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    Author Correction: Widespread extinction debts and colonization credits in United States breeding bird communities

    In the version of this article initially published, there were errors in equations and notations in the Methods “Model development” subsection which arose during manuscript preparation; the errors affect presentation of the study but not the analysis, results, or code provided with the article. Clarifications to text and equations follow.In Equation (1), “N” replaces “Normal”; in Equations (2), (3), (7) and in text directly below Equations (3), (5) and (7), “ys,i,z” now replaces “Δxs,t1, t2.” In the two paragraphs below Equation (2), “t2 = 2016” and “t1 = 2001” now replace “2016” and “2001” in five instances. Further, Equations (5)–(7) have been revised as follows:$$begin{array}{ll}fleft( {x_{s,t}} right) = {{{mathrm{exp}}}} & left( {beta _0 + mathop {sum }limits_{i = 1}^{I = 5} beta _{1,i} x_{s,i,t} + mathop {sum }limits_{i = 1}^{I = 5} mathop {sum }limits_{k = i}^{K = 5} beta _{2,i,k}x_{s,i,t}x_{k,s,t}}right. \ & quad quad left. {+ mathop {sum }limits_{i = 1}^{I = 5} mathop {sum }limits_{k = 1, k neq i}^{K = 5} beta _{3,i,k}x_{s,i,t}x_{k,s,t}} right)end{array} {rm{Revised}} {rm{Eq}}. (5)$$$$begin{array}{ll}fleft( {x_{s,t}} right) \ = expleft( {beta _0 + mathop {sum }limits_{i = 1}^{I = 5} mathop {sum }limits_{j = 1}^{J = 2} beta _{0,i,j,}x_{i,s,t}^j + mathop {sum }limits_{i = 1}^{I = 5} mathop {sum }limits_{k = i + 1}^{K = 6} beta _{1,i,k}x_{i,s,t}x_{k,s,t}} right) {mathrm{Original}} {rm{Eq}}. (5)end{array}$$$$y_{s,i,z} = left{ {begin{array}{*{20}{l}} {y_{s,i,1} = left| {Delta x_{s,i}} right|,} hfill & {y_{s,i,2} = 0,} hfill & {{{{mathrm{if}}}},Delta x_{s,i} < 0} hfill \ {y_{s,i,1} = 0,} hfill & {y_{s,i,2} = Delta x_{s,i}} hfill & {{{{mathrm{otherwise}}}}} hfill end{array}} right. {rm{Revised}} {rm{Eq}}. (6)$$$$x_{i,s,} = left{ {begin{array}{*{20}{l}} {x_{1,i,s} = left| {Delta x_{i,s}} right|,} hfill & {x_{2,i,s} = 0,} hfill & {if,Delta x_{i,s} < 0} hfill \ {x_{1,i,s} = 0,} hfill & {x_{2,i,s} = Delta x_{i,s},} hfill & {otherwise} hfill end{array}} right. {rm{Original}} {rm{Eq}}. (6)$$$$omega left( {y_{s,i,z};gamma } right) = {{{mathrm{exp}}}}left( {mathop {sum }limits_{i = 1}^{I = 5} mathop {sum }limits_{z = 1}^{Z = 2} - gamma _{i,z} y_{s,i,z}} right) {rm{Revised}} {rm{Eq}}. (7)$$$$omega left( {Delta x_{s,t_1,t_2};gamma } right) = expleft( {mathop {sum }limits_{i = 1}^{I = 5} - gamma _{i,z}Delta x_{z,s,i}} right) {rm{Original}} {rm{Eq}}. (7)$$All changes have been made in the HTML and PDF versions of the article. More

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    Plankton response to global warming is characterized by non-uniform shifts in assemblage composition since the last ice age

    Brett, C. E. Sequence stratigraphy, paleoecology, and evolution: biotic clues and responses to sea-level fluctuations. Palaios 13, 241–262 (1998).Article 

    Google Scholar 
    Brett, C. E., Hendy, A. J. W., Bartholomew, A. J., Bonelli, J. R. & McLaughlin, P. I. Response of shallow marine biotas to sea-level fluctuations: a review of faunal replacement and the process of habitat tracking. Palaios 22, 228–244 (2007).Article 

