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    Palau’s warmest reefs harbor thermally tolerant corals that thrive across different habitats

    Baker, A. C., Glynn, P. W. & Riegl, B. Climate change and coral reef bleaching: an ecological assessment of long-term impacts, recovery trends and future outlook. Estuar. Coast Shelf Sci. 80, 435–471 (2008).Article 

    Google Scholar 
    Hughes, T. P. et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359, 80–83 (2018).Article 
    CAS 

    Google Scholar 
    Normille, D. El Niño’s warmth devastating reefs worldwide. Science 352, 2015–2016 (2016).
    Google Scholar 
    Morikawa, M. K. & Palumbi, S. R. Using naturally occurring climate resilient corals to construct bleaching-resistant nurseries. Proc Natl Acad Sci USA 116, 10586–10591 (2019).Safaie, A. et al. High frequency temperature variability reduces the risk of coral bleaching. Nat. Commun. 9, 1671 (2018).Article 

    Google Scholar 
    Thomas, L. et al. Mechanisms of thermal tolerance in Reef-building corals across a fine-grained environmental mosaic: lessons from Ofu. Am. Samoa. Front Mar. Sci. 4, 434 (2018).Article 

    Google Scholar 
    Kenkel, C. D., Meyer, E. & Matz, M. V. Gene expression under chronic heat stress in populations of the mustard hill coral (Porites astreoides) from different thermal environments. Mol. Ecol. 22, 4322–4334 (2013).Article 
    CAS 

    Google Scholar 
    Gomulkiewicz, R. & Holt, R. D. When does evolution by natural selection prevent extinction? Evolution 49, 201–207 (1995).
    Google Scholar 
    Bruno, J. F., Siddon, C. E., Witman, J. D., Colin, P. L. & Toscano, M. A. El Niño related coral bleaching in Palau, western Caroline Islands. Coral Reefs 20, 127–136 (2001).Article 

    Google Scholar 
    Golbuu, Y. et al. Palau’s coral reefs show differential habitat recovery following the 1998-bleaching event. Coral Reefs 26, 319–332 (2007).Article 

    Google Scholar 
    van Woesik, R. et al. Climate-change refugia in the sheltered bays of Palau: analogs of future reefs. Ecol. Evol. 2, 2474–2484 (2012).Article 

    Google Scholar 
    Barkley, H. C. & Cohen, A. L. Skeletal records of community-level bleaching in Porites corals from Palau. Coral Reefs 35, 1407–1417 (2016).Article 

    Google Scholar 
    Gouezo, M. et al. Drivers of recovery and reassembly of coral reef communities. Proc. R. Soc. B Biol. Sci. 286, 20182908 (2019).Shamberger, K. E. F. et al. Diverse coral communities in naturally acidified waters of a Western Pacific reef. Geophys. Res. Lett. 41, 499–504 (2014).Article 

    Google Scholar 
    Barkley, H. C. et al. Changes in coral reef communities across a natural gradient in seawater pH. Sci. Adv. 1, e1500328 (2015).Article 

    Google Scholar 
    Fabricius, K. E., Mieog, J. C., Colin, P. L., Idip, D. & van Oppen, M. J. H. Identity and diversity of coral endosymbionts (zooxanthellae) from three Palauan reefs with contrasting bleaching, temperature and shading histories. Mol. Ecol. 13, 2445–2458 (2004).Article 
    CAS 

    Google Scholar 
    Anthony, K. R. N., Kline, D. I., Diaz-Pulido, G., Dove, S. & Hoegh-Guldberg, O. Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc. Natl Acad. Sci. USA 105, 17442–17446 (2008).Article 
    CAS 

    Google Scholar 
    Gibbin, E. M., Putnam, H. M., Gates, R. D., Nitschke, M. R. & Davy, S. K. Species-specific differences in thermal tolerance may define susceptibility to intracellular acidosis in reef corals. Mar. Biol. 162, 717–723 (2015).Article 
    CAS 

    Google Scholar 
    Boulay, J. N., Hellberg, M. E., Cortés, J. & Baums, I. B. Unrecognized coral species diversity masks differences in functional ecology. Proc. R. Soc. B Biol. Sci. 281, 20131580 (2013).Baums, I. B., Boulay, J. N., Polato, N. R. & Hellberg, M. E. No gene flow across the Eastern Pacific Barrier in the reef-building coral Porites lobata. Mol. Ecol. 21, 5418–5433 (2012).Article 

    Google Scholar 
    Forsman, Z. H., Wellington, G. M., Fox, G. E. & Toonen, R. J. Clues to unraveling the coral species problem: Distinguishing species from geographic variation in Porites across the Pacific with molecular markers and microskeletal traits. PeerJ 3, e751 (2015).Article 

    Google Scholar 
    Levas, S. J., Grottoli, A. G., Hughes, A., Osburn, C. L. & Matsui, Y. Physiological and biogeochemical traits of bleaching and recovery in the mounding species of coral Porites lobata: implications for resilience in mounding corals. PLoS ONE 8, e63267 (2013).Article 
    CAS 

    Google Scholar 
    Linsley, B. K. et al. Coral carbon isotope sensitivity to growth rate and water depth with Paleo-sea level implications. Nat. Commun. 10, 1–9 (2019).
    Google Scholar 
    Peyrot-Clausade, M., Hutchings, P. & Richard, G. Temporal variations of macroborers in massive Porites lobata on Moorea, French Polynesia. Coral Reefs 11, 161–166 (1992).Article 

    Google Scholar 
    Nanami, A. & Nishihira, M. Microhabitat association and temporal stability in reef fish assemblages on massive Porites microatolls. Ichthyol. Res. 51, 165–171 (2004).Article 

    Google Scholar 
    Cantin, N. E. & Lough, J. M. Surviving coral bleaching events: porites growth anomalies on the Great Barrier Reef. PLoS ONE 9, e88720 (2014).Article 

    Google Scholar 
    Carilli, J. E., Norris, R. D., Black, B., Walsh, S. M. & Mcfield, M. Century-scale records of coral growth rates indicate that local stressors reduce coral thermal tolerance threshold. Glob. Chang Biol. 16, 1247–1257 (2010).Article 

    Google Scholar 
    Cantin, N. E., Cohen, A. L., Karnauskas, K. B., Tarrant, A. M. & McCorkle, D. C. Ocean warming slows coral growth in the central Red Sea. Science 329, 322–325 (2010).Article 
    CAS 

    Google Scholar 
    Lough, J. M. & Cooper, T. F. New insights from coral growth band studies in an era of rapid environmental change. Earth Sci. Rev. 108, 170–184 (2011).Article 
    CAS 

    Google Scholar 
    Mollica, N. R. N. et al. Skeletal records of bleaching reveal different thermal thresholds of Pacific coral reef assemblages. Coral Reefs 38, 743–757 (2019).Article 

    Google Scholar 
    Barkley, H. C. et al. Repeat bleaching of a central Pacific coral reef over the past six decades (1960–2016). Commun. Biol. 1, 177 (2018).DeCarlo, T. M. & Cohen, A. L. Dissepiments, density bands and signatures of thermal stress in Porites skeletons. Coral Reefs 36, 749–761 (2017).Article 

    Google Scholar 
    DeCarlo, T. M. et al. Acclimatization of massive reef-building corals to consecutive heatwaves. Proc. R. Soc. B 286, 20190235 (2019).DeCarlo, T. M. The past century of coral bleaching in the Saudi Arabian central Red Sea. PeerJ 8, e10200 (2020).Article 

    Google Scholar 
    Silverstein, R. N., Cunning, R. & Baker, A. C. Change in algal symbiont communities after bleaching, not prior heat exposure, increases heat tolerance of reef corals. Glob. Chang Biol. 21, 236–249 (2015).Article 

    Google Scholar 
    Fabricius, K. E. Effects of irradiance, flow, and colony pigmentation on the temperature microenvironment around corals: Implications for coral bleaching? Limnol. Oceanogr. 51, 30–37 (2006).Article 

    Google Scholar 
    Edmunds, P. J., Putnam, H. M. & Gates, R. D. Photophysiological consequences of vertical stratification of Symbiodinium in tissue of the coral Porites lutea. Biol. Bull. 223, 226–235 (2012).Article 
    CAS 

    Google Scholar 
    Smith, L. W., Wirshing, H., Baker, A. C. & Birkeland, C. Environmental versus genetic influences on growth rates of the corals Pocillopora eydouxi and Porites lobata. Pac. Sci. 62, 57–69 (2008).Article 

    Google Scholar 
    Kenkel, C. D. & Bay, L. K. Exploring mechanisms that affect coral cooperation: symbiont transmission mode, cell density and community composition. PeerJ 2018, e6047 (2018).Article 

    Google Scholar 
    Sunde, J., Yıldırım, Y., Tibblin, P. & Forsman, A. Comparing the performance of microsatellites and RADseq in population genetic studies: analysis of data for Pike (Esox lucius) and a synthesis of previous studies. Front. Genet. 11, 218 (2020).Article 

    Google Scholar 
    Barkley, H. C., Cohen, A. L., McCorkle, D. C. & Golbuu, Y. Mechanisms and thresholds for pH tolerance in Palau corals. J. Exp. Mar. Biol. Ecol. 489, 7–14 (2017).Article 
    CAS 

    Google Scholar 
    Mollica, N. R. et al. Ocean acidification affects coral growth by reducing skeletal density. Proc. Natl Acad. Sci. USA 115, 1754–1759 (2018).Article 
    CAS 

    Google Scholar 
    DeCarlo, T. M. et al. Coral macrobioerosion is accelerated by ocean acidification and nutrients. Geology 43, 7–10 (2014).Article 

    Google Scholar 
    Manzello, D. P. et al. Role of host genetics and heat-tolerant algal symbionts in sustaining populations of the endangered coral Orbicella faveolata in the Florida Keys with ocean warming. Glob. Chang Biol. 25, 1016–1031 (2019).Article 

    Google Scholar 
    Rippe, J. P., Dixon, G., Fuller, Z. L., Liao, Y. & Matz, M. Environmental specialization and cryptic genetic divergence in two massive coral species from the Florida Keys Reef Tract. Mol. Ecol. 1–17 https://doi.org/10.1111/mec.15931 (2021).Schoepf, V. et al. Thermally variable, macrotidal Reef habitats promote rapid recovery from mass coral bleaching. Front. Mar. Sci. 7, 245 (2020).Article 

    Google Scholar 
    Dixon, G. B. et al. Genomic determinants of coral heat tolerance across latitudes. Science 348, 1460–1462 (2015).Article 
    CAS 

    Google Scholar 
    Baums, I. B. et al. Considerations for maximizing the adaptive potential of restored coral populations in the western Atlantic. Ecol. Appl. 29, 1–23 (2019).Article 

    Google Scholar 
    Gosselin, L. A. & Qian, P.-Y. Juvenile mortality in benthic marine invertebrates. Mar. Ecol. Prog. Ser. 146, 265–282 (1997).Article 

    Google Scholar 
    Gouezo, M. et al. Modelled larval supply predicts coral population recovery potential following disturbance. Mar. Ecol. Prog. Ser. 661, 127–145 (2021).Golbuu, Y., Gouezo, M., Kurihara, H., Rehm, L. & Wolanski, E. Long-term isolation and local adaptation in Palau’s Nikko Bay help corals thrive in acidic waters. Coral Reefs 35, 909–918 (2016).Article 

    Google Scholar 
    Golbuu, Y. et al. Predicting coral recruitment in Palau’s complex reef archipelago. PLoS ONE 7, e50998 (2012).Article 
    CAS 

    Google Scholar 
    Barshis, D. J., Birkeland, C., Toonen, R. J., Gates, R. D. & Stillman, J. H. High-frequency temperature variability mirrors fixed differences in thermal limits of the massive coral Porites lobata (Dana, 1846). J. Exp. Biol. jeb.188581 https://doi.org/10.1242/jeb.188581 (2018).Shamberger, K. E. F., Lentz, S. J. & Cohen, A. L. Low and variable ecosystem calcification in a coral reef lagoon under natural acidification. Limnol. Oceanogr. https://doi.org/10.1002/lno.10662 (2017).Cacciapaglia, C. & van Woesik, R. Climate-change refugia: shading reef corals by turbidity. Glob. Chang Biol. 22, 1145–1154 (2016).Article 

    Google Scholar 
    Anthony, K. R. Enhanced energy status of corals on coastal, high-turbidity reefs. Mar. Ecol. Prog. Ser. 319, 111–116 (2006).Article 

    Google Scholar 
    Houlbrèque, F. & Ferrier-Pagès, C. Heterotrophy in tropical scleractinian corals. Biol. Rev. Camb. Philos. Soc. 84, 1–17 (2009).Article 

    Google Scholar 
    Aichelman, H. E. et al. Heterotrophy mitigates the response of the temperate coral Oculina arbuscula to temperature stress. Ecol. Evol. 6, 6758–6769 (2016).Article 

