre for Biodiversity and Environment Research at University College London, she developed an interest in natural-capital accounting, the process of calculating the total stocks and flows of natural resources and services in an ecosystem or region. Her blending of economics and ecological theory to define a risk register for natural capital helped to provide an effective focus for monitoring and data gathering. It also contributed to a common understanding of priorities across fields.
    Mace bridged the gaps between genetics, population ecology and macroecology, sub-disciplines in which she regularly supervised students, networked and published. She also demonstrated the importance of conservationists engaging with researchers in other disciplines, such as climate science, economics and social science. She excelled in building consensus, a key step towards evidence-based policy.
    Mace was coordinating lead author for biodiversity on the Millennium Ecosystem Assessment, launched in 2001, which demonstrated that rapidly growing demand for food, fresh water, timber, fibre and fuel resulted in a large and largely irreversible loss in biodiversity. She supported the development of assessments for the biodiversity target of the UN Convention on Biological Diversity in 2010 and, most recently, acted as review editor for the Global Assessment of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services. She held similarly pivotal roles at the national level, on UK climate and environmental assessments.
    She broke several glass ceilings. Mace was the first president of the international Society for Conservation Biology from outside North America, and the first female president of the British Ecological Society. Her many awards and honours included a fellowship of the Royal Society and, in 2016, she was made a dame.
    Georgina was a role model: firm but fair, collaborative, reliable, unassuming, approachable — the kind of critical friend we all need. She supported the career progression of numerous ecologists and influenced many more. She’d nominate you for a post even when you didn’t think she had noticed your work; she’d make a witty remark in the middle of a heated discussion. Few knew that she had cancer. Never one to make a fuss about herself, nine days before she died, she published a paper on habitat conversion and biodiversity loss (D. Leclère et al. Nature 585, 551–556; 2020). Her death leaves a void: she will be sorely missed.

    Nature 586, 495 (2020)

    Latest on:

    Biodiversity

    An essential round-up of science news, opinion and analysis, delivered to your inbox every weekday.

    Related Articles More

  • in

    Species composition and invasion risks of alien ornamental freshwater fishes from pet stores in Klang Valley, Malaysia

    1.
    Strecker, A. L., Campbell, P. M. & Olden, J. D. The aquarium trade as an invasion pathway in the Pacific Northwest. Fisheries 36, 74–85 (2011).
    Article  Google Scholar 
    2.
    Magalhães, A. L. et al. Small size today, aquarium dumping tomorrow: sales of juvenile non-native large fish as an important threat in Brazil. Neotrop. Ichthyol. 15, 1–10 (2017).
    Google Scholar 

    3.
    Maceda-Veiga, A., Escribano-Alacid, J., de Sostoa, A. & García-Berthou, E. The aquarium trade as a potential source of fish introductions in Southwestern Europe. Biol. Invasions 15, 2707–2716 (2014).
    Article  Google Scholar 

    4.
    Gertzen, E., Familiar, O. & Leung, B. Quantifying invasion pathways: fish introductions from the aquarium trade. Can. J. Fish. Aquat. Sci. 65, 1265–1273 (2008).
    Article  Google Scholar 

    5.
    Ishikawa, T. & Tachihara, K. Introduction history of non-native freshwater fish in Okinawa-Jima Island: ornamental aquarium fish pose the greatest risk for future invasions. Ichthyol. Res. 61, 17–26 (2014).
    Article  Google Scholar 

    6.
    Khairul-Adha, R., Yuzine, E. & Aziz, A. The influence of alien fish species on native fish community structure in Malaysian waters. Kuroshio Sci. 7, 81–93 (2013).
    Google Scholar 

    7.
    Department of Fisheries (DOF). Annual Fisheries Statistics, Department of Fisheries, Ministry of Agriculture and Agro-Based Industry, Putrajaya, Malaysia. https://www.dof.gov.my/index.php/pages/view (2007).

    8.
    Department of Fisheries (DOF). Annual Fisheries Statistics, Department of Fisheries, Ministry of Agriculture and Agro-Based Industry, Putrajaya, Malaysia. https://www.dof.gov.my/index.php/pages/view (2014).

    9.
    Duggan, I. C., Rixon, C. A. & MacIsaac, H. J. Popularity and propagule pressure: determinants of introduction and establishment of aquarium fish. Biol. Invasions 8, 377–382 (2006).
    Article  Google Scholar 

    10.
    Simonovic, P. et al. Risk assessment of non-native fishes in the Balkans Region using FISK, the invasiveness screening tool for non-native freshwater fishes. Mediterr. Mar. Sci. 14, 369–376 (2013).
    Article  Google Scholar 

    11.
    Singh, A. K. & Lakra, W. S. Risk and benefit assessment of alien fish species of the aquaculture and aquarium trade into India. Rev. Aquacult. 3, 3–18 (2011).
    Article  Google Scholar 

    12.
    Puntila, R., Vilizzi, L., Lehtiniemi, M. & Copp, G. H. First application of FISK, the Freshwater Fish Invasiveness Screening Kit, in Northern Europe: example of Southern Finland. Risk Anal. 33, 1397–1403 (2013).
    PubMed  Article  Google Scholar 

    13.
    Tarkan, A. S., Ekmekçi, F. G., Vilizzi, L. & Copp, G. H. Risk screening of non-native freshwater fishes at the frontier between Asia and Europe: first application in Turkey of the Fish Invasiveness Screening Kit. J. Appl. Ichthyol. 30, 392–398 (2014).
    Article  Google Scholar 

    14.
    Mendoza, R., Luna, S. & Aguilera, C. Risk assessment of the ornamental fish trade in Mexico: analysis of freshwater species and effectiveness of the FISK (Fish Invasiveness Screening Kit). Biol. Invasions 17, 3491–3502 (2015).
    Article  Google Scholar 

    15.
    Perdikaris, C. et al. Risk screening of non-native, translocated and traded aquarium freshwater fishes in Greece using Fish Invasiveness Screening Kit. Fisheries Manag. Ecol. 23, 32–43 (2016).
    Article  Google Scholar 

    16.
    Tarkan, A. S. et al. Identification of potentially invasive freshwater fishes, including translocated species, in Turkey using the Aquatic Species Invasiveness Screening Kit (AS-ISK). Int. Rev. Hydrobiol. 102, 47–56 (2017).
    Article  Google Scholar 

    17.
    Bilge, G., Filiz, H., Yapici, S., Tarkan, A. S. & Vilizzi, L. A risk screening study on the potential invasiveness of Lessepsian fishes in the South-Western coasts of Anatolia. Acta. Ichthyol. Piscat. 49, 23–31 (2019).
    Article  Google Scholar 

    18.
    Kiruba-Sakar, R. et al. Invasive species in freshwater ecosystems – threats to ecosystem services. In Biodiversity and Climate Change Adaptation in Tropical Islands(eds. Chandrakasan, S., Velmurugan, A., Singh, A. & Jaisankar, I.) 257–289 (Elsevier Inc. USA, 2018).

    19.
    Gaygusuz, Ö et al. Stocking of common carp (Cyprinus carpio) into some newly-established reservoirs of North-West Anatolia may enhance the spread of non-native fish. Turk. J. Fish. Aquat. S. 15, 833–840 (2015).
    Google Scholar 

    20.
    Rashid, M. F. A. & Ishak, A. G. The importance of internal migration: in the context of urban planning decision making. (International Conference on Built Environment in Developing Countries, Penang Malaysia, 2–3 December 2009. Penang, Malaysia, 2009).

    21.
    Naji, A., Ismail, A., Kamrani, E. & Sohrabi, T. Correlation of MT levels in livers and gills with heavy metals in wild tilapia (Oreochromis mossambicus) from the Klang River Malaysia. B. Environ. Contam. Tox. 92, 674–679 (2014).
    CAS  Article  Google Scholar 

    22.
    Rainboth, W. J. Fishes of the Cambodian Mekong. Mekong River Commission, Food and Agriculture Organization, Rome. https://library.enaca.org/inland/fishes-cambodian-mekong.pdf (1996).

    23.
    Mohsin, A. K. & Ambak, M. A. Ikan air tawar di Semenanjung Malaysia. (Freshwater fishes of Peninsular Malaysia). (Dewan Bahasa dan Pustaka, Kuala Lumpur, Malaysia, 1991).

    24.
    Berra, T. M. Freshwater fish distribution (The University of Chicago Press, Chicago, 2001).
    Google Scholar 

    25.
    Ng, H. H. & Tan, H. H. An annotated checklist of the non-native freshwater fish species in the reservoirs of Singapore. Cosmos. 6, 95–116 (2010).
    Article  Google Scholar 

    26.
    Tran, D. D. et al. Fishes of Mekong Delta (Can Tho University Publisher, Vietnam, 2010).
    Google Scholar 

    27.
    Ng, C. K. C., Lim, T. Y., Ahmad, A. B. & Khaironizam, M. Z. Provisional checklist of freshwater fish diversity and distribution in Perak, Malaysia, and some latest taxonomic concerns. Zootaxa 4567, 515–545 (2019).
    Article  Google Scholar 

    28.
    Zakaria-Ismail, M., Fatimah, A. & Khaironizam, M. Z. Fishes of the freshwater ecosystems of Peninsular Malaysia (Lambert Academic Publishing, Saarbrücken, 2019).
    Google Scholar 

    29.
    Froese, R. & Pauly, D. (eds.) FishBase. World Wide Web Electronic Publication. https://www.fishbase.org/search.php (2019).

    30.
    Fricke, R., Eschmeyer, W. N. & van der Laan, R. (eds.) Catalog of fishes: genera, species, references. California Academy of Sciences. https://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp (2020).

    31.
    Papavlasopoulou, I. et al. Ornamental fish in pet stores in Greece: a threat to biodiversity?. Mediterr. Mar. Sci. 15, 126–134 (2014).
    Article  Google Scholar 

    32.
    IUCN. The IUCN Red List of Threatened Species. Version 2020–1. https://www.iucnredlist.org. (2020).

    33.
    Lawson, L. L., Vilizzi, L, Hill, J. E., Hardin, S. & Copp, G. H. Revisions of the Fish Invasiveness Scoring Kit (FISK) for its application in warmer climatic zones, with particular reference to Peninsular Florida. Risk Anal. 33, 1414–1431 (2013).

    34.
    Garcia de León, F. J. G., González-García, L., Herrera-Castillo, J. M., Winemiller, K. O. & Banda-Valdés, A. Ecology of the alligator gar, Atractosteus spatula, in the Vicente Guerrero Reservoir, Tamaulipas, Mexico. Southwest Nat.46, 151–157 (2001).

    35.
    Carman, S. M. Special animal abstract for Lepisosteus oculatus (spotted gar). (Michigan Natural Features Inventory, Lansing, MI.) https://mnfi.anr.msu.edu/abstracts/zoology/Lepisosteus_oculatus.pdf (2002).

    36.
    COSEWIC. Committee on the status of endangered wildlife in Canada (COSEWIC) assessment and update status report on the lake sturgeon Acipenser fulvescens in Canada, https://wildlife-species.canada.ca/species-risk-registry/virtual_sara/files/cosewic/sr_Lake%20Sturgeon_2017_e.pdf (2006).

    37.
    Roberts, D. “Atractosteus spatula”, Animal Diversity Web. https://animaldiversity.org/accounts/Atractosteus_spatula/ (2006).

    38.
    Herder, F. et al. Alien invasion in Wallace’s Dreamponds: records of the hybridogenic “flowerhorn” cichlid in Lake Matano, with an annotated checklist of fish species introduced to the Malili Lakes system in Sulawesi. Aquat. Invasions 7, 521–535 (2012).
    Article  Google Scholar 

    39.
    Speigel, J. “Potamotrygon motoro”, Animal Diversity Web., https://animaldiversity.org/accounts/Potamotrygon_motoro/ (2013).

    40.
    Franklin, P. A. Dissolved oxygen criteria for freshwater fish in New Zealand: a revised approach. New Zeal. J. Mar. Fresh. 48, 112–126 (2014).
    CAS  Article  Google Scholar 

    41.
    Felterman, M. A. Population dynamics, reproductive biology, and diet of alligator gar Atractosteus spatula in Terrebonne Estuary and Rockefeller Wildlife Refuge. Master’s Thesis, Nicholls State University, Thibodaux, Louisiana, USA. (2015).

    42.
    Fuller, P. Atractosteus spatula (Lacepède, 1803): U.S. geological survey, non-indigenous aquatic species database, Gainesville, Florida, USA. https://nas.er.usgs.gov/queries/FactSheet.aspx?speciesID=755 (2019).