    Google Scholar 
    Parmesan, C. Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Evol. Syst. 37, 637–669 (2006).Article 

    Google Scholar 
    Root, T. L. et al. Fingerprints of global warming on wild animals and plants. Nature 421, 57–60 (2003).CAS 
    PubMed 
    Article 

    Google Scholar 
    Walther, G.-R. et al. Ecological responses to recent climate change. Nature 416, 389–395 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    Lenoir, J. et al. Species better track climate warming in the oceans than on land. Nat. Ecol. Evol. 4, 1044–1059 (2020).PubMed 
    Article 

    Google Scholar 
    Poloczanska, E. S. et al. Global imprint of climate change on marine life. Nat. Clim. Change 3, 919–925 (2013).Article 

    Google Scholar 
    Rillo, M. C., Woolley, S. & Hillebrand, H. Drivers of global pre‐industrial patterns of species turnover in planktonic foraminifera. Ecography 2022, e05892 (2021).Article 

    Google Scholar 
    Van der Putten, W. H., Macel, M. & Visser, M. E. Predicting species distribution and abundance responses to climate change: why it is essential to include biotic interactions across trophic levels. Phil. Trans. R. Soc. B 365, 2025–2034 (2010).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Antão, L. H. et al. Temperature-related biodiversity change across temperate marine and terrestrial systems. Nat. Ecol. Evol. 4, 927–933 (2020).PubMed 
    Article 

    Google Scholar 
    Chen, I. C. et al. Asymmetric boundary shifts of tropical montane Lepidoptera over four decades of climate warming. Glob. Ecol. Biogeogr. 20, 34–45 (2011).Article 

    Google Scholar 
    García Molinos, J. et al. Climate velocity and the future global redistribution of marine biodiversity. Nat. Clim. Change 6, 83–88 (2015).Article 

    Google Scholar 
    Beaugrand, G., Edwards, M., Raybaud, V., Goberville, E. & Kirby, R. R. Future vulnerability of marine biodiversity compared with contemporary and past changes. Nat. Clim. Change 5, 695–701 (2015).Article 

    Google Scholar 
    Benedetti, F. et al. Major restructuring of marine plankton assemblages under global warming. Nat. Commun. 12, 5226 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Occhipinti-Ambrogi, A. Global change and marine communities: alien species and climate change. Mar. Pollut. Bull. 55, 342–352 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    Williams, J. W. & Jackson, S. T. Novel climates, no-analog communities, and ecological surprises. Front. Ecol. Environ. 5, 475–482 (2007).Article 

    Google Scholar 
    Burrows, M. T. et al. Ocean community warming responses explained by thermal affinities and temperature gradients. Nat. Clim. Change 9, 959–963 (2019).Article 

    Google Scholar 
    Dornelas, M. et al. BioTIME: a database of biodiversity time series for the Anthropocene. Glob. Ecol. Biogeogr. 27, 760–786 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Jonkers, L. et al. Integrating palaeoclimate time series with rich metadata for uncertainty modelling: strategy and documentation of the PalMod 130k marine palaeoclimate data synthesis. Earth Syst. Sci. Data 12, 1053–1081 (2020).Article 

    Google Scholar 
    Buitenhuis, E. T. et al. MAREDAT: towards a world atlas of MARine Ecosystem DATa. Earth Syst. Sci. Data 5, 227–239 (2013).Article 

    Google Scholar 
    Yasuhara, M., Tittensor, D. P., Hillebrand, H. & Worm, B. Combining marine macroecology and palaeoecology in understanding biodiversity: microfossils as a model. Biol. Rev. 92, 199–215 (2017).PubMed 
    Article 

    Google Scholar 
    Aze, T. et al. A phylogeny of Cenozoic macroperforate planktonic foraminifera from fossil data. Biol. Rev. 86, 900–927 (2011).PubMed 
    Article 

    Google Scholar 
    Takagi, H. et al. Characterizing photosymbiosis in modern planktonic foraminifera. Biogeosciences 16, 3377–3396 (2019).CAS 
    Article 