    Google Scholar 
    Gómez‐Corrales, M. & Prada, C. Cryptic lineages respond differently to coral bleaching. Mol. Ecol. 0, 1–9 (2020).
    Google Scholar 
    Fifer, J. E., Yasuda, N., Yamakita, T., Bove, C. B. & Davies, S. W. Genetic divergence and range expansion in a western North Pacific coral. Sci. Total Environ. 152423 https://doi.org/10.1016/J.SCITOTENV.2021.152423 (2021).Euclide, P. T. et al. Attack of the PCR clones: rates of clonality have little effect on RAD-seq genotype calls. Mol. Ecol. Resour. 20, 66–78 (2020).Article 
    CAS 

    Google Scholar 
    Noonan, S. H. C., DiPerna, S., Hoogenboom, M. O. & Fabricius, K. E. Effects of variable daily light integrals and elevated CO2 on the adult and juvenile performance of two Acropora corals. Mar. Biol. 169, 1–15 (2022).Article 

    Google Scholar 
    Martins, C. P. P. et al. Growth response of reef-building corals to ocean acidification is mediated by interplay of taxon-specific physiological parameters. Front. Mar. Sci. 0, 879 (2022).
    Google Scholar 
    Bairos-Novak, K. R., Hoogenboom, M. O., van Oppen, M. J. H. & Connolly, S. R. Coral adaptation to climate change: meta-analysis reveals high heritability across multiple traits. Glob. Chang. Biol. 27, 5694–5710 (2021).Article 
    CAS 

    Google Scholar 
    Kenkel, C. D., Setta, S. P. & Matz, M. V. Heritable differences in fitness-related traits among populations of the mustard hill coral, Porites astreoides. Heredity 115, 509–516 (2015).Article 
    CAS 

    Google Scholar 
    Dziedzic, K. E., Elder, H., Tavalire, H. & Meyer, E. Heritable variation in bleaching responses and its functional genomic basis in reef-building corals (Orbicella faveolata). Mol. Ecol. 28, 2238–2253 (2019).Article 

    Google Scholar 
    Quigley, K. M., Bay, L. K. & Oppen, M. J. H. Genome‐wide SNP analysis reveals an increase in adaptive genetic variation through selective breeding of coral. Mol. Ecol. 2176–2188 https://doi.org/10.1111/mec.15482 (2020).Veron, J. E. N. Corals of the World (Australian Institute of Marine Science, 2000).Polato, N. R., Concepcion, G. T., Toonen, R. J. & Baums, I. B. Isolation by distance across the Hawaiian Archipelago in the reef-building coral Porites lobata. Mol. Ecol. 19, 4661–4677 (2010).Article 
    CAS 

    Google Scholar 
    Catchen, J., Hohenlohe, P. A., Bassham, S., Amores, A. & Cresko, W. A. Stacks: an analysis tool set for population genomics. Mol. Ecol. 22, 3124–3140 (2013).Article 

    Google Scholar 
    Puritz, J. B., Hollenbeck, C. M. & Gold, J. R. dDocent: a RADseq, variant-calling pipeline designed for population genomics of non-model organisms. PeerJ 2, e431 (2014).Article 

    Google Scholar 
    Li, W. & Godzik, A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658–1659 (2006).Article 
    CAS 

    Google Scholar 
    Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. ArXiv (2013).Garrison, E. & Marth, G. Haplotype-based variant detection from short-read sequencing. ArXiv (2012).Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156–2158 (2011).Article 
    CAS 

    Google Scholar 
    Kopelman, N. M., Mayzel, J., Jakobsson, M. & Rosenberg, N. A. CLUMPAK: a program for identifying clustering modes and packaging population structure inferences across K. Mol. Ecol. Resour. 15, 1179–1191 (2015).Article 
    CAS 

    Google Scholar 
    Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000).Article 
    CAS 

    Google Scholar 
    Evanno, G., Regnaut, S. & Goudet, J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14, 2611–2620 (2005).Article 
    CAS 

    Google Scholar 
    Puechmaille, S. J. The program STRUCTURE does not reliably recover the correct population structure when sampling is uneven: subsampling and new estimators alleviate the problem. Mol. Ecol. Resour. 16, 608–627 (2016).Article 

    Google Scholar 
    Jombart, T. & Ahmed, I. adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27, 3070–3071 (2011).Article 
    CAS 

    Google Scholar 
    Goudet, J. Hierfstat, a package for R to compute and test hierarchical F-statistics. Molecular Ecology Notes. 5, 184–186 (2005).Zeileis, A. & Grothendieck, G. zoo: S3 infrastructure for regular and irregular time series. J. Stat. Softw. 14, 1–27 (2005).Ryan, J. A. & Ulrich, J. M. xts: eXtensible Time Series. Package at https://cran.r-project.org/package=xts (2018).LaJeunesse, T. C. Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar. Biol. 141, 387–400 (2002).Article 

    Google Scholar 
    LaJeunesse, T. C. & Trench, R. K. Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biol. Bull. 199, 126–134 (2000).Article 
    CAS 

    Google Scholar  More

  • in

    An evolution towards scientific consensus for a sustainable ocean future

    IPCC. In IPCC Special Report on the Ocean and Cryosphere in a Changing Climate (IPCC, 2019).IOC-UNESCO. Global Ocean Science Report 2020-Charting Capacity for Ocean Sustainability (UNESCO Publishing, 2020).Sala, E. et al. Protecting the global ocean for biodiversity, food and climate. Nature 592, 397–402 (2021).Article 
    CAS 

    Google Scholar 
    Boyce, D. G., Lotze, H. K., Tittensor, D. P., Carozza, D. A. & Worm, B. Future ocean biomass losses may widen socioeconomic equity gaps. Nat. Commun. 11, 1–11 (2020).Article 

    Google Scholar 
    Foundation Prince Albert II of Monaco. “Which Knowledge for Which Sustainable Ocean Governance?” in Livre de restitution de la Monaco Ocean Week 2021 (2021).Swilling, M. et al. The Ocean Transition: What to learn from System Transitions (World Resources Institute, 2020).OECD. The Ocean Economy in 2016 (OECD Publishing, 2016).High Level Panel for a Sustainable Ocean Economy. Transformations for a Sustainable Ocean Economy – a vision for Protection, Production and Prosperity (2020).Landrigan, P. J. et al. Human health and ocean pollution. Ann. Global Health 86, 151 (2020).Article 

    Google Scholar 
    OECD. Development Co-operation Report 2016: the Sustainable Development Goals as Business Opportunities (OECD Publishing, 2016).OECD. Development Co-operation Report 2020: Learning from Crises, Building Resilience (OECD Publishing, 2020).Hoegh-Guldberg, O. et al. The Ocean as a Solution to Climate Change: Five Opportunities for Action. (World Resources Institute, 2019).Gattuso, J. P. et al. Ocean solutions to address climate change and its effects on marine ecosystems. Front. Mar. Sci. 5, 337 (2018).Article 

    Google Scholar 
    Heinze, C. et al. The quiet crossing of ocean tipping points. Proc. Natl Acad. Sci. USA 118, e2008478118 (2021).Article 
    CAS 

    Google Scholar 
    IPBES. Global Assessment Report on Biodiversity and Ecosystem Services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (eds. Brondizio, E. S., Settele, J., Díaz, S. & Ngo, H. T.) (IPBES Secretariat, 2019).IPCC. IPCC Special Report on the Ocean and Cryosphere in a Changing Climate (IPCC, 2019).Nash, K. L. et al. Planetary boundaries for a blue planet. Nat. Ecol. Evol. 1, 1625–1634 (2017).Article 

    Google Scholar 
    UN General Assembly. General Assembly Resolution Declaration of Principles Governing the Seabed and Ocean Floor. A/RES/25/2749. (1970).Brodie Rudolph, T. et al. A transition to sustainable ocean governance. Nat. Commun 11, 1–14 (2020).Article 

    Google Scholar 
    Claudet, J., Amon, D. J. & Blasiak, R. Opinion: transformational opportunities for an equitable ocean commons. Proc. Natl Acad. Sci. USA 118, e2117033118 (2021).Article 
    CAS 

    Google Scholar 
    Laffoley, D. et al. Evolving the narrative for protecting a rapidly changing ocean, post‐ COVID‐19. Aquatic Conserv. 31, 1512–1534 (2021).Article 
    CAS 

    Google Scholar 
    Folke, C. et al. Our future in the Anthropocene biosphere. Ambio 50, 834–869 (2021).Article 

    Google Scholar 
    Bennett, N. J. et al. Towards a sustainable and equitable blue economy. Nat. Sustain. 2, 991–993 (2019).Article 

    Google Scholar 
    United Nations General Assembly. Oceans and the law of the sea A/RES/72/73 (5 December 2017).De Santo, E. M. et al. Protecting biodiversity in areas beyond national jurisdiction: an earth system governance perspective. Earth Syst. Governance 2, 100029 (2019).Röckmann, C., van Leeuwen, J., Goldsborough, D., Kraan, M. & Piet, G. The interaction triangle as a tool for understanding stakeholder interactions in marine ecosystem based management. Mar. Pol. 52, 155–162 (2015).Article 

    Google Scholar 
    Kotzé, L. J. Fragmentation revisited in the context of global environmental law and governance. SALJ 131, 548–582 (2014).
    Google Scholar 
    Claudet, J. et al. A roadmap for using the UN decade of ocean science for sustainable development in support of science, policy, and action. One Earth 2, 34–42 (2020).Article 

    Google Scholar 
    Pörtner, H. O. et al. IPBES-IPCC Co-sponsored Workshop Report on Biodiversity and Climate Change (IPBES and IPCC, 2021).Picourt, L. et al. Swimming the Talk: How to Strengthen Collaboration and Synergies between the Climate and Biodiversity Conventions? (Ocean & Climate Platform, 2021).Valdes, L. The UN architecture for ocean science knowledge and governance. Chapter 18. In Handbook on the Economics and Management of Sustainable Oceans (eds. Paulo A.L.D. Nunes, P.A.L.D., Svensson, L. E. & Markandya, A. (Edward Elgar Publishing, 2017).Valdés, L. Mees, J. & Enevoldsen, H. International organizations supporting ocean science. In IOC-UNESCO, Global Ocean Science Report—The current status of ocean science around the world (eds. Valdés, L. et al.) 146–169 (UNESCO, 2017).Fawkes, K., Ferse, S., Scheffers, A. & Cummins, V. Learning from experience: what the emerging global marine assessment community can learn from the social processes of other global environmental assessments. Anthropocene Coasts 4, 87–114 (2021).Article 

    Google Scholar 
    Tessnow-von Wysocki, I. & Vadrot, A. B. M. The voice of science on marine biodiversity negotiations: a systematic literature review. Front. Mar. Sci. 7, 614282 (2020).Article 

    Google Scholar 
    Dalton, K. et al. Marine-related learning networks: shifting the paradigm toward collaborative ocean governance. Front. Mar. Sci. 7, 1–16 (2020).Article 

    Google Scholar 
    Gerbara, M. F. Understanding international bricolage. What drives behaviour change towards sustainable land use in the Eastern Amazon? Int. J. Commons 13, 1 (2019).
    Google Scholar 
    Jabbour, J. & Flachsland, C. 40 years of global environmental assessments: a retrospective analysis. Environ. Sci. Policy 77, 193–202 (2017).Article 

    Google Scholar 
    Messerli, P. et al. Expansion of sustainability science needed for the SDGs. Nat. Sustain. 2 10, 892–894 (2019).Article 

    Google Scholar 
    The Because the Ocean Initiative. Ocean for climate – Ocean-related measures in climate strategies (Nationally determined contributions, national adaptation plans, adaptation communications and national policy frameworks) (2019).Vieross, M. K. et al. Considering indigenous peoples and local communities in the governance of the global ocean commons. Mar. Pol. 119, 104039 (2020).Article 

    Google Scholar 
    Halpern, B. et al. Spatial and temporal changes in cumulative human impacts on the world’s ocean. Nat. Commun. 6, 1–7 (2015).Article 

    Google Scholar 
    Watson-Wright, W., & Valdes, J.L. Fragmented Governance of Our One Global Ocean. In The Future of Ocean Governance and Capacity Development – Essays in Honor of Elisabeth Mann Borgese (1918–2002) 16–22 (Brill, Nijhoff, 2019).United Nations Framework Convention on Climate Change. Chile Madrid Time for Action. FCCC/CO/2019/13.Add.1 Decision 1/CP (2020).Fawkes, K. & Cummins, V. Beneath the surface of the first world ocean assessment: an investigation into the global process’ support for sustainable development. Front. Mar. Sci. 6, 612 (2019).Article 

    Google Scholar 
    Bayliss-Brown, G., Cavaleri Gerhardinger, L. & Starger, C. Networked knowledge to action in support of ocean sustainability. Coast. Manage. 4, 4, 235–237 (2020).
    Google Scholar 
    Gerhardinger, L. C., Holzkämper, E., de Andrade, M. M., Corrêa, M. R. & Turra, A. Envisioning ocean governability transformations through network-based marine spatial planning. Marit. Stud. 21, 1, 131–152 (2022).Article 

    Google Scholar 
    Wyborn, C. et al. Imagining transformative biodiversity futures. Nat. Sustain. 3, 670–672 (2021).Article 