    43.
    Islam, M. A., Uddin, M. H., Uddin, M. J. & Shahjahan, M. Temperature changes influenced the growth performance and physiological functions of Thai Pangas Pangasianodon hypophthalmus. Aquacult. Rep. 13, 100179 (2019).
    Article  Google Scholar 

    44.
    Lawson, L. L., Hill, J. E., Hardin, S., Vilizzi, L. & Copp, G. H. Evaluation of the fish invasiveness screening kit (FISK v2) for peninsular Florida. Manag. of Biol. Invasions 6, 413–422 (2015).
    Article  Google Scholar 

    45.
    Copp, G. H. et al. Calibration of FISK, an invasiveness screening tool for non-native freshwater fishes. Risk Anal. 29, 457–467 (2009).
    PubMed  Article  Google Scholar 

    46.
    Almeida, D., Ribeiro, F., Leunda, P. M., Vilizzi, L. & Copp, G. H. Effectiveness of FISK, an invasiveness screening tool for non-native freshwater fishes, to perform risk identification assessments in the Iberian Peninsula. Risk Anal. 33, 1404–1413 (2013).
    PubMed  Article  Google Scholar 

    47.
    Youden, W. J. Index for rating diagnostic tests. Cancer 3, 32–35 (1950).
    CAS  PubMed  Article  Google Scholar 

    48.
    Bewick, V., Cheek, L. & Ball, J. Statistics review 13: receiver operating characteristic curves. Crit. Care 8, 508–512 (2004).
    PubMed  PubMed Central  Article  Google Scholar 

    49.
    Tricarico, E., Vilizzi, L., Gherardi, F. & Copp, G. H. Calibration of FI-ISK, an invasiveness screening tool for nonnative freshwater invertebrates. Risk Anal. 30, 285–292 (2010).
    PubMed  Article  Google Scholar 

    50.
    Chang, A. L. et al. Tackling aquatic invasions: risks and opportunities for the aquarium fish industry. Biol. Invasions 11, 773–785 (2009).
    Article  Google Scholar 

    51.
    Magalhães, A. L. & Jacobi, C. M. Invasion risks posed by ornamental freshwater fish trade to south eastern Brazilian rivers. Neotrop. Ichthyol. 11, 433–441 (2013).
    Article  Google Scholar 

    52.
    Reis, R. E. et al. Fish biodiversity and conservation in South America. J. Fish. Biol. 89, 12–47 (2016).
    CAS  PubMed  Article  Google Scholar 

    53.
    Rixon, C. A., Duggan, I. C., Bergeron, N. M., Ricciardi, A. & Macisaac, H. J. Invasion risks posed by the aquarium trade and live fish markets on the Laurentian Great Lakes. Biodivers. Conserv. 14, 1365–1381 (2005).
    Article  Google Scholar 

    54.
    Cucherousset, J. & Olden, J. D. Ecological impacts of non-native freshwater fishes. Fisheries 36, 215–230 (2011).
    Article  Google Scholar 

    55.
    Ng, C. K. C. et al. A working checklist of the freshwater fish diversity for habitat management and conservation work in Sabah, Malaysia North Borneo. Biodiversitas 18, 560–574 (2017).
    Article  Google Scholar 

    56.
    Zakaria, R. Alien fish devouring local species in Sg Pahang. New Strait Times. https://www.nst.com.my/news/nation/2019/02/462595/alien-fish-devouring-local-species-sg-pahang (2019).

    57.
    Sharifudin, M. & Sharip, Z. Fisheries practices and fish diversity in Muda and Beris Lakes: a preliminary survey study. Geografia 16, 1–12 (2020).
    Article  Google Scholar 

    58.
    Zakaria, R. Alien fish ‘killing’ local boat operators. New Strait Times. https://www.nst.com.my/news/nation/2017/04/231359/alien-fish-killing-local-boat-operators/ (2017).

    59.
    Chong, V. C., Lee, P. K. Y. & Lau, C. M. Diversity, extinction risk and conservation of Malaysian fishes. J. Fish Biol. 76, 2009–2066 (2010).
    CAS  PubMed  Article  Google Scholar 

    60.
    NWGIAS. National Working Group on Invasive Alien Species (NWGIAS). National action plan for prevention, eradication, containment and control of aquatic invasive alien species in Malaysia. Department of Agriculture, Putrajaya (2014).

    61.
    Samat, A. et al. Reproductive biology of the introduced sailfin catfish Pterygoplichthys pardalis (Pisces: Loricariidae) in Peninsular Malaysia. Indian. J. Fish. 63, 35–41 (2016).
    Google Scholar 

    62.
    Tan, B. Bottom-feeding fish sucking life out of Johor Rivers, nature society warns. Malay Mail, https://www.malaymail.com/news/malaysia/2019/01/14/bottom-feeding-fish-suckinglife-out-of-johor-rivers-nature-society-warns/1712205 (2019).

    63.
    Hussan, A., Choudhury, T. G., Das, A. & Gita, S. Suckermouth sailfin catfishes: A future threat to aquatic ecosystems of India. Aquaculture Times 2, 20–22 (2016).
    Google Scholar 

    64.
    Ng, C. The ornamental freshwater fish trade in Malaysia. UTAR Agric Sci. J. 2, 7–18 (2016).
    Google Scholar 

    65.
    Lokman, E. D. et al. Use of GIS and remote sensing on ornamental fish farm’s activities monitoring in Layang-Layang, Kluang Johor. Adv. Ecol. Envir. Res. 4, 211–230 (2019).
    Google Scholar 

    66.
    Evers, H. G., Pinnegar, J. K. & Taylor, M. I. Where are they all from?–sources and sustainability in the ornamental freshwater fish trade. J. Fish Biol. 94, 909–916 (2019).
    PubMed  PubMed Central  Google Scholar 

    67.
    Chan, F. T. et al. Leaving the fish bowl: the ornamental trade as a global vector for freshwater fish invasions. Aquat. Ecosyst. Health 22, 417–439 (2019).
    Article  Google Scholar 

    68.
    Banha, F., Diniz, A. & Anastácio, P. M. Patterns and drivers of aquarium pet discharge in the wild. Ecol. Indicat. 106, 105513 (2019).
    Article  Google Scholar 

    69.
    Zakaria, R. & Bahrin, H. B. Two more foreign predatory fishes threaten survival of native species. New Strait Times, https://www.nst.com.my/news/exclusive/2018/05/372369/two-more-foreign-predatory-fishes-threaten-survival-native-species (2018).

    70.
    Daehler, C. C., Denslow, J. S., Ansari, S. & Kuo, S. A risk assessment system for screening out invasive pest plants from Hawaii and other Pacific islands. Conserv. Biol. 18, 360–368 (2004).
    Article  Google Scholar 

    71.
    Marchetti, M. P., Moyle, P. B. & Levine, R. Invasive species profiling? Exploring the characteristics of non-native fishes across invasion stages in California. Freshwater Biol. 49, 646–661 (2004).
    Article  Google Scholar 

    72.
    Piria, M. et al. Risk screening of non-native freshwater fishes in Croatia and Slovenia using the Fish Invasiveness Screening Kit. Fisheries Manag. Ecol. 23, 21–31 (2016).
    Article  Google Scholar 

    73.
    Marr, S. M. et al. Evaluating invasion risk for freshwater fishes in South Africa. Bothalia 47, 1–10 (2017).
    Article  Google Scholar 

    74.
    Thompson, K. A., Hill, J. E. & Nico, L. G. Eastern mosquitofish resists invasion by nonindigenous poeciliids through agnostic behaviors. Biol. Invasions 14, 1515–1529 (2012).
    Article  Google Scholar 

    75.
    Onikura, N. et al. Evaluating the potential for invasion by alien freshwater fishes in northern Kyushu Island, Japan, using the Fish Invasiveness Scoring Kit. Ichthyol. Res. 58, 382–387 (2011).
    Article  Google Scholar 

    76.
    Troca, D. A. & Vieira, J. P. Potential invasive non-native fish farmed in the coastal region of Rio Grande Do Sul Brazil. Boletim do Instituto de Pesca 38, 109–120 (2012).
    Google Scholar 

    77.
    Vilizzi, L. V. & Copp, G. H. Application of FISK, an invasiveness screening tool for non-native freshwater fishes, in the Murray-Darling Basin (Southeastern Australia). Risk Anal. 33, 1432–1440 (2013).
    PubMed  Article  PubMed Central  Google Scholar  More

  • in

    Diel vertical migration into anoxic and high-pCO2 waters: acoustic and net-based krill observations in the Humboldt Current

    1.
    Pachauri, R. K. & Meyer, L. A. Intergovernmental panel on climate change (IPCC). In Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (2014).
    2.
    Feely, R. A., Sabine, C. L., Hernández-Ayon, J. M., Ianson, D. & Hales, B. Evidence for upwelling of corrosive “acidified” water onto the continental shelf. Science 320, 1490–1492 (2008).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    3.
    Escribano, R., Hidalgo, P. & Krautz, C. Zooplankton associated with the oxygen minimum zone system in the northern upwelling region of Chile during March 2000. Deep Sea Res. II 56, 1083–1094 (2009).
    Article  Google Scholar 

    4.
    Paulmier, A. & Ruiz-Pino, D. Oxygen minimum zones (OMZs) in the modern ocean. Prog. Oceanogr. 80, 113–128 (2009).
    ADS  Article  Google Scholar 

    5.
    Ulloa, O., Canfield, D. E., DeLong, E. F., Letelier, R. M. & Stewart, F. J. Microbial oceanography of anoxic oxygen minimum zones. Proc. Natl. Acad. Sci. 109, 15996–16003 (2012).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    6.
    Thamdrup, B., Dalsgaard, T. & Revsbech, N. P. Widespread functional anoxia in the oxygen minimum zone of the eastern South Pacific. Deep Sea Res. I 65, 36–45 (2012).
    CAS  Article  Google Scholar 

    7.
    Chan, F. et al. Emergence of anoxia in the California current large marine ecosystem. Science 319, 920–920 (2008).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    8.
    Diaz, R. J. & Rosenberg, R. Spreading dead zones and consequences for marine ecosystems. Science 321, 926–929 (2008).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    9.
    Friederich, G. E., Ledesma, J., Ulloa, O. & Chavez, F. P. Air–sea carbon dioxide fluxes in the coastal southeastern tropical Pacific. Prog. Oceanogr. 79, 156–166 (2008).
    ADS  Article  Google Scholar 

    10.
    Feely, R. A. et al. The combined effects of ocean acidification, mixing, and respiration on pH and carbonate saturation in an urbanized estuary. Estuar. Coast. Shelf Sci. 88, 442–449 (2010).
    ADS  CAS  Article  Google Scholar 

    11.
    Torres, R. et al. Air-sea CO2 fluxes along the coast of Chile: From CO2 outgassing in central northern upwelling waters to CO2 uptake in southern Patagonian fjords. J. Geophys. Res. 116, C09006. https://doi.org/10.1029/2010JC006344 (2011).
    ADS  CAS  Article  Google Scholar 

    12.
    Vargas, C. A. et al. Influences of riverine and upwelling waters on the coastal carbonate system off Central Chile and their ocean acidification implications. J. Geophys. Res. Biogeosci. 121, 15. https://doi.org/10.1002/2015JG003213 (2016).
    Article  Google Scholar 

    13.
    Vargas, C. A. et al. Species-specific responses to ocean acidification should account for local adaptation and adaptive plasticity. Nat. Ecol. Evol. 1, 0084. https://doi.org/10.1038/s41559-017-0084 (2017).
    Article  Google Scholar 

    14.
    Booth, J. A. et al. Natural intrusions of hypoxic, low pH water into nearshore marine environments on the California coast. Cont. Shelf Res. 45, 108–115 (2012).
    ADS  Article  Google Scholar 

    15.
    Forward, R. B. Diel vertical migration: zooplankton photobiology and behaviour. Oceanogr. Mar. Biol. Annu. Rev 26, 1–393 (1988).
    Google Scholar 

    16.
    Cohen, J. H. & Forward, R. B. Jr. Zooplankton diel vertical migration: A review of proximate control. Oceanogr. Mar. Biol. Ann. Rev 47, 77–110 (2009).
    Google Scholar 

    17.
    Brinton, E. Vertical migration and avoidance capability of euphausiids in the California current. Limnol. Oceanogr. 12, 451–483 (1967).
    ADS  PubMed  PubMed Central  Article  Google Scholar 

    18.
    McQuinn, I. H., Dion, M. & St. Pierre, J.-F. The acoustic multifrequency classification of two sympatric euphausiid species (Meganyctiphanes norvegica and Thysanoessa raschii), with empirical and SDWBA model validation. ICES J. Mar. Sci. 70, 636–649 (2013).
    Article  Google Scholar 

    19.
    Tremblay, N. & Abele, D. Response of three krill species to hypoxia and warming: An experimental approach to oxygen minimum zones expansion in coastal ecosystems. Mar. Ecol. 37, 179–199 (2016).
    ADS  CAS  Article  Google Scholar 

    20.
    Ambriz-Arreola, I. et al. Vertical pelagic habitat of euphausiid species assemblages in the Gulf of California. Deep Sea Res. I 123, 75–89 (2017).
    CAS  Article  Google Scholar 

    21.
    Cooper, H. L., Potts, D. & Paytan, A. Metabolic responses of the North Pacific krill, Euphausia pacifica, to short- and long-term pCO2 exposure. Mar. Biol. 163, 207 (2016).
    Article  CAS  Google Scholar 

    22.
    Seibel, B. A., Schneider, J. L., Kaartvedt, S., Wishner, K. F. & Daly, K. L. Hypoxia tolerance and metabolic suppression in Oxygen Minimum Zone euphausiids: Implications for ocean deoxygenation and biogeochemical cycles. Integr. Comp. Biol. 56, 510–523 (2016).
    CAS  PubMed  Article  Google Scholar 

    23.
    Barry, J. P., Hall-Spencer, J. M. & Tyrrell, T. In Guide to Best Practices for Ocean Acidification Research and Data Reporting (eds. Riebesell, U., Fabry, V. J., Hansson, L. & Gattuso, J. P.) 53–66 (Publications Office of the European Union, 2010).