    Google Scholar 
    Schiebel, R. & Hemleben, C. Planktic Foraminifers in the Modern Ocean (Springer, 2017).Morey, A. E., Mix, A. C. & Pisias, N. G. Planktonic foraminiferal assemblages preserved in surface sediments correspond to multiple environment variables. Quat. Sci. Rev. 24, 925–950 (2005).Article 

    Google Scholar 
    Fenton, I. S., Pearson, P. N., Dunkley Jones, T. & Purvis, A. Environmental predictors of diversity in recent planktonic foraminifera as recorded in marine sediments. PLoS ONE 11, e0165522 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rutherford, S., D’Hondt, S. & Prell, W. Environmental controls on the geographic distribution of zooplankton diversity. Nature 400, 749–753 (1999).CAS 
    Article 

    Google Scholar 
    Tittensor, D. P. et al. Global patterns and predictors of marine biodiversity across taxa. Nature 466, 1098–1101 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    Yasuhara, M., Hunt, G., Dowsett, H. J., Robinson, M. M. & Stoll, D. K. Latitudinal species diversity gradient of marine zooplankton for the last three million years. Ecol. Lett. 15, 1174–1179 (2012).PubMed 
    Article 

    Google Scholar 
    Yasuhara, M. et al. Past and future decline of tropical pelagic biodiversity. Proc. Natl Acad. Sci. USA 117, 12891–12896 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Jonkers, L., Hillebrand, H. & Kucera, M. Global change drives modern plankton communities away from the pre-industrial state. Nature 570, 372–375 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Beaugrand, G., Reid, P. C., Ibañez, F., Lindley, J. A. & Edwards, M. Reorganization of North Atlantic marine copepod biodiversity and climate. Science 296, 1692–1694 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hinder, S. L. et al. Changes in marine dinoflagellate and diatom abundance under climate change. Nat. Clim. Change 2, 271–275 (2012).Article 

    Google Scholar 
    Southward, A. J., Hawkins, S. J. & Burrows, M. T. Seventy years’ observations of changes in distribution and abundance of zooplankton and intertidal organisms in the western English Channel in relation to rising sea temperature. J. Therm. Biol. 20, 127–155 (1995).Article 

    Google Scholar 
    Fenton, I. S. et al. Triton, a new species-level database of Cenozoic planktonic foraminiferal occurrences. Sci. Data 8, 160 (2021).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kucera, M., Rosell-Melé, A., Schneider, R., Waelbroeck, C. & Weinelt, M. Multiproxy approach for the reconstruction of the glacial ocean surface (MARGO). Quat. Sci. Rev. 24, 813–819 (2005).Kucera, M. et al. Reconstruction of sea-surface temperatures from assemblages of planktonic foraminifera: multi-technique approach based on geographically constrained calibration data sets and its application to glacial Atlantic and Pacific Oceans. Quat. Sci. Rev. 24, 951–998 (2005).Article 

    Google Scholar 
    Siccha, M. & Kucera, M. ForCenS, a curated database of planktonic foraminifera census counts in marine surface sediment samples. Sci. Data 4, 170109 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ezard, T. H. G., Aze, T., Pearson, P. N. & Purvis, A. Interplay between changing climate and species’ ecology drives macroevolutionary dynamics. Science 332, 349–351 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    Fenton, I. S. et al. The impact of Cenozoic cooling on assemblage diversity in planktonic foraminifera. Phil. Trans. R. Soc. B 371, 20150224 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Lowery, C. M. & Fraass, A. J. Morphospace expansion paces taxonomic diversification after end Cretaceous mass extinction. Nat. Ecol. Evol. 3, 900–904 (2019).PubMed 
    Article 

    Google Scholar 
    Wade, B. S., Pearson, P. N., Berggren, W. A. & Pälike, H. Review and revision of Cenozoic tropical planktonic foraminiferal biostratigraphy and calibration to the geomagnetic polarity and astronomical time scale. Earth Sci. Rev. 104, 111–142 (2011).Article 

    Google Scholar 
    Antell, G. S., Fenton, I. S., Valdes, P. J. & Saupe, E. E. Thermal niches of planktonic foraminifera are static throughout glacial-interglacial climate change. Proc. Natl. Acad. Sci. USA https://doi.org/10.1073/pnas.2017105118 (2021).Fauth, J. E. et al. Simplifying the jargon of community ecology: a conceptual approach. Am. Nat. 147, 282–286 (1996).Article 

    Google Scholar 
    Jackson, S. T. & Overpeck, J. T. Responses of plant populations and communities to environmental changes of the late Quaternary. Paleobiology 26, 194–220 (2000).Article 

    Google Scholar 
    Bard, E., Rostek, F., Turon, J.-L. & Gendreau, S. Hydrological impact of Heinrich events in the subtropical Northeast Atlantic. Science 289, 1321–1324 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    Broecker, W. S. Massive iceberg discharges as triggers for global climate change. Nature 372, 421–424 (1994).CAS 
    Article 

    Google Scholar 
    Ruddiman, W. F. Late Quaternary deposition of ice-rafted sand in the subpolar North Atlantic (lat 40° to 65°N). Geol. Soc. Am. Bull. 88, 1813–1827 (1977).Article 

    Google Scholar 
    Hubbell, S. P. The Unified Neutral Theory of Biodiversity and Biogeography (Princeton Univ. Press, 2001).Liow, L. H., Van Valen, L. & Stenseth, N. C. Red Queen: from populations to taxa and communities. Trends Ecol. Evol. 26, 349–358 (2011).PubMed 
    Article 

    Google Scholar 
    Hillebrand, H. et al. Biodiversity change is uncoupled from species richness trends: consequences for conservation and monitoring. J. Appl. Ecol. 55, 169–184 (2018).Article 

    Google Scholar 
    Jackson, S. T. & Sax, D. F. Balancing biodiversity in a changing environment: extinction debt, immigration credit and species turnover. Trends Ecol. Evol. 25, 153–160 (2010).PubMed 
    Article 

    Google Scholar 
    Williams, J. W., Ordonez, A. & Svenning, J. C. A unifying framework for studying and managing climate-driven rates of ecological change. Nat. Ecol. Evol. 5, 17–26 (2021).PubMed 
    Article 

    Google Scholar 
    Van Meerbeeck, C. J., Renssen, H. & Roche, D. M. How did Marine Isotope Stage 3 and Last Glacial Maximum climates differ? Perspectives from equilibrium simulations. Clim. Past 5, 33–51 (2009).Article 

    Google Scholar 
    Jonkers, L. & Kučera, M. Global analysis of seasonality in the shell flux of extant planktonic Foraminifera. Biogeosciences 12, 2207–2226 (2015).Article 

    Google Scholar 
    Ofstad, S. et al. Development, productivity, and seasonality of living planktonic foraminiferal faunas and Limacina helicina in an area of intense methane seepage in the Barents Sea. J. Geophys. Res. Biogeosci. 125, e2019JG005387 (2020).CAS 
    Article 

    Google Scholar 
    Bova, S., Rosenthal, Y., Liu, Z., Godad, S. P. & Yan, M. Seasonal origin of the thermal maxima at the Holocene and the last interglacial. Nature 589, 548–553 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Rillo, M. C. et al. On the mismatch in the strength of competition among fossil and modern species of planktonic Foraminifera. Glob. Ecol. Biogeogr. 28, 1866–1878 (2019).Article 

    Google Scholar 
    Lisiecki, L. E. & Stern, J. V. Regional and global benthic δ18O stacks for the last glacial cycle. Paleoceanography 31, 1368–1394 (2016).Article 

    Google Scholar 
    Reimer, P. J. et al. IntCal13 and Marine13 radiocarbon age calibration curves 0–50,000 years cal BP. Radiocarbon 55, 1869–1887 (2013).CAS 
    Article 

    Google Scholar 
    Butzin, M., Köhler, P. & Lohmann, G. Marine radiocarbon reservoir age simulations for the past 50,000 years. Geophys. Res. Lett. 44, 8473–8480 (2017).CAS 
    Article 

    Google Scholar 
    Langner, M. & Mulitza, S. Technical Note: PaleoDataView—A software toolbox for the collection, homogenization and visualization of marine proxy data. Clim 15, 2067–2072 (2019).
    Google Scholar 
    Mix, A. C., Bard, E. & Schneider, R. Environmental processes of the ice age: land, oceans, glaciers (EPILOG). Quat. Sci. Rev. 20, 627–657 (2001).Article 

    Google Scholar 
    Osman, M. B. et al. Globally resolved surface temperatures since the Last Glacial Maximum. Nature 599, 239–244 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Horn, H. S. Measurement of ‘overlap’ in comparative ecological studies. Am. Nat. 100, 419–424 (1966).Article 

    Google Scholar 
    Jost, L., Chao, A. & Chazdon, R. L. in Biological diversity: frontiers in measurement and assessment (eds Anne E. Magurran & Brian J. McGill) 66–84 (Oxford University Press, 2011).Ferrier, S., Manion, G., Elith, J. & Richardson, K. Using generalized dissimilarity modelling to analyse and predict patterns of beta diversity in regional biodiversity assessment. Divers. Distrib. 13, 252–264 (2007).Article 

    Google Scholar 
    Shannon, C. E. A mathematical theory of communication. Bell Syst. Tech. J. 27, 379–423 (1948).Article 

    Google Scholar 
    R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2022).Wickham, H. et al. Welcome to the Tidyverse. J. Open Source Softw. 4, 1686 (2019).Article 

    Google Scholar 
    Firke, S. janitor: Simple tools for examining and cleaning dirty data. R package version 2.1.0 https://CRAN.R-project.org/package=janitor (2021).Oksanen, J. et al. vegan: Community ecology package. R package version 2.5-7 https://CRAN.R-project.org/package=vegan (2020).Hallett, L. M. et al. codyn: an R package of community dynamics metrics. Methods Ecol. Evol. 7, 1146–1151 (2016).Article 

    Google Scholar 
    Juggins, S. rioja: Analysis of quaternary science data. R package version 0.9-26 https://cran.r-project.org/package=rioja (2020).Lê, S., Josse, J. & Husson, F. FactoMineR: an R package for multivariate analysis. J. Stat. Softw. 25, 1–18 (2008).Article 

    Google Scholar 
    Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2016).Hijmans, R. J. raster: Geographic data analysis and modeling. R package version 3.4-13 https://CRAN.R-project.org/package=raster (2021).Garnier, S. viridis: Default color maps from ‘matplotlib’. R package version 0.6.1 https://CRAN.R-project.org/package=viridis (2021.)Locarnini, R. A. et al. World Ocean Atlas 2018, Vol. 1: Temperature. NOAA Atlas NESDIS 81 (NOAA, 2019). More

  • in

    Early Mars habitability and global cooling by H2-based methanogens

    Cockell, C. S. et al. Habitability: a review. Astrobiology 16, 89–117 (2016).ADS 
    Article 

    Google Scholar 
    Michalski, J. R. et al. The Martian subsurface as a potential window into the origin of life. Nat. Geosci. 11, 21–26 (2018).ADS 
    Article 

    Google Scholar 
    Fairén, A. G. et al. Stability against freezing of aqueous solutions on early Mars. Nature 459, 401–404 (2009).ADS 
    Article 

    Google Scholar 
    Clifford, S. M. et al. Depth of the Martian cryosphere: Revised estimates and implications for the existence and detection of subpermafrost groundwater. J. Geophys. Res. 115, E07001 (2010).ADS 
    Article 

    Google Scholar 
    Rivera-Valentín, E. G., Chevrier, V. F., Soto, A. & Martínez, G. Distribution and habitability of (meta)stable brines on present-day Mars. Nat. Astron. 4, 756–761 (2020).ADS 
    Article 

    Google Scholar 
    Stevens, A. H., Patel, M. R. & Lewis, S. R. Numerical modelling of the transport of trace gases including methane in the subsurface of Mars. Icarus 250, 587–594 (2015).ADS 
    Article 

    Google Scholar 
    Sholes, S. F., Krissansen-Totton, J. & Catling, D. C. A maximum subsurface biomass on mars from untapped free energy: CO and H2 as potential antibiosignatures. Astrobiology 19, 655–668 (2019).ADS 
    Article 

    Google Scholar 
    Wordsworth, R. D. The climate of early Mars. Annu. Rev. Earth Planet. Sci. 44, 381–408 (2016).ADS 
    Article 

    Google Scholar 
    Liu, J. et al. Anoxic chemical weathering under a reducing greenhouse on early Mars. Nat. Astron. 5, 503–509 (2021).ADS 
    Article 

    Google Scholar 
    Battistuzzi, F. U., Feijao, A. & Hedges, S. B. A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land. BMC Evol. Biol. 4, 44 (2004).Article 

    Google Scholar 
    Martin, W. F. & Sousa, F. L. Early microbial evolution: the age of anaerobes. Cold Spring Harbor Perspect. Biol 8, a018127 (2016).Article 

    Google Scholar 
    Sauterey, B. et al. Co-evolution of primitive methane-cycling ecosystems and early Earth’s atmosphere and climate. Nat. Commun. 11, 2705 (2020).ADS 
    Article 

    Google Scholar 
    Affholder, A. et al. Bayesian analysis of Enceladus’s plume data to assess methanogenesis. Nat. Astron. 5, 805–814 (2021).ADS 
    Article 

    Google Scholar 
    Wordsworth, R. et al. Transient reducing greenhouse warming on early Mars. Geophys. Res. Lett. 44, 665–671 (2017).ADS 
    Article 

    Google Scholar 
    Turbet, M., Boulet, C. & Karman, T. Measurements and semi-empirical calculations of CO2 + CH4 and CO2 + H2 collision-induced absorption across a wide range of wavelengths and temperatures. Application for the prediction of early Mars surface temperature. Icarus 346, 113762 (2020).Article 

    Google Scholar 
    Price, P. B. & Sowers, T. Temperature dependence of metabolic rates for microbial growth, maintenance, and survival. Proc. Nat. Acad. Sci. USA 101, 4631–4636 (2004).ADS 
    Article 

    Google Scholar 
    Taubner, R.-S. et al. Biological methane production under putative Enceladus-like conditions. Nat. Commun. 9, 748 (2018).ADS 
    Article 

    Google Scholar 
    Ramirez, R. M. A warmer and wetter solution for early Mars and the challenges with transient warming. Icarus 297, 71–82 (2017).ADS 
    Article 

    Google Scholar 
    Kharecha, P., Kasting, J. & Siefert, J. A coupled atmosphere–ecosystem model of the early Archean Earth. Geobiology 3, 53–76 (2005).Article 

    Google Scholar 
    Tarnas, J. D. et al. Radiolytic H2 production on Noachian Mars: implications for habitability and atmospheric warming. Earth Planet. Sci. Lett. 502, 133–145 (2018).ADS 
    Article 

    Google Scholar 
    Yung, Y. L. et al. Methane on Mars and habitability: challenges and responses. Astrobiology 18, 1221–1242 (2018).ADS 
    Article 

    Google Scholar 
    Knutsen, E. W. et al. Comprehensive investigation of Mars methane and organics with ExoMars/NOMAD. Icarus 357, 114266 (2021).Article 

    Google Scholar 
    Cockell, C. S. Trajectories of martian habitability. Astrobiology 14, 182–203 (2014).ADS 
    Article 

    Google Scholar 
    Westall, F. et al. Biosignatures on Mars: What, where, and how? Implications for the search for Martian life. Astrobiology 15, 998–1029 (2015).ADS 
    Article 

    Google Scholar 
    Lepot, K. Signatures of early microbial life from the Archean (4 to 2.5 Ga) eon. Earth Sci. Rev. 209, 103296 (2020).Article 

    Google Scholar 
    Fastook, J. L. & Head, J. W. Glaciation in the late noachian icy highlands: Ice accumulation, distribution, flow rates, basal melting, and top-down melting rates and patterns. Planet. Space Sci. 106, 82–98 (2015).ADS 
    Article 

    Google Scholar 
    Fassett, C