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    Manganese distribution in the Mn-hyperaccumulator Grevillea meisneri from New Caledonia

    1.Baker, A. & Brooks, R. Terrestrial higher plants which hyperaccumulate metallic elements, a review of their distribution, ecology and phytochemistry. Biorecovery 1, 81–126 (1989).CAS 

    Google Scholar 
    2.Reeves, R. D. et al. A global database for plants that hyperaccumulate metal and metalloid trace elements. New Phytol. 218, 407–411 (2018).PubMed 

    Google Scholar 
    3.Reeves, R. D., Baker, A. J. M., Borhidi, A. & Berazaín, R. Nickel-accumulating plants from the ancient serpentine soils of Cuba. New Phytol. 133, 217–224 (1996).CAS 
    PubMed 

    Google Scholar 
    4.Reeves, R., Baker, A., Borhidi, A. & Berazaín Iturralde, R. Nickel hyperaccumulation in the serpentine flora of Cuba. Ann. Bot. 83, 29–38 (1999).CAS 

    Google Scholar 
    5.Whiting, S. N. et al. Research priorities for conservation of metallophyte biodiversity and their potential for restoration and site remediation. Restor. Ecol. 12, 106–116 (2004).
    Google Scholar 
    6.Jaffré, T., Pillon, Y., Thomine, S. & Merlot, S. The metal hyperaccumulators from New Caledonia can broaden our understanding of nickel accumulation in plants. Front. Plant Sci. 4, 279 (2013).PubMed 
    PubMed Central 

    Google Scholar 
    7.Losfeld, G. et al. Leaf-age and soil–plant relationships: Key factors for reporting trace-elements hyperaccumulation by plants and design applications. Environ. Sci. Pollut. Res. Int. 22, 5620–5632 (2015).CAS 
    PubMed 

    Google Scholar 
    8.Gei, V. et al. Tools for the discovery of hyperaccumulator plant species and understanding their ecophysiology. In Agromining: Farming for metals: Extracting unconventional resources using plants (eds Van der Ent, A. et al.) 117–133 (Springer International Publishing, 2018). https://doi.org/10.1007/978-3-319-61899-9_7.Chapter 

    Google Scholar 
    9.Gei, V. et al. A systematic assessment of the occurrence of trace element hyperaccumulation in the flora of New Caledonia. Bot. J. Linn. Soc. 194, 1–22 (2020).
    Google Scholar 
    10.Grison, C., Escande, V. & Biton, J. Ecocatalysis: A New Integrated Approach to Scientific Ecology (Elsevier, 2015).
    Google Scholar 
    11.Grison, C. Special issue in environmental science and pollution research: Combining phytoextraction and ecocatalysis: an environmental, ecological, ethic and economic opportunity. Environ. Sci. Pollut. Res. 22, 5589–5698 (2015).
    Google Scholar 
    12.Grison, C., Escande, V. & Olszewski, T. K. Ecocatalysis: A new approach toward bioeconomy, chapter 25. In Bioremediation and Bioeconomy (ed. Prasad, M. N. V.) 629–663 (Elsevier, 2016). https://doi.org/10.1016/B978-0-12-802830-8.00025-3.Chapter 

    Google Scholar 
    13.Deyris, P.-A. & Grison, C. Nature, ecology and chemistry: An unusual combination for a new green catalysis, ecocatalysis. Curr. Opin. Green Sustain. Chem. 10, 6–10 (2018).
    Google Scholar 
    14.Grison, C. & LockToyKi, Y. Ecocatalysis, a new vision of green and sustainable chemistry. Curr. Opin. Green Sustain. Chem. 29, 100461 (2021).
    Google Scholar 
    15.Chaney, R. L., Angle, J. S., Li, Y.-M. & Baker, A. J. M. Recuperation de metaux presents dans des sols (2000).16.Chaney, R. L. et al. Improved understanding of hyperaccumulation yields commercial phytoextraction and phytomining technologies. J. Environ. Qual. 36, 1429–1443 (2007).CAS 
    PubMed 

    Google Scholar 
    17.Li, Y.-M. et al. Development of a technology for commercial phytoextraction of nickel: Economic and technical considerations. Plant Soil 249, 107–115 (2003).CAS 

    Google Scholar 
    18.Strawn, K. Unearthing the habitat of a hyperaccumulator: Case study of the invasive plant yellowtuft (Alyssum; Brassicaceae) in Southwest Oregon, USA. Manag. Biol. Invasions 4, 249–259 (2013).
    Google Scholar 
    19.Grison, C. et al. Psychotria douarrei and Geissois pruinosa, novel resources for the plant-based catalytic chemistry. RSC Adv. 3, 22340–22345 (2013).ADS 
    CAS 

    Google Scholar 
    20.Lange, B. et al. Copper and cobalt mobility in soil and accumulation in a metallophyte as influenced by experimental manipulation of soil chemical factors. Chemosphere 146, 75–84 (2016).ADS 
    CAS 
    PubMed 

    Google Scholar 
    21.Grison, C. M. et al. The leguminous species Anthyllis vulneraria as a Zn-hyperaccumulator and eco-Zn catalyst resources. Environ. Sci. Pollut. Res. 22, 5667–5676 (2015).CAS 

    Google Scholar 
    22.Escande, V. et al. Ecological catalysis and phytoextraction: Symbiosis for future. Appl. Catal. B 146, 279–288 (2014).CAS 

    Google Scholar 
    23.Liu, C. et al. Element case studies: Rare earth elements. In Agromining: Farming for Metals (Springer, 2018). https://doi.org/10.1007/978-3-319-61899-9_1924.Lahl, U. & Hawxwell, K. A. REACH—The new European chemicals law. Environ. Sci. Technol. 40, 7115–7121 (2006).ADS 
    CAS 
    PubMed 

    Google Scholar 
    25.Sarrailh, J.-M. La revégétalisation des exploitations minières: l’exemple de la Nouvelle-Calédonie. Bois For. Trop. (2002).26.Losfeld, G. et al. Phytoextraction from mine spoils: Insights from New Caledonia. Environ. Sci. Pollut. Res. 22, 5608–5619 (2015).CAS 

    Google Scholar 
    27.Garel, C. et al. Structure and composition of first biosourced Mn-rich catalysts with a unique vegetal footprint. Mater. Today Sustain. https://doi.org/10.1016/j.mtsust.2019.100020 (2019).Article 

    Google Scholar 
    28.Jaffré, T. Accumulation du manganèse par les Protéacées de Nouvelle Calédonie. Compt. Rend. Acad. Sci. (Paris) Sér. D 289, 425–428 (1979).
    Google Scholar 
    29.Jaffré, T. Plantes de Nouvelle Calédonie permettant de revégétaliser des sites miniers (SLN, 1992).
    Google Scholar 
    30.Jaffré, T. Accumulation du manganèse par des espèces associées aux terrains ultrabasiques de Nouvelle Calédonie. Compt. Rend. Acad. Sci. Paris Sér. D 284, 1573–1575 (1977).
    Google Scholar 
    31.Luçon, S., Marion, F., Niel, J. F. & Pelletier, B. Réhabilitation des sites miniers sur roches ultramafiques en Nouvelle-Calédonie. In Ecologie des milieux sur roches ultramafiques et sur sols métallifères: actes de la deuxième conférence internationale sur l’écologie des milieux serpentiniques Vol. III (eds Jaffré, T. et al.) 297–303 (ORSTOM, 1997).
    Google Scholar 
    32.Reeves, R. D. Tropical hyperaccumulators of metals and their potential for phytoextraction. Plant Soil 249, 57–65 (2003).CAS 

    Google Scholar 
    33.L’Huillier, L. et al. La restauration des sites miniers. In Mines et environnement en Nouvelle Calédonie: les milieux sur substrats ultramafiques et leur restauration (eds L’Huillier, L. et al.) 147–230 (IAC, 2010).
    Google Scholar 
    34.Udo, H., Barrault, J. & Gâteblé, G. Multiplication et valorisation horticole de plantes indigènes à la Nouvelle-Calédonie: Compte-rendu des essais 2011 (2011).35.Jaffré, T. Etude écologique du peuplement végétal des sols dérivés de roches ultrabasiques en Nouvelle Calédonie (ORSTOM, 1980).
    Google Scholar 
    36.Baker, A., Mcgrath, S., Reeves, R. & Smith, J. A. C. Metal hyperaccumulator plants: A review of the ecology and physiology of a biological resource for phytoremediation of metal-polluted soils. Phytoremediat. Contamin. Soil Water. https://doi.org/10.1201/9780367803148-5 (2000).Article 

    Google Scholar 
    37.Bihanic, C., Richards, K., Olszewski, T. K. & Grison, C. Eco-Mn ecocatalysts: Toolbox for sustainable and green Lewis acid catalysis and oxidation reactions. ChemCatChem 12, 1529–1545 (2020).CAS 

    Google Scholar 
    38.Pillon, Y., Munzinger, J., Amir, H. & Lebrun, M. Ultramafic soils and species sorting in the flora of New Caledonia. J. Ecol. 98, 1108–1116 (2010).
    Google Scholar 
    39.Bidwell, S. D., Woodrow, I. E., Batianoff, G. N. & Sommer-Knudsen, J. Hyperaccumulation of manganese in the rainforest tree Austromyrtus bidwillii (Myrtaceae) from Queensland, Australia. Funct. Plant Biol. 29, 899–905 (2002).CAS 
    PubMed 

    Google Scholar 
    40.Fernando, D. R. et al. Foliar Mn accumulation in eastern Australian herbarium specimens: Prospecting for ‘new’ Mn hyperaccumulators and potential applications in taxonomy. Ann. Bot. 103, 931–939 (2009).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    41.Mizuno, T. et al. Age-dependent manganese hyperaccumulation in Chengiopanax sciadophylloides (Araliaceae). J. Plant Nutr. 31, 1811–1819 (2008).CAS 

    Google Scholar 
    42.Xue, S. G. et al. Manganese uptake and accumulation by the hyperaccumulator plant Phytolacca acinosa Roxb. (Phytolaccaceae). Environ. Pollut. 131, 393–399 (2004).CAS 
    PubMed 

    Google Scholar 
    43.Yang, S. X., Deng, H. & Li, M. S. Manganese uptake and accumulation in a woody hyperaccumulator, Schima superba. Plant Soil Environ. 54, 441–446 (2008).CAS 

    Google Scholar 
    44.Proctor, J., Phillipps, C., Duff, G. K., Heaney, A. & Robertson, F. M. Ecological studies on Gunung Silam, a small ultrabasic Mountain in Sabah, Malaysia. II. Some Forest Processes. J. Ecol. 77, 317–331 (1989).CAS 

    Google Scholar 
    45.Graham, R. D., Hannam, R. J. & Uren, N. C. Manganese in Soils and Plants. https://doi.org/10.1007/978-94-009-2817-6 (Springer Netherlands, 1988).46.Loneragan, J. F. Distribution and movement of manganese in plants. In Manganese in Soils and Plants (eds Graham, R. D. et al.) 113–124 (Springer Netherlands, 1988). https://doi.org/10.1007/978-94-009-2817-6_9.Chapter 

    Google Scholar 
    47.Taiz, L. & Zeiger, E. Plant Physiology 3rd edn. (Sinauer Associates Inc., 2002).
    Google Scholar 
    48.Burnell, J. N. The biochemistry of manganese in plants. In Manganese in Soils and Plants (eds Graham, R. D. et al.) 125–137 (Springer Netherlands, 1988). https://doi.org/10.1007/978-94-009-2817-6_10.Chapter 