    24.
    Paulmier, A., Ruiz-Pino, D., Garçon, V. & Farías, L. Maintaining of the eastern south Pacific oxygen minimum zone (OMZ) off Chile. Geophys. Res. Lett. 33, L20601 (2006).
    ADS  Article  CAS  Google Scholar 

    25.
    Stramma, L., Johnson, G. C., Sprintall, J. & Mohrholz, V. Expanding oxygen-minimum zones in the tropical oceans. Science 320, 655–658 (2008).
    ADS  CAS  PubMed  Article  Google Scholar 

    26.
    Gilly, W. F., Beman, J. M., Litvin, S. Y. & Robison, B. H. Oceanographic and biological effects of shoaling of the oxygen minimum zone. Ann. Rev. Mar. Sci. 5, 393–420 (2013).
    PubMed  Article  Google Scholar 

    27.
    Garcia-Robledo, E. et al. Cryptic oxygen cycling in anoxic marine zones. Proc. Natl. Acad. Sci. USA 114, 8319–8324 (2017).
    ADS  CAS  PubMed  Article  Google Scholar 

    28.
    Bianchi, D., Galbraith, E. D., Carozza, D. A., Mislan, K. A. S. & Stock, C. A. Intensification of open-ocean oxygen depletion by vertically migrating animals. Nat. Geosci. 6, 545–548 (2013).
    ADS  CAS  Article  Google Scholar 

    29.
    Wishner, K. F. et al. Ocean deoxygenation and zooplankton: Very small oxygen differences matter. Sci. Adv. 4, eaa518 (2018).
    Article  CAS  Google Scholar 

    30.
    Kawaguchi, S. et al. Will krill fare well under Southern Ocean acidification?. Biol. Lett. 7, 288–291 (2011).
    PubMed  Article  PubMed Central  Google Scholar 

    31.
    Sperfeld, E., Mangor-Jensen, A. & Dalpadado, P. Effect of increasing seawater pCO2 on the northern Atlantic krill species Nyctiphanes couchii. Mar. Biol. 165, 116. https://doi.org/10.1007/s00227-018-3370-7 (2014).
    CAS  Article  Google Scholar 

    32.
    Cooper, H. L., Potts, D. C. & Paytan, A. Effects of elevated pCO2 on the survival, growth, and moulting of the Pacific krill species, Euphausia pacifica. ICES J. Mar. Sci. 74, 1005–1012. https://doi.org/10.1093/icesjms/fsw021 (2017).
    Article  Google Scholar 

    33.
    Ericson, J. A. et al. Adult Antarctic krill proves resilient in a simulated high CO2 ocean. Commun. Biol. 1, 190 (2018).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    34.
    Opstad, I. et al. Effects of high pCO2 on the northern krill Thysanoessa inermis in relation to carbonate chemistry of its collection area, Rijpfjorden. Mar. Biol. 165, 116 (2018).
    Article  CAS  Google Scholar 

    35.
    Powers, E. B. The physiology of the respiration of fishes relation to the hydrogen ion concentration of the medium. J. Gen. Physiol. 4, 305–317 (1922).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    36.
    Mayol, E., Ruiz-Halpern, S., Duarte, C. M., Castilla, J. C. & Pelegrí, J. L. Coupled CO2 and O2-driven compromises to marine life in summer along the Chilean sector of the Humboldt Current System. Biogeosciences 9, 1183–1194 (2012).
    ADS  CAS  Article  Google Scholar 

    37.
    González, H. E., Ortiz, V. C. & Sobarzo, M. The role of faecal material in the particulate organic carbon flux in the northern Humboldt Current, Chile (23 S), before and during the 1997–1998 El Niño. J. Plankton Res. 22, 499–529 (2000).
    Article  Google Scholar 

    38.
    González, H. E. et al. Carbon fluxes within the epipelagic zone of the Humboldt Current System off Chile: The significance of euphausiids and diatoms as key functional groups for the biological pump. Progr. Oceanogr. 83, 217–227 (2009).
    ADS  Article  Google Scholar 

    39.
    Dagg, M. J., Jackson, G. A. & Checkley, D. M. The distribution and vertical flux of fecal pellets from large zooplankton in Monterey Bay and coastal California. Deep Sea Res. 94, 72–86 (2014).
    Article  Google Scholar 

    40.
    Sato, M., Dower, J. F., Kunze, E. & Dewey, R. Second-order seasonal variability in diel vertical migration timing of euphausiids in a coastal inlet. Mar. Ecol. Prog. Ser. 480, 39–56 (2013).
    ADS  Article  Google Scholar 

    41.
    Platt, S. A. & Sanislow, C. A. Norm-of-reaction: Definition and misinterpretation of animal research. J. Comp. Psychol. 102, 254–261 (1988).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    42.
    Wishner, K. F., Outram, D. M., Seibel, B. A., Daly, K. & Williams, R. L. Zooplankton in the Eastern Tropical North Pacific: Boundary effects of oxygen minimum zone expansion. Deep Sea Res. I 79, 122–140 (2013).
    CAS  Article  Google Scholar 

    43.
    Dickson, A. G., Afghan, J. D. & Anderson, G. C. Reference materials for oceanic CO2 analysis: A method for the certification of total alkalinity. Mar. Chem. 80, 185–197 (2003).
    CAS  Article  Google Scholar 

    44.
    Pierrot, D.E., Lewis, E. & Wallace, D.W.R. MS Excel program developed for CO2system calculations. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy (2006). https://cdiac.ornl.gov/ftp/co2sys.

    45.
    Mehrbach, C., Culberson, C., Hawley, J. & Pytkovicz, R. Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol. Oceanogr. 18, 897–907 (1973).
    ADS  CAS  Article  Google Scholar 

    46.
    Dickson, A. G. & Millero, F. J. A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res. 34, 1733–1743 (1987).
    ADS  CAS  Article  Google Scholar 

    47.
    Dickson, A. G. Standard potential of the reaction: AgCl(s) + 12 H 2 (g) 1⁄4 Ag(s) + HCl (aq), and the standard acidity constant of the ion HSO in synthetic seawater from 273.15 to 318.15 K. J. Chem. Thermodyn. 22, 113–127 (1990).
    CAS  Article  Google Scholar 

    48.
    Mitson, R. B. Underwater noise of research vessels: Review and recommendations. ICES Coop. Res. Rep. 209, 61 (1995).
    Google Scholar 

    49.
    Simrad. Simrad ER60 scientific echo sounder manual. Reference Manual. Release 2.2.0, Kongsberg Maritime AS, Norway, 226 (2008).

    50.
    Mair, A., Fernandes, P., Lebourges-Dhaussy, A. & Brierley, A. An investigation into the zooplankton composition of a prominent 38-khz scattering layer in the North Sea. J. Plank. Res. 27, 623–633 (2005).
    CAS  Article  Google Scholar 

    51.
    Cade, D. E. & Benoit-Bird, K. J. Depths, migration rates and environmental associations of acoustic scattering layers in the Gulf of California. Deep Sea Res. I 102, 78–89 (2015).
    Article  Google Scholar 

    52.
    Sato, M. et al. Impacts of moderate hypoxia on fish and zooplankton prey distributions in a coastal fjord. Mar. Ecol. Prog. Ser 560, 57–72 (2016).
    ADS  CAS  Article  Google Scholar 

    53.
    Pérez-Santos, I. et al. Turbulence and hypoxia contribute to dense biological scattering layers in a Patagonian fjord system. Ocean Sci. 14, 1185–1206 (2018).
    ADS  Article  CAS  Google Scholar 

    54.
    Díaz-Astudillo, M., Cáceres, M. & Landaeta, M. Zooplankton structure and vertical migration: Using acoustics and biomass to compare stratified and mixed fjord systems. Cont. Shelf Res 148, 208–218 (2017).
    ADS  Article  Google Scholar 

    55.
    MacLennan, D. N., Fernandez, P. G. & Dalen, J. A consistent approach to definitions and symbols in fisheries acoustics, ICES. J. Mar. Sci. 59, 365–369 (2002).
    Google Scholar 

    56.
    Ballón, M. et al. Is there enough zooplankton to feed forage fish populations off Peru? An acoustic (positive) answer. Prog. Oceanogr. 91, 360–381 (2011).
    ADS  Article  Google Scholar 

    57.
    Clarke, K.R. & Gorley, R.N. PRIMER v7: User Manual/Tutorial PRIMER-E: Plymouth (2015).

    58.
    Kloser, R. J., Ryan, T., Sakov, P., Williams, A. & Koslow, J. A. Species identification in deep water using multiple acoustic frequencies. Can. J. Fish. Aquat. Sci. 59, 1065–1077 (2002).
    Article  Google Scholar 

    59.
    Werner, T. & Buchholz, F. Diel vertical migration behaviour in Euphausiids of the northern Benguela current: Seasonal adaptations to food availability and strong gradients of temperature and oxygen. J. Plankton Res. 35, 792–812 (2013).
    CAS  Article  Google Scholar 

    60.
    Bertrand, A., Ballón, M. & Chaigneau, A. Acoustic observation of living organisms reveals the upper limit of the oxygen minimum zone. PLoS ONE 5(4), e10330 (2010).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    61.
    McLaskey, A. K. et al. Development of Euphausia pacifica (krill) larvae is impaired under pCO2 levels currently observed in the Northeast Pacific. Mar. Ecol. Prog. Ser. 555, 65–78 (2016).
    ADS  CAS  Article  Google Scholar 

    62.
    Flores, H. et al. Impact of climate change on Antarctic krill. Mar. Ecol. Prog. Ser. 458, 1–19 (2012).
    ADS  Article  Google Scholar 

    63.
    Brewer, P. G. & Peltzer, E. T. Limits to marine life. Science 324, 347–348 (2009).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    64.
    Montgomery, D. W. et al. Rising CO2 enhances hypoxia tolerance in a marine fish. Sci. Rep. 9, 15152 (2019).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    65.
    Kiko, R., Hauss, H., Buchholz, F. & Melzner, F. Ammonium excretion and oxygen respiration of tropical copepods and euphausiids exposed to oxygen minimum zone conditions. Biogeosciences 13, 2241–2255 (2016).
    ADS  CAS  Article  Google Scholar 

    66.
    Antezana, T. Adaptive behaviour of Euphausia mucronata in relation to the oxygen minimum layer of the Humboldt Current. In Oceanography of the Eastern Pacific (ed. J. Farber), vol. 2, 29–40 (2002).

    67.
    Torres, J. J. & Childress, J. J. Relationship of oxygen consumption to swimming speed in Euphausia pacifica. Mar. Biol. 74, 79–86 (1983).
    Article  Google Scholar 

    68.
    Anderson, M.J., Gorley R.N. & Clarke K.R. PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. PRIMER-E: Plymouth, UK (2008)

    69.
    Hansen, H.P. & Koroleff, F. Determination of nutrients. In Methods sof Seawater Analysis (eds. K. Grasshoff, K. Kremling & M. Ehrhardt) 159–228 https://doi.org/10.1002/9783527613984.ch10 (2007).