    Google Scholar 
    Jacobs, S. et al. Use your power for good: plural valuation of nature – the Oaxaca statement. Glob. Sustain. 3, e8 (2020).Article 

    Google Scholar 
    Herbst, D. F., Gerhardinger, L. C., Vila-Nova, D. A., de Carvalho, F. G. & Hanazaki, N. Integrated and deliberative multidimensional assessment of a subtropical coastal-marine ecosystem (Babitonga bay, Brazil). Ocean Coast. Manag. 196, 105279 (2020).Article 

    Google Scholar 
    McCrory, G., Holmén, J., Schäpke, N. & Holmberg, J. Sustainability-oriented labs in transitions: an empirically grounded typology. Environ. Innov. Soc. Transit. 43, 99–117 (2022).Article 

    Google Scholar 
    Gerhardinger, L. C., Andrade, M. M. de, Corrêa, M. R., & Turra, A. Crafting a sustainability transition experiment for the Brazilian blue economy. Mar. Pol. 120, 104157 (2020).Pereira, L., Sitas, N., Ravera, F., Jimenez-Aceituno, A. & Merrie, A. Building capacities for transformative change towards sustainability: imagaination in Intergovernmental Science-Policy Processes. Elem. Sci.Anth 7, 35 (2019).Article 

    Google Scholar 
    Flannery, W., Toonen, H., Jay, S. & Vince, J. A critical turn in marine spatial planning. Marit. Stud. 1987, 223–228 (2020).Article 

    Google Scholar 
    Clarke, J. & Flannery, W. The post-political nature of marine spatial planning and modalities for its re-politicisation. J. Envir. Policy Plan. 22 2, 170–183 (2020).Article 

    Google Scholar 
    von Schuckmann, K. et al. Copernicus marine service ocean state report 5th issue. J. Oper.Oceanogr. 14, 1–185 (2021).
    Google Scholar 
    Mercator International. Digital twin of the ocean. https://www.mercator-ocean.eu/en/digital-twin-ocean/ (2022).Geomar. Digital twin ocean. https://www.geomar.de/en/research/irf/digital-twin-ocean (2022).Creative Commons. https://creativecommons.org/licenses/ (2022).Orchid. Connecting research and researchers. https://orcid.org/#:~:text=ORCID%20provides%20a%20persistent%20digital,%2C%20peer%20review%2C%20and%20more (2022).Jasanoff, S. Technologies of humility. Nature 450, 33 (2007).Article 
    CAS 

    Google Scholar 
    Pörtner, H.-O. et al. Technical summary. In Climate Change 2022: Impacts, Adaptation, and Vulnerability. Contribution of Working Group II to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change (eds Pörtner, H.-O. et al.) (Cambridge Univ. Press, 2022).Pereira, L. M., Hichert, T., Hamann, M., Preiser, R. & Biggs, R. Using futures methods to create transformative spaces: visions of a good anthropocene in Southern Africa. Ecol. Soc. 23, 1, https://doi.org/10.5751/ES-09907-230119 (2018).Article 

    Google Scholar 
    TWI2050 Report. Transformations to Achieve the Sustainable Development Goals. Report prepared by World in 2050 Initiative. International Institute for Applied Systems Analysis (IIASA). www.twi2050.org (2018).Mitchell, R. B., Clark, W. C., Cash, D. W., & Dickson, N. M. Global Environmental Assessments: Information and Influence (MIT Press, 2016).Norström, A. V. et al. Principles for knowledge co-production in sustainability research. Nat. Sustain. 3, 182–190 (2020).Article 

    Google Scholar 
    Galland, G., Harrould-Kolieb, E. & Herr, D. The ocean and climate change policy. Clim. Pol. 12, 6, 764–771 (2012).Article 

    Google Scholar 
    Pereira, L. M. et al. Developing multiscale and integrative nature–people scenarios using the nature futures framework. People Nat. 2, 1172–1195 (2020).Article 

    Google Scholar 
    Evans, K. et al. Transferring complex scientific knowledge to useable products for society: the role of the global integrated ocean assessment and challenges in the effective delivery of ocean knowledge. Front. Environ. Sci 9, 626532 (2021).Article 

    Google Scholar 
    United Nations Ocean Conference. An international panel for ocean sustainability side event. (2022).Foundation Prince Albert II of Monaco. “Why an IPOS” in Livre de restitution de la Monaco Ocean Week 2022 (2022).Convention on Biodiversity. Open ended working group on the post 2020 global biodiversity framework. 3rd meeting. First Draft of the post-2020 global biodiversity framework (2021).Sitas, N. et al. Exploring the usefulness of scenario archetypes in science-policy processes: experience across IPBES assessments. Ecol. Soc. 24, 35 (2019).Article 

    Google Scholar 
    Laffoley, D. et al. The forgotten ocean: why COP26 must call for vastly greater ambition and urgency to address ocean change. Aquatic Conserv. 32, 1–12 (2021).
    Google Scholar 
    Martin, M. A. et al. Ten new insights in climate science 2021: a horizon scan. Glob.Sustain. 4, 1–20 (2021).Article 

    Google Scholar 
    Poli, R. Anticipation: what about turning the human and social sciences upside down? Futures 64, 15–18 (2014).Article 

    Google Scholar 
    Dasgupta, P. The Economics of Biodiversity: The Dasgupta Review (HM Treasury, 2021).Sumaila, U. R. et al. Financing a sustainable ocean economy. Nat. Commun. 12, 3259 (2021).Article 
    CAS 

    Google Scholar 
    Muiderman, K., Gupta, A., Vervoort, J. & Biermann, F. Four approaches to anticipatory climate governance: different conceptions of the future and implications for the present. WIREs Clim. Change 11, e673 (2020).Article 

    Google Scholar 
    Obermeister, N. Local knowledge, global ambitions: IPBES and the advent of multi-scale models and scenarios. Sustain. Sci. 14, 843–856 (2019).Article 

    Google Scholar 
    Vadrot, A., Rankovic, A., Lapeyre, R., Aubert, P. & Laurans, Y. Why are social sciences and humanitites needed in the workds of IPBES? A systematic review of the literature. Innovation 31, S78–S100 (2018).
    Google Scholar 
    Edenhofer, O. & Kowarsch, M. Cartography of pathways: a new model for environemntal policy assessments. Enviro.Sci.Policy 51, 56–64 (2015).Article 

    Google Scholar 
    Kowarsch, M. et al. An road map for global assessments. Nat. Clim. Change 7, 379–382 (2017).Article 

    Google Scholar 
    European Commission Press Release. International Ocean Governance: EU’s Contribution for Setting the Course of a Blue Planet. https://ec.europa.eu/commission/presscorner/detail/en/IP_22_3742 (2022).Seafood Business for Ocean Stewardship (SeaBOS). http://www.seabos.org/ (2022). More

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    The success of woody plant removal depends on encroachment stage and plant traits

    Deng, Y., Li, X., Shi, F. & Hu, X. Woody plant encroachment enhanced global vegetation greening and ecosystem water-use efficiency. Glob. Ecol. Biogeogr. 30, 2337–2353 (2021).Article 

    Google Scholar 
    Brandt, J., Haynes, M., Kuemmerle, T., Waller, D. & Radeloff, V. Regime shift on the roof of the world: alpine meadows converting to shrublands in the southern Himalayas. Biol. Conserv. 158, 116–127 (2013).Article 

    Google Scholar 
    García Criado, M., Myers-Smith, I. H., Bjorkman, A. D., Lehmann, C. E. R. & Stevens, N. Woody plant encroachment intensifies under climate change across tundra and savanna biomes. Glob. Ecol. Biogeogr. 29, 925–943 (2020).Article 

    Google Scholar 
    van Auken, O. Causes and consequences of woody plant encroachment into western North American grasslands. J. Environ. Manage. 90, 2931–2942 (2009).Article 
    CAS 

    Google Scholar 
    Bond, W. J., Midgley, G. F. & Woodward, F. I. The importance of low atmospheric CO2 and fire in promoting the spread of grasslands and savannas. Glob. Chang. Biol. 9, 973–982 (2010).Article 

    Google Scholar 
    D’Odorico, P., Okin, G. S. & Bestelmeyer, B. T. A synthetic review of feedbacks and drivers of shrub encroachment in arid grasslands. Ecohydrology 5, 520–530 (2012).Article 

    Google Scholar 
    Kulmatiski, A. & Beard, K. H. Woody plant encroachment facilitated by increased precipitation intensity. Nat. Clim. Change 3, 833–837 (2013).Article 
    CAS 

    Google Scholar 
    Eldridge, D. J. & Soliveres, S. Are shrubs really a sign of declining ecosystem function? Disentangling the myths and truths of woody encroachment in Australia. Aust. J. Bot. 62, 594–608 (2015).Article 

    Google Scholar 
    Domine, F., Barrere, M. & Morin, S. The growth of shrubs on high Arctic tundra at Bylot Island: impact on snow physical properties and permafrost thermal regime. Biogeosciences 13, 6471–6486 (2016).Article 

    Google Scholar 
    Maestre, F. T., Callaway, R. M., Valladares, F. & Lortie, C. J. Refining the stress-gradient hypothesis for competition and facilitation in plant communities. J. Ecol. 97, 199–205 (2009).Article 

    Google Scholar 
    Eldridge, D. J. et al. Impacts of shrub encroachment on ecosystem structure and functioning: towards a global synthesis. Ecol. Lett. 14, 709–722 (2011).Article 

    Google Scholar 
    Archer, S. R. & Predick, K. I. An ecosystem services perspective on brush management: research priorities for competing land-use objectives. J. Ecol. 102, 1394–1407 (2014).Article 

    Google Scholar 
    Eldridge, D. J. & Ding, J. Remove or retain: ecosystem effects of woody encroachment and removal are linked to plant structural and functional traits. N. Phytol. 229, 2637–2646 (2020).Article 

    Google Scholar 
    Albrecht, M. A., Becknell, R. E. & Long, Q. Habitat change in insular grasslands: woody encroachment alters the population dynamics of a rare ecotonal plant. Biol. Conserv. 196, 93–102 (2016).Article 

    Google Scholar 
    Stanton, R. A. et al. Shrub encroachment and vertebrate diversity: a global meta-analysis. Glob. Ecol. Biogeogr. 27, 368–379 (2017).Article 

    Google Scholar 
    Archer, S. R. et al. in Rangeland Systems: Processes, Management and Challenges (ed. Briske, D.) 25–84 (Springer, 2017).Anadón, J. D., Sala, O. E., Turner, B. L. & Bennett, E. M. Effect of woody-plant encroachment on livestock production in North and South America. Proc. Natl Acad. Sci. USA 111, 12948–12953 (2014).Article 

    Google Scholar 
    Maestre, F. T. et al. Structure and functioning of dryland ecosystems in a changing world. Annu. Rev. Eco. Evol. Syst. 47, 215–237 (2016).Article 

    Google Scholar 
    Teague, W. et al. Sustainable management strategies for mesquite rangeland: the Waggoner Kite project. Rangelands 19, 4–9 (1997).
    Google Scholar 
    Hamilton, W. T., McGinty, A., Ueckert, D. N., Hanselka, C. W. & Lee, M. R. Brush Management: Past, Present, Future (A&M Univ. Press, 2004).Bestelmeyer, B. T. et al. The grassland–shrubland regime shift in the southwestern United States: misconceptions and their implications for management. BioScience 68, 678–690 (2018).Article 

    Google Scholar 
    Ding, J. & Eldridge, D. J. Contrasting global effects of woody plant removal on ecosystem structure, function and composition. Perspect. Plant Ecol. Evol. Syst. 39, 125460 (2019).Article 

    Google Scholar 
    Huxman, T. E. et al. Ecohydrological implication of woody plant encroachment. Ecology 86, 308–319 (2005).Article 

    Google Scholar 
    Schmutz, E. M., Cable, D. R. & Warwick, J. J. Effect of shrub removal on the vegetation of a semidesert grass-shrub range. Rangel. Ecol. Manag. 12, 34–37 (1959).Article 

    Google Scholar 
    Noble, J. C. & Walker, P. Integrated shrub management in semi-arid woodlands of eastern Australia: a systems-based decision support model. Agric. Syst. 88, 332–359 (2006).Article 

    Google Scholar 
    Eldridge, D. J. et al. The pervasive and multifaceted influence of biocrusts on water in the world’s drylands. Glob. Chang. Biol. 26, 6003–6014 (2020).Article 

    Google Scholar 
    Bestelmeyer, B. T., Goolsby, D. P. & Archer, S. R. Spatial perspectives in state-and-transition models: a missing link to land management. J. Appl. Ecol. 48, 746–757 (2011).Article 

    Google Scholar 
    Riginos, C. & Young, T. P. Positive and negative effects of grass, cattle, and wild herbivores on Acacia saplings in an East African savanna. Oecologia 153, 985–995 (2007).Article 

    Google Scholar 
    Soliveres, S. et al. Plant diversity and ecosystem multifunctionality peak at intermediate levels of woody cover in global drylands. Glob. Ecol. Biogeogr. 23, 1408–1416 (2014).Article 

    Google Scholar 
    Soliveres, S. & Eldridge, D. J. Do changes in grazing pressure and the degree of shrub encroachment alter the effects of individual shrubs on understorey plant communities and soil function? Funct. Ecol. 28, 530–537 (2013).Article 

    Google Scholar 
    Maestre, F. T., Bowker, M. A., Puche, M., Hinojosa, M. B. & Escudero, A. Shrub encroachment can reverse desertification in semi-arid Mediterranean grasslands. Ecol. Lett. 12, 930–941 (2010).Article 

    Google Scholar 
    Abreu, R. C. R., Durigan, G., Melo, A. C. G., Pilon, N. A. L. & Hoffmann, W. A. Facilitation by isolated trees triggers woody encroachment and a biome shift at the savanna-forest transition. J. Appl. Ecol. 58, 2650–2660 (2021).Article 

    Google Scholar 
    North, M., Oakley, B., Fiegener, R. & Barbour, G. M. Influence of light and soil moisture on Sierran mixed-conifer understory communities. Plant Ecol. 177, 13–24 (2005).Article 

    Google Scholar 
    Muvengwi, J., Mbiba, M., Jimu, L., Mureva, A. & Dodzo, B. An assessment of the effectiveness of cut and ring barking as a method for control of invasive Acacia mearnsii in Nyanga National Park, Zimbabwe. For. Ecol. Manag. 427, 1–6 (2018).Article 

    Google Scholar 
    Abella, S. R. & Chiquoine, L. P. The good with the bad: when ecological restoration facilitates native and non-native species. Restor. Ecol. 27, 343–351 (2019).Article 

    Google Scholar 
    Bestelmeyer, B., Ward, J., Herrick, E. J. & Tugel, A. J. Fragmentation effects on soil aggregate stability in a patchy arid grassland. Rangel. Ecol. Manag. 59, 406–415 (2006).Article 

    Google Scholar 
    Okin, G. S., Gillette, D. A. & Herrick, J. E. Multi-scale controls on and consequences of aeolian processes in landscape change in arid and semi-arid environments. J. Arid. Environ. 65, 253–275 (2006).Article 

    Google Scholar 
    Hu, X., Li, X. Y., Zhao, Y., Gao, Z. & Zhao, S. J. Changes in soil microbial community during shrub encroachment process in the Inner Mongolia grassland of northern China. Catena 202, 105230 (2021).Article 
    CAS 

    Google Scholar 
    D’Odorico, P. et al. Positive feedback between microclimate and shrub encroachment in the northern Chihuahuan desert. Ecosphere 1, 1–11 (2010).Article 

    Google Scholar 
    Eldridge, D. J., Soliveres, S., Bowker, M. A. & Val, J. Grazing dampens the positive effects of shrub encroachment on ecosystem functions in a semi‐arid woodland. J. Appl. Ecol. 50, 1028–1038 (2013).Article 

    Google Scholar 
    Daryanto, S., Eldridge, D. J. & Throop, H. L. Managing semi-arid woodlands for carbon storage: grazing and shrub effects on above- and belowground carbon. Agric. Ecosyst. Environ. 169, 1–11 (2013).Article 

    Google Scholar 
    Paynter, Q. & Flanagan, G. J. Integrating herbicide and mechanical control treatments with fire and biological control to manage an invasive wetland shrub, Mimosa pigra. J. Appl. Ecol. 41, 615–629 (2004).Article 

    Google Scholar 
    Throop, H. L., Reichmann, L. G., Sala, O. E. & Archer, S. R. Response of dominant grass and shrub species to water manipulation: an ecophysiological basis for shrub invasion in a Chihuahuan Desert grassland. Oecologia 169, 373–383 (2012).Article 

    Google Scholar 
    Brantley, S. T. & Young, D. R. Shifts in litterfall and dominant nitrogen sources after expansion of shrub thickets. Oecologia 155, 337–345 (2008).Article 

    Google Scholar 
    Ding, J. & Eldridge, D. J. The fertile island effect varies with aridity and plant patch type across an extensive continental gradient. Plant Soil 459, 173–183 (2020).Article 

    Google Scholar 
    Mihoč, M. et al. Soil under nurse plants is always better than outside: a survey on soil amelioration by a complete guild of nurse plants across a long environmental gradient. Plant Soil 408, 31–41 (2016).Article 

    Google Scholar 
    Ochoa-Hueso, R. et al. Soil fungal abundance and plant functional traits drive fertile island formation in global drylands. J. Ecol. 106, 242–253 (2018).Article 
    CAS 

    Google Scholar 
    Soliveres, S., Eldridge, D. J., Hemmings, F. & Maestre, F. T. Nurse plant effects on plant species richness in drylands: the role of grazing, rainfall and species specificity. Perspect. Plant Ecol. Evol. Syst. 14, 402–410 (2012).Article 

    Google Scholar 
    Schlesinger, W. et al. Biological feedbacks in global desertification. Science 147, 1043–1048 (1990).Article 

    Google Scholar 
    Ding, J. & Eldridge, D. J. Climate and plants regulate the spatial variation in soil multifunctionality across a climatic gradient. Catena 201, 105233 (2021).Article 
    CAS 

    Google Scholar 
    Ding, J., Travers, S. K., Delgado-Baquerizo, M. & Eldridge, D. J. Multiple trade-offs regulate the effects of woody plant removal on biodiversity and ecosystem functions in global rangelands. Glob. Chang. Biol. 26, 709–720 (2020).Article 

    Google Scholar 
    De Soyza, A. G., Whitford, W. G., Martinez-Meza, E. & Van Zee, J. W. Variation in creosotebush (Larrea tridentata) canopy morphology in relation to habitat, soil fertility and associated annual plant communities. Am. Nat. 137, 13–26 (1997).Article 

    Google Scholar 
    Breemen, N. V. Nutrient cycling strategies. Plant Soil 168, 321–326 (1995).Li, J., Gilhooly, W. P. III., Okin, G. S. & Blackwell, J. III. Abiotic processes are insufficient for fertile island development: a 10-year artificial shrub experiment in a desert grassland. Geophys. Res. Lett. 44, 2245–2253 (2017).Article 

    Google Scholar 
    Ward, D. et al. Large shrubs increase soil nutrients in a semi-arid savanna. Geoderma 310, 153–162 (2018).Article 
    CAS 

    Google Scholar 
    Miwa, C. Persistence of Western Juniper Resource Islands following Canopy Removal. MSc thesis, Oregon State Univ. (2007).Zhou, L. et al. Shrub-encroachment induced alterations in input chemistry and soil microbial community affect topsoil organic carbon in an Inner Mongolian grassland. Biogeochemistry 136, 311–324 (2017).Article 
    CAS 

    Google Scholar 
    Kwok, A. B. C. & Eldridge, D. J. The influence of shrub species and fine-scale plant density on arthropods in a semiarid shrubland. Rangel. J. 38, 381–389 (2016).Article 

    Google Scholar 
    Young, J. A., Evans, R. A. & Rimbey, C. Weed control and revegetation following western juniper (Juniperus occidentalis) control. Weed Sci. 33, 513–517 (1985).Article 

    Google Scholar 
    Wiedemann, H. T. & Kelly, P. J. Turpentine (Eremophila sturtii) control by mechanical uprooting. Rangel. J. 23, 173–181 (2001).Article 

    Google Scholar 
    Bowker, M. A., Belnap, J., Chaudhary, V. B. & Johnson, N. C. Revisiting classic water erosion models in drylands: the strong impact of biological soil crusts. Soil Biol. Biochem. 40, 2309–2316 (2008).Article 
    CAS 

    Google Scholar 
    Ding, J. & Eldridge, D. J. Biotic and abiotic effects on biocrust cover vary with microsite along an extensive aridity gradient. Plant Soil 450, 429–441 (2020).Article 
    CAS 

    Google Scholar 
    Blaum, N., Seymour, C., Rossmanith, E., Schwager, M. & Jeltsch, F. Changes in arthropod diversity along a land use driven gradient of shrub cover in savanna rangelands: identification of suitable indicators. Biodivers. Conserv. 18, 1187–1199 (2009).Article 

    Google Scholar 
    Eldridge, D. J., Poore, A., Ruiz-Colmenero, M., Letnic, M. & Soliveres, S. Ecosystem structure, function and composition in rangelands are negatively affected by livestock grazing. Ecol. Appl. 26, 1273–1283 (2016).Article 

    Google Scholar 
    Maestre, F. T. & Cortina, J. Insights into ecosystem composition and function in a sequence of degraded semiarid steppes. Restor. Ecol. 12, 494–502 (2004).Article 

    Google Scholar 
    Nakagawa, S. in Ecological Statistics: Contemporary Theory and Application (eds Fox, G. A. et al.) Ch. 4 (Oxford Univ. Press, 2015).Fick, S. E. & Hijmans, R. J. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315 (2017).Article 

    Google Scholar 
    Zomer, R. J., Trabucco, A., Bossio, D. A. & Verchot, L. V. Climate change mitigation: a spatial analysis of global land suitability for clean development mechanism afforestation and reforestation. Agric. Ecosyst. Environ. 126, 67–80 (2008).Article 

    Google Scholar 
    Tavşanoğlu, Ç. & Pausas, J. G. A functional trait database for mediterranean basin plants. Sci. Data 5, 180135 (2018).Article 

    Google Scholar 
    The PLANTS Database (USDA, 2019); https://plants.usda.gov/Kattge, J. et al. TRY—a global database of plant traits. Glob. Chang. Biol. 17, 2905–2935 (2011).Article 

    Google Scholar 
    Hedges, L. V., Gurevitch, J. & Curtis, P. S. The meta-analysis of response ratios in experimental ecology. Ecology 80, 1150–1156 (1999).Article 

    Google Scholar 
    Mallen-Cooper, M. et al. Global synthesis reveals strong multifaceted effects of eucalypts on soils. Glob. Ecol. Biogeogr. 31, 1667–1678 (2022).Article 

    Google Scholar 
    Chen, X., Chen, H. Y. & Chang, S. X. Meta-analysis shows that plant mixtures increase soil phosphorus availability and plant productivity in diverse ecosystems. Nat. Ecol. Evol. 6, 1112–1121 (2022).Article 

    Google Scholar 
    Noble, D. W. A., Lagisz, M., O’dea, R. E. & Nakagawa, S. Nonindependence and sensitivity analyses in ecological and evolutionary meta-analyses. Mol. Ecol. 26, 2410–2425 (2017).Article 

    Google Scholar 
    Nakagawa, S. & Santos, E. Methodological issues and advances in biological meta-analysis. Ecol. Evol. 26, 1253–1274 (2012).Article 

    Google Scholar 
    Grace, J. B. Structural Equation Modeling and Natural Systems (Cambridge Univ. Press, 2006).Viechtbauer, W. Conducting meta-analyses in R with the metafor package. J. Stat. Softw. 36, 1–48 (2010).Article 

    Google Scholar 
    Archer, E. rfPermute v2.1.1 (R Foundation for Statistical Computing, 2010).Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2009).Stefan, V. & Levin, S. plotbiomes: plot Whittaker biomes with ggplot2 (R package version 0009001, 2021).Kahle, D. & Wickham, H. ggmap: spatial visualization with ggplot2. R. J. 5, 144–161 (2013).Article 

    Google Scholar 
    R Core Team. MOSR connections (R Foundation for Statistical Computing, 2013). More

  • in

    Global predictions for the risk of establishment of Pierce’s disease of grapevines

    Thermal requirements to develop PDWe examined the response of a wide spectrum of European grapevine varieties to XfPD infection in three independent experiments conducted in 2018, 2019, and 2020. Overall, 86.1% (n = 764) of 886 inoculated plants, comprising 36 varieties and 57 unique scion/rootstock combinations, developed PD symptoms 16 weeks after inoculation. European V. vinifera varieties exhibited significant differences in their susceptibility to XfPD (Supplementary Table S1). All varieties, however, showed PD symptoms to some extent, confirming previous field observations of general susceptibility to XfPD9,12,37. We also found significant differences in virulence (χ2 = 68.73, df = 1, P = 2.2 × 10−16) between two XfPD strains isolated from grapevines in Majorca across grapevine varieties (Supplementary Fig. S1). Full details on the results of the inoculation tests are available in “Methods”, Supplementary Note 1, Supplementary Table S1 and Supplementary Data 1.Growing degree days (GDD) have traditionally been used to describe and predict phenological events of plants and insect pests, but rarely in plant diseases58. We took advantage of data collated in the inoculation trials together with temperature to relate symptom development to the accumulated heat units at weeks eight, 10, 12, 14, and 16 after inoculation (Supplementary Data 1). Rather than counting GDDs linearly above a threshold temperature, we consider Xf ’s specific growth rate in vitro within its cardinal temperatures. The empirical growth rates come from the seminal work by Feil & Purcell38 shown in the inset of Fig. 1a. This Arrhenius plot was transformed, as explained in Supplementary Note 2A, to obtain a a piece-wise function f(T) Eq. (1). Our model and risk maps are based on f(T) (red line in Fig. 1a) because it provides the best fit to the experimental data when compared with the commonly used Beta function (blue line) for representing the thermal response in biological processes59,60. This Modified Growing Degree Day (MGDD) profile Eq. (1) enables to measure the thermal integral from hourly average temperatures, improving the prediction scale of the biological process61. MGDD also provides an excellent metric to link XfPD growth in culture with PD development as, once the pathogen is injected into the healthy vine, symptoms progression mainly depends upon the bacterial load (i.e., multiplication) and the movement through the xylem vessel network, which are fundamentally temperature-dependent processes38,62. Moreover, MGDD can be mathematically related to the exponential or logistic growth of the pathogen within the plant (Supplementary Note 2B).Fig. 1: Climatic and transmission layers composing the epidemiological model.a MGDD profile fitted to the in vitro data of Xf growth rate in Feil & Purcell 200138. The original Arrhenius plot in Kelvin degrees (inset) was converted to Celsius, as explained in (Supplementary Note 2A), to obtain the fit shown in the main plot red line; the blue line represents the fit with a Beta function. b Correlation between CDD and the average ({T}_{min }) of the coldest month between 1981 and 2019. Plotted black dots (worldwide) and yellow dots (main wine-producing zones) depict climatic data from 6,487,200 cells at 0.1∘ × 0.1∘ resolution, spread globally and retrieved from ERA5-Land dataset. The red solid line depicts the fitted exponential function for worldwide data and the blue solid line for main vineyard zones. c Nonlinear relationship between MGDD (red line) and CDD (blue line) and the likelihood of developing chronic infections. Black dots depict the cumulative proportion of grapevine plants in the population of 36 inoculated varieties showing five or more symptomatic leaves at each of the 15 MGDD levels (see Supplementary Information). Vertical bars are the 95% CI. d Combined ranges of MGDD and CDD on the likelihood of developing chronic infection. e Transmission layer in the dynamic equation (1) of the SIR compartmental model. f Relationship between the exponential growth of the number of infected plants with the risk index and their ranks.Full size imageInterannual infection survival in grapevines plays a relevant role when modelling PD epidemiology. In our model, we assumed a threshold of five or more symptomatic leaves for these chronic infections based on the relationship between the timing and severity of the infection during the growing season and the likelihood of winter recovery38,39,42. This five-leaf cut-off was grounded on: (i) the bimodal distribution in the frequency of the number of symptomatic leaves among the population of inoculated grapevines (Supplementary Fig. S1), whereby vines that generally show less than five symptomatic leaves at 12 weeks after inoculation remain so in the following weeks, while those that pass that threshold continue to produce symptomatic leaves, and (ii) the observed correlation between the acropetal and basipetal movement of Xf along the cane (Supplementary Fig. S1). The likelihood of developing chronic infections as a function of accumulated MGDD among the population of grapevine varieties was modelled using survival analysis with data fitted to a logistic distribution ({{{{{{{mathcal{F}}}}}}}}({{{{{rm{MGDD}}}}}})). A minimum window of MGDD = 528 was needed to develop chronic infections (var. Tempranillo), about 975 for a median estimate, while a cumulative MGDD  > 1159 indicate over 90% probability within a growing season (red curve in Fig. 1c and “Methods”).Next, we intended to model the probability of disease recovery by exposure to cold temperatures. Previous works had specifically modelled cold curing on Pinot Noir and Cabernet Sauvignon varieties in California as the effect of temperature and duration39 by assuming a progressive elimination of the bacterial load with cold temperatures42. In the absence of appropriate empirical data to formulate a general average pattern of winter curing among grapevine varieties, we combined the approach of Lieth et al.39 and the empirical observations of Purcell on the distribution of PD in the US related to the average minimum temperature of the coldest month, Tmin, isolines41. To consider the accumulation of cold units in an analogy of the MGDD, we searched for a general correlation between Tmin and the cold degree days (CDDs) with base temperature = 6 ∘C (see “Methods”). We found an exponential relation, ({{{{{rm{CDD}}}}}} sim 230exp (-0.26cdot {T}_{min })), where specifically, CDD ≳ 306 correspond to ({T}_{min } < -1.{1},^{circ }{{{{{rm{C}}}}}}) (Fig. 1b). To transform this exponential relationship to a probabilistic function analogous to ({{{{{{{mathcal{F}}}}}}}}({{{{{rm{MGDD}}}}}})), hereafter denoted ({{{{{{{mathcal{G}}}}}}}}({{{{{rm{CDD}}}}}})), ranging between 0 and 1, we considered the sigmoidal family of functions (f(x)=frac{A}{B+{x}^{C}}) with A = 9 × 106, B = A and C = 3 (Fig. 1c), fulfilling the limit ({{{{{{{mathcal{G}}}}}}}}({{{{{rm{CDD}}}}}}=0)=1), i.e., no winter curing when no cold accumulated, and a conservative 75% of the infected plants recovered at ({T}_{min }=-1.{1},^{circ }{{{{{rm{C}}}}}}) instead of 100% to reflect uncertainties on the effect of winter curing.MGDD/CDD distribution mapsMGDD were used to compute annual risk maps of developing PD during summer for the period 1981–2019 (see “Methods”). The resulting averaged map identifies all known areas with a recent history of severe PD in the US corresponding to ({{{{{{{mathcal{F}}}}}}}}({{{{{rm{MGDD}}}}}}) , > , 90 %) (i.e., high-risk), such as the Gulf Coast states (Texas, Alabama, Mississippi, Louisiana, Florida), Georgia and Southern California sites (e.g., Temecula Valley) (Fig. 2a), while captures areas with a steep gradation of disease endemicity in the north coast of California (({{{{{{{mathcal{F}}}}}}}}({{{{{rm{MGDD}}}}}} , > , 50 % )). Overall, more than 95% of confirmed PD sites (n = 155) in the US (Supplementary Data 2) fall in grid cells with ({{{{{{{mathcal{F}}}}}}}}({{{{{rm{MGDD}}}}}}) , > , 50 %).Fig. 2: Average thermal-dependent maps for Pierce’s disease (PD) development and recovery in North America and Europe.PD development during the growing season based on average ({{{{{{{mathcal{F}}}}}}}}({{{{{rm{MGDD}}}}}})) estimations between 1981 and 2019 in North America (a) and Europe (b) derived from the results of the inoculation experiments on 36 grapevine varieties. Large differences in the areal extension with favourable MGDDs can be observed between the US and Europe. The winter curing effect is reflected in the distribution of the average ({{{{{{{mathcal{G}}}}}}}}({{{{{rm{CDD}}}}}})) for the 1981–2019 period in the United States (c) and Europe (d). A snapshot of the temperature-driven probability of chronic infection averaged for the 1981–2019 period is obtained from the joint effect of MGDD and CDD in North America (e) and Europe (f). Warmer colours indicate more favourable conditions for chronic PD and the dashed line highlights the threshold of chronic infection probability being 0.5.Full size imageThe average MGDD-projected map for Europe during 1981–2019 spots a high risk for the coast, islands and major river valleys of the Mediterranean Basin, southern Spain, the Atlantic coast from Gibraltar to Oporto, and continental areas of central and southeast Europe (Fig. 2b). Of these, however, only some Mediterranean islands, such as Cyprus and Crete, show ({{{{{{{mathcal{F}}}}}}}}({{{{{rm{MGDD}}}}}}) , > , 99 %) comparable to areas with high disease incidence in the Gulf Coast states of the US and California. Almost all the Atlantic coast from Oporto (Portugal) to Denmark are below suitable MGDD, with an important exception in the Garonne river basin in France (Bordeaux Area) with low to moderate MGDD (Fig. 2b).Figure 2a shows how the area with high-risk MGDD values extends further north of the current known PD distribution in the southeastern US, suggesting that winter temperatures limit the expansion of PD northwards9. A comparison between MGDD and CDD maps (Fig. 2a vs. Fig. 2c, Fig. 2e) further supports the idea that winter curing is restricting PD northward migration from the southeastern US. However, consistent with growing concern among Midwest states winegrowers on PD northward migration led by climate change63, we found a mean increase of 0.12% y−1 in the areal extent with CDD  0.075) in 22.3% of the vineyards in Europe. However, no vineyard is in epidemic-risk zones with a high-risk index and only 2.9% of the vineyard surface is at moderate risk (Supplementary Table S8). The areas with the highest risk index (r(t) between 0.70 and 0.88) are mainly located in the Mediterranean islands of Crete, Cyprus and the Balearic Islands or at pronounced peninsulas like Apulia (Italy) and Peloponnese (Greece) in the continent (Fig. 6a and Supplementary Table S8). Most vineyards are in non-risk zones (42.1%), whereas 35.6% are located in transition zones with presently non-risk but where XfPD could become established in the next decades causing some sporadic outbreaks. In Supplementary Data 4 and Supplementary Table S8, we provide full details of the total vineyard areas currently at risk for each country and region.Fig. 6: Intersection between Corine-land-cover vineyard distribution map and PD-risk maps for 2020 and 2050.Data were obtained from Corine-land-cover (2018) and the layer of climatic suitability forP. spumarius in Europe from35. The surface of the vineyard contour has been enlarged to improve the visualisation of the risk zones and disease-incidence growth-rate ranks. a PD risk map for 2019 and its projection for 2050 (b). Blue colours represent non-risk zones and transient risk zones for chronic PD (R0  More

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    Quantification of biological nitrogen fixation by Mo-independent complementary nitrogenases in environmental samples with low nitrogen fixation activity

    Direct injection method for ethylene and acetylene δ13C analyses by GC-C-IRMSFollowing the direct injection approach of classical ISARA12 with a few modifications, ARA samples with high ethylene yield ( > 500 ppmv) in 10% v/v acetylene were manually injected into a Thermo Scientific Trace GC Ultra-Isolink with an Agilent HP-PLOT/Q  capillary GC column (30 m, i.d. = 0.32 mm, f.t. = 20 μm) and a combustion reactor connected to a Thermo Scientific Delta V Plus isotope ratio mass spectrometer (GC-C-IRMS; Fig. 1a). Modifications include the replacement of silver ferrules in the GC oven with Valcon polymide (graphite reinforced polymer) ferrules to limit memory effects from acetylene. The combustion reactor was oxidized with pure oxygen for 1 h before each run and brief (15 min) seed oxidations were performed between measurement batches (i.e., required every ~ 6–8 ethylene injections, ~ 4–6 acetylene injections) to regenerate reactor oxidation capacity and minimize drift of δ13C values. See Supplementary Table S1a online for additional instrument settings.Ethylene Pre-Concentration (EPCon) methodARA samples with  More

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    Soil fertility analysis in the Republic of Bashkortostan

    Soil studies were carried out on 115,896.2 hectares of agricultural lands in fifteen villages of the municipal district obtained by subtracting from the available area of the village industrial lands, populated areas, forest plots occupied by water, etc.As a result of the land reform and redistribution of land for various purposes for the period from 1972 to 2021, the area of agricultural land decreased by 12.7% compared to the data of the previous survey.In the research area, the largest territories are occupied by black soils, which amount to 52,826.24 ha, including bleached soils—42,605.9 ha, alkaline – 6983.8 ha and shortened – 3236.54 ha. Slightly inferior to the black soils are dark gray forest soils with an area of 37,043.63 hectares, alluvial—12,287.4 hectares, gray forest—6371.96 hectares and forest soils of a rooted profile – 5058.94 hectares. The share of sod-carbonate soils accounts for 7792.7 hectares of land, which is 6.2%. The gradation did not include the soils of the ravine-beam complex, sand and gravel masses, existing ravines and disturbed lands, and quarries that occupy 5,452.4 hectares of territory (4.3%).One of the important indicators of soils, especially used in agricultural production, is the humus state. Thus, over 49 years there has been a slight decrease in the area under obese (high-humus) soils in the hectare ratio, due to a general decrease in the area of farmland, but in the context of the security group, they have increased by 1.3% (Table 1). The remaining levels of security have remained almost at the same level. The increase in the amount of fat chernozems was facilitated by the withdrawal of arable land from circulation and their transfer to perennial plantations. Earlier researches conducted on experimental fields of the Bashkir State Agrarian University identified and revealed changes in the quantitative and qualitative composition of organic matter from 15 to 30% when introducing a land plot for arable land26. To preserve and improve soil fertility, it is recommended to carry out a complex of agrotechnical, agrochemical and reclamation measures and the use of various meliorants, organic and mineral fertilizers27.Studies of the capacity of the humus horizon have shown that low–sized soils have become the most widespread—69,660.2 hectares or 60.1% of the total area of agricultural land (Fig. 2). A smaller area is occupied by medium-sized soils – 38,128.7 hectares (32.9%), not included in the gradation – 8107.3 hectares or 7.0%, respectively. It should be noted that the specific gravity of the soil of the ravine-beam complex, sand and gravel masses, active ravines and disturbed lands, and quarries increased by 2.5%.Figure 2Distribution of soils by humus horizon thickness by region.Full size imageThe granulometric composition of the soil is also of great agronomic importance28. Physical, physico-chemical, physico-mechanical properties and water, air, and nutrient regimes of soils depend on it29,30. In the Salavatskiy district there were practically no changes in soil areas in terms of granulometric composition, mainly clay soil varieties predominate. According to the mechanical composition of the soil there were distributed as follows: light clay – 71,807.38 ha or 62% (in 1972, 86,375 ha or 65.1%) of the total area of agricultural land and heavy loamy – 34,745.24 ha (30%) (in 1972—39,614 ha or 29.8%). The share of medium-loamy varieties accounts for 0.8% (in 1972—0.84%) (Fig. 3).Figure 3Distribution of Salavatskiy district soil areas by granulometric composition, %.Full size imageThe gradation did not include 8362.27 hectares of land. Heavy loamy, medium clay, sandy loam and sandy soils have not been identified.All arable soils of the analyzed territory are slightly susceptible to erosion processes, the processes of water and, to a lesser extent, wind erosion have developed. 67,445.21 hectares of land, or 58.2% (in 1972, 77,702 hectares) of the total area of agricultural lands are occupied under lightly washed soils, the share of medium and heavily washed accounts for 3.9% and 0.1%, respectively. Unwashed soils are distributed on 36,985.46 hectares (31.9%) (Table 2).Table 2 Soil areas by category of erosion feature (Salavatskiy district of the Republic of Bashkortostan).Full size tableAccording to the results of the field research and laboratory agrochemical analyses of soils, land refinements related to agricultural land were carried out. The basis for correcting and digitizing the contours of soil varieties were in the maps made in 1972 (Fig. 4).Figure 4Soil map within the boundaries of the Salavatskiy district of the Republic of Bashkortostan, 1972.Full size imageDigitization included scanning the topographic basis, then assigning coordinates to a raster image, decrypting and digitizing orthophotos (Fig. 5).Figure 5Orthophotoplan within the boundaries of the Salavatskiy district of the Republic of Bashkortostan, 2007.Full size imageAfter the carried-out activities, a soil map was obtained in the digital format of the Mapinfo program, after which it was converted into a raster basis with reference to the local coordinate system MSK 02 zone 1. The digitization of the 1972 soil map was carried out manually by outlining the contours of the topographic base and the scanned map.During digitization, information partially lost due to its wear and distortion during scanning was restored. A necessary condition is the use of the originals of the soil maps of the previous survey (1972).As a planned basis on which the created layers can be opened and information on soils can be obtained, a raster basis was ordinated into a local coordinate system (Fig. 6).Figure 6Completed soil map within the boundaries of the Salavat district of the Republic of Belarus, 2021.Full size imageThe result of the conducted research is the developed electronic digital soil map of the municipal district of Salavatskiy district which unites 15 rural settlements. The electronic soil map is presented in the form of a complex of electronic layers with the names of the type and subtype of soils, soil variety, mechanical or granulometric composition, soil-forming and underlying rocks. It also includes indicators of organic carbon, humus, mobile phosphorus, exchangeable potassium, soil acidity by pH value and the capacity of the humus-accumulative horizon. More

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    Evolution of self-organised division of labour driven by stigmergy in leaf-cutter ants

    Wilson, E. O. Success and dominance in ecosystems: the case of the social insects. Vol. 2 I-XXI (Ecology Institute, 1990).Anderson, C., Franks, N. R. & McShea, D. W. The complexity and hierarchical structure of tasks in insect societies. Anim. Behav. 62, 643–651. https://doi.org/10.1006/anbe.2001.1795 (2001).Article 

    Google Scholar 
    Theraulaz, G. & Deneubourg, J.-L. in The Ethological roots of Culture (eds Gardner RA, Chiarelli AB, Gardner BT, & Ploojd FX) 1–19 (Kluwer Academic Publishers, 1994).Theraulaz, G. & Bonabeau, E. Modelling the collective building of complex architectures in social insects with lattice swarms. J. Theor. Biol. 177, 381–400. https://doi.org/10.1006/jtbi.1995.0255 (1995).Article 
    ADS 

    Google Scholar 
    Bonabeau, E., Theraulaz, G., Deneubourg, J.-L., Aron, S. & Camazine, S. Self-organization in social insects. Trends Ecol. Evol. 12, 188–193 (1997).Article 

    Google Scholar 
    Gordon, D. M. The organization of work in social insect colonies. Nature 380, 121–124 (1996).Article 
    ADS 

    Google Scholar 
    Gordon, D. M. The evolution of the algorithms for collective behavior. Cell Syst. 3, 514–520 (2016).Article 

    Google Scholar 
    Grüter, C. et al. Negative feedback enables fast and flexible collective decision-making in ants. PLoS ONE 7, e44501. https://doi.org/10.1371/journal.pone.0044501 (2012).Article 
    ADS 

    Google Scholar 
    Wehner, R., Harkness, R. D. & Schmid-Hempel, P. Foraging Strategies in Individually Searching Ants. (Fischer, 1983).Oster, G. F. & Wilson, E. O. Caste and Ecology in the Social Insects. (Princeton University Press, 1978).Anderson, C. & Franks, N. R. Teams in animal societies. Behav. Ecol. 12, 534–540. https://doi.org/10.1093/beheco/12.5.534 (2001).Article 

    Google Scholar 
    Jeanne, R. L. The evolution of the organization of work in social insects. Monitore Zool. Italiano-Ital. J. Zool. 20, 119–133. https://doi.org/10.1080/00269786.1986.10736494 (1986).Article 

    Google Scholar 
    Ratnieks, F. L. & Anderson, C. Task partitioning in insects societies. Insectes Soc. 46, 95–108 (1999).Article 

    Google Scholar 
    Anderson, C., Boomsma, J. J. & Bartholdi, J. J. Task partitioning in insect societies: bucket brigades. Insectes Soc. 49, 171–180. https://doi.org/10.1007/s00040-002-8298-7 (2002).Article 

    Google Scholar 
    Jeanson, R. & Weidenmüller, A. Interindividual variability in social insects–proximate causes and ultimate consequences. Biol. Rev. 89, 671–687 (2014).Article 

    Google Scholar 
    Leighton, G. M., Charbonneau, D. & Dornhaus, A. Task switching is associated with temporal delays in Temnothorax rugatulus ants. Behav. Ecol. 28, 319–327. https://doi.org/10.1093/beheco/arw162 (2017).Article 

    Google Scholar 
    Grassé, P.-P. La reconstruction du nid et les coordinations interindividuelles chez Bellicositermes natalensis et Cubitermes sp. la théorie de la stigmergie: Essai d’interprétation du comportement des termites constructeurs. Insectes Soc. 6, 41–80 (1959).Article 

    Google Scholar 
    Theraulaz, G. & Bonabeau, E. A brief history of stigmergy. Artif. Life 5, 97–116. https://doi.org/10.1162/106454699568700 (1999).Article 

    Google Scholar 
    Karsai, I. Decentralized control of construction behavior in paper wasps: an overview of the stigmergy approach. Artif. Life 5, 117–136. https://doi.org/10.1162/106454699568719 (1999).Article 

    Google Scholar 
    Karsai, I. & Penzes, Z. Comb Building in Social Wasps – Self-Organization and Stigmergic Script. J. Theor. Biol. 161, 505–525. https://doi.org/10.1006/jtbi.1993.1070 (1993).Article 
    ADS 

    Google Scholar 
    Dorigo, M., Bonabeau, E. & Theraulaz, G. Ant algorithms and stigmergy. Fut. Gen. Comput. Syst. 16, 851–871 (2000).Article 

    Google Scholar 
    Camazine, S. Self-organizing pattern-formation on the combs of Honey-Bee Colonies. Behav. Ecol. Sociobiol. 28, 61–76. https://doi.org/10.1007/bf00172140 (1991).Article 

    Google Scholar 
    Camazine, S., Sneyd, J., Jenkins, M. J. & Murray, J. D. A Mathematical-model of self-organized pattern-formation on the combs of Honeybee Colonies. J. Theor. Biol. 147, 553–571. https://doi.org/10.1016/S0022-5193(05)80264-4 (1990).Article 
    ADS 

    Google Scholar 
    Deneubourg, J.-L. et al. in Simulation of Adaptive Behavior: From Animals to Animats (eds J.A. Meyer & S.W. Wilson) 356–365 (The MIT Press/Bradford Books, 1991).Franks, N. R. & Sendovafranks, A. B. Brood Sorting by Ants – Distributing the Workload over the Work-Surface. Behav. Ecol. Sociobiol. 30, 109–123 (1992).Article 

    Google Scholar 
    Sendova-Franks, A. B., Scholes, S. R., Franks, N. R. & Melhuish, C. Brood sorting by ants: two phases and differential diffusion. Anim. Behav. 68, 1095–1106. https://doi.org/10.1016/j.anbehav.2004.02.013 (2004).Article 

    Google Scholar 
    Lan, T., Liu, S. & Yang, S. X. in 2006 6th World Congress on Intelligent Control and Automation. 441–445 (IEEE).Renucci, M., Tirard, A. & Provost, E. Complex undertaking behavior in Temnothorax lichtensteini ant colonies: from corpse-burying behavior to necrophoric behavior. Insectes Soc. 58, 9–16 (2011).Article 

    Google Scholar 
    Detrain, C. & Deneubourg, J. L. Collective decision-making and foraging patterns in Ants and Honeybees. Advances in Insect Physiology 35(35), 123–173. https://doi.org/10.1016/S0065-2806(08)00002-7 (2008).Article 

    Google Scholar 
    Couzin, I. D. & Franks, N. R. Self-organized lane formation and optimized traffic flow in army ants. Proc Biol Sci 270, 139–146. https://doi.org/10.1098/rspb.2002.2210 (2003).Article 

    Google Scholar 
    Gulyas, L., Laufer, L. & Szabo, R. in International Workshop on Engineering Self-Organising Applications 50–65 (Springer).Langridge, E. A., Franks, N. R. & Sendova-Franks, A. B. Improvement in collective performance with experience in ants. Behav. Ecol. Sociobiol. 56, 523–529. https://doi.org/10.1007/s00265-004-0824-3 (2004).Article 

    Google Scholar 
    Oberst, S. et al. Revisiting stigmergy in light of multi-functional, biogenic, termite structures as communication channel. Comput. Struct. Biotechnol. J. 18, 2522–2534 (2020).Article 

    Google Scholar 
    Hart, A., Anderson, C. & Ratnieks, F. Task partitioning in leafcutting ants. Acta Ethologica 5, 1–11. https://doi.org/10.1007/s10211-002-0062-5 (2002).Article 

    Google Scholar 
    Hart, A. G. & Ratnieks, F. L. Leaf caching in the leafcutting ant Atta colombica: organizational shift, task partitioning and making the best of a bad job. Anim. Behav. 62, 227–234 (2001).Article 

    Google Scholar 
    Röschard, J. & Roces, F. Sequential load transport in grass-cutting ants (Atta vollenweideri): maximization of plant delivery rate or improved information transfer? Psyche 2011 (2011).Nickele, M. A., Reis Filho, W. & Pie, M. R. Sequential load transport during foraging in Acromyrmex (Hymenoptera: Formicidae) leaf-cutting ants. Myrmecol News 21, 73–82 (2015).Ferrante, E., Turgut, A. E., Duenez-Guzman, E., Dorigo, M. & Wenseleers, T. Evolution of Self-Organized Task Specialization in Robot Swarms. PLoS Comp. Biol. 11, e1004273. https://doi.org/10.1371/journal.pcbi.1004273 (2015).Article 
    ADS 

    Google Scholar 
    Grueter, C. et al. Negative feedback enables fast and flexible collective decision-making in ants. (2012).Holcombe, M. et al. Modelling complex biological systems using an agent-based approach. Integr. Biol. 4, 53–64 (2012).Article 

    Google Scholar 
    Fourcassié, V., Dussutour, A. & Deneubourg, J.-L. Ant traffic rules. J. Exp. Biol. 213, 2357–2363 (2010).Article 

    Google Scholar 
    Modlmeier, A. P., Keiser, C. N., Shearer, T. A. & Pruitt, J. N. Species-specific influence of group composition on collective behaviors in ants. Behav. Ecol. Sociobiol. 68, 1929–1937 (2014).Article 

    Google Scholar 
    Modlmeier, A. P., Liebmann, J. E. & Foitzik, S. Diverse societies are more productive: a lesson from ants. Proc. R. Soc. B 279, 2142–2150 (2012).Article 

    Google Scholar 
    Walsh, J. T., Garnier, S. & Linksvayer, T. A. Ant collective behavior is heritable and shaped by selection. Am. Nat. 196, 541–554 (2020).Article 

    Google Scholar 
    Tannenbaum, E. When does division of labor lead to increased system output?. J. Theor. Biol. 247, 413–425 (2007).Article 
    ADS 
    MathSciNet 
    MATH 

    Google Scholar 
    Wahl, L. M. Evolving the division of labour: Generalists, specialists and task allocation. J. Theor. Biol. 219, 371–388 (2002).Article 
    ADS 
    MathSciNet 

    Google Scholar 
    Wakano, J., Nakata, K. & Yamamura, N. Dynamic model of optimal age polyethism in social insects under stable and fluctuating environments. J. Theor. Biol. 193, 153–165 (1998).Article 
    ADS 

    Google Scholar 
    Goldsby, H. J., Dornhaus, A., Kerr, B. & Ofria, C. Task-switching costs promote the evolution of division of labor and shifts in individuality. Proc. Natl. Acad. Sci. 109, 13686–13691 (2012).Article 
    ADS 

    Google Scholar 
    Rueffler, C., Hermisson, J. & Wagner, G. P. Evolution of functional specialization and division of labor. Proc. Natl. Acad. Sci. 109, E326–E335 (2012).Article 
    ADS 

    Google Scholar 
    Lopes, J. F., Forti, L. C., Camargo, R. S., Matos, C. A. & Verza, S. S. The effect of trail length on task partitioning in three Acromyrmex species (Hymenoptera: Formicidae). Sociobiology 42, 87–92 (2003).
    Google Scholar 
    Duarte, A., Weissing, F. J., Pen, I. & Keller, L. An evolutionary perspective on self-organized division of labor in social insects. Annu. Rev. Ecol. Evol. Syst. 42(42), 91–110. https://doi.org/10.1146/annurev-ecolsys-102710-145017 (2011).Article 

    Google Scholar 
    Duarte, A., Pen, I., Keller, L. & Weissing, F. J. Evolution of self-organized division of labor in a response threshold model. Behav. Ecol. Sociobiol. 66, 947–957. https://doi.org/10.1007/s00265-012-1343-2 (2012).Article 

    Google Scholar 
    Floreano, D. & Keller, L. Evolution of adaptive behaviour in robots by means of Darwinian selection. PLoS Biol. 8, e1000292 (2010).Article 

    Google Scholar 
    Floreano, D., Mitri, S., Magnenat, S. & Keller, L. Evolutionary conditions for the emergence of communication in robots. Curr. Biol. 17, 514–519 (2007).Article 

    Google Scholar 
    Mitri, S., Floreano, D. & Keller, L. The evolution of information suppression in communicating robots with conflicting interests. Proc. Natl. Acad. Sci. 106, 15786–15790 (2009).Article 
    ADS 

    Google Scholar 
    Abiodun, O. I. et al. State-of-the-art in artificial neural network applications: A survey. Heliyon 4, e00938 (2018).Article 

    Google Scholar 
    Dingemanse, N. J., Kazem, A. J., Réale, D. & Wright, J. Behavioural reaction norms: Animal personality meets individual plasticity. Trends Ecol. Evol. 25, 81–89 (2010).Article 

    Google Scholar 
    Van den Berg, P. & Weissing, F. J. The importance of mechanisms for the evolution of cooperation. Proc. R. Soc. B 282, 20151382 (2015).Article 

    Google Scholar 
    Wetterer, J. K. Ontogenetic changes in forager polymorphism and foraging ecology in the leaf-cutting ant Atta cephalotes. Oecologia 98, 235–238. https://doi.org/10.1007/BF00341478 (1994).Article 
    ADS 

    Google Scholar 
    Wetterer, J. K. Forager size and ecology of Acromyrmex coronatus and other leaf-cutting ants in Costa Rica. Oecologia 104, 409–415. https://doi.org/10.1007/BF00341337 (1995).Article 
    ADS 

    Google Scholar 
    Evison, S. E. F. & Hughes, W. O. Genetic caste polymorphism and the evolution of polyandry in Atta leaf-cutting ants. Naturwissenschaften 98, 643–649 (2011).Article 
    ADS 

    Google Scholar 
    Hughes, W. O., Oldroyd, B. P., Beekman, M. & Ratnieks, F. L. Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320, 1213–1216 (2008).Article 
    ADS 

    Google Scholar 
    Villesen, P., Murakami, T., Schultz, T. R. & Boomsma, o. J. Identifying the transition between single and multiple mating of queens in fungus-growing ants. Proc. R. Soc. Lond. Ser. B: Biol. Sci. 269, 1541–1548 (2002).Mueller, U. G. & Rabeling, C. A breakthrough innovation in animal evolution. Proc. Natl. Acad. Sci. 105, 5287–5288 (2008).Article 
    ADS 

    Google Scholar 
    Schultz, T. R. & Brady, S. G. Major evolutionary transitions in ant agriculture. Proc. Natl. Acad. Sci. 105, 5435–5440 (2008).Article 
    ADS 

    Google Scholar 
    Fowler, H. G. Latitudinal gradients and diversity of the leaf-cutting ants (Atta and Acromyrmex)(Hymenoptera: Formicidae). Rev. Biol. Trop. 31, 213–216 (1983).
    Google Scholar 
    Jackson, D. E. & Ratnieks, F. L. Communication in ants. Curr. Biol. 16, R570–R574 (2006).Article 

    Google Scholar 
    Roces, F. & Hölldobler, B. Vibrational communication between hitchhikers and foragers in leaf-cutting ants (Atta cephalotes). Behav. Ecol. Sociobiol. 37, 297–302 (1995).Article 

    Google Scholar 
    Hubbell, S. P., Johnson, L. K., Stanislav, E., Wilson, B. & Fowler, H. Foraging by bucket-brigade in leaf-cutter ants. Biotropica 1, 210–213 (1980).Article 

    Google Scholar 
    Boi, S., Couzin, I. D., Buono, N. D., Franks, N. & Britton, N. Coupled oscillators and activity waves in ant colonies. Proc. R. Soc. Lond. Ser. B: Biol. Sci. 266, 371–378 (1999).Cole, B. J. Short-term activity cycles in ants: generation of periodicity by worker interaction. Am. Nat. 137, 244–259 (1991).Article 

    Google Scholar 
    Cornejo, A., Dornhaus, A., Lynch, N. & Nagpal, R. in International Symposium on Distributed Computing. 46–60 (Springer).Franks, N. R., Bryant, S., Griffiths, R. & Hemerik, L. Synchronization of the behaviour within nests of the antleptothorax acervorum (fabricius)—I. Discovering the phenomenon and its relation to the level of starvation. Bull. Math. Biol. 52, 597–612 (1990).Pagliara, R., Gordon, D. M. & Leonard, N. E. Regulation of harvester ant foraging as a closed-loop excitable system. PLoS Comp. Biol. 14, e1006200 (2018).Article 
    ADS 

    Google Scholar 
    Schmickl, T. & Karsai, I. Integral feedback control is at the core of task allocation and resilience of insect societies. Proc. Natl. Acad. Sci. 115, 13180–13185 (2018).Article 
    ADS 

    Google Scholar 
    Solé, R. V., Miramontes, O. & Goodwin, B. C. Oscillations and chaos in ant societies. J. Theor. Biol. 161, 343–357 (1993).Article 
    ADS 

    Google Scholar 
    Gordon, D. M., Goodwin, B. C. & Trainor, L. E. A parallel distributed model of the behaviour of ant colonies. J. Theor. Biol. 156, 293–307 (1992).Article 
    ADS 

    Google Scholar 
    Aoki, S. K. et al. A universal biomolecular integral feedback controller for robust perfect adaptation. Nature 570, 533–537 (2019).Article 

    Google Scholar 
    Ma, W., Trusina, A., El-Samad, H., Lim, W. A. & Tang, C. Defining network topologies that can achieve biochemical adaptation. Cell 138, 760–773 (2009).Article 

    Google Scholar 
    Niemeyer, N., Schleimer, J.-H. & Schreiber, S. Biophysical models of intrinsic homeostasis: Firing rates and beyond. Curr. Opin. Neurobiol. 70, 81–88 (2021).Article 

    Google Scholar 
    Rombouts, J., Vandervelde, A. & Gelens, L. Delay models for the early embryonic cell cycle oscillator. PLoS ONE 13, e0194769 (2018).Article 

    Google Scholar 
    Tyson, J. J., Chen, K. C. & Novak, B. Sniffers, buzzers, toggles and blinkers: dynamics of regulatory and signaling pathways in the cell. Curr. Opin. Cell Biol. 15, 221–231 (2003).Article 

    Google Scholar 
    Bryant, B. D. & Miikkulainen, R. Foundations of Trusted Autonomy 87–115 (Springer, 2018).
    Google Scholar 
    Masad, D. & Kazil, J. in 14th PYTHON in Science Conference. 53–60 (Citeseer).Knaden, M. & Graham, P. The sensory ecology of ant navigation: from natural environments to neural mechanisms. Annu. Rev. Entomol. 61, 63–76 (2016).Article 

    Google Scholar  More

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    Multistressor global change drivers reduce hatch and viability of Lingcod embryos, a benthic egg layer in the California Current System

    IPCC Climate Change The physical science basis. In Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change (eds Masson-Delmotte, V. et al.) (Cambridge University Press, 2021).
    Google Scholar 
    Doney, S. C. et al. Climate change impacts on marine ecosystems. Annu. Rev. Mar. Sci. 4, 11–37 (2012).Article 
    ADS 

    Google Scholar 
    Song, H. et al. Thresholds of temperature change for mass extinctions. Nat. Commun. 12, 4694 (2021).Article 
    ADS 
    CAS 

    Google Scholar 
    Free, C. M. et al. Impacts of historical warming on marine fisheries production. Science 363, 979–983 (2019).Article 
    ADS 
    CAS 

    Google Scholar 
    Cheung, W. W. L. et al. Large-scale redistribution of maximum fisheries catch potential in the global ocean under climate change: Climate change impacts on catch potential. Glob. Change Biol. 16, 24–35 (2010).Article 
    ADS 

    Google Scholar 
    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).Article 
    ADS 

    Google Scholar 
    Dahlke, F. T., Wohlrab, S., Butzin, M. & Pörtner, H.-O. Thermal bottlenecks in the life cycle define climate vulnerability of fish. Science 369, 65–70 (2020).Article 
    ADS 
    CAS 

    Google Scholar 
    Hodgson, E. E., Essington, T. E. & Kaplan, I. C. Extending vulnerability assessment to include life stages considerations. PLoS ONE 11, e0158917 (2016).Article 

    Google Scholar 
    Peck, M. A., Reglero, P., Takahashi, M. & Catalán, I. A. Life cycle ecophysiology of small pelagic fish and climate-driven changes in populations. Prog. Oceanogr. 116, 220–245 (2013).Article 
    ADS 

    Google Scholar 
    Tsoukali, S., Visser, A. W. & MacKenzie, B. R. Functional responses of North Atlantic fish eggs to increasing temperature. Mar. Ecol. Prog. Ser. 555, 151–165 (2016).Article 
    ADS 

    Google Scholar 
    Pörtner, H. O. & Peck, M. A. Climate change effects on fishes and fisheries: Towards a cause-and-effect understanding. J. Fish Biol. 77, 1745–1779 (2010).Article 

    Google Scholar 
    Pankhurst, N. W. & Munday, P. L. Effects of climate change on fish reproduction and early life history stages. Mar. Freshw. Res. 62, 1015–1026 (2011).Article 
    CAS 

    Google Scholar 
    Brauner, C. J. Acid-base balance. In Fish Larval physiology (eds Finn, R. N. & Kapoor, B. G.) 185–198 (Science Publishers, 2008).
    Google Scholar 
    Dahlke, F. T. et al. Effects of ocean acidification increase embryonic sensitivity to thermal extremes in Atlantic cod, Gadus morhua. Glob. Chang. Biol. 23, 1499–1510 (2017).Article 
    ADS 

    Google Scholar 
    Shelbourne, J. E. Significance of the subdermal space in pelagic fish embryos and larvae. Nature 176, 743–744 (1955).Article 
    ADS 

    Google Scholar 
    Sundby, S. & Kristiansen, T. The principles of buoyancy in marine fish eggs and their vertical distributions across the world oceans. PLoS ONE 10, e0138821 (2015).Article 

    Google Scholar 
    Shei, M., Mies, M. & Olivotto, I. Other demersal spawners and mouthbrooders. Marine ornamental species aquaculture, 223–250 (2017).Beaudreau, A. H. The predatory role of lingcod (Ophiodon elongatus) in the San Juan Archipelago, Washington. (University of Washington, 2009).Love, M. Certainly More Than You Want to Know About the Fishes of the Pacific Coast: A Postmodern Experience. (Really Big Press, 2011).Pauly, D. & Christensen, V. Primary production required to sustain global fisheries. Nature 374, 255–257 (1995).Article 
    ADS 
    CAS 

    Google Scholar 
    Reum, J. C. et al. Interpretation and design of ocean acidification experiments in upwelling systems in the context of carbonate chemistry co-variation with temperature and oxygen. ICES J. Mar. Sci. 73, 582–595 (2016).Article 

    Google Scholar 
    Cheresh, J. & Fiechter, J. Physical and biogeochemical drivers of alongshore pH and oxygen variability in the California Current System. Geophys. Res. Lett. 47, e2020089553 (2020).Article 
    ADS 

    Google Scholar 
    Gruber, N. et al. Rapid progression of ocean acidification in the California Current System. Science 337, 220–223 (2012).Article 
    ADS 
    CAS 

    Google Scholar 
    Hauri, C. et al. Spatiotemporal variability and long-term trends of ocean acidification in the California Current System. Biogeosciences 10, 193–216 (2013).Article 
    ADS 

    Google Scholar 
    Pepin, P. Effect of temperature and size on development, mortality, and survival rates of the pelagic early life history stages of marine fish. Can. J. Fish. Aquat. Sci. 48, 503–518 (1991).Article 

    Google Scholar 
    Lauel, B. J. & Blood, D. M. The Effects of Temperature on Hatching and Survival of Northern Rock Sole Larvae (Lepidopsetta polyxystra) (Springer, 2011).
    Google Scholar 
    Guevara-Fletcher, C., Alvarez, P., Sanchez, J. & Iglesias, J. Effect of temperature on the development and mortality of European hake (Merluccius merluccius L.) eggs from southern stock under laboratory conditions. J. Exp. Mar. Biol. Ecol. 476, 50–57 (2016).Article 

    Google Scholar 
    Collins, L. A. & Nelson, S. G. Effects of temperature on oxygen consumption, growth, and development of embryos and yolk-sac larvae of Siganus randalli (Pisces: Siganidae). Mar. Biol. 117, 195–204 (1993).Article 

    Google Scholar 
    Cook, M. A., Guthrie, K. M., Rust, M. B. & Plesha, P. D. Effects of salinity and temperature during incubation on hatching and development of lingcod Ophiodon elongatus Girard, embryos. Aquac. Res. 36, 1298–1303 (2005).Article 

    Google Scholar 
    Pörtner, H. Integrating climate-related stressor effects on marine organisms: Unifying principles linking molecule to ecosystem-level changes. Mar. Ecol. Prog. Ser. 470, 273–290 (2012).Article 
    ADS 

    Google Scholar 
    Laurel, B. J., Copeman, L. A., Spencer, M. & Iseri, P. Comparative effects of temperature on rates of development and survival of eggs and yolk-sac larvae of Arctic cod (Boreogadus saida) and walleye pollock (Gadus chalcogrammus). ICES J. Mar. Sci. 75, 2403–2412 (2018).Article 

    Google Scholar 
    Jordaan, A., Hayhurst, S. E. & Kling, L. J. The influence of temperature on the stage at hatch of laboratory reared Gadus morhua and implications for comparisons of length and morphology. J. Fish Biol. 68, 7–24 (2006).Article 

    Google Scholar 
    Peña, R., Dumas, S., Zavala-Leal, I. & Contreras-Olguín, M. Effect of incubation temperature on the embryonic development and yolk-sac larvae of the Pacific red snapper Lutjanus peru (Nichols & Murphy, 1922). Aquac Res 45, 519–527 (2014).Article 

    Google Scholar 
    Breitburg, D. Effects of hypoxia, and the balance between hypoxia and enrichment, on coastal fishes and fisheries. Estuaries 25, 767–781 (2002).Article 

    Google Scholar 
    Hassell, K. L., Coutin, P. C. & Nugegoda, D. Hypoxia impairs embryo development and survival in black bream (Acanthopagrus butcheri). Mar. Pollut. Bull. 57, 302–306 (2008).Article 
    CAS 

    Google Scholar 
    Giorgi, A. E. The Environmental Biology of the Embryos, Egg Masses and Nesting Sites of the Lingcod, Ophiodon elongatus. (University of Washington, 1981).Oseid, D. M. & Smith, L. L. Survival and hatching of walleye eggs at various dissolved oxygen levels. Progress. Fish-Cult. 33, 81–85 (1971).Article 
    CAS 

    Google Scholar 
    Shumway, D. L., Warren, C. E. & Doudoroff, P. Influence of oxygen concentration and water movement on the growth of steelhead trout and coho salmon embryos. Trans. Am. Fish. Soc. 93, 342–356 (1964).Article 

    Google Scholar 
    Baumann, H., Talmage, S. C. & Gobler, C. J. Reduced early life growth and survival in a fish in direct response to increased carbon dioxide. Nat. Clim Change 2, 38–41 (2012).Article 
    ADS 
    CAS 

    Google Scholar 
    Faria, A. M. et al. Effects of high pCO2 on early life development of pelagic spawning marine fish. Mar. Freshw. Res. 68, 2106–2114 (2017).Article 
    CAS 

    Google Scholar 
    Frommel, A. Y. et al. Severe tissue damage in Atlantic cod larvae under increasing ocean acidification. Nat. Clim. Change 2, 42–46 (2012).Article 
    ADS 
    CAS 

    Google Scholar 
    Munday, P. L. et al. Effects of elevated CO2 on early life history development of the yellowtail kingfish, Seriola lalandi, a large pelagic fish. ICES J. Mar. Sci. 73, 641–649 (2016).Article 

    Google Scholar 
    Hurst, T. P., Fernandez, E. R. & Mathis, J. T. Effects of ocean acidification on hatch size and larval growth of walleye pollock (Theragra chalcogramma). ICES J. Mar. Sci. 70, 812–822 (2013).Article 

    Google Scholar 
    Wang, X., Song, L., Chen, Y., Ran, H. & Song, J. Impact of ocean acidification on the early development and escape behavior of marine medaka (Oryzias melastigma). Mar. Environ. Res. 131, 10–18 (2017).Article 

    Google Scholar 
    Franke, A. & Clemmesen, C. Effect of ocean acidification on early life stages of Atlantic herring (Clupea harengus L.). Biogeosciences 8, 3697–3707 (2011).Article 
    ADS 
    CAS 

    Google Scholar 
    Forsgren, E., Dupont, S., Jutfelt, F. & Amundsen, T. Elevated CO 2 affects embryonic development and larval phototaxis in a temperate marine fish. Ecol. Evol. 3, 3637–3646 (2013).Article 

    Google Scholar 
    Bromhead, D. et al. The potential impact of ocean acidification upon eggs and larvae of yellowfin tuna (Thunnus albacares). Deep Sea Res. II 113, 268–279 (2015).Article 
    CAS 

    Google Scholar 
    Garrido, S. et al. Born small, die young: Intrinsic, size-selective mortality in marine larval fish. Sci. Rep. 5, 17065 (2015).Article 
    ADS 
    CAS 

    Google Scholar 
    Sampaio, E. et al. Impacts of hypoxic events surpass those of future ocean warming and acidification. Nat. Ecol. Evol. 5, 311–321 (2021).Article 

    Google Scholar 
    Crain, C. M., Kroeker, K. & Halpern, B. S. Interactive and cumulative effects of multiple human stressors in marine systems. Ecol. Lett. 11, 1304–1315 (2008).Article 

    Google Scholar 
    Pörtner, H. O. Synergistic effects of temperature extremes, hypoxia, and increases in CO2 on marine animals: From Earth history to global change. J. Geophys. Res. 110, 0910 (2005).Article 

    Google Scholar 
    Piggott, J. J., Townsend, C. R. & Matthaei, C. D. Reconceptualizing synergism and antagonism among multiple stressors. Ecol. Evol. 5, 1538–1547 (2015).Article 

    Google Scholar 
    Boyd, P. W. et al. Experimental strategies to assess the biological ramifications of multiple drivers of global ocean change: A review. Glob. Change Biol 24, 2239–2261 (2018).Article 
    ADS 

    Google Scholar 
    Giorgi, A. E. & Congleton, J. L. Effects of current velocity on development and survival of lingcod, Ophiodon elongatus, embryos. Environ. Biol. Fish 10, 15–27 (1984).Article 

    Google Scholar 
    Liu, G., Zhu, S., Liu, D. & Ye, Z. Effect of the C/N ratio on inorganic nitrogen control and the growth and physiological parameters of tilapia s fingerlings, Oreochromis niloticu reared in biofloc systems. Aquac. Res. 49, 2429–2439 (2018).Article 
    CAS 

    Google Scholar 
    Houde, E. D. Fish early life dynamics and recruitment variability. Am. Fish. Soc. Symp. 2, 17–29 (1987).ADS 

    Google Scholar 
    Miller, T. J., Crowder, L. B., Rice, J. A. & Marschall, E. A. Larval size and recruitment mechanisms in fishes: Toward a conceptual framework. Can. J. Fish. Aquat. Sci. 45, 1657–1670 (1988).Article 

    Google Scholar 
    Doi, H., Akamatsu, F. & González, A. L. Starvation effects on nitrogen and carbon stable isotopes of animals: An insight from meta-analysis of fasting experiments. R. Soc. open sci. 4, 170633 (2017).Article 
    ADS 

    Google Scholar 
    Pimentel, M. S. et al. Defective skeletogenesis and oversized otoliths in fish early stages in a changing ocean. J. Exp. Biol. 1, 092635. https://doi.org/10.1242/jeb.092635 (2014).Article 

    Google Scholar 
    Politis, S. N., Dahlke, F. T., Butts, I. A., Peck, M. A. & Trippel, E. A. Temperature, paternity and asynchronous hatching influence early developmental characteristics of larval Atlantic cod, Gadus morhua. J. Exp. Mar. Biol. Ecol. 459, 70–79 (2014).Article 

    Google Scholar 
    Appelbaum, S. et al. Studies on rearing of lingcod Ophiodon elongatus. Aquaculture 135, 219–227 (1995).Article 

    Google Scholar 
    Hempel, G. Early life history of marine fish: The egg stage. Washington Sea Grant. (University of Washington Press, 1979)Gadomski, D. M. & Caddell, S. M. Effects of temperature on the development and survival of eggs of four coastal California fishes. Fish. Bull. 94, 41–48 (1996).
    Google Scholar 
    Parker, L. M. et al. Adult exposure influences offspring response to ocean acidification in oysters. Glob. Change Biol. 18, 82–92 (2012).Article 
    ADS 

    Google Scholar 
    Rombough, P. The effects of temperature on embryonic and larval development. In Global Warming: Implications for Freshwater and Marine Fish (Society for Experimental Biology Seminar Series) (eds Wood, C. & McDonald, D.) 177–224 (Cambridge University Press, 1997).Chapter 

    Google Scholar 
    Bownds, C., Wilson, R. & Marshall, D. J. Why do colder mothers produce larger eggs? An optimality approach. J. Exp. Biol. 213, 3796–3801 (2010).Article 

    Google Scholar 
    Longo, G. C. et al. Strong population differentiation in lingcod ( Ophiodon elongatus ) is driven by a small portion of the genome. Evol. Appl. 13, 2536–2554 (2020).Article 
    CAS 

    Google Scholar 
    Silberberg, K. R., Laidig, T. E., Adams, P. B. & Albin, D. Analysis of maturity in lingcod, Ophiodon elongatus. California Fish Game 87, 139–152 (2001).
    Google Scholar 
    Palumbi, S. R. Why mothers matter. Nature 430, 621–622 (2004).Article 
    ADS 
    CAS 

    Google Scholar 
    Berkeley, S. A., Chapman, C. & Sogard, S. M. Maternal age as a determinant of larval growth and survival in a marine fish, Sebastes melanops. Ecology 85, 1258–1264 (2004).Article 

    Google Scholar 
    Miller, D. J., & Geibel, J. J. Summary of Blue Rockfish and Lingcod Life Histories, a Reef Ecology Study, and Giant Kelp, Macrocystis Pyrifera, Experiments in Monterey Bay, California. (State of California, Resources Agency, Department of Fish and Game, 1973).Low, C. J. & Beamish, R. J. A study of the nesting behavior of lingcod (Ophiodon elongatus) in the strait of Georgia, British Columbia. Can. Fish. Mar. Serv. Tech. Rep. 843, 1–10 (1978).
    Google Scholar 
    King, J. R. & Withler, R. E. Male nest site fidelity and female serial polyandry in lingcod (Ophiodon elongatus, Hexagrammidae): Lingcod nest site fidelity. Mol. Ecol. 14, 653–660 (2005).Article 

    Google Scholar 
    Withler, R. E. et al. Polygamous mating and high levels of genetic variation in lingcod, Ophiodon elongatus of the Strait of Georgia, British Columbia. In Genetics of Subpolar Fish and Invertebrates 345–357 (Springer, 2004).
    Google Scholar 
    Perkins, M. J. et al. Application of nitrogen and carbon stable isotopes (δ15N and δ13C) to quantify food chain length and trophic structure. PLoS ONE 9, e93281 (2014).Article 
    ADS 

    Google Scholar 
    Earth Systems Research Laboratory (ESRL). NOAA’s Ocean Climate Change Web Portal. http://www.esrl.noaa.gov/psd/ipcc/ocn/ (2019).Feely, R., Doney, S. & Cooley, S. Ocean acidification: Present conditions and future changes in a high-CO2 world. Oceanography 22, 36–47 (2009).Article 

    Google Scholar 
    Frieder, C. A., Nam, S. H., Martz, T. R. & Levin, L. A. High temporal and spatial variability of dissolved oxygen and pH in a nearshore California kelp forest. Biogeosciences 9, 3917–3930 (2012).Article 
    ADS 
    CAS 

    Google Scholar 
    Olito, C., White, C. R., Marshall, D. J. & Barneche, D. R. Estimating monotonic rates from biological data using local linear regression. J. Exp. Biol. 1, 148775. https://doi.org/10.1242/jeb.148775 (2017).Article 

    Google Scholar 
    Brooks, M. E. et al. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J. 9(2), 378–400 (2017).Article 

    Google Scholar  More