    Google Scholar 
    49.Lidon, F. C., Barreiro, M. G. & Ramalho, J. C. Manganese accumulation in rice: Implications for photosynthetic functioning. J. Plant Physiol. 161, 1235–1244 (2004).CAS 
    PubMed 

    Google Scholar 
    50.Rengel, Z. Availability of Mn, Zn and Fe in the rhizosphere. J. Soil Sci. Plant Nutr. 15, 397–409 (2015).
    Google Scholar 
    51.Schmidt, S. B., Jensen, P. E. & Husted, S. Manganese deficiency in plants: The impact on photosystem II. Trends Plant Sci. 21, 622–632 (2016).CAS 
    PubMed 

    Google Scholar 
    52.Wissemeier, A. H. & Horst, W. J. Simplified methods for screening cowpea cultivars for manganese leaf-tissue tolerance. Crop Sci. 31, 435–439 (1991).CAS 

    Google Scholar 
    53.Joardar Mukhopadhyay, M. & Sharma, A. Manganese in cell metabolism of higher plants. Bot. Rev. 57, 117–149 (1991).
    Google Scholar 
    54.Lynch, J. & St. Clair, S. Mineral stress: The missing link in understanding how global climate change will affect plants in real world soils. Field Crops Res. 90, 101–115 (2004).
    Google Scholar 
    55.Alejandro, S., Höller, S., Meier, B. & Peiter, E. Manganese in plants: From acquisition to subcellular allocation. Front. Plant Sci 11, 300 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    56.Shao, J. F., Yamaji, N., Shen, R. F. & Ma, J. F. The key to Mn homeostasis in plants: Regulation of Mn transporters. Trends Plant Sci. 22, 215–224 (2017).CAS 
    PubMed 

    Google Scholar 
    57.Millaleo, R., Reyes-Diaz, M., Ivanov, A. G., Mora, M. L. & Alberdi, M. Manganese as essential and toxic element for plants: Transport, accumulation and resistance mechanisms. J. Soil Sci. Plant Nutr. 10, 470–481 (2010).
    Google Scholar 
    58.Vázquez, M. D. et al. Localization of zinc and cadmium in Thlaspi caerulescens (Brassicaceae), a metallophyte that can hyperaccumulate both metals. J. Plant Physiol. 140, 350–355 (1992).
    Google Scholar 
    59.Krämer, U., Grime, G. W., Smith, J. A. C., Hawes, C. R. & Baker, A. J. M. Micro-PIXE as a technique for studying nickel localization in leaves of the hyperaccumulator plant Alyssum lesbiacum. Nucl. Instrum. Methods Phys. Res. Sect. B 130, 346–350 (1997).ADS 

    Google Scholar 
    60.Küpper, H., Lombi, E., Zhao, F.-J. & McGrath, S. P. Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 212, 75–84 (2000).PubMed 

    Google Scholar 
    61.Küpper, H., Lombi, E., Zhao, F.-J., Wieshammer, G. & McGrath, S. P. Cellular compartmentation of nickel in the hyperaccumulators Alyssum lesbiacum, Alyssum bertolonii and Thlaspi goesingense. J. Exp. Bot. 52, 2291–2300 (2001).PubMed 

    Google Scholar 
    62.Mesjasz-Przybyłowicz, J., Przybyłowicz, W. & Pineda, C. Nuclear microprobe studies of elemental distribution in apical leaves of the Ni hyperaccumulator Berkheya coddii. S. Afr. J. Sci. 97, 591 (2001).
    Google Scholar 
    63.Robinson, B. H., Lombi, E., Zhao, F. J. & McGrath, S. P. Uptake and distribution of nickel and other metals in the hyperaccumulator Berkheya coddii. New Phytol. 158, 279–285 (2003).CAS 

    Google Scholar 
    64.Bidwell, S. D., Crawford, S. A., Woodrow, I. E., Sommer-Knudsen, J. & Marshall, A. T. Sub-cellular localization of Ni in the hyperaccumulator, Hybanthus floribundus (Lindley) F. Muell. Plant Cell Environ. 27, 705–716 (2004).CAS 

    Google Scholar 
    65.Memon, A. R., Chino, M., Takeoka, Y., Hara, K. & Yatazawa, M. Distribution of manganese in leaf tissues of manganese accumulator: Acanthopanax sciadophylloides as revealed by Electronprobe X-Ray Microanalyzer. J. Plant Nutr. 2, 457–476 (1980).CAS 

    Google Scholar 
    66.Memon, A. R., Chino, M., Hara, K. & Yatazawa, M. Microdistribution of manganese in the leaf tissues of different plant species as revealed by X-ray microanalyzer. Physiol. Plant. 53, 225–232 (1981).CAS 

    Google Scholar 
    67.Xu, X. et al. Distribution and mobility of manganese in the hyperaccumulator plant Phytolacca acinosa Roxb. (Phytolaccaceae). Plant Soil 285, 323–331 (2006).CAS 

    Google Scholar 
    68.Fernando, D. R. et al. Novel pattern of foliar metal distribution in a manganese hyperaccumulator. Funct. Plant Biol. 35, 193 (2008).CAS 
    PubMed 

    Google Scholar 
    69.Fernando, D. R. et al. Foliar manganese accumulation by Maytenus founieri (Celastraceae) in its native New Caledonian habitats: Populational variation and localization by X-ray microanalysis. New Phytol. 177, 178–185 (2008).CAS 
    PubMed 

    Google Scholar 
    70.Fernando, D. R. et al. Manganese accumulation in the leaf mesophyll of four tree species: A PIXE/EDAX localization study. New Phytol. 171, 751–757 (2006).CAS 
    PubMed 

    Google Scholar 
    71.Fernando, D. R. et al. Variability of Mn hyperaccumulation in the Australian rainforest tree Gossia bidwillii (Myrtaceae). Plant Soil 293, 145–152 (2007).CAS 

    Google Scholar 
    72.Fernando, D. R., Marshall, A., Baker, A. J. M. & Mizuno, T. Microbeam methodologies as powerful tools in manganese hyperaccumulation research: present status and future directions. Front. Plant Sci. 4, 319 (2013).73.Fernando, D. R., Woodrow, I. E., Baker, A. J. M. & Marshall, A. T. Plant homeostasis of foliar manganese sinks: Specific variation in hyperaccumulators. Planta 236, 1459–1470 (2012).CAS 
    PubMed 

    Google Scholar 
    74.Fernando, D. R., Marshall, A. T. & Green, P. T. Cellular ion interactions in two endemic tropical rainforest species of a novel metallophytic tree genus. Tree Physiol. 38, 119–128 (2018).CAS 
    PubMed 

    Google Scholar 
    75.Bihanic, C. et al. Eco-CaMnOx: A greener generation of eco-catalysts for eco-friendly oxidation processes. ACS Sustain. Chem. Eng. 8, 4044–4057 (2020).CAS 

    Google Scholar 
    76.Park, Y. J. & Doeff, M. M. Synthesis and electrochemical characterization of M2Mn3O8 (M = Ca, Cu) compounds and derivatives. Solid State Ion. 177, 893–900 (2006).CAS 

    Google Scholar 
    77.Harper, F. A. et al. Metal coordination in hyperaccumulating plants studied using EXAFS. In Synchrotron Radiation Department Scientific Reports 102 (eds Murphy, B. et al.) (Central Laboratory of Research Councils, 1999).
    Google Scholar 
    78.Rabier, J., Laffont-Schwob, I., Notonier, R., Fogliani, B. & Bouraïma-Madjèbi, S. Anatomical element localization by EDXS in Grevillea exul var. exul under nickel stress. Environ. Pollut. 156, 1156–1163 (2008).CAS 
    PubMed 

    Google Scholar 
    79.Fernando, D. R., Mizuno, T., Woodrow, I. E., Baker, A. J. M. & Collins, R. N. Characterization of foliar manganese (Mn) in Mn (hyper)accumulators using X-ray absorption spectroscopy. New Phytol. 188, 1014–1027 (2010).CAS 
    PubMed 

    Google Scholar 
    80.Fritsch, E. Les sols. In Atlas de la Nouvelle Calédonie (eds Bonvallot, J. et al.) 73–76 (IRD, 2012).
    Google Scholar 
    81.Isnard, S., L’huillier, L., Rigault, F. & Jaffré, T. How did the ultramafic soils shape the flora of the New Caledonian hotspot?. Plant Soil 403, 53–76 (2016).CAS 

    Google Scholar 
    82.Jaffré, T. Composition chimique et conditions de l’alimentation minérale des plantes sur roches ultrabasiques (Nouvelle Calédonie). Cah. ORSTOM. Sér. Biol. 11, 53–63 (1976).
    Google Scholar 
    83.Majourau, P. & Pillon, Y. A review of Grevillea (Proteaceae) from New Caledonia with the description of two new species. Phytotaxa 477, 243–252 (2020).
    Google Scholar 
    84.Jaffré, T. & Latham, M. Contribution à l’étude des relations sol-végétation sur un massif de roches ultrabasiques de la côte Ouest de la Nouvelle Calédonie: le Boulinda. Adansonia. Série 2(14), 311–336 (1974).
    Google Scholar 
    85.L’Huillier, L. et al. Mines et environnement en Nouvelle-Caledonie: les milieux sur substrats ultramafiques et leur restauration (IAC, 2010).
    Google Scholar 
    86.Purnell, H. M. Studies of the family Proteaceae. I. Anatomy and morphology of the roots of some Victorian species. Aust. J. Bot. 8, 38–50 (1960).
    Google Scholar 
    87.Lamont, B. B. Structure, ecology and physiology of root clusters—A review. Plant Soil 248, 1–19 (2003).CAS 

    Google Scholar 
    88.Shane, M. W. & Lambers, H. Manganese accumulation in leaves of Hakea prostrata (Proteaceae) and the significance of cluster roots for micronutrient uptake as dependent on phosphorus supply. Physiol. Plant. 124, 441–450 (2005).CAS 

    Google Scholar 
    89.Dinkelaker, B., Hengeler, C. & Marschner, H. Distribution and function of proteoid roots and other root clusters. Bot. Acta 108, 183–200 (1995).
    Google Scholar 
    90.Castillo-Michel, H. A., Larue, C., Pradas del Real, A. E., Cotte, M. & Sarret, G. Practical review on the use of synchrotron based micro- and nano- X-ray fluorescence mapping and X-ray absorption spectroscopy to investigate the interactions between plants and engineered nanomaterials. Plant Physiol. Biochem. 110, 13–32 (2017).CAS 
    PubMed 

    Google Scholar 
    91.Vantelon, D. et al. The LUCIA beamline at SOLEIL. J. Synchrotron Radiat. 23, 635–640 (2016).CAS 
    PubMed 

    Google Scholar 
    92.Solé, V. A., Papillon, E., Cotte, M., Walter, P. & Susini, J. A multiplatform code for the analysis of energy-dispersive X-ray fluorescence spectra. Spectrochim. Acta Part B 62, 63–68 (2007).ADS 

    Google Scholar 
    93.Ravel, B. & Newville, M. ATHENA, ARTEMIS, HEPHAESTUS: Data analysis for X-ray absorption spectroscopy using IFEFFIT. J. Synchrotron Radiat. 12, 537–541 (2005).CAS 
    PubMed 

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

    Google Scholar 
    95.Losfeld, G. L’association de la phytoextraction et de l’écocatalyse : un nouveau concept de chimie verte, une opportunité pour la remédiation de sites miniers. (Montpellier 2, 2014).96.van der Ent, A. et al. X-ray fluorescence elemental mapping of roots, stems and leaves of the nickel hyperaccumulators Rinorea cf. bengalensis and Rinorea cf. javanica (Violaceae) from Sabah (Malaysia), Borneo. Plant Soil. https://doi.org/10.1007/s11104-019-04386-2 (2020).Article 

    Google Scholar 
    97.Belli, M. et al. X-ray absorption near edge structures (XANES) in simple and complex Mn compounds. Solid State Commun. 35, 355–361 (1980).ADS 
    CAS 

    Google Scholar 
    98.van der Ent, A. et al. X-ray elemental mapping techniques for elucidating the ecophysiology of hyperaccumulator plants. New Phytol. 218, 432–452 (2018).PubMed 

    Google Scholar 
    99.Neumann, G. & Martinoia, E. Cluster roots—An underground adaptation for survival in extreme environments. Trends Plant Sci. 7, 162–167 (2002).CAS 
    PubMed 

    Google Scholar 
    100.Memon, A. R. & Yatazawa, M. Nature of manganese complexes in manganese accumulator plant—Acanthopanax sciadophylloides. J. Plant Nutr. 7, 961–974 (1984).CAS 

    Google Scholar 
    101.Xu, X., Shi, J., Chen, X., Chen, Y. & Hu, T. Chemical forms of manganese in the leaves of manganese hyperaccumulator Phytolacca acinosa Roxb. (Phytolaccaceae). Plant Soil 318, 197 (2008).
    Google Scholar 
    102.Fernando, D. R., Baker, A. J. M. & Woodrow, I. E. Physiological responses in Macadamia integrifolia on exposure to manganese treatment. Aust. J. Bot. 57, 406 (2009).CAS 

    Google Scholar 
    103.Fernando, D. R., Batianoff, G. N., Baker, A. J. & Woodrow, I. E. In vivo localization of manganese in the hyperaccumulator Gossia bidwillii (Benth.) N. Snow & Guymer (Myrtaceae) by cryo-SEM/EDAX. Plant Cell Environ. 29, 1012–1020 (2006).CAS 
    PubMed 

    Google Scholar 
    104.Léon, V. et al. Effects of three nickel salts on germinating seeds of Grevillea exul var. rubiginosa, an endemic serpentine Proteaceae. Ann. Bot. https://doi.org/10.1093/aob/mci066 (2005).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    105.Jaffré, T., Latham, M. & Schmid, M. Aspects de l’influence de l’extraction du minerai de nickel sur la végétation et les sols en Nouvelle-Calédonie. Cah. ORSTOM. Sér. Biol. 12, 307–321 (1977).
    Google Scholar 
    106.Boyd, R. S. & Martens, S. The raison d’etre for metal hyperaccumulation by plants (1992).107.Krämer, U., Pickering, I. J., Prince, R. C., Raskin, I. & Salt, D. E. Subcellular localization and speciation of nickel in hyperaccumulator and non-accumulator Thlaspi species. Plant Physiol. 122, 1343–1353 (2000).PubMed 
    PubMed Central 

    Google Scholar 
    108.Asemaneh, T., Ghaderian, S. M., Crawford, S. A., Marshall, A. T. & Baker, A. J. M. Cellular and subcellular compartmentation of Ni in the Eurasian serpentine plants Alyssum bracteatum, Alyssum murale (Brassicaceae) and Cleome heratensis (Capparaceae). Planta 225, 193–202 (2006).CAS 
    PubMed 

    Google Scholar 
    109.Küpper, H., Jie Zhao, F. & McGrath, S. P. Cellular compartmentation of zinc in leaves of the hyperaccumulator Thlaspi caerulescens. Plant Physiol. 119, 305–312 (1999).PubMed Central 

    Google Scholar 
    110.Abubakari, F. et al. Incidence of hyperaccumulation and tissue-level distribution of manganese, cobalt and zinc in the genus Gossia (Myrtaceae). Metallomics https://doi.org/10.1093/mtomcs/mfab008 (2021).Article 
    PubMed 

    Google Scholar 
    111.White, P. J. Long-distance transport in the xylem and phloem, chapter 3. In Marschner’s Mineral Nutrition of Higher Plants 3rd edn (ed. Marschner, P.) 49–70 (Academic Press, 2012). https://doi.org/10.1016/B978-0-12-384905-2.00003-0.Chapter 

    Google Scholar 
    112.Marschner, H. Marschner’s Mineral Nutrition of Higher Plants (Academic Press, 2012). https://doi.org/10.1016/C2009-0-63043-9.Book 

    Google Scholar 
    113.Fernando, D. R. et al. Does foliage metal accumulation influence plant-insect interactions? A field study of two sympatric tree metallophytes. Funct. Plant Biol. 45, 945–956 (2018).CAS 
    PubMed 

    Google Scholar 
    114.Pearson, R. G. Hard and soft acids and bases, HSAB, part 1: Fundamental principles. J. Chem. Educ. 45, 581 (1968).CAS 

    Google Scholar 
    115.Alejandro, S., Höller, S., Meier, B. & Peiter, E. Manganese in plants: From acquisition to subcellular allocation. Front. Plant Sci. 11, 300 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    116.Hirschi, K. D., Korenkov, V. D., Wilganowski, N. L. & Wagner, G. J. Expression of Arabidopsis CAX2 in tobacco. Altered metal accumulation and increased manganese tolerance. Plant Physiol. 124, 125–134 (2000).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    117.Wu, Z. et al. An endoplasmic reticulum-bound Ca(2+)/Mn(2+) pump, ECA1, supports plant growth and confers tolerance to Mn(2+) stress. Plant Physiol. 130, 128–137 (2002).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    118.Pittman, J. K. Managing the manganese: Molecular mechanisms of manganese transport and homeostasis. New Phytol. 167, 733–742 (2005).CAS 
    PubMed 

    Google Scholar 
    119.Mills, R. F. et al. ECA3, a Golgi-localized P2A-type ATPase, plays a crucial role in manganese nutrition in Arabidopsis. Plant Physiol. 146, 116–128 (2008).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    120.Mizuno, T., Emori, K. & Ito, S. Manganese hyperaccumulation from non-contaminated soil in Chengiopanax sciadophylloides Franch. et Sav. and its correlation with calcium accumulation. Soil Sci. Plant Nutr. 59, 591–602 (2013).CAS 

    Google Scholar 
    121.Tordoff, G. M., Baker, A. J. M. & Willis, A. J. Current approaches to the revegetation and reclamation of metalliferous mine wastes. Chemosphere 41, 219–228 (2000).ADS 
    CAS 
    PubMed 

    Google Scholar 
    122.Grossnickle, S. & Ivetic, V. Direct seeding in reforestation—A field performance review. REFORESTA https://doi.org/10.21750/REFOR.4.07.46 (2017).Article 

    Google Scholar 
    123.Bermúdez-Contreras, A. I., Ede, F., Waymouth, V., Miller, R. & Aponte, C. Revegetation technique changes root mycorrhizal colonisation and root fungal communities: The advantage of direct seeding over transplanting tube-stock in riparian ecosystems. Plant Ecol. https://doi.org/10.1007/s11258-020-01031-2 (2020).Article 

    Google Scholar  More

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    Elevated growth and biomass along temperate forest edges

    OverviewWe used data from the national forest inventory conducted by the US Department of Agriculture, Forest Service, Forest Inventory and Analysis (FIA) program to quantify tree biomass and growth along forest edges and within the forest interior. We estimated the causal impact of the forest edge environment on patterns of tree biomass and growth, while accounting for potentially confounding variables. We then used the regression models to estimate the aggregate difference in growth attributable to forest edges throughout the northeastern U.S. Finally, to better understand the implications of our findings, we quantified the degree of forest fragmentation throughout temperate and tropical forest biomes world-wide, using a 30 m forest cover map.Study areaOur analyses of edge impacts on forest biomass and growth were conducted throughout twenty-states (1.7 million km2) in the northeastern and upper mid-west of the United States (Supplementary Fig. 1). This region contains 765,000 km2 of forest and encompasses gradients of dominant land-uses, climatic conditions, and forest composition while remaining within deciduous, coniferous, and mixed temperate forest ecosystems.Identifying edges in forest inventory dataThe FIA collects measurements of tree size, growth, and land-use within a nested plot design across the country19. Each FIA plot is composed of four individual subplots; within each subplot, the diameter at breast height (dbh) of every tree >12.7 cm is measured during each measurement period. The re-measurement frequency for FIA plots in our study area is between 5 and 7 years, but this can differ between Forest Service regions. In addition to tree measurements, the database details land-use condition data that includes the proportion of the area that is forested and, on some plots, the land-cover class of the non-forest area (FIA User’s Manual, Condition Table). FIA plots are considered forested if some portion of the plot includes a contiguous forest patch (including potentially outside of the plot area) of greater than 4047 m2 that has more than 10% canopy cover. With a memorandum of understanding between the USFS and Harvard University, we had access to the true, unfuzzed plot coordinates, which are not publicly available. Evaluating >48,000 plots in the USFS Northern Region sampled from 2010 to 2020 and selecting the most recent measurement cycle for each plot, we identified subplots that contained both a forest and a non-forest condition and categorized these as edges (Supplementary Table 1). Only subplots that included a forest condition in both the most recent and previous measurement were included. Subplots where the mapped condition changed from forest to non-forest were excluded. Changes in the amount of mapped forest condition were included and are incorporated into the calculation of response variables using the most recent condition area. We identified FIA plots where all four subplots were fully forested as interior plots to be used for comparison. Subplots located within the same plot as an edge subplot (i.e., edge-proximate subplots) were excluded from this study due to limitations in our ability to quantify their distance from an edge. The spatial configuration of subplots is such that a fully forested subplot may be up to ~65 m away from an identified forest edge within another subplot. Studies suggest that the distance of edge influence in temperate forest does not extend more than 30 m into the forest interior15,33. Since the FIA does not contain information about the geometry of non-forest conditions beyond the subplot boundary, we deemed that the large uncertainty in the relationship between these subplots to a non-forest edge precluded their inclusion in the study. The FIA plot configuration prevented quantification of the distance of edge influence in our analysis; the exclusion of subplots adjacent to edge-subplots may limit direct comparisons with other fragmentation studies.We used the FIA condition data to characterize the non-forest land use in edge subplots. Information on adjacent non-forest land cover is not collected on all FIA plots (4327 of 6607 edge subplots). We aggregated FIA land-cover classification to a binary anthropogenic or unknown edge type designation and present results from all edge subplots and the anthropogenic edge subset (FIA User’s Manual Condition Table, Section 2.4.50).For each subplot (168 m2 in area), we calculated two primary response variables of interest: total live tree BA and BAI. Notably, trees smaller than 12.7 cm dbh) in m2. BAI was calculated on a per-tree basis as the difference in radial growth of live adult trees between the most recent and previous measurements, and then divided by the number of years between measurements (m2 yr−1). In addition, we aggregated individual tree diameter measurements to calculate mean stem density (stems ha−1) and mean tree diameter for each subplot (Fig. 2).We accounted for variable subplot area by normalizing both BA and BAI to a per-hectare of forested area basis, resulting in units of m2 ha−1 and m2 ha−1 yr−1, respectively. To account for potential small-area bias, we performed a sensitivity analysis on the relationship between BA and subplot forested area (Supplementary Fig. 2). We subsequently excluded 1284 subplots under 30 m2 in area as the area to BA relationship asymptotes relationship above this threshold. Finally, we accounted for errors in field dbh measurements, sometimes resulting in negative BAI values, by excluding the 97.5% quantiles of both BA and BAI distributions.Given their spatial configuration, FIA subplots are not fully independent measurements, potentially introducing issues with pseudo-replication and spatial autocorrelation within our dataset. To test for spatial autocorrelation we examined the semivariance of model residuals36, and found that there was high correlation only at distances of less than 1 km. The spatial stratification of the FIA plot design minimizes issues of plot–plot proximity within our study. However, to account for autocorrelation between subplots, we filtered our pre-matched dataset to only including one subplot from each FIA plot. For plots containing multiple edge subplots, we selected the subplot with the largest forested area. For interior plots, we selected the central subplot and excluded all others.Isolating the effect of edges on growthAbiotic controlsTo account for environmental controls on forest growth we included the most critical abiotic predictors of terrestrial vegetation productivity (light, water, temperature, and nitrogen deposition) as covariates in the regression models (Supplementary Fig. 4, Supplementary Table 2). Light, water, and temperature data were drawn from spatial raster maps (0.5° resolution) as unit-less indices of relative limitation on vegetation productivity, ranging from 0 to 13. Nitrogen data were drawn from the 2018 NADP gridded inorganic wet nitrogen deposition product (4 km spatial resolution; kg of N ha−1)37. To interpolate across small gaps in the raster data (usually along water bodies), we used the Nibble tool from ArcGis Pro (ESRI Team). We then used FIA plot locations to extract values from each raster layer for all FIA subplots.Forest compositionTree species may vary in their responses to biogeochemical changes that occur on forest edges. Overall forest community response emerges from complex interactions between species. We used aggregations of tree species, termed forest composition groups (or forest types)38, to assess if species composition influenced the response to altered edge condition. Forest type classifications for each subplot are provided by the FIA (FIA User’s Manual, Condition Table) and are defined in Appendix D therein. We aggregated the FIA forest types into eight broader species groups, following Thompson et al.23, and defined in Supplementary Table 1.Matching, GLM regressions, and model selectionAll statistical analyses and most of the data processing were conducted in R, version 3.439. Using a causal inference framework, we created a quasi-experimental statistical design that included pre-matching followed by a GLM regression analysis40. Matching emulates an experimental design using observational data by identifying control groups of untreated (forest interior) plots that were as similar as possible to treated (forest edge) plots in terms of observable confounders. By capturing key differences in abiotic variables we control for the fundamental drivers of forest productivity, allowing for a direct estimation of the average treatment effect of edges. Similarity was defined by nearest-neighbor covariate matching determined by Malahanobis distance, implemented in the MatchIt library in R41, the simplest and best method when the dataset is robust enough to find a match for every treated plot20. This method excludes forest interior plots that are not matched with an edge plot. Given differences in sample size between the full edge dataset and the subset designated as anthropogenic edges, we performed matching separately on the two datasets. To assess the efficacy of matching on reducing the differences in covariate distributions, we used summary statistics calculated with the MatchIt library and report the pre- and post-matched covariate balance in Supplementary Table 4 and Supplementary Table 5 (sensu Schleicher et al.42). Matching was highly successful, largely eliminating differences in all covariate distributions in both datasets.Our primary response variables of interest, BA and BAI, were right-skewed, non-normally distributed and violated the assumptions of normality necessary for ordinary least squares regression43. We, therefore, used a GLM to better fit the structure of our data. GLMs are an extension of linear regression that allow more freedom in the choice of probability distribution function through the use of a link function to model relationships between predictors and response variables44. The gamma probability distribution is frequently chosen to model BA, given its assumptions of positive, continuous values and flexible model form23,45. We performed a series of GLM regressions on our post-matched datasets, using a gamma probability distribution with an inverse link function to model the relationship of BA and BA with a suite of predictor variables, using the glm function as implemented in the R Core stats package39. Due to differences in sample size between the all-edge dataset and the anthropogenic-edge subset, we modeled these two datasets separately for each of BA and BAI, resulting in four separate regression analyses. We used a model selection framework to identify the most parsimonious model within each of the model sets based on the Akaike Information Criterion (AIC) and residual deviance statistic46,47. We report the model-selection and model-fit results for each of our separate analyses, including model forms, AIC, Nagelkerke Pseudo-R2, and residual deviance in Supplementary Table 2. Across all four regression analyses, the best-performing model was one that included an interaction between the edge-status and forest type categorical variables, as well as the variables of temperature-limitation, light-limitation, water-limitation, and nitrogen deposition.We then used the best performing model from each analysis to compare the differences in BA and BAI between forest edge and interior across each forest type. We estimated the treatment effect of edge-state within each forest type using the ggeffects package48 to calculate marginal effects with the continuous predictors (temperature, light, water, and nitrogen deposition) held at their within-forest type regional means. The results of this analysis are displayed in Fig. 1 and Supplementary Table 3; primary error bars on the interior point show the 95% confidence interval of the marginal effect from the full edge model, while secondary error bars show the CI from the anthropogenic edge model. Due to the smaller sample size in the anthropogenic model, estimates of the mean marginal effect of the interior plots vary slightly (though non-significantly) from those from the full dataset. The main text description reports outputs from both models, calculated from separate interior mean estimates. For visual clarity, we only display one set of interior means in Fig. 1.Mortality and timber harvestIn tropical forests, large reductions in productivity along edges are associated with increased tree mortality.9 To assess differences in tree mortality across our study region, we applied a simplified GLM analysis, including edge-state as our only predictor variable. The FIA differentiates between mortality attributed to timber harvest and that attributed to other, non-harvest causes. The results of this analysis are presented as marginal effects of each edge category in Supplementary Fig. 3. There are no significant differences in biogenic mortality between edge groups and no difference in overall mortality (combined biogenic and anthropogenic); there is a small, but statistically significant (p  More

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    Community similarity and species overlap between habitats provide insight into the deep reef refuge hypothesis

    1.Wilson, E. O. Introduction. in Biodiversity II: understanding and protecting our biological resources (eds. Reaka-Kudla, M. L., Wilson, D. E. & Wilson, E. O.) 1–3 (Joseph Henry Press, 1997).2.Lovejoy, T. E. Biodiversity: what is it? in Biodiversity II: Understanding and protecting our biological resources (eds. Reaka-Kudla, M. L., Wilson, D. E. & Wilson, E. O.) 7–14 (Joseph Henry Press, 1997).3.Ehrlich, P. R. & Wilson, E. O. Biodiversity studies: Science and policy. Science 253, 758–762 (1991).ADS 
    CAS 
    Article 

    Google Scholar 
    4.Myers, R. A. & Ottensmeyers, C. A. Extinction risk in marine species. in Marine Conservation Biology: The Science of Maintaining the Sea’s Biodiversity (eds. Norse, E. A. & Crowder, L. B.) 58–79 (Island Press, 2005).5.Reaka-Kudla, M. L. The global biodiversity of coral reefs: a comparison with rain forests. in Biodiversity II: understanding and protecting our biological resources (eds. Reaka-Kudla, M. L., Wilson, D. E. & Wilson, E. O.) 83–108 (Joseph Henry Press, 1997).6.Briggs, J. C. Marine extinctions and conservation. Mar. Biol. 158, 485–488 (2011).Article 

    Google Scholar 
    7.Harley, C. D. G. et al. The impacts of climate change in coastal marine systems: Climate change in coastal marine systems. Ecol. Lett. 9, 228–241 (2006).ADS 
    Article 

    Google Scholar 
    8.Dupont, S., Dorey, N. & Thorndyke, M. What meta-analysis can tell us about vulnerability of marine biodiversity to ocean acidification?. Estuar. Coast. Shelf Sci. 89, 182–185 (2010).ADS 
    Article 

    Google Scholar 
    9.Stork, N. E. Measuring global biodiversity and its decline. in Biodiversity II: understanding and protecting our biological resources (eds. Reaka-Kudla, M. L., Wilson, D. E. & Wilson, E. O.) 41–68 (Joseph Henry Press, 1997).10.Richards, Z. T. & Day, J. C. Biodiversity of the Great Barrier Reef—How adequately is it protected? PeerJ 6, e4747 (2018).11.Pyle, R. L. & Copus, J. M. Mesophotic Coral Ecosystems: introduction and overview. in Mesophotic Coral Ecosystems (eds. Loya, Y., Puglise, K. A. & Bridge, T. C. L.) vol. 12 3–27 (Springer International Publishing, 2019).12.Hinderstein, L. M. et al. Theme section on ‘Mesophotic coral ecosystems: Characterization, ecology, and management’. Coral Reefs 29, 247–251 (2010).ADS 
    Article 

    Google Scholar 
    13.Bongaerts, P., Ridgway, T., Sampayo, E. M. & Hoegh-Guldberg, O. Assessing the ‘deep reef refugia’ hypothesis: Focus on Caribbean reefs. Coral Reefs 29, 309–327 (2010).Article 

    Google Scholar 
    14.Bongaerts, P. & Smith, T. B. Beyond the “Deep Reef Refuge” hypothesis: a conceptual framework to characterize persistence at depth. in Mesophotic Coral Ecosystems (eds. Loya, Y., Puglise, K. A. & Bridge, T. C. L.) vol. 12, 881–895 (Springer International Publishing, 2019).15.Vermeij, G. J. Survival during biotic crises: the properties and evolutionary significance of refuges. Dyn. Extinct. 231–246 (1986).16.Glynn, P. W. Coral reef bleaching: Facts, hypotheses and implications. Glob. Change Biol. 2, 495–509 (1996).ADS 
    Article 

    Google Scholar 
    17.Riegl, B. & Piller, W. E. Possible refugia for reefs in times of environmental stress. Int. J. Earth Sci. 92, 520–531 (2003).Article 

    Google Scholar 
    18.Halfar, J., Godinez-Orta, L., Riegl, B., Valdez-Holguin, J. E. & Borges, J. M. Living on the edge: high-latitude Porites carbonate production under temperate eutrophic conditions. Coral Reefs 24, 582–592 (2005).ADS 
    Article 

    Google Scholar 
    19.Loya, Y., Eyal, G., Treibitz, T., Lesser, M. P. & Appeldoorn, R. Theme section on mesophotic coral ecosystems: Advances in knowledge and future perspectives. Coral Reefs 35, 1–9 (2016).ADS 
    Article 

    Google Scholar 
    20.Laverick, J. H. et al. To what extent do mesophotic coral ecosystems and shallow reefs share species of conservation interest? A systematic review. Environ. Evid. 7, 15 (2018).Article 

    Google Scholar 
    21.Smith, T. B., Glynn, P. W., Maté, J. L., Toth, L. T. & Gyory, J. A depth refugium from catastrophic coral bleaching prevents regional extinction. Ecology 95, 1663–1673 (2014).Article 

    Google Scholar 
    22.Smith, T. B. et al. Caribbean mesophotic coral ecosystems are unlikely climate change refugia. Glob. Change Biol. 22, 2756–2765 (2016).ADS 
    Article 

    Google Scholar 
    23.Holstein, D. M., Smith, T. B., Gyory, J. & Paris, C. B. Fertile fathoms: Deep reproductive refugia for threatened shallow corals. Sci. Rep. 5 (2015).24.Holstein, D. M., Paris, C. B., Vaz, A. C. & Smith, T. B. Modeling vertical coral connectivity and mesophotic refugia. Coral Reefs 35, 23–37 (2016).ADS 
    Article 

    Google Scholar 
    25.Holstein, D. M., Smith, T. B. & Paris, C. B. Depth-independent reproduction in the reef coral Porites astreoides from shallow to mesophotic zones. PLoS ONE 11, e0146068 (2016).26.Assis, J. et al. Deep reefs are climatic refugia for genetic diversity of marine forests. J. Biogeogr. 43, 833–844 (2016).Article 

    Google Scholar 
    27.Bongaerts, P. et al. Deep reefs are not universal refuges: Reseeding potential varies among coral species. Sci. Adv. 3, e1602373 (2017).28.Muir, P. R., Marshall, P. A., Abdulla, A. & Aguirre, J. D. Species identity and depth predict bleaching severity in reef-building corals: Shall the deep inherit the reef?. Proc. R. Soc. B. 284, 20171551 (2017).Article 

    Google Scholar 
    29.Semmler, R. F., Hoot, W. C. & Reaka, M. L. Are mesophotic coral ecosystems distinct communities and can they serve as refugia for shallow reefs?. Coral Reefs 36, 433–444 (2017).ADS 
    Article 

    Google Scholar 
    30.Kavousi, J. & Keppel, G. Clarifying the concept of climate change refugia for coral reefs. ICES J. Mar. Sci. 75, 43–49 (2018).Article 

    Google Scholar 
    31.Morais, J. & Santos, B. A. Limited potential of deep reefs to serve as refuges for tropical Southwestern Atlantic corals. Ecosphere 9, e02281 (2018).32.Pereira, P. H. C., Macedo, C. H., Nunes, J. de A. C. C., Marangoni, L. F. de B. & Bianchini, A. Effects of depth on reef fish communities: Insights of a “deep refuge hypothesis” from Southwestern Atlantic reefs. PLoS ONE 13, e0203072 (2018).33.Rocha, L. A. et al. Mesophotic coral ecosystems are threatened and ecologically distinct from shallow water reefs. Science 361, 281–284 (2018).ADS 
    CAS 
    Article 

    Google Scholar 
    34.Slattery, M. et al. The Pulley Ridge deep reef is not a stable refugia through time. Coral Reefs 37, 391–396 (2018).ADS 
    Article 

    Google Scholar 
    35.Kavousi, J. Biological interactions: The overlooked aspects of marine climate change refugia. Glob. Change Biol. 25, 3571–3573 (2019).ADS 
    Article 

    Google Scholar 
    36.Baselga, A. The relationship between species replacement, dissimilarity derived from nestedness, and nestedness: Species replacement and nestedness. Glob. Ecol. Biogeogr. 21, 1223–1232 (2012).Article 

    Google Scholar 
    37.Fisher, R. et al. Species richness on coral reefs and the pursuit of convergent global estimates. Curr. Biol. 25, 500–505 (2015).CAS 
    Article 

    Google Scholar 
    38.Montgomery, A. D., Fenner, D. & Toonen, R. J. Annotated checklist for stony corals of American Sāmoa with reference to mesophotic depth records. ZK 849, 1–170 (2019).39.Colwell, R. K. et al. Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. J. Plant Ecol. 5, 3–21 (2012).Article 

    Google Scholar 
    40.Rooney, J. et al. Mesophotic coral ecosystems in the Hawaiian Archipelago. Coral Reefs 29, 361–367 (2010).ADS 
    Article 

    Google Scholar 
    41.Bridge, T. C. L. et al. Diversity of Scleractinia and Octocorallia in the mesophotic zone of the Great Barrier Reef, Australia. Coral Reefs 31, 179–189 (2012).ADS 
    Article 

    Google Scholar 
    42.Pyle, R. L. et al. A comprehensive investigation of mesophotic coral ecosystems in the Hawaiian Archipelago. PeerJ 4, e2475 (2016).43.Muir, P. R. & Pichon, M. Biodiversity of reef-building, Scleractinian corals. in Mesophotic Coral Ecosystems (eds. Loya, Y., Puglise, K. A. & Bridge, T. C. L.) vol. 12, 589–620 (Springer International Publishing, 2019).44.Spalding, H. L. et al. The Hawaiian Archipelago. in Mesophotic Coral Ecosystems (eds. Loya, Y., Puglise, K. A. & Bridge, T. C. L.) vol. 12, 445–464 (Springer International Publishing, 2019).45.Turak, E. & DeVantier, L. Reef-building corals of the upper mesophotic zone of the Central Indo-West Pacific. in Mesophotic Coral Ecosystems (eds. Loya, Y., Puglise, K. A. & Bridge, T. C. L.) vol. 12, 621–651 (Springer International Publishing, 2019).46.Vermeij, G. J. & Grosberg, R. K. Rarity and persistence. Ecol. Lett. 21, 3–8 (2018).Article 

    Google Scholar 
    47.Kammer, T. W., Baumiller, T. K. & Ausich, W. I. Evolutionary significance of differential species longevity in Osagean-Meramecian (Mississippian) crinoid clades. Paleobiology 24, 155–176 (1998).
    Google Scholar 
    48.Jones, G. P., Julian, C. M. & Munday, P. L. Rarity in coral reef fish communities. in Coral reef fishes: dynamics and diversity in a complex ecosystem (ed. Sale, P. F.) 81–102 (Academic Press, 2006).49.Yang, Q., Liu, G., Casazza, M., Gonella, F. & Yang, Z. Three dimensions of biodiversity: New perspectives and methods. Ecol. Indic. 130, 108099 (2021).50.Richards, Z. T. Rarity in the coral genus Acropora: Implications for biodiversity conservation. (James Cook University, 2009).51.Soares, M. de O. Marginal reef paradox: A possible refuge from environmental changes? Ocean Coast. Manag. 185, 105063 (2020).52.Soares, M. de O. et al. Why do mesophotic coral ecosystems have to be protected? Sci. Total Environ. 726, 138456 (2020).53.White, K. N. et al. Typhoon damage on a shallow mesophotic reef in Okinawa, Japan. PeerJ 1, e151 (2013).54.Smith, T. B., Holstein, D. M. & Ennis, R. S. Disturbance in mesophotic coral ecosystems and linkages to conservation and management. in Mesophotic Coral Ecosystems (eds. Loya, Y., Puglise, K. A. & Bridge, T. C. L.) vol. 12, 911–929 (Springer International Publishing, 2019).55.Pinheiro, H. T., Eyal, G., Shepherd, B. & Rocha, L. A. Ecological insights from environmental disturbances in mesophotic coral ecosystems. Ecosphere 10, e02666 (2019).56.Veron, J. E. N. Corals of the world. (Australian Institute of Marine Science, 2000).57.Luzon, K. S., Lin, M.-F., Ablan Lagman, Ma. C. A., Licuanan, W. R. Y. & Chen, C. A. Resurrecting a subgenus to genus: molecular phylogeny of Euphyllia and Fimbriaphyllia (order Scleractinia; Family Euphyllidae; clade V). PeerJ 5, e4074 (2017).58.Eyal, G. et al. Euphyllia paradivisa, a successful mesophotic coral in the northern Gulf of Eilat/Aqaba, Red Sea. Coral Reefs 35, 91–102 (2016).ADS 
    Article 

    Google Scholar 
    59.Eyal, G., Tamir, R., Kramer, N., Eyal-Shaham, L. & Loya, Y. The Red Sea: Israel. in Mesophotic Coral Ecosystems (eds. Loya, Y., Puglise, K. A. & Bridge, T. C. L.) vol. 12, 199–214 (Springer International Publishing, 2019).60.Tamir, R., Eyal, G., Kramer, N., Laverick, J. H. & Loya, Y. Light environment drives the shallow‐to‐mesophotic coral community transition. Ecosphere 10 (2019).61.Fujii, T., Kitano, Y. F. & Tachikawa, H. New distributional records of three species of Euphylliidae (Cnidaria, Anthozoa, Hexacorallia, Scleractinia) from the Ryukyu Islands, Japan. Spec. Div. 25, 275–282 (2020).Article 

    Google Scholar 
    62.Longenecker, K., Roberts, T. E. & Colin, P. L. Papua New Guinea. in Mesophotic Coral Ecosystems (eds. Loya, Y., Puglise, K. A. & Bridge, T. C. L.) vol. 12 321–336 (Springer International Publishing, 2019).63.NOAA, [National Oceanic and Atmospheric Administration]. Endangered and threatened species; Critical habitat for the threatened Indo-Pacific corals. 85 FR 76262 (50 CFR Part 223 and 226) 76262–76299 (2020).64.Maragos, J. E., Hunter, C. L. & Meier, K. Z. Reefs and corals observed during the 1991–92 American Samoa coastal resources inventory. 50 (1994).65.Coles, S. et al. Introduced marine species in Pago Pago Harbor, Fagatele Bay and the National Park Coast, American Samoa. 182 (2003).66.Montgomery, A. D. et al. American Samoa. in Mesophotic Coral Ecosystems (eds. Loya, Y., Puglise, K. A. & Bridge, T. C. L.) vol. 12 387–407 (Springer International Publishing, 2019).67.Wallace, C. C. Staghorn corals of the world: A revision of the coral genus Acropora (Scleractinia; Astrocoeniina; Acroporidae) worldwide, with emphasis on morphology, phylogeny and biogeography. (Csiro Publishing, 1999).68.Hoeksema, B. W. Taxonomy, phylogeny and biogeography of mushroom corals (Scleractinina: Fungiidae). Zoologische Verhandelingen 254, 1–295 (1989).
    Google Scholar 
    69.World Register of Marine Species: WoRMS. Available online: http://www.marinespecies.org/. Accessed on 9/9/2020 (2020). https://doi.org/10.14284/170.70.Hsieh, T. C., Ma, K. H. & Chao, A. Interpolation and extrapolation for species diversity. (2020).71.Chao, A. et al. Rarefaction and extrapolation with Hill numbers: A framework for sampling and estimation in species diversity studies. Ecol. Monogr. 84, 45–67 (2014).Article 

    Google Scholar 
    72.Baselga, A. et al. Partitioning beta diversity into turnover and nestedness components ver. 1.5.2. (2020).73.Anderson, M. J., Gorley, R. N. & Clarke, K. R. PERMANOVA+ for Primer: Guide to software and statistical methods. 218 (2008).74.Clarke, K. R. & Gorley, R. N. Getting started with PRIMER 7. 18 http://updates.primer-e.com/primer7/manuals/Getting_started_with_PRIMER_7.pdf (2015).75.Gaston, K. What is rarity? in Rarity 1–21 (Chapman & Hall, 1994). More

  • in

    Past climate conditions predict the influence of nitrogen enrichment on the temperature sensitivity of soil respiration

    1.Bond-Lamberty, B. & Thomson, A. Temperature-associated increases in the global soil respiration record. Nature 464, 579–582 (2010).CAS 

    Google Scholar 
    2.Raich, J. W., Potter, C. S. & Bhagawati, D. Interannual variability in global soil respiration, 1980–94. Glob. Change Biol. 8, 800–812 (2002).
    Google Scholar 
    3.Davidson, E. A. & Janssens, I. A. Temperature sensitivity of soil carbon decomposition feedbacks to climate change. Nature 440, 165–173 (2006).CAS 

    Google Scholar 
    4.Feng, X., Simpson, A. J., Wilson, K. P., Williams, D. D. & Simpson, M. J. Increased cuticular carbon sequestration and lignin oxidation in response to soil warming. Nat. Geosci. 1, 836–839 (2008).CAS 

    Google Scholar 
    5.Heimann, H. & Reichstein, R. Terrestrial ecosystem carbon dynamics and climate feedbacks. Nature 451, 289–292 (2008).CAS 

    Google Scholar 
    6.Fang, C. et al. Impacts of warming and nitrogen addition on soil autotrophic and heterotrophic respiration in a semi-arid environment. Agr. Forest Meteorol. 248, 449–457 (2018).
    Google Scholar 
    7.Wang, Q., Liu, S., Wang, Y., Tian, P. & Sun, T. Influences of N deposition on soil microbial respiration and its temperature sensitivity depend on N type in a temperate forest. Agr. Forest Meteorol. 260–261, 240–246 (2018).
    Google Scholar 
    8.Zhong, Y. Q. W., Yan, W. M., Zong, Y. Z. & Shangguan, Z. P. The effects of nitrogen enrichment on soil CO2 fluxes depending on temperature and soil properties. Global Ecol. Biogeogr. 25, 475–488 (2016).
    Google Scholar 
    9.Yu, G. R. et al. Stabilization of atmospheric nitrogen deposition in China over the past decade. Nat. Geosci. 12, 424–429 (2019).CAS 

    Google Scholar 
    10.Coucheney, E., Strömgren, M., Lerch, T. Z. & Herrmann, A. M. Long-term fertilization of a boreal Norway spruce forest increases the temperature sensitivity of soil organic carbon mineralization. Ecol. Evol. 3, 5177–5188 (2013).
    Google Scholar 
    11.Jiang, J. S., Guo, S. L., Wang, R., Liu, Q. F. & Sun, Q. Q. Effects of nitrogen fertilization on soil respiration and temperature sensitivity in spring maize field in semi-arid regions on loess plateau. Environ. Sci. 36, 1802–1809 (2015).
    Google Scholar 
    12.Wang, Q., Zhao, X., Tian, P., Liu, S. & Sun, Z. Bioclimate and arbuscular mycorrhizal fungi regulate continental biogeographic variations in effect of nitrogen deposition on the temperature sensitivity of soil organic carbon decomposition. Land Degrad. Dev. 32, 936–945 (2021).
    Google Scholar 
    13.Schindlbacher, A., Zechmeister-Boltenstern, S. & Jandl, R. Carbon losses due to soil warming: do autotrophic and heterotrophic soil respiration respond equally? Glob. Change Biol. 15, 901–903 (2009).
    Google Scholar 
    14.Carey, J. C. et al. Temperature response of soil respiration largely unaltered with experimental warming. Proc. Natl Acad. Sci. 113, 13797–13802 (2016).CAS 

    Google Scholar 
    15.Lyu, M., Giardina, C. P. & Litton, C. M. Interannual variation in rainfall modulates temperature sensitivity of carbon allocation and flux in a tropical montane wet forest. Glob. Change Biol. 27, 3824–3836 (2021).
    Google Scholar 
    16.Wang, Q. et al. Global synthesis of temperature sensitivity of soil organic carbon decomposition: latitudinal patterns and mechanisms. Funct. Ecol. 33, 514–523 (2019).
    Google Scholar 
    17.Li, J. et al. Biogeographic variation in temperature sensitivity of decomposition in forest soils. Glob. Change Biol. 26, 1873–1885 (2020).
    Google Scholar 
    18.Delgado-Baquerizo, M. et al. Palaeoclimate explains a unique proportion of the global variation in soil bacterial communities. Nat. Ecol. Evol. 1, 1339–1347 (2017).
    Google Scholar 
    19.Delgado-Baquerizo, M. et al. Climate legacies drive global soil carbon stocks in terrestrial ecosystems. Sci. Adv. 3, e1602008 (2017).
    Google Scholar 
    20.Delgado-Baquerizo, M. et al. Ecological drivers of soil microbial diversity and soil biological networks in the southern hemisphere. Ecology 99, 583–596 (2018).
    Google Scholar 
    21.Ding, J. Y. & Eldridge, D. J. Contrasting global effects of woody plant removal on ecosystem structure, function and composition. Perspect. Plant Ecol. 39, 125460 (2019).
    Google Scholar 
    22.Eldridge, D. J. & Delgado-Baquerizo, M. The influence of climatic legacies on the distribution of dryland biocrust communities. Glob. Change Biol. 25, 327–336 (2019).
    Google Scholar 
    23.Pärtel, M., Chiarucci, A., Chytrý, M. & Pillar, V. D. Mapping plant community ecology. J. Veg. Sci. 26, 1–3 (2017).
    Google Scholar 
    24.Richter, D. D. & Yaalon, D. H. “The changing model of soil” revisited. Soil Sci. Soc. Am. J. 76, 766–778 (2012).CAS 

    Google Scholar 
    25.Lyons, S. K. et al. Holocene shifts in the assembly of plant and animal communities implicate human impacts. Nature 529, 80–83 (2016).
    Google Scholar 
    26.Schmidt, M. W. I. et al. Persistence of soil organic matter as an ecosystem property. Nature 478, 49–56 (2011).CAS 

    Google Scholar 
    27.Delgado-Baquerizo, M. et al. Carbon content and climate variability drive global soil bacterial diversity patterns. Ecol. Monogr. 86, 373–390 (2016).
    Google Scholar 
    28.Maestre, F. T., Delgado-Baquerizo, M., Jeffries, T. C., Eldridge, D. J. & Singh, B. K. Increasing aridity reduces soil microbial diversity and abundance in global drylands. Proc. Natl Acad. Sci. 112, 15684–15689 (2015).CAS 

    Google Scholar 
    29.Monger, C. et al. Legacy effects in linked ecological–soil–geomorphic systems of drylands. Front. Ecol. Environ. 13, 13–19 (2016).
    Google Scholar 
    30.Cox, P. M., Betts, R. A., Jones, C. D., Spall, S. A. & Totterdell, I. J. Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model. Nature 408, 184–187 (2000).CAS 

    Google Scholar 
    31.Fierer, N., Colman, B. P., Schimel, J. P. & Jackson, R. B. Predicting the temperature dependence of microbial respiration in soil: a continental-scale analysis. Glob. Biogeochem. Cy. 20, GB3026 (2006).
    Google Scholar 
    32.Peng, S., Piao, S., Wang, T., Sun, J. & Shen, Z. Temperature sensitivity of soil respiration in different ecosystems in China. Soil Biol. Biochem. 41, 1008–1014 (2009).CAS 

    Google Scholar 
    33.Xu, Z. et al. Temperature sensitivity of soil respiration in China’s forest ecosystems: patterns and controls. Appl. Soil Ecol. 93, 105–110 (2015).
    Google Scholar 
    34.Niu, B. et al. Warming homogenizes apparent temperature sensitivity of ecosystem respiration. Sci. Adv. 7, eabc7358 (2021).
    Google Scholar 
    35.Janssens, I. A. et al. Reduction of forest soil respiration in response to nitrogen deposition. Nat. Geosci. 3, 315–322 (2010).CAS 

    Google Scholar 
    36.Yan, G. Y. et al. Sequestration of atmospheric CO2 in boreal forest carbon pools in northeastern China: Effects of nitrogen deposition. Agr. Forest Meteorol. 248, 70–81 (2018).
    Google Scholar 
    37.Du, E. Z. et al. Global patterns of terrestrial nitrogen and phosphorus limitation. Nat. Geosci. 13, 221–226 (2020).CAS 

    Google Scholar 
    38.Chen, Z. M. et al. Nitrogen fertilization stimulated soil heterotrophic but not autotrophic respiration in cropland soils: A greater role of organic over inorganic fertilizer. Soil Biol. Biochem. 116, 253–264 (2018).CAS 

    Google Scholar 
    39.Chen, F. et al. Effects of N addition and precipitation reduction on soil respiration and its components in a temperate forest. Agr. Forest Meteorol. 271, 336–345 (2019).
    Google Scholar 
    40.Zhang, C. et al. Effects of simulated nitrogen deposition on soil respiration components and their temperature sensitivities in a semiarid grassland. Soil Biol. Biochem. 75, 113–123 (2014).CAS 

    Google Scholar 
    41.Moinet, G. Y. K. et al. The temperature sensitivity of soil organic matter decomposition is constrained by microbial access to substrates. Soil Biol. Biochem. 116, 333–339 (2018).CAS 

    Google Scholar 
    42.Li, Y. et al. Soil acid cations induced reduction in soil respiration under nitrogen enrichment and soil acidification. Sci. Total Environ. 615, 1535–1546 (2018).CAS 

    Google Scholar 
    43.Sanderman, J. Comment on “Climate legacies drive global soil carbon stocks in terrestrial ecosystems”. Sci. Adv. 4, e1701482 (2018).
    Google Scholar 
    44.Ding, J. et al. The paleoclimatic footprint in the soil carbon stock of the Tibetan permafrost region. Nat. Commun. 10, 4195 (2019).
    Google Scholar 
    45.Gershenson, A., Bader, N. E. & Cheng, W. X. Effects of substrate availability on the temperature sensitivity of soil organic matter decomposition. Glob. Change Biol. 15, 176–183 (2009).
    Google Scholar 
    46.Doetterl, S. et al. Soil carbon storage controlled by interactions between geochemistry and climate. Nat. Geosci. 8, 780–783 (2015).CAS 

    Google Scholar 
    47.Bellard, C., Bertelsmeier, C., Leadley, P., Thuiller, W. & Courchamp, F. Impacts of climate change on the future of biodiversity. Ecol. Lett. 15, 365–377 (2012).
    Google Scholar 
    48.Li, J., Ziegler, S. E., Lane, C. S. & Billings, S. A. Legacies of native climate regime govern responses of boreal soil microbes to litter stoichiometry and temperature. Soil Biol. Biochem. 66, 204–213 (2013).CAS 

    Google Scholar 
    49.Xu, M. et al. High microbial diversity stabilizes the responses of soil organic carbon decomposition to warming in the subsoil on the Tibetan Plateau. Glob. Chang. Biol. 27, 2061–2075 (2021).
    Google Scholar 
    50.Du, Y. et al. The response of soil respiration to precipitation change is asymmetric and differs between grasslands and forests. Glob. Chang. Biol. 26, 6015–6024 (2020).
    Google Scholar 
    51.Meier, I. C. & Leuschner, C. Leaf size and leaf area index in Fagus sylvatica forests: competing effects of precipitation, temperature, and nitrogen availability. Ecosystems 11, 655–669 (2008).CAS 

    Google Scholar 
    52.Li, J., Pei, J., Pendall, E., Fang, C. & Nie, M. Spatial heterogeneity of temperature sensitivity of soil respiration: A global analysis of field observations. Soil Biol. Biochem. 141, 107675 (2020).CAS 

    Google Scholar 
    53.Katz, M. H. Multivariable Analysis: A Practical Guide for Clinicians and Public Health Researchers (Cambridge Univ. Press, Cambridge, 2006).54.Leff, J. W. et al. Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proc. Natl Acad. Sci. 112, 10967–10972 (2015).CAS 

    Google Scholar 
    55.Grace, J. B. Structural Equation Modeling Natural Systems (Cambridge Univ. Press, Cambridge, 2006).56.Lefcheck, J. S. PiecewiseSEM: piecewise structural equation modelling in r for ecology, evolution, and systematics. Methods Ecol. Evol 7, 573–579 (2016).
    Google Scholar 
    57.Bates, D. et al. lme4: Linear mixed-effects models using Eigen and S4. R package version 1, 1–13 (2017).
    Google Scholar  More

  • in

    Large diatom bloom off the Antarctic Peninsula during cool conditions associated with the 2015/2016 El Niño

    Due to contrasts in oceanographic properties along the NAP24, the sampling grid was split in two subregions: north and south (Fig. 1; see “Methods”). The north and south subregions showed from the satellite data a much higher spring/summer (November–February) mean chlorophyll-a (Chl-a) in 2015/2016 than the decadal average time series (2010–2019; Table 1). In agreement with the El Niño effects10,16, the sea surface temperature (SST) and the air temperature showed substantially lower mean values during the spring/summer of 2015/2016 along the subregions (Table 1). However, there was an evident spatial/temporal variability in sea ice concentration/duration between the subregions, with a northward (southward) lower (higher) mean value during 2015/2016 in relation to the decadal average (Table 1). Along the south subregion during the spring/summer of 2015/2016, the increased Chl-a during January followed the decline in the sea ice concentration over the spring and early summer, concurrent with increased SST, which was markedly colder throughout the seasonal phytoplankton succession (Fig. 2a). These results to the south subregion are consistent with previous studies along the WAP, in which years characterized by longer sea ice cover in winter have led to higher phytoplankton biomass in the following summer associated with a more stable water column11,16,26. To the north subregion, however, although there was a similar pattern between Chl-a and SST, the increased Chl-a during January was not related with the sea ice retreat (Fig. 2b). Moreover, there was a clear difference between the Chl-a peaks (the highest Chl-a value reached) along the subregions from the satellite data. The Chl-a peak in the south subregion occurred in early January (10 January 2016, reaching 1.73 mg m–3), whereas in the north subregion the Chl-a peak was observed in late January (29 January 2016, reaching 2.23 mg m–3).Fig. 1: Study area.Location of hydrographic stations is marked by open circles (November), stars (January), and blue circles (February). The black dashed lines indicate the subregions (north and south) along the NAP and delimit the areas used to estimate average remote sensing measurements. The decadal-mean (2010–2019) remote sensing chlorophyll-a (Chl-a) is exhibited in the background, indicating the biomass (Chl-a) distribution of phytoplankton along the NAP in the last decade. An inset map in the lower right corner shows the location of the NAP within the Atlantic sector of the Southern Ocean.Full size imageTable 1 Biological production and ocean/atmosphere parameters by measurements of remote sensing and local meteorological stations during spring/summer in the NAP subregions.Full size tableFig. 2: Biological production and sea ice dynamics in the NAP seasonal phytoplankton succession of 2015/2016.Continuum remote sensing measurements of chlorophyll-a (Chl-a; solid green line), sea surface temperature (SST; solid blue line), and sea ice concentration (gray area) along the NAP, in south (a) and north (b) subregions during spring/summer of 2015/2016. The dashed green, blue and gray lines indicate the decadal average (2010–2019) of Chl-a, SST, and sea ice concentration, respectively. The solid light green lines represent the Chl-a interpolated values. The background shades show the in situ data sampling periods. It is important to note that Chl-a remote sensing data in Antarctic coastal waters are typically underestimated in respect to in situ Chl-a data (see Supplementary Fig. 1)12,29.Full size imageIt has been estimated that drifters entrained in the Gerlache Strait Current and the Bransfield Strait Current exit the Bransfield Strait in 10–20 days17, which is consistent with the interval of 19 days between both Chl-a peaks when considering the extreme distance between the subregions (see Fig. 1). These authors also estimated that drifters deployed in the Gerlache Strait Current were quickly advected out of the Gerlache Strait in less than 1 week (i.e., low residence time)17, which supports the similar diatom species assemblages identified in our microscopic analysis between stations of the Gerlache Strait and southwestern Bransfield Strait24. Therefore, it is plausible that phytoplankton growth in the north of the Gerlache Strait may be laterally advected northward into the Bransfield Strait, explaining the observed concomitant increase of satellite Chl-a data in both subregions from spring, associated with sea ice retreat southward (Fig. 2). In addition, as phytoplankton biomass tends to accumulate northward17,27,28, the advection processes could also explain the temporal and intensity differences of the Chl-a peaks along the subregions (see Fig. 2). This suggests that there was a link between the sea ice dynamics, phytoplankton biomass (Chl-a) and advection processes along the NAP during the spring/summer of 2015/2016, in which the sea ice melting first triggered an increase in phytoplankton biomass through water column stratification along the south subregion, and the advection processes led to a subsequent increase northward.The satellite Chl-a data require extensive validation with in situ data, especially in polar regions, where cloud cover is ubiquitous and performance is typically poor, due to not properly accurate Chl-a algorithms12,29. For that, although the mean Chl-a in 2015/2016 from the satellite data was approximately twice as large as the decadal average, there was a severe discrepancy in the mean Chl-a values observed between the in situ and remote sensing data (see Table 1 and Supplementary Table 1). This highlights the importance of the in situ dataset reported here, especially evident during February 2016, when the signal of an intense diatom bloom ( > 40 mg m–3 Chl-a)24 was not captured in the satellite data (Supplementary Fig. 1), supporting that phytoplankton biomass accumulation during this summer was much higher than recorded by remote sensing observations (see Table 1). In general, the in situ Chl-a achieved its maximum (40 mg m–3) and higher mean value (17.4 mg m–3) during February comparing to November and January (Supplementary Table 1).Phytoplankton community structure during the spring/summer of 2015/2016 was assessed through Chemical taxonomy (CHEMTAX) software, using accessory pigments versus in situ Chl-a concentrations measured via high-performance liquid chromatography (HPLC; see “Methods”). The main phytoplankton group over the season were diatoms, followed by haptophytes (Phaeocystis antarctica), cryptophytes, and dinoflagellates, according to the succession stage (Fig. 3a). Diatoms dominated the phytoplankton community composition in relation to the other groups along the whole in situ sampling period, although their relative biomass (to the total in situ Chl-a) was lower in some stations compared to others in different moments during spring/summer (Fig. 3a). To assess the degree to which the water column structure was a primary driver for development and intensity of diatom growth3,24, the mixed layer depth (MLD) and water column stability were calculated as a function of seawater potential density (see “Methods”). There was an inverse polynomial relationship between MLD and mean upper ocean stability (averaged over 5−150 m depth; hereafter referred to as upper ocean stability) (Fig. 3b). The significant positive exponential relationship between the upper ocean stability and diatom absolute concentrations (in situ Chl-a) demonstrates that stability, associated with MLD, was an important driver of diatom dynamics (Fig. 3b). This elucidates the increase in biological production during summer months of 2016, when upper ocean physical structures (MLD and stability) were sufficiently shallow and stable to produce the high phytoplankton biomass (in situ Chl-a) registered here. However, as MLD and stability showed similar values between summer months (Supplementary Table 1), only the upper ocean physical structures cannot be accounted for the high differences of in situ Chl-a values observed between diatom blooms in January (maximum of 12 mg m–3) and February (maximum of 40 mg m–3). Likewise, also not explaining these differences of in situ Chl-a values between summer months, macronutrients were highly abundant throughout the seasonal phytoplankton succession (Supplementary Table 1). Furthermore, although no measurements of dissolved iron, which can be considered as a limiting factor to primary productivity30, were carried out here, the Antarctic Peninsula continental shelves have been depicted as a substantial source of this micronutrient to the upper ocean, not limiting phytoplankton growth even during intense blooms31,32.Fig. 3: Phytoplankton community composition and upper ocean physical structures along the NAP seasonal phytoplankton succession of 2015/2016.a Relative biomass (to the total in situ chlorophyll-a; Chl-a) distribution of phytoplankton groups on surface, via HPLC/CHEMTAX analysis, during spring/summer of 2015/2016 along the NAP subregions. The black open circles indicate diatoms, the blue squares indicate Phaeocystis antarctica, the gray diamonds with crosses indicate cryptophytes, the green triangles indicate dinoflagellates, and the light gray open circles indicate green flagellates. b Exponential curve (R2 = 0.57; p 40% the community composition proportion in respect to the total Chl-a (considering the three fractionated size classes). Symbol color indicates the sampling month in respect to November (brown), January (gray), and February (black). The inset shows the polynomial inverse relationship (R2 = 0.51; p  70 µm in length; ref. 24), during January a large number ( > 2.5 × 106 cells L–1) of small ( More

  • in

    Include biodiversity representation indicators in area-based conservation targets

    1.Report of the Open-Ended Working Group on the Post-2020 Global Biodiversity Framework on its Third Meeting (Part I) CBD/WG2020/3/5 (CBD, 2021).2.Maxwell, S. L. et al. Nature 586, 217–227 (2020).CAS 
    Article 

    Google Scholar 
    3.Protected Planet Live Report 2021 (UNEP-WCMC, IUCN, NGS, 2021).4.Díaz, S. et al. Science 366, eaax3100 (2019).Article 

    Google Scholar 
    5.Visconti, P. et al. Science 364, 239–241 (2019).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    6.Maron, M. et al. Conserv. Lett. 14, e12816 (2021).Article 

    Google Scholar 
    7.Pressey, R. L. et al. Trends Ecol. Evol. 36, 808–821 (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    8.Global Assessment Report on Biodiversity and Ecosystem Services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Service (IPBES Secretariat, 2019).9.Living Planet Report 2020 (WWF, 2020).10.Jetz, W. et al. Nat. Ecol. Evol. 3, 539–551 (2019).Article 
    PubMed 

    Google Scholar 
    11.Powers, R. P. & Jetz, W. Nat. Clim. Change 9, 323–329 (2019).Article 

    Google Scholar 
    12.Wilson, E. O. Half-Earth: Our Planet’s Fight for Life (WW Norton & Company, 2016).13.Sala, E. et al. Nature 592, 397–402 (2021).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    14.Rinnan, D. S., Sica, Y., Ranipeta, A., Wilshire, J. & Jetz, W. Preprint at bioRxiv https://doi.org/10.1101/2020.02.05.936047 (2020).15.Beger, M. et al. Nat. Commun. 6, 8208 (2015).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    16.Armstrong, C. Conserv. Biol. 33, 554–560 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    17.Post-2020 Global Biodiversity Framework: Scientific and Technical Information to Support the Review of the Updated Goals and Targets, and Related Indicators and Baselines CBD/SBSTTA/24/3 (CBD, 2020).18.Moilanen, A., Wilson, K. A. & Possingham, H. Spatial Conservation Prioritization: Quantitative Methods and Computational Tools (Oxford Univ. Press, 2009).19.Jung, M. et al. Nat. Ecol. Evol. 5, 1499–1509 (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    20.Navarro, L. M. et al. Curr. Opin. Environ. Sustain. 29, 158–169 (2017).Article 

    Google Scholar 
    21.Jantke, K., Kuempel, C. D., McGowan, J., Chauvenet, A. L. M. & Possingham, H. P. Divers. Distrib. 25, 170–175 (2019).Article 

    Google Scholar 
    22.Bhola, N. et al. Conserv. Biol. 35, 168–178 (2021).Article 
    PubMed 

    Google Scholar 
    23.Hansen, A. J. et al. Conserv. Lett. 14, e12822 (2021).Article 

    Google Scholar 
    24.Measuring Ecosystem Integrity (Goal A) in the Post-2020 Global Biodiversity Framework: The Geo Bon Species Habitat Index CBD/WG2020/3/INF/6 (CBD Secretariat, 2021).25.Rondinini, C. & Visconti, P. Conserv. Biol. 29, 1028–1036 (2015).Article 

    Google Scholar 
    26.McGeoch, M. A. et al. Preprint at bioRxiv https://doi.org/10.1101/2021.08.26.457851 (2021).27.Hoskins, A. J. et al. Environ. Model. Softw. 132, 104806 (2020).Article 

    Google Scholar 
    28.Adams, V. M., Visconti, P., Graham, V. & Possingham, H. P. One Earth 4, 901–906 (2021).Article 

    Google Scholar 
    29.Heiner, M. et al. Conserv. Sci. Pract. 1, e110 (2019).
    Google Scholar  More

  • in

    Global warming and China’s crop pests

    1.Tian, H. et al. Proc. Natl Acad. Sci. USA 108, 14521–14526 (2011).ADS 
    CAS 
    Article 

    Google Scholar 
    2.Sugihara, G. Nature 378, 559–560 (1995).ADS 
    CAS 
    Article 

    Google Scholar 
    3.Bebber, D. P., Ramotowski, M. A. T. & Gurr, S. J. Nat. Clim. Change 3, 985–988 (2013).ADS 
    Article 

    Google Scholar 
    4.Bebber, D. P. et al. Glob. Change Biol. 25, 2703–2713 (2019).ADS 
    Article 

    Google Scholar 
    5.Wang, C. et al. Nat. Food https://doi.org/10.1038/s43016-021-00428-0 (2021).6.Pasiecznik, N. M. et al. EPPO Bull. 35, 1–7 (2005).Article 

    Google Scholar 
    7.Paini, D. R. et al. Proc. Natl Acad. Sci. USA 113, 7575–7579 (2016).CAS 
    Article 

    Google Scholar 
    8.Chaloner, T. M., Gurr, S. J. & Bebber, D. P. Nat. Clim. Change 11, 710–715 (2021).ADS 
    Article 

    Google Scholar 
    9.Deutsch, C. A. et al. Science 361, 916–919 (2018).ADS 
    CAS 
    Article 

    Google Scholar 
    10.Delgado-Baquerizo, M. et al. Nat. Clim. Change 10, 550–554 (2020).ADS 
    Article 

    Google Scholar 
    11.Wright, B. D. Appl. Econ. Perspect. Policy 33, 32–58 (2011).Article 

    Google Scholar  More

  • in

    Occurrence of crop pests and diseases has largely increased in China since 1970

    1.Foley, J. A. et al. Solutions for a cultivated planet. Nature 478, 337–342 (2011).ADS 
    CAS 

    Google Scholar 
    2.The Future of Food and Agriculture—Alternative Pathways to 2050 (Food and Agriculture Organization of the United Nations, 2018).3.Tilman, D., Balzer, C., Hill, J. & Befort, B. L. Global food demand and the sustainable intensification of agriculture. Proc. Natl Acad. Sci. USA 108, 20260–20264 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    4.Mueller, N. D. et al. Closing yield gaps through nutrient and water management. Nature 490, 254–257 (2012).ADS 
    CAS 

    Google Scholar 
    5.Zhang, W. et al. Closing yield gaps in China by empowering smallholder farmers. Nature 537, 671–674 (2016).ADS 
    CAS 

    Google Scholar 
    6.Chakraborty, S. & Newton, A. C. Climate change, plant diseases and food security: an overview. Plant Pathol. 60, 2–14 (2011).
    Google Scholar 
    7.Oerke, E. C. Crop losses to pests. J. Agri. Sci. 144, 31–43 (2005).
    Google Scholar 
    8.Bebber, D. P., Ramotowski, M. A. T. & Gurr, S. J. Crop pests and pathogens move polewards in a warming world. Nat. Clim. Change 3, 985–988 (2013).ADS 

    Google Scholar 
    9.Deutsch, C. A. et al. Increase in crop losses to insect pests in a warming climate. Science 361, 916–919 (2018).ADS 
    CAS 
    Article 

    Google Scholar 
    10.Delcour, I., Spanoghe, P. & Uyttendaele, M. Literature review: impact of climate change on pesticide use. Food Res. Int. 68, 7–15 (2015).
    Google Scholar 
    11.Ziska, L. H. Increasing minimum daily temperatures are associated with enhanced pesticide use in cultivated soybean along a latitudinal gradient in the mid-western United States. PLoS ONE 9, e98516 (2014).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    12.Lamichhane, J. R. et al. Robust cropping systems to tackle pests under climate change. A review. Agron. Sustain. Dev. 35, 443–459 (2014).
    Google Scholar 
    13.Bebber, D. P. et al. Many unreported crop pests and pathogens are probably already present. Glob. Change Biol. 25, 2703–2713 (2019).ADS 

    Google Scholar 
    14.Bale, J. S. et al. Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Glob. Change Biol. 8, 1–16 (2002).ADS 

    Google Scholar 
    15.Garrett, K. A., Dendy, S. P., Frank, E. E., Rouse, M. N. & Travers, S. E. Climate change effects on plant disease: genomes to ecosystems. Annu. Rev. Phytopathol. 44, 489–509 (2006).CAS 

    Google Scholar 
    16.Hruska, A. J. Fall armyworm (Spodoptera frugiperda) management by smallholders. CAB Rev. 14, 1–11 (2019).
    Google Scholar 
    17.Sutherst, R. W. et al. Adapting to crop pest and pathogen risks under a changing climate. Wiley Interdiscip. Rev. Clim. Change 2, 220–237 (2011).
    Google Scholar 
    18.Donatelli, M. et al. Modelling the impacts of pests and diseases on agricultural systems. Agric. Syst. 155, 213–224 (2017).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    19.Jones, J. W. et al. Toward a new generation of agricultural system data, models, and knowledge products: state of agricultural systems science. Agric. Syst. 155, 269–288 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    20.Miller, S. A., Beed, F. D. & Harmon, C. L. Plant disease diagnostic capabilities and networks. Annu. Rev. Phytopathol. 47, 15–38 (2009).CAS 

    Google Scholar 
    21.Bebber, D. P., Holmes, T., Smith, D. & Gurr, S. J. Economic and physical determinants of the global distributions of crop pests and pathogens. New Phytol. 202, 901–910 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    22.Savary, S. et al. The global burden of pathogens and pests on major food crops. Nat. Ecol. Evol. 3, 430–439 (2019).
    Google Scholar 
    23.An early warning news about the mirgating condition of Fall Armyworm in China from National Agro-Tech Extension and Service Center https://www.natesc.org.cn/News/des?id=eaf064ae-6582-47c1-a9f3-a58969fd47b3&kind=HYTX (in Chinese, available in Nov.2021).24.Piao, S. et al. The impacts of climate change on water resources and agriculture in China. Nature 467, 43–51 (2010).ADS 
    CAS 

    Google Scholar 
    25.Chown, S. L., Sorensen, J. G. & Terblanche, J. S. Water loss in insects: an environmental change perspective. J. Insect Physiol. 57, 1070–1084 (2011).CAS 

    Google Scholar 
    26.Bjorkman, A. D. et al. Plant functional trait change across a warming tundra biome. Nature 562, 57–62 (2018).ADS 
    CAS 

    Google Scholar 
    27.National Agricultural Technology Extension and Service Center. Technical Specification Manual of Major Crop Pest and Disease Observation and Forecast in China (China Agriculture Press, 2010).28.Olfert, O., Weiss, R. M. & Elliott, R. H. Bioclimatic approach to assessing the potential impact of climate change on wheat midge (Diptera: Cecidomyiidae) in North America. Can. Entomol. 148, 52–67 (2015).
    Google Scholar 
    29.Savary, S., Teng, P. S., Willocquet, L. & Nutter, F. W. Quantification and modeling of crop losses: a review of purposes. Annu. Rev. Phytopathol. 44, 89–112 (2006).CAS 

    Google Scholar 
    30.Chakraborty, S. Migrate or evolve: options for plant pathogens under climate change. Glob. Change Biol. 19, 1985–2000 (2013).ADS 

    Google Scholar 
    31.Deutsch, C. A. et al. Impacts of climate warming on terrestrial ectotherms across latitude. Proc. Natl Acad. Sci. USA 105, 6668–6672 (2008).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    32.Chaloner, T. M., Gurr, S. J. & Bebber, D. P. Plant pathogen infection risk tracks global crop yields under climate change. Nat. Clim. Change 11, 710–715 (2021).ADS 

    Google Scholar 
    33.Carvalho, J. L. N. et al. Agronomic and environmental implications of sugarcane straw removal: a major review. Glob. Change Biol. Bioenergy 9, 1181–1195 (2017).CAS 

    Google Scholar 
    34.Savary, S., Horgan, F., Willocquet, L. & Heong, K. L. A review of principles for sustainable pest management in rice. Crop Prot. 32, 54–63 (2012).
    Google Scholar 
    35.Frolking, S. et al. Combining remote sensing and ground census data to develop new maps of the distribution of rice agriculture in China. Glob. Biogeochem. Cycles 16, 38-31–38-10 (2002).
    Google Scholar 
    36.Harris, I., Jones, P. D., Osborn, T. J. & Lister, D. H. Updated high-resolution grids of monthly climatic observations—the CRU TS3.10 dataset. Int. J. Climatol. 34, 623–642 (2014).
    Google Scholar 
    37.Harvell, C. D. et al. Climate warming and disease risks for terrestrial and marine biota. Science 296, 2158–2162 (2002).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    38.Scherm, H. Climate change: can we predict the impacts on plant pathology and pest management? Can. J. Plant Pathol. 26, 267–273 (2004).
    Google Scholar 
    39.Cheke, R. A. & Tratalos, J. A. Migration, patchiness, and population processes illustrated by two migrant pests. Bioscience 57, 145–154 (2007).
    Google Scholar 
    40.Eyring, V. et al. Overview of the Coupled Model Intercomparison Project phase 6 (CMIP6) experimental design and organization. Geosci. Model Dev. 9, 1937–1958 (2016).ADS 

    Google Scholar 
    41.O’Neill, B. C. et al. The Scenario Model Intercomparison Project (ScenarioMIP) for CMIP6. Geosci. Model Dev. 9, 3461–3482 (2016).ADS 

    Google Scholar 
    42.van Vuuren, D. P. et al. The representative concentration pathways: an overview. Climatic Change 109, 5–31 (2011).ADS 

    Google Scholar 
    43.Lange, S. Trend-preserving bias adjustment and statistical downscaling with ISIMIP3BASD (v1.0). Geosci. Model Dev. 12, 3055–3070 (2019).ADS 

    Google Scholar 
    44.Gregory, P. J., Johnson, S. N., Newton, A. C. & Ingram, J. S. Integrating pests and pathogens into the climate change/food security debate. J. Exp. Bot. 60, 2827–2838 (2009).CAS 

    Google Scholar 
    45.Allen, R. G., Pereira, L. S., Raes, D. & Smith, M. Crop Evapotranspiration—Guidelines for Computing Crop Water Requirements FAO irrigation and drainage paper 56 (FAO, 1998).46.Harris, I., Osborn, T. J., Jones, P. & Lister, D. Version 4 of the CRU TS monthly high-resolution gridded multivariate climate dataset. Sci. Data 7, 109 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    47.Kahiluoto, H. et al. Decline in climate resilience of European wheat. Proc. Natl Acad. Sci. USA 116, 123–128 (2019).CAS 

    Google Scholar 
    48.Folke, C. et al. Regime shifts, resilience, and biodiversity in ecosystem management. Annu. Rev. Ecol. Evol. Syst. 35, 557–581 (2004).
    Google Scholar 
    49.Renard, D. & Tilman, D. National food production stabilized by crop diversity. Nature 571, 257–260 (2019).ADS 
    CAS 

    Google Scholar 
    50.Clark, J. S. Why environmental scientists are becoming Bayesians. Ecol. Lett. 8, 2–14 (2005).
    Google Scholar 
    51.Clark, J. S. & Gelfand, A. E. A future for models and data in environmental science. Trends Ecol. Evol. 21, 375–380 (2006).
    Google Scholar 
    52.Gelfand, A. E. & Smith, A. F. M. Sampling-based approaches to calculating marginal densities. J. Am. Stat. Assoc. 85, 398–409 (1990).MathSciNet 
    MATH 

    Google Scholar 
    53.Lunn, D., Spiegelhalter, D., Thomas, A. & Best, N. The BUGS project: evolution, critique and future directions. Stat. Med. 28, 3049–3067 (2009).MathSciNet 

    Google Scholar 
    54.Brooks, S. P. & Gelman, A. General methods for monitoring convergence of iterative simulations. J. Comput. Graph. Stat. 7, 434–455 (1998).MathSciNet 

    Google Scholar  More