    70.
    Tremblay, N., Hünerlage, K. & Werner, T. Hypoxia tolerance of 10 Euphausiid species in relation to vertical temperature and oxygen gradients. Front. Physiol. 11, 248. https://doi.org/10.3389/fphys.2020.00248 (2020).
    Article  PubMed  PubMed Central  Google Scholar 

    71.
    Tremblay, N., Gómez-Gutiérrez, J., Zenteno-Savín, T., Robinson, C. & Sánchez-Velascoa, L. Role of oxidative stress in seasonal and daily vertical migration of three krill species in the Gulf of California. Limnol. Oceanogr. 55, 2570–2584 (2010).
    ADS  CAS  Article  Google Scholar 

    72.
    Herrera, I. et al. Vertical variability of Euphausia distinguenda metabolic rates during diel migration into the oxygen minimum layer of the Eastern Tropical Pacific off Mexico. J. Plankton Res. 41, 165–176 (2019).
    CAS  Article  Google Scholar 

    73.
    Hernández-León, S., Calles, S. & Fernández de Puelles, M. L. The estimation of metabolism in the mesopelagic zone: Disentangling deep-sea zooplankton respiration. Progr. Oceanogr. 178, 102163 (2019).
    Article  Google Scholar 

    74.
    Hernández-León, S. et al. Carbon export through zooplankton active flux in the Canary Current. J. Mar. Syst. 189, 12–21 (2019).
    Article  Google Scholar 

    75.
    Baker, A. de C., Boden, B.P. & Brinton, E. A Practical Guide to the Euphausiids of the World. British Museum (Natural History), London, 96 pp. (1990).

    76.
    Alegría, N., Arana, P.M. & Sepúlveda, A. Hydroacoustic survey around Elephant Island (Sub-area 48.1) and South Orkney Islands (Subarea 48.2), austral summer 2016. 2017 IEEE/OES Acoustics in Underwater Geosciences Symposium (RIO Acoustics), 5 pp. (2017).

    77.
    Ryan, T. E., Downie, R. A., Kloser, R. J. & Keith, G. Reducing bias due to noise and attenuation in open-ocean echo integration data. ICES J. Mar. Sci. 72, 2482–2493 (2015).
    Article  Google Scholar 

    78.
    De Robertis, A. & Higginbottom, I. A post-processing technique to estimate the signal-to-noise ratio and remove echosounder background noise. ICES J. Mar. Sci. 64, 1282–1291 (2007).
    Article  Google Scholar 

    79.
    Hewitt, R. P. & Demer, D. A. The use of acoustic sampling to estimate the dispersion and abundance of euphausiids, with an emphasis on Antarctic krill (Euphausia superba). Fish. Res. 47, 215–229 (2000).
    Article  Google Scholar 

    80.
    Watkins, J. & Brierley, A. Verification of the acoustic techniques used to identify Antarctic krill. ICES J. Mar. Sci. 59, 1326–1336 (2002).
    Article  Google Scholar 

    81.
    Simmonds, E. & MacLennan, D. Observation and measurement of fish. In Fisheries Acoustics: Theory and Practice (ed. Pitcher, T. J.) 163–215 (Blackwell Science, Oxford, UK, 2005).
    Google Scholar 

    82.
    Reiss, C. S., Cossio, A. M., Loeb, V. & Demer, D. A. Variations in the biomass of Antarctic krill (Euphausia superba) around the South Shetland Islands, 1996–2006. ICES J. Mar. Sci. 65, 497–508 (2008).
    Article  Google Scholar 

    83.
    Santora, J. A. et al. Submarine canyons represent an essential habitat network for krill hotspots in a Large Marine Ecosystem. Sci. Rep. 8, 7579 (2018).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    84.
    Hartin, C. A., Bond-Lamberty, B., Patel, P. & Mundra, A. Ocean acidification over the next three centuries using a simple global climate carbon-cycle model: projections and sensitivities. Biogeosciences 13, 4329–4342 (2016).
    ADS  CAS  Article  Google Scholar  More

  • in

    Plant species determine tidal wetland methane response to sea level rise

    1.
    Bridgham, S. D., Megonigal, J. P., Keller, J. K., Bliss, N. B. & Trettin, C. The carbon balance of North American wetlands. Wetlands 26, 889–916 (2006).
    Article  Google Scholar 
    2.
    Windham-Myers, L. et al. Tidal wetlands and estuaries. in Second State of the Carbon Cycle Report (eds Cavallaro, N. et al.) 596–648 (U.S. Global Change Research Program, 2018)

    3.
    Poulter, B. et al. Global wetland contribution to 2000–2012 atmospheric methane growth rate dynamics. Environ. Res. Lett. 12, https://doi.org/10.1088/1748-9326/aa8391 (2017).

    4.
    Saunois, M. et al. The global methane budget 2000–2017. Earth Syst. Sci. 12, 1561–1623 (2020).
    ADS  Article  Google Scholar 

    5.
    Megonigal, J. P., Hines, M. E. & Visscher, P. T. Anaerobic metabolism: linkages to trace gases and aerobic processes. in Biogeochemistry (ed. Schlesinger, W. H.) 317–424 (Elsevier-Pergamon, 2004).

    6.
    Poffenbarger, H. J., Needelman, B. A. & Megonigal, J. P. Salinity influence on methane emissions from tidal marshes. Wetlands 31, 831–842 (2011).
    Article  Google Scholar 

    7.
    Al-Haj, A. N. & Fulweiler, R. W. A synthesis of methane emissions from shallow vegetated coastal ecosystems. Glob. Change Biol 26, 2988–3005 (2020).
    ADS  Article  Google Scholar 

    8.
    Oreska, M. P. J. et al. The greenhouse gas offset potential from seagrass restoration. Sci. Rep. https://doi.org/10.1038/s41598-020-64094-1 (2020).

    9.
    Rosentreter, J. A., Maher, D. T., Erler, D. V., Murray, R. H. & Eyre, B. D. Methane emissions partially offset “blue carbon” burial in mangroves. Sci. Adv. https://doi.org/10.1126/sciadv.aao4985 (2018).

    10.
    Crooks, S. et al. Coastal wetland management as a contribution to the US National Greenhouse Gas Inventory. Nat. Clim. Chang. 8, 1109–1112 (2018).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    11.
    Chamberlain, S. D. et al. Soil properties and sediment accretion modulate methane fluxes from restored wetlands. Glob. Chang. Biol. 24, 4107–4121 (2018).
    Article  Google Scholar 

    12.
    Call, M. et al. Spatial and temporal variability of carbon dioxide and methane fluxes over semi-diurnal and spring-neap-spring timescales in a mangrove creek. Geochim. Cosmochim. Acta 150, 211–225 (2015).
    ADS  CAS  Article  Google Scholar 

    13.
    van der Nat, F.-J. W. A. & Middelburg, J. J. Effects of two common macrophytes on methane dynamics in freshwater sediments. Biogeochemistry 43, 79–104 (1998).
    Article  Google Scholar 

    14.
    Mueller, P. et al. Complex invader-ecosystem interactions and seasonality mediate the impact of non-native Phragmites on CH4 emissions. Biol. Invasions 18, 2635–2647 (2016).
    Article  Google Scholar 

    15.
    Tong, C., Morris, J. T., Huang, J., Xu, H. & Wan, S. Changes in pore-water chemistry and methane emission following the invasion of Spartina alterniflora into an oliogohaline marsh. Limnol. Oceanogr. 63, 384–396 (2018).
    ADS  CAS  Article  Google Scholar 

    16.
    Macreadie, P. I. et al. The future of Blue Carbon science. Nat. Commun. 10, 3998 (2019).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    17.
    Spivak, A. C., Sanderman, J., Bowen, J. L., Canuel, E. A. & Hopkinson, C. S. Global-change controls on soil-carbon accumulation and loss in coastal vegetated ecosystems. Nat. Geosci. 12, 685–692 (2019).
    ADS  CAS  Article  Google Scholar 

    18.
    Kirwan, M. L. & Megonigal, J. P. Tidal wetland stability in the face of human impacts and sea-level rise. Nature 504, 53–60 (2013).
    ADS  CAS  PubMed  Article  Google Scholar 

    19.
    Duarte, C. M., Losada, I. J., Hendriks, I. E., Mazarrasa, I. & Marba, N. The role of coastal plant communities for climate change mitigation and adaptation. Nat. Clim. Chang. 3, 961–968 (2013).
    ADS  CAS  Article  Google Scholar 

    20.
    Rogers, K. et al. Wetland carbon storage controlled by millennial-scale variation in relative sea-level rise. Nature 567, 91–95 (2019).
    ADS  CAS  PubMed  Article  Google Scholar 

    21.
    Megonigal, J. P. & Schlesinger, W. H. Enhanced CH4 emissions from a wetland soil exposed to elevated CO2. Biogeochemistry 37, 77–88 (1997).
    CAS  Article  Google Scholar 

    22.
    Beaulieu, J. J., DelSontro, T. & Downing, J. A. Eutrophication will increase methane emissions from lakes and impoundments during the 21st century. Nat. Commun. 10, 1375 (2019).
    Article  CAS  Google Scholar 

    23.
    Wilson, R. M. et al. Stability of peatland carbon to rising temperatures. Nat. Commun. 7, 13723 (2016).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    24.
    Stocker, B. D. et al. Multiple greenhouse-gas feedbacks from the land biosphere under future climate change scenarios. Nat. Clim. Chang. 3, 666–672 (2013).
    ADS  CAS  Article  Google Scholar 

    25.
    Knoblauch, C., Beer, C., Liebner, S., Grigoriev, M. N. & Pfeiffer, E. M. Methane production as key to the greenhouse gas budget of thawing permafrost. Nat. Clim. Chang. 8, 309–312 (2018).
    ADS  CAS  Article  Google Scholar 

    26.
    Whiting, G. J. & Chanton, J. P. Primary production control of methane emission from wetlands. Nature 364, 794–795 (1993).
    ADS  CAS  Article  Google Scholar 

    27.
    Langley, J. A., Mozdzer, T. J., Shepard, K. A., Hagerty, S. B. & Megonigal, J. P. Tidal marsh plant responses to elevated CO2, nitrogen fertilization, and sea level rise. Glob. Chang. Biol. 19, 1495–1503 (2013).
    Article  Google Scholar 

    28.
    Mueller, P. et al. Global-change effects on early-stage decomposition processes in tidal wetlands—implications from a global survey using standardized litter. Biogeosciences 15, 3189–3202 (2018).
    ADS  CAS  Article  Google Scholar 

    29.
    Kirwan, M. L. & Guntenspergen, G. R. Feedbacks between inundation, root production, and shoot growth in a rapidly submerging brackish marsh. J. Ecol. 100, 764–770 (2012).
    Article  Google Scholar 

    30.
    Redelstein, R., Dinter, T., Hertel, D. & Leuschner, C. Effects of inundation, nutrient availability and plant species diversity on fine root mass and morphology across a saltmarsh flooding gradient. Front. Plant Sci. 9, 1–15 (2018).
    Article  Google Scholar 

    31.
    Morris, J. T. Estimating net primary production of salt marsh macrophytes. in Principles and Standards for Measuring Primary Production (eds Fahey, T. J. & Knapp, A. K.) 106–119 (Oxford University Press, 2007).

    32.
    Arp, W. J., Drake, B. G., Pockman, W. T., Curtis, P. S. & Whigham, D. F. Interactions between C3 and C4 salt marsh plant species during four years of exposure to elevated atmospheric CO2. Vegetatio. 104, 133–143 (1993).
    Article  Google Scholar 

    33.
    Erickson, J. E., Megonigal, J. P., Peresta, G. & Drake, B. G. Salinity and sea level mediate elevated CO2 effects on C3-C4 plant interactions and tissue nitrogen in a Chesapeake Bay tidal wetland. Glob. Chang. Biol. 13, 202–215 (2007).
    ADS  Article  Google Scholar 

    34.
    Drake, B. G. Rising sea level, temperature, and precipitation impact plant and ecosystem responses to elevated CO2 on a Chesapeake Bay wetland: Review of a 28-year study. Glob. Chang. Biol. 20, 3329–3343 (2014).
    ADS  PubMed  Article  Google Scholar 

    35.
    Kirwan, M. L., Langley, J. A., Guntenspergen, G. R. & Megonigal, J. P. The impact of sea-level rise on organic matter decay rates in Chesapeake Bay brackish tidal marshes. Biogeosciences 10, 1869–1876 (2013).
    ADS  CAS  Article  Google Scholar 

    36.
    Phillips, R. P., Finzi, A. C. & Bernhardt, E. S. Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol. Lett. 14, 187–194 (2011).
    PubMed  Article  Google Scholar 

    37.
    Phillips, R. P., Bernhardt, E. S. & Schlesinger, W. H. Elevated CO2 increases root exudation from loblolly pine (Pinus taeda) seedlings as an N-mediated response. Tree Physiol. 29, 1513–1523 (2009).
    CAS  PubMed  Article  Google Scholar 

    38.
    Lin, G., Ehleringer, J. R., Rygiewicz, P. T., Johnson, M. G. & Tingey, D. T. Elevated CO2 and temperature impacts on different components of soil CO2 efflux in Douglas-fir terracosms. Glob. Chang. Biol. 5, 157–168 (1999).
    ADS  Article  Google Scholar 

    39.
    Megonigal, J. P. et al. A plant-soil-atmosphere microcosm for tracing radiocarbon from photosynthesis through methanogenesis. Soil Sci. Soc. Am. J. 63, 665–671 (1999).
    ADS  CAS  Article  Google Scholar 

    40.
    Dacey, J. W. H., Drake, B. G. & Klug, M. J. Stimulation of methane emission by carbon dioxide enrichment of marsh vegetation. Nature 370, 47–49 (1994).
    ADS  CAS  Article  Google Scholar 

    41.
    Keller, J. K., Wolf, A. A., Weisenhorn, P. B., Drake, B. G. & Megonigal, J. P. Elevated CO2 affects porewater chemistry in a brackish marsh. Biogeochemistry 96, 101–117 (2009).
    CAS  Article  Google Scholar 

    42.
    Langley, J. A. & Megonigal, J. P. Ecosystem response to elevated CO2 levels limited by nitrogen-induced plant species shift. Nature 466, 96–99 (2010).
    ADS  CAS  PubMed  Article  Google Scholar 

    43.
    Langley, J. A., McKee, K. L., Cahoon, D. R., Cherry, J. A. & Megonigal, J. P. Elevated CO2 stimulates marsh elevation gain, counterbalancing sea-level rise. Proc. Natl Acad. Sci. U.S.A. 106, 6182–6186 (2009).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    44.
    Langley, J. A. et al. Ambient changes exceed treatment effects on plant species abundance in global change experiments. Glob. Chang. Biol. 24, 5668–5679 (2018).
    ADS  PubMed  Article  Google Scholar 

    45.
    Bhullar, G. S., Edwards, P. J. & Olde Venterink, H. Variation in the plant-mediated methane transport and its importance for methane emission from intact wetland peat mesocosms. J. Plant Ecol. 6, 298–304 (2013).
    Article  Google Scholar 

    46.
    van der Nat, F.-J. W. A., Middelburg, J. J., Van Meteren, D. & Wielemakers, A. Diel methane emission patterns from Scirpus lacustris and Phragmites australis. Biogeochemistry 41, 1–22 (1998).
    Article  Google Scholar 

    47.
    Van Der Nat, F. J. W. A. & Middelburg, J. J. Seasonal variation in methane oxidation by the rhizosphere of Phragmites australis and Scirpus lacustris. Aquat. Bot. 61, 95–110 (1998).
    Article  Google Scholar 

    48.
    Wolf, A. A., Drake, B. G., Erickson, J. E. & Megonigal, J. P. An oxygen-mediated positive feedback between elevated carbon dioxide and soil organic matter decomposition in a simulated anaerobic wetland. Glob. Chang. Biol. 13, 2036–2044 (2007).
    ADS  Article  Google Scholar 

    49.
    Bernal, B., Megonigal, J. P. & Mozdzer, T. J. An invasive wetland grass primes deep soil carbon pools. Glob. Chang. Biol. 23, 2104–2116 (2017).
    ADS  PubMed  Article  Google Scholar 

    50.
    Mueller, P., Jensen, K. & Megonigal, J. P. Plants mediate soil organic matter decomposition in response to sea level rise. Glob. Chang. Biol. 22, 404–414 (2016).
    ADS  PubMed  Article  Google Scholar 

    51.
    Yuan, J. et al. Spartina alterniflora invasion drastically increases methane production potential by shifting methanogenesis from hydrogenotrophic to methylotrophic pathway in a coastal marsh. J. Ecol. 107, 2436–2450 (2019).
    CAS  Article  Google Scholar 

    52.
    Marsh, A. S., Rasse, D. P., Drake, B. G. & Megonigal, J. P. Effect of elevated CO2 on carbon pools and fluxes in a brackish marsh. Estuaries 28, 694–704 (2005).
    CAS  Article  Google Scholar 

    53.
    Broome, S. W., Mendelssohn, I. A. & McKee, K. L. Relative growth of Spartina patens (Ait.) Muhl. and Scirpus olneyi gray occurring in a mixed stand as affected by salinity and flooding depth. Wetlands 15, 20–30 (1995).
    Article  Google Scholar 

    54.
    Mozdzer, T. J., Langley, J. A., Mueller, P. & Megonigal, J. P. Deep rooting and global change facilitate spread of invasive grass. Biol. Invasions 18, 2619–2631 (2016).
    Article  Google Scholar 

    55.
    IPCC. United Nations Framework Convention on Climate Change. United Nations Framew. Conv. Clim. Chang. https://doi.org/10.1111/j.1467-9388.1992.tb00046.x (2014).

    56.
    Noyce, G. L., Kirwan, M. L., Rich, R. L. & Megonigal, J. P. Asynchronous nitrogen supply and demand produce nonlinear plant allocation responses to warming and elevated CO2. Proc. Natl Acad. Sci. U.S.A. 116, 21623–21628 (2019).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    57.
    Megonigal, J. P. & Rabenhorst, M. Reduction–oxidation potential and oxygen. in Methods in Biogeochemistry of Wetlands (eds DeLaune, R. D., Reddy, K. R., Richardson, C. J. & Megonigal, J. P.) 71–85 (Soil Science Society of America, Inc., 2013).

    58.
    Aselmann, I. & Crutzen, P. J. Global distribution of natural freshwater wetlands and rice paddies, their net primary productivity, seasonality and possible methane emissions. J. Atmos. Chem. 8, 307–358 (1989).
    CAS  Article  Google Scholar 

    59.
    Hammer, Ø., Harper, D. A. T. & Ryan, P. D. Past: paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4, 4 (2001).
    Google Scholar  More

  • in

    An integrated analysis of Maglemose bone points reframes the Early Mesolithic of Southern Scandinavia

    1.
    Jessen, C. A. et al. Early Maglemosian culture in the Preboreal landscape: archaeology and vegetation from the earliest Mesolithic site in Denmark at Lundby Mose Sjælland. Quat. Int. 378, 73–87 (2015).
    Article  Google Scholar 
    2.
    Mortensen, M. F., Henriksen, P. S., Christensen, C., Petersen, P. V. & Olsen, J. Vegetation development in south-east Denmark during the Weichselian Late Glacial: palaeoenvironmental studies close to the Palaeolithic site of Hasselø. Danish J. Archaeol. 3, 33–51 (2014).
    Article  Google Scholar 

    3.
    Sarauw, G. F. L. En Stenalders Boplads i Maglemose ved Mullerup Sammenholdt med Beslægtede Fund (H.H Thieles Bogtrykkeri, København, 1903).
    Google Scholar 

    4.
    Broholm, H. C. Nye fund fra den Ældste Stenalder, Holmegaard- og Sværdborgfundene. Aarbøger for Nordisk Oldkyndighed og Historie 1–144 (1924).

    5.
    Mathiassen, T., Troels-Smith, J. & Degerbøl, M. Stenalderbopladser i Aamosen. (1943).

    6.
    Clark, J. G. D. The Mesolithic Settlement of Northern Europe: A Study of the Food-Gathering Peoples of Northern Europe During the Early Post-Glacial Period (Greenwood Press, New York, 1936).
    Google Scholar 

    7.
    Verhart, L. B. M. Stone Age Bone and Antler As Indicators for ‘Social Territories’ in the European Mesolithic. In Contributions to the Mesolithic in Europe (eds Vermeersch, P. M. & Van Peer, P.) 139–151 (Leuven University Press, Leuven, 1990).
    Google Scholar 

    8.
    Larsson, L., Sjöström, A. & Nilsson, B. Lost at the bottom of the lake. Early and Middle Mesolithic leister points found in the bog Rönneholms Mosse, southern Sweden. In Working at the Sharp End: From Bone and Antler to Early Mesolithic Life in Northern Europe (eds Groß, D. et al.) 1–8 (Wacholtz, Kiel, 2019).
    Google Scholar 

    9.
    Andersen, K. Stenalder bebyggelsen i den Vestsjællandske Åmose (Fredningsstyrelsen, Copenhagen, 1983).
    Google Scholar 

    10.
    David, E. L’industrie en matières dures animale du Mésolithique ancien et moyen d’ Europe du nord, contribution de l’ analyse technologique à la définition du Maglemosien. (Université Paris X-Nanterre, 1999).

    11.
    Leduc, C. Ungulates exploitation for subsistence and raw material, during the Maglemose culture in Denmark: the example of Mullerup site (Sarauw’s Island) in Sjælland. Danish J. Archaeol. 1, 62–81 (2012).
    Article  Google Scholar 

    12.
    David, É The osseous technology of Hohen Viecheln: a Maglemosian idiosyncrasy? In From Bone and Antler to Early Mesolithic Life in Northern Europe (eds Groß, D. et al.) 1–36 (Wachholtz Verlag, Neumünster, 2019).
    Google Scholar 

    13.
    Gummesson, S. & Molin, F. Points of bone and antler from the Late Mesolithic settlement in Motala, eastern central Sweden. In Working at the Sharp End: From Bone and Antler to Early Mesolithic Life in Northern Europe (eds Groß, D. et al.) 1–25 (Wacholtz, Kiel, 2019).
    Google Scholar 

    14.
    Fischer, A. At the border of human habitat. The late Palaeolithic and early Mesolithic in Scandinavia. In The Earliest Settlement of Scandinavia and Its Relationship with Neighbouring Areas (ed. Larsson, L.) 157–176 (Almquist & Wiksell, Stockholm, 1996).
    Google Scholar 

    15.
    Fischer, A. Tissø og Amoserne som trafikforbindelse og kultsted i stenalderen. Historisk Samfund for Holbæk Amt 27–44 (2003).

    16.
    Ramsey, C. B. Methods for summarizing radiocarbon datasets. Radiocarbon 59, 1809–1833 (2017).
    CAS  Article  Google Scholar 

    17.
    Welker, F. et al. Palaeoproteomic evidence identifies archaic hominins associated with the Châtelperronian at the Grotte du Renne. Proc. Natl. Acad. Sci. USA 113, 11162–11167 (2016).
    CAS  PubMed  Article  Google Scholar 

    18.
    Buckley, M. & Collins, M. J. Collagen survival and its use for species identification in Holocene-lower Pleistocene bone fragments from British archaeological and paleontological sites. Antiqua 1, 1–7 (2011).
    Article  Google Scholar 

    19.
    Rodriguez, J., Gupta, N., Smith, R. D. & Pevzner, P. A. Does trypsin cut before proline?. J. Proteome Res. 7, 300–305 (2008).
    CAS  PubMed  Article  Google Scholar 

    20.
    Ekström, J. The Late Quaternary history of the urus (Bos primigenius Bojanus 1827) in Sweden. vol. 29 (Lund Univ., Dep. of Quaternary Geology, 1993).

    21.
    Aaris-Sørensen, K., Mühldorff, R. & Petersen, E. B. The Scandinavian reindeer (Rangifer tarandus L.) after the last glacial maximum: time, seasonality and human exploitation. J. Archaeol. Sci.34, 914–923 (2007/6).

    22.
    Aaris-Sørensen, K. Diversity and dynamics of the mammalian fauna in Denmark throughout the last glacial-interglacial cycle, 115–0 kyr bp. Fossils Strata 57, 1–59 (2010).
    Google Scholar 

    23.
    Aaris-Sørensen, K. Diversity and Dynamics of the Mammalian Fauna in Denmark Throughout the Last Glacial-Interglacial Cycle, 115–0 kyr BP (Wiley, New York, 2010).
    Google Scholar 

    24.
    Aaris-Sørensen, K. Depauperation of the Mammalian Fauna of the Island of Zealand during the Atlantic Period. Vidensk. Meddr Dansk Naturh. Foren. 142, 131–138 (1980).
    Google Scholar 

    25.
    Noe-Nygaard, N., Price, T. D. & Hede, S. Diet of aurochs and early cattle in southern Scandinavia: evidence from N and C stable isotopes. J. Archaeol. Sci. 32, 855–871 (2005).
    Article  Google Scholar 

    26.
    McGrath, K. et al. Identifying archaeological bone via non-destructive ZooMS and the materiality of symbolic expression: examples from iroquoian bone points. Sci. Rep. 9, 11027 (2019).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    27.
    Sjöström, A. Mesolitiska lämningar i Rönneholms mosse. Arkeologisk förundersökning 2010: Hassle 32:18, Stehag socken, Eslövs kommun 1–79 (Skåne. Lund University, Lund, 2011).
    Google Scholar 

    28.
    Sjöström, A. Mesolitiska lämningar i Rönneholms mosse. Arkeologisk förundersökning. Hassle 32:18, Stehag socken, Eslövs kommun Skåne 1–84 (. Lund University, Lund, 2014).
    Google Scholar 

    29.
    Fischer, A. Dating the early trapeze horizon. Radiocarbon dates from submerged settlements in Musholm Bay and Kalø Vig, Denmark. Mesolithc Misc. 15, 1–7 (1994).
    Google Scholar 

    30.
    Sørensen, S. A. Kongemosekulturen i Sydskandinavien (Egnsmuseet Færgegården, Jægerspris, 1996).
    Google Scholar 

    31.
    Sjöström, A. Ringsjöholm. A boreal-early atlantic settlement in Central Scania, Sweden. Lund Archaeol. Rev. 3, 5–20 (1997).
    Google Scholar 

    32.
    Fischer, A. People and the sea—settlement and fishing along the mesolithic coasts. In The Danish Storebælt Since the Ice Age—Man, Sea and Forest (eds Pedersen, L. et al.) 63–77 (A/S Storebælt Fixed Link, Copenhagen, 1997).
    Google Scholar 

    33.
    Tauber, H. Copenhagen radiocarbon dates VII. Radiocarbon 8, 213–234 (1966).
    Article  Google Scholar 

    34.
    Tauber, H. Copenhagen radiocarbon dates X. Radiocarbon 15, 86–112 (1973).
    Article  Google Scholar 

    35.
    Fischer, A. Food for Feasting? An evaluation of explanations of the neolithisation of Denmark and southern Sweden. In The Neolithisation of Denmark—150 Years of Debate (eds Fischer, A. & Krisiansen, K.) 343–393 (J. R Collis, Sheffield, 2002).
    Google Scholar 

    36.
    Andersen, S. H. & Petersen, P. V. Maglemosekulturens stortandede harpuner. Aarbøger Nordisk Oldkynd. Hist. 2004, 7–41 (2009).
    Google Scholar 

    37.
    Larsson, L. The colonization of South Sweden during the deglaciation. In The Earliest Settlement of Scandinavia and Its Relationship with Neighbouring Areas 24 (ed. Larsson, L.) 141–155 (Acta Archaeologica Ludensia, Stockholm, 1996).
    Google Scholar 

    38.
    Sørensen, L. & Casati, C. Hunter-gatherers living in a flooded world: the change of climate, landscapes and settlement patterns during the Late Palaeolithic and Mesolithic on Bornholm, Denmark. In Climate and Ancient Societies (eds Kerner, S. et al.) 41–69 (Museum Tusculanum, Copenhagen, 2015).
    Google Scholar 

    39.
    Sørensen, M. Early mesolithic regional mobility and social organization: evidence from lithic blade technology and microlithic production in southern Scandinavia. In Technology of Early Settlement in Northern Europe—Transmission of Knowledge and Culture (eds Knutsson, K. et al.) 173–201 (Equinox Publishing, London, 2018).
    Google Scholar 

    40.
    Bond, G. et al. A pervasive millennial-scale cycle in North Atlantic Holocene and Glacial Climates. Science 278, 1257–1266 (1997).
    ADS  CAS  Article  Google Scholar 

    41.
    Björck, S. et al. High-resolution analyses of an early Holocene climate event may imply decreased solar forcing as an important climate trigger. Geology 29, 1107–1110 (2001).
    ADS  Article  Google Scholar 

    42.
    Dahl, S. O., Nesje, A., Lie, Ø, Fjordheim, K. & Matthews, J. A. Timing, equilibrium-line altitudes and climatic implications of two early-Holocene glacier readvances during the Erdalen Event at Jostedalsbreen, western Norway. Holocene 12, 17–25 (2002).
    ADS  Article  Google Scholar 

    43.
    Nesje, A., Dahl, S. O. & Bakke, J. Were abrupt Lateglacial and early-Holocene climatic changes in northwest Europe linked to freshwater outbursts to the North Atlantic and Arctic Oceans?. Holocene 14, 299–310 (2004).
    ADS  Article  Google Scholar 

    44.
    Bakke, J., Dahl, S. O. & Nesje, A. Lateglacial and early Holocene palaeoclimatic reconstruction based on glacier fluctuations and equilibrium-line altitudes at northern Folgefonna, Hardanger, Western Norway. J. Quat. Sci. 2, 179–198 (2005).
    Article  Google Scholar 

    45.
    Nesje, A. Latest Pleistocene and Holocene alpine glacier fluctuations in Scandinavia. Quat. Sci. Rev. 28, 2119–2136 (2009).
    ADS  Article  Google Scholar 

    46.
    Berner, K. S., Koç, N. & Godtliebsen, F. High frequency climate variability of the Norwegian Atlantic Current during the early Holocene period and a possible connection to the Gleissberg cycle. Holocene 20, 245–255 (2010).
    ADS  Article  Google Scholar 

    47.
    Balascio, N. L. & Bradley, R. S. Evaluating Holocene climate change in northern Norway using sediment records from two contrasting lake systems. J. Paleolimnol. 48, 259–273 (2012).
    ADS  Article  Google Scholar 

    48.
    Jørgensen, S. Early Postglacial in Aamosen: Geological and Pollen-analytical Investigations of Maglemosian Settlements in the West-Zealand Bog Aamosen (Reitzel, Aigle, 1963).
    Google Scholar 

    49.
    Noe-Nygaard, N. Sedimentary, geochemical and ecological evolution of a Lateglacial-Postglacial lacustrine basin: lakelevel and climatic influence on flora, fauna and human population (Aamosen, Denmark). Foss. Strata 37, 1–436 (1995).
    Google Scholar 

    50.
    Noe-Nygaard, N., Abildtrup, C. H., Albrechtsen, T., Gotfredsen, A. B. & Richter, J. Palæobiologiske, sedimentologiske og geokemiske undersøgelser af Sen Weichel og Holocæne aflejringer i Store Åmose Danmark. Geol. tidsskr. 2, 1–65 (1998).
    Google Scholar 

    51.
    Gedda, B. Environmental and climatic aspects of the early to mid Holocene calcareous tufa and land mollusc fauna in southern Sweden (Lund University, Lund, 2001).
    Google Scholar 

    52.
    Digerfeldt, G., Björck, S., Hammarlund, D. & Persson, T. Reconstruction of Holocene lake-level changes in Lake Igelsjön, southern Sweden. GFF 135, 162–170 (2013).
    CAS  Article  Google Scholar 

    53.
    Gaillard, M.-J. Postglacial paleoclimatic changes in Scandinavia and Central Europe. A tentative correlation based on studies of lake-level fluctuations. Ecol. Mediterr. 11, 159–175 (1985).
    Article  Google Scholar 

    54.
    Nilsson, T. Die pollenanalytische Zonengliederung der spät- und postglazialen Bildungen Schonens. Geol. Föreningen Stockh. Förhandlingar 57, 385–562 (1935).
    Article  Google Scholar 

    55.
    Digerfeldt, G. Reconstruction and regional correlation of Holocene lake-level fluctuations in Lake Bysjon South Sweden. Boreas 17, 165–182 (1988).
    Article  Google Scholar 

    56.
    Dreibrodt, S. et al. Are mid-latitude slopes sensitive to climatic oscillations? Implications from an Early Holocene sequence of slope deposits and buried soils from eastern Germany. Geomorphology 122, 351–369 (2010).
    ADS  Article  Google Scholar 

    57.
    Olsson, F., Gaillard, M. J., Lemdahl, G. & Greisman, A. A continuous record of fire covering the last 10,500 calendar years from southern Sweden—the role of climate and human activities. Palaeogeogr. Palaeoclimatol. Palaeoecol. 291, 128–141 (2010).
    Article  Google Scholar 

    58.
    Manninen, M. A., Tallavaara, M. & Seppä, H. Human responses to early Holocene climate variability in eastern Fennoscandia. Quat. Int. 465, 287–297 (2018).
    Article  Google Scholar 

    59.
    Grünberg, J. The Mesolithic burials of the Middle Elbe-Saale region. In: Mesolithic burials—Rites, symbols and socialorganisation of early postglacial communities (eds. Judith M. Grünberg, B. G., Larsson, L., Orscheidt, J. & Meller, H.) vol. 13,1 257–290 (Halle (Saale) Landesamt für Denkmalpflege und Archäologie Sachsen-Anhalt, Landesmuseum für Vorgeschichte 2016, 2016).

    60.
    Crombé, P. Mesolithic projectile variability along the southern North Sea basin (NW Europe): hunter-gatherer responses to repeated climate change at the beginning of the Holocene. PLoS ONE 14, e0219094 (2019).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    61.
    Solheim, S., Damlien, H. & Fossum, G. Technological transitions and human-environment interactions in Mesolithic southeastern Norway, 11 500–6000 cal. BP. Quat. Sci. Rev. 246, 106501 (2020).
    Article  Google Scholar 

    62.
    Hammarlund, D., Björck, S., Buchardt, B., Israelson, C. & Thomsen, C. T. Rapid hydrological changes during the Holocene revealed by stable isotope records of lacustrine carbonates from Lake Igelsjön, southern Sweden. Quat. Sci. Rev. 22, 353–370 (2003).
    ADS  Article  Google Scholar 

    63.
    Cziesla, E. & Pettitt, P. B. AMS-14C-Datieirungen von spätpaläolithischen und mesolithischen Funden aus dem Bützsee (Brandenburg). Archäol. Korresp. 33, 21–38 (2003).
    Google Scholar 

    64.
    Nordqvist, B. The Mesolithic settlements of the west coast of Sweden-with special emphasis on chronology and topography of coastal settlements. In Man and the Sea in the Mesolithic: Coastal Settlements Above and Below Present Sea Level; 1993; Kalundborg; Denmark (ed. Fischer, A.) 185–196 (Oxbow Books, Oxford, 1995).
    Google Scholar 

    65.
    Nordqvist, B. Coastal Adaptations in the Mesolitic [Mesolithic]: A Study of Coastal Sites with Organic Remains from the Boreal and Atlantic Periods in Western Sweden (Department of Archaeology Göteborg University, Gothenburg, 2000).
    Google Scholar 

    66.
    Johansson, G. En 10 000 år gammal boplats med organiskt material i Mölndal. Ytterligare en överlagrad Sandarnaboplats vid Balltorp. Västra Götalands län, Västergötland, Mölndal stad, Balltorp Ytterligare en överlagrad Sandarnaboplats vid Balltorp Västra Götalands län, Västergötland, Mölndal stad, Balltorp 1:124, Mölndal 182 Dnr 3.1.1-04306-2008(2014).

    67.
    Boethius, A. Fishing for Ways to Thrive: Integrating Zooarchaeology to Understand Subsistence Strategies and Their Implications Among EARLY and Middle Mesolithic Southern Scandinavian Foragers (Lunds University, Lund, 2018).
    Google Scholar 

    68.
    Astrup, P. M. Sea-Level Change in Mesolithic Southern Scandinavia. Long- and Short-Term Effects on Society and the Environment 106 (Jutland Archaeological Society Publications, Højbjerg, 2018).
    Google Scholar 

    69.
    Fischer, A. & Petersen, P. V. Denmark—a sea of archaeological plenty. In Oceans of Archaeology (eds Fischer, A. & Pedersen, L.) 68–83 (Jutland Archaeological Society, Højbjerg, 2018).
    Google Scholar 

    70.
    Fischer, A. et al. Coast–inland mobility and diet in the Danish Mesolithic and Neolithic: evidence from stable isotope values of humans and dogs. J. Archaeol. Sci. 34, 2125–2150 (2007).
    Article  Google Scholar 

    71.
    Ahlström, T. & Sjögren, K.-G. Kvinnan från Österöd—ett tidigmesolitiskt skelett från Bohuslän. In Situ Archaeologica 7, 47–69 (2007).
    Google Scholar 

    72.
    Ahlström, T. Mesolithic human skeletal remains from Tågerup, Scania, Sweden. In: Mesolithic on the Move. Papers Presented at the Sixth International Conference on the Mesolithic in Europe, Stockholm 2000 (eds. Larsson, L., Kindgren, H., Knutsson, K., Loeffler, D. & Åkerlund, A.) 478–484 (Oxbow Books, Oxford, 2003).

    73.
    Desrosiers, P. M. The Emergence of Pressure Blade Making: From Origin to Modern Experimentation (Springer, Berlin, 2012).
    Google Scholar 

    74.
    Sørensen, M. The arrival and development of pressure blade technology in Southern Scandinavia. In The Emergence of Pressure Blade Making: From Origin to Modern Experimentation (ed. Desrosiers, P. M.) 237–259 (Springer, Cham, 2012).
    Google Scholar 

    75.
    Sørensen, M. et al. The first eastern migrations of people and knowledge into Scandinavia: evidence from studies of Mesolithic Technology, 9th-8th Millennium BC. Nor. Archaeol. Rev. 46, 19–56 (2013).
    Article  Google Scholar 

    76.
    Günther, T. et al. Population genomics of Mesolithic Scandinavia: investigating early postglacial migration routes and high-latitude adaptation. PLoS Biol. 16, 1–22 (2018).
    Article  CAS  Google Scholar 

    77.
    Kashuba, N. et al. Ancient DNA from mastics solidifies connection between material culture and genetics of mesolithic hunter–gatherers in Scandinavia. Nat. Commun. Biol. 2, 1–10 (2019).
    Article  Google Scholar 

    78.
    Damlien, H., Kjällquist, M. & Knutsson, K. The pioneer settlement of Scandinavia and its aftermath: new evidence from Western and Central Scandinavia. In The Technology of Early Settlement in Northern Europe—Transmission of Knowledge and Culture 2 (eds Knutsson, K. et al.) 99–137 (Equinox Publishing, Sheffield, 2018).
    Google Scholar 

    79.
    Brock, F., Higham, T., Ditchfield, P. & Ramsey, C. B. Current pretreatment methods for AMS radiocarbon dating at the Oxford radiocarbon accelerator unit (Orau). Radiocarbon 52, 103–112 (2010).
    CAS  Article  Google Scholar 

    80.
    Dee, M. & Bronk Ramsey, C. Refinement of graphite target production at ORAU. Nucl. Instrum. Methods Phys. Res. B 172, 449–453 (2000).
    ADS  CAS  Article  Google Scholar 

    81.
    Ramsey, C. B., Higham, T. & Leach, P. Towards high-precision AMS: progress and limitations. Radiocarbon 46, 17–24 (2004).
    CAS  Article  Google Scholar 

    82.
    Ramsey, C. B. C. B. Bayesian analysis of radiocarbon dates. Radiocarbon 51, 337–360 (2009).
    CAS  Article  Google Scholar 

    83.
    Buckley, M., Collins, M., Thomas-Oates, J. & Wilson, J. C. Species identification by analysis of bone collagen using matrix-assisted laser desorption/ionisation time-of-flight mass spectrometry. Rapid Commun. Mass Spectrom. 23, 3843–3854 (2009).
    ADS  CAS  PubMed  Article  Google Scholar 

    84.
    van Doorn, N. L., Hollund, H. & Collins, M. J. A novel and non-destructive approach for ZooMS analysis: ammonium bicarbonate buffer extraction. Archaeol. Anthropol. Sci. 3, 281 (2011).
    Article  Google Scholar 

    85.
    Kirby, D. P., Buckley, M., Promise, E., Trauger, S. A. & Holdcraft, T. R. Identification of collagen-based materials in cultural heritage. Analyst 138, 4849–4858 (2013).
    ADS  CAS  PubMed  Article  Google Scholar 

    86.
    Perez-Riverol, Y. et al. The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucl. Acids Res. 47, D442–D450 (2019).
    CAS  PubMed  Article  Google Scholar  More

  • in

    Effects of canopy midstory management and fuel moisture on wildfire behavior

    1.
    Westerling, A. L. Increasing western us forest wildfire activity: sensitivity to changes in the timing of spring. Philos. Trans. R. Soc. B 371, 20150178 (2016).
    Article  Google Scholar 
    2.
    Dennison, P. E., Brewer, S. C., Arnold, J. D. & Moritz, M. A. Large wildfire trends in the western united states, 1984–2011. Geophys. Res. Lett. 41, 2928–2933 (2014).
    ADS  Article  Google Scholar 

    3.
    Kasischke, E. S. & Turetsky, M. R. Recent changes in the fire regime across the North American boreal region—spatial and temporal patterns of burning across Canada and Alaska. Geophys. Res. Lett. 33 (2006).

    4.
    Littell, J. S., McKenzie, D., Peterson, D. L. & Westerling, A. L. Climate and wildfire area burned in western US ecoprovinces, 1916–2003. Ecol. Appl. 19, 1003–1021 (2009).
    PubMed  Article  Google Scholar 

    5.
    Abatzoglou, J. T. & Kolden, C. A. Relationships between climate and macroscale area burned in the western United States. Int. J. Wildland Fire 22, 1003–1020 (2013).
    Article  Google Scholar 

    6.
    Kelly, R. et al. Recent burning of boreal forests exceeds fire regime limits of the past 10,000 years. Proc. Natl. Acad. Sci. 110, 13055–13060 (2013).
    ADS  CAS  PubMed  Article  Google Scholar 

    7.
    Abatzoglou, J. T. & Williams, A. P. Impact of anthropogenic climate change on wildfire across western US forests. Proc. Natl. Acad. Sci. 113, 11770–11775 (2016).
    ADS  CAS  PubMed  Article  Google Scholar 

    8.
    Williams, A. P. & Abatzoglou, J. T. Recent advances and remaining uncertainties in resolving past and future climate effects on global fire activity. Curr. Clim. Change Rep. 2, 1–14 (2016).
    Article  Google Scholar 

    9.
    Seager, R. et al. Climatology, variability, and trends in the us vapor pressure deficit, an important fire-related meteorological quantity. J. Appl. Meteorol. Climatol. 54, 1121–1141 (2015).
    ADS  Article  Google Scholar 

    10.
    Radeloff, V. C. et al. Rapid growth of the us wildland–urban interface raises wildfire risk. Proc. Natl. Acad. Sci. 115, 3314–3319 (2018).
    ADS  CAS  PubMed  Article  Google Scholar 

    11.
    Fried, J. S. et al. Predicting the effect of climate change on wildfire behavior and initial attack success. Clim. Change 87, 251–264 (2008).
    Article  Google Scholar 

    12.
    Agee, J. K. & Skinner, C. N. Basic principles of forest fuel reduction treatments. For. Ecol. Manag. 211, 83–96 (2005).
    Article  Google Scholar 

    13.
    Schwilk, D. W. et al. The national fire and fire surrogate study: effects of fuel reduction methods on forest vegetation structure and fuels. Ecol. Appl. 19, 285–304 (2009).
    PubMed  Article  Google Scholar 

    14.
    Whitehead, R. et al. Effect of a spaced thinning in mature lodgepole pine on within-stand microclimate and fine fuel moisture content. In Andrews, P. L., & Butler, B. W., comps. Fuels Management-How to Measure Success: Conference Proceedings. 28–30 March 2006; Portland, OR. Proceedings RMRS-P-41. Fort Collins, CO: US Department of Agriculture, Forest Service, Rocky Mountain Research Station, vol. 41, 523–536 (2006).

    15.
    Whitehead, R. J. et al. Effect of commercial thinning on within-stand microclimate and fine fuel moisture conditions in a mature lodgepole pine stand in southeastern British Columbia. Canadian Forest Service, Canadian Wood Fibre Centre. British Columbia, Information Report, FI-X-004 (2008).

    16.
    Parsons, R. A. et al. Modeling thinning effects on fire behavior with standfire. Ann. For. Sci. 75, 7 (2018).
    Article  Google Scholar 

    17.
    Kalies, E. L. & Kent, L. L. Y. Tamm review: Are fuel treatments effective at achieving ecological and social objectives? A systematic review. For. Ecol. Manag. 375, 84–95 (2016).
    Article  Google Scholar 

    18.
    Banerjee, T. Impacts of forest thinning on wildland fire behavior. Forests 11, 918 (2020).
    Article  Google Scholar 

    19.
    Syifa, M., Panahi, M. & Lee, C.-W. Mapping of post-wildfire burned area using a hybrid algorithm and satellite data: the case of the camp fire wildfire in California, USA. Remote Sensing 12, 623 (2020).
    ADS  Article  Google Scholar 

    20.
    Storey, M. A., Price, O. F., Sharples, J. J. & Bradstock, R. A. Drivers of long-distance spotting during wildfires in south-eastern Australia. Int. J. Wildland Fire (2020).

    21.
    Arienti, M. C., Cumming, S. G. & Boutin, S. Empirical models of forest fire initial attack success probabilities: the effects of fuels, anthropogenic linear features, fire weather, and management. Can. J. For. Res. 36, 3155–3166 (2006).
    Article  Google Scholar 

    22.
    Van Wagner, C. E. Fire Behaviour Mechanisms in a Red Pine Plantation: Field and Laboratory Evidence, vol. 1229 (Ministry of Forestry and Rural Development, 1968).

    23.
    Wagner, C. V. Conditions for the start and spread of crown fire. Can. J. For. Res. 7, 23–34 (1977).
    Article  Google Scholar 

    24.
    Graham, R. T., Harvey, A. E., Jain, T. B. & Tonn, J. R. Effects of thinning and similar stand treatments on fire behavior in western forests. USDA Forest Service, Pacific Northwest Research Station, General Technical Report PNW-GTR-463 (1999).

    25.
    Graham, R. T., McCaffrey, S. & Jain, T. B. Science basis for changing forest structure to modify wildfire behavior and severity. The Bark Beetles, Fuels, and Fire Bibliography 167 (2004).

    26.
    Varner, M. & Keyes, C. R. Fuels treatments and fire models: errors and corrections. Fire Manag. Today 69, 47–50 (2009).
    Google Scholar 

    27.
    Amiro, B., Stocks, B., Alexander, M., Ana, F. & Wotton, B. Fire, climate change, carbon and fuel management in the Canadian boreal forest. Int. J. Wildland Fire 10, 405–4 (2001).
    Article  Google Scholar 

    28.
    Pollet, J. & Omi, P. N. Effect of thinning and prescribed burning on crown fire severity in ponderosa pine forests. Int. J. Wildland Fire 11, 1–10 (2002).
    Article  Google Scholar 

    29.
    Peterson, D. L. et al. Forest structure and fire hazard in dry forests of the western United States. Gen. Tech. Rep. PNW-GTR-628. Portland, OR: US Department of Agriculture, Forest Service, Pacific Northwest Research Station. 30 p 628 (2005).

    30.
    Stephens, S. L. & Moghaddas, J. J. Experimental fuel treatment impacts on forest structure, potential fire behavior, and predicted tree mortality in a california mixed conifer forest. For. Ecol. Manag. 215, 21–36 (2005).
    Article  Google Scholar 

    31.
    Safford, H. D., Schmidt, D. A. & Carlson, C. H. Effects of fuel treatments on fire severity in an area of wildland-urban interface, angora fire, lake Tahoe basin, California. For. Ecol. Manag. 258, 773–787 (2009).
    Article  Google Scholar 

    32.
    Stephens, S. L. et al. Fire treatment effects on vegetation structure, fuels, and potential fire severity in western us forests. Ecol. Appl. 19, 305–320 (2009).
    PubMed  Article  Google Scholar 

    33.
    Hudak, A. et al. Review of fuel treatment effectiveness in forests and rangelands and a case study from the 2007 megafires in central Idaho USA (no. rmrs-gtr-252). Fort Collins, CO: Rocky Mountain Research Station Publishing Services (2011).

    34.
    Waldrop, T. A. & Goodrick, S. L. Introduction to prescribed fires in southern ecosystems. Science Update SRS-054. Asheville, NC: US Department of Agriculture Forest Service, Southern Research Station. 80 p. 54, 1–80 (2012).

    35.
    Martinson, E. J. & Omi, P. N. Fuel treatments and fire severity: a meta-analysis. Res. Pap. RMRS-RP-103WWW. Fort Collins, CO: US Department of Agriculture, Forest Service, Rocky Mountain Research Station. 38, p. 103 (2013).

    36.
    Kennedy, M. C. & Johnson, M. C. Fuel treatment prescriptions alter spatial patterns of fire severity around the wildland–urban interface during the Wallow Fire, Arizona, USA. For. Ecol. Manag. 318, 122–132 (2014).
    Article  Google Scholar 

    37.
    Barnett, K., Parks, S. A., Miller, C. & Naughton, H. T. Beyond fuel treatment effectiveness: characterizing interactions between fire and treatments in the US. Forests 7, 237 (2016).
    Article  Google Scholar 

    38.
    Just, M. G., Hohmann, M. G. & Hoffmann, W. A. Where fire stops: vegetation structure and microclimate influence fire spread along an ecotonal gradient. Plant Ecol. 217, 631–644 (2016).
    Article  Google Scholar 

    39.
    Veenendaal, E. M. et al. On the relationship between fire regime and vegetation structure in the tropics. New Phytol. 218, 153–166 (2018).
    PubMed  Article  PubMed Central  Google Scholar 

    40.
    Bessie, W. & Johnson, E. The relative importance of fuels and weather on fire behavior in subalpine forests. Ecology 76, 747–762 (1995).
    Article  Google Scholar 

    41.
    Rothermel, R. C. A mathematical model for predicting fire spread in wildland fuels. Res. Pap. INT-115. Ogden, UT: US Department of Agriculture, Intermountain Forest and Range Experiment Station. 40 p. 115 (1972).

    42.
    Hoffman, C. M. et al. Surface fire intensity influences simulated crown fire behavior in lodgepole pine forests with recent mountain pine beetle-caused tree mortality. For. Sci. 59, 390–399 (2012).
    Article  Google Scholar 

    43.
    Keyes, C. & Varner, J. Pitfalls in the silvicultural treatment of canopy fuels. Fire Management Today (2006).

    44.
    Moon, K., Duff, T. & Tolhurst, K. Sub-canopy forest winds: understanding wind profiles for fire behaviour simulation. Fire Saf. J. 105, 320–329 (2016).
    Article  Google Scholar 

    45.
    Beer, T. The interaction of wind and fire. Boundary-Layer Meteorol.https://doi.org/10.1007/BF00183958 (1991).
    ADS  Article  Google Scholar 

    46.
    Cheney, N., Gould, J. & Catchpole, W. The influence of fuel, weather and fire shape variables on fire-spread in grasslands. Int. J. Wildland Fire 3, 31–44 (1993).
    Article  Google Scholar 

    47.
    Cochrane, M. A. Fire science for rainforests. Nature 421, 913 (2003).
    ADS  CAS  PubMed  Article  Google Scholar 

    48.
    Fulé, P. Z., McHugh, C., Heinlein, T. A. & Covington, W. W. Potential fire behavior is reduced following forest restoration treatments (Technical Report 2001).

    49.
    Fulé, P. Z., Crouse, J. E., Roccaforte, J. P. & Kalies, E. L. Do thinning and/or burning treatments in western USA ponderosa or Jeffrey pine-dominated forests help restore natural fire behavior?. For. Ecol. Manag. 269, 68–81 (2012).
    Article  Google Scholar 

    50.
    Contreras, M. A., Parsons, R. A. & Chung, W. Modeling tree-level fuel connectivity to evaluate the effectiveness of thinning treatments for reducing crown fire potential. For. Ecol. Manag. 264, 134–149 (2012).
    Article  Google Scholar 

    51.
    White, D. L., Waldrop, T. A. & Jones, S. M. Forty years of prescribed burning on the santee fire plots: effects on understory vegetation. Gen. Tech. Rep. SE-69. Asheville, NC: US Department of Agriculture, Forest Service, Southeastern Forest Experiment Station. pp. 51–59 (1990).

    52.
    Davies, G., Domenech-Jardi, R., Gray, A. & Johnson, P. Vegetation structure and fire weather influence variation in burn severity and fuel consumption during peatland wildfires. Biogeosciences 12, 15737–15762 (2016).
    Article  Google Scholar 

    53.
    Keeley, J. E. & Syphard, A. D. Twenty-first century California, USA, wildfires: fuel-dominated vs. wind-dominated fires. Fire Ecol. 15, 24 (2019).
    Article  Google Scholar 

    54.
    Hiers, J. K. et al. Fine dead fuel moisture shows complex lagged responses to environmental conditions in a saw palmetto (Serenoa repens) flatwoods. Agric. For. Meteorol. 266, 20–28 (2019).
    ADS  Article  Google Scholar 

    55.
    Finney, M. A. et al. Role of buoyant flame dynamics in wildfire spread. Proc. Natl. Acad. Sci. 112, 9833–9838 (2015).
    ADS  CAS  PubMed  Article  Google Scholar 

    56.
    Reisner, J., Wynne, S., Margolin, L. & Linn, R. Coupled atmospheric-fire modeling employing the method of averages. Mon. Weather Rev. 128, 3683–3691 (2000).
    ADS  Article  Google Scholar 

    57.
    Mell, W., Maranghides, A., McDermott, R. & Manzello, S. L. Numerical simulation and experiments of burning douglas fir trees. Combust. Flame 156, 2023–2041 (2009).
    CAS  Article  Google Scholar 

    58.
    Morvan, D. Physical phenomena and length scales governing the behaviour of wildfires: a case for physical modelling. Fire Technol. 47, 437–460 (2011).
    Article  Google Scholar 

    59.
    Parsons, R. A., Mell, W. E. & McCauley, P. Linking 3d spatial models of fuels and fire: effects of spatial heterogeneity on fire behavior. Ecol. Model. 222, 679–691 (2011).
    Article  Google Scholar 

    60.
    Parsons, R. et al. STANDFIRE: An IFT-DSS module for spatially explicit, 3d fuel treatment analysis (Technical Report 2015).

    61.
    Hoffman, C. M., Linn, R., Parsons, R., Sieg, C. & Winterkamp, J. Modeling spatial and temporal dynamics of wind flow and potential fire behavior following a mountain pine beetle outbreak in a lodgepole pine forest. Agric. For. Meteorol. 204, 79–93 (2015).
    ADS  Article  Google Scholar 

    62.
    Hoffman, C. et al. Evaluating crown fire rate of spread predictions from physics-based models. Fire Technol. 52, 221–237 (2016).
    Article  Google Scholar 

    63.
    Pimont, F. et al. Modeling fuels and fire effects in 3d: model description and applications. Environ. Model. Softw. 80, 225–244 (2016).
    Article  Google Scholar 

    64.
    Pimont, F., Dupuy, J.-L., Linn, R. R., Parsons, R. & Martin-StPaul, N. Representativeness of wind measurements in fire experiments: lessons learned from large-eddy simulations in a homogeneous forest. Agric. For. Meteorol. 232, 479–488 (2017).
    ADS  Article  Google Scholar 

    65.
    Pimont, F., Dupuy, J.-L., Linn, R. R. & Dupont, S. Impacts of tree canopy structure on wind flows and fire propagation simulated with FIRETEC. Ann. For. Sci. 68, 523 (2011).
    Article  Google Scholar 

    66.
    Linn, R. R., Sieg, C. H., Hoffman, C. M., Winterkamp, J. L. & McMillin, J. D. Modeling wind fields and fire propagation following bark beetle outbreaks in spatially-heterogeneous Pinyon–Juniper woodland fuel complexes. Agric. For. Meteorol. 173, 139–153 (2013).
    ADS  Article  Google Scholar 

    67.
    Kiefer, M. T., Heilman, W. E., Zhong, S., Charney, J. J. & Bian, X. Mean and turbulent flow downstream of a low-intensity fire: influence of canopy and background atmospheric conditions. J. Appl. Meteorol. Climatol. 54, 42–57 (2015).
    ADS  Article  Google Scholar 

    68.
    Clements, C. B. et al. Observing the dynamics of wildland grass fires: fireflux—a field validation experiment. Bull. Am. Meteorol. Soc. 88, 1369–1382 (2007).
    ADS  Article  Google Scholar 

    69.
    Clements, C. B., Zhong, S., Bian, X., Heilman, W. E. & Byun, D. W. First observations of turbulence generated by grass fires. J. Geophys. Res. Atmos. 113, D22 (2008).
    Article  Google Scholar 

    70.
    Seto, D., Clements, C. B. & Heilman, W. E. Turbulence spectra measured during fire front passage. Agric. For. Meteorol. 169, 195–210. https://doi.org/10.1016/j.agrformet.2012.09.015 (2013).
    ADS  Article  Google Scholar 

    71.
    Heilman, W. E. et al. Observations of fire-induced turbulence regimes during low-intensity wildland fires in forested environments: implications for smoke dispersion. Atmos. Sci. Lett. 16, 453–460 (2015).
    ADS  Article  Google Scholar 

    72.
    Clements, C. B. et al. The fireflux II experiment: a model-guided field experiment to improve understanding of fire–atmosphere interactions and fire spread. Int. J. Wildland Fire 28, 308–326 (2019).
    Article  Google Scholar 

    73.
    Banerjee, T. & Katul, G. Logarithmic scaling in the longitudinal velocity variance explained by a spectral budget. Phys. Fluids 25, 125106 (2013).
    ADS  Article  CAS  Google Scholar 

    74.
    Heilman, W. E. et al. Atmospheric turbulence observations in the vicinity of surface fires in forested environments. J. Appl. Meteorol. Climatol. 56, 3133–3150 (2017).
    ADS  Article  Google Scholar 

    75.
    Keeley, J. E. & Zedler, P. H. Large, high-intensity fire events in southern California shrublands: debunking the fine-grain age patch model. Ecol. Appl. 19, 69–94 (2009).
    PubMed  Article  Google Scholar 

    76.
    Jin, Y. et al. Contrasting controls on wildland fires in southern California during periods with and without Santa Ana winds. J. Geophys. Res. Biogeosciences 119, 432–450 (2014).
    ADS  Article  Google Scholar 

    77.
    Hiers, J. K., O’Brien, J. J., Will, R. E. & Mitchell, R. J. Forest floor depth mediates understory vigor in xeric pinus palustris ecosystems. Ecol. Appl. 17, 806–814 (2007).
    PubMed  Article  Google Scholar 

    78.
    Parresol, B. R., Shea, D. & Ottmar, R. Creating a fuels baseline and establishing fire frequency relationships to develop a landscape management strategy at the savannah river site. In Andrews, P. L. & Butler, B. W., comps Fuels Management-How to Measure Success: Conference Proceedings. 28–30 March 2006; Portland, OR. Proceedings RMRS-P-41. Fort Collins, CO: US Department of Agriculture, Forest Service, Rocky Mountain Research Station, vol. 41, pp 351–366 (2006).

    79.
    Sackett, S. S. & Haase, S. M. Fuel loadings in southwestern ecosystems of the United States. United States Department of Agriculture, Forest Service General Technical Report 187–192 (1996).

    80.
    Bigelow, S. W. & North, M. P. Microclimate effects of fuels-reduction and group-selection silviculture: implications for fire behavior in Sierran mixed-conifer forests. For. Ecol. Manag. 264, 51–59 (2012).
    Article  Google Scholar 

    81.
    Faiella, S. M. & Bailey, J. D. Fluctuations in fuel moisture across restoration treatments in semi-arid ponderosa pine forests of northern Arizona, USA. Int. J. Wildland Fire 16, 119–127 (2007).
    Article  Google Scholar 

    82.
    Estes, B. L., Knapp, E. E., Skinner, C. N. & Uzoh, F. C. Seasonal variation in surface fuel moisture between unthinned and thinned mixed conifer forest, northern California, USA. Int. J. Wildland Fire 21, 428–435 (2012).
    Article  Google Scholar 

    83.
    Pook, E. & Gill, A. Variation of live and dead fine fuel moisture in pinus radiata plantations of the Australian-capital-territory. Int. J. Wildland Fire 3, 155–168 (1993).
    Article  Google Scholar 

    84.
    Weatherspoon, C. P. & Skinner, C. Fire-silviculture relationships in sierra forests. Sierra nevada ecosystem project: final report to congress 2, 1167–1176 (1996).

    85.
    Countryman, C. Old-growth conversion also converts fire climate. US Forest Service Fire Control Notes 17, 15–19 (1955).
    Google Scholar 

    86.
    Linn, R. R. A transport model for prediction of wildfire behavior. Technical Report, Los Alamos National Lab., NM (United States) (1997).

    87.
    Linn, R., Winterkamp, J., Colman, J. J., Edminster, C. & Bailey, J. D. Modeling interactions between fire and atmosphere in discrete element fuel beds. Int. J. Wildland Fire 14, 37–48 (2005).
    Article  Google Scholar 

    88.
    Linn, R. R. & Cunningham, P. Numerical simulations of grass fires using a coupled atmosphere-fire model: basic fire behavior and dependence on wind speed. J. Geophys. Res. Atmos. 110, D13 (2005).
    Article  Google Scholar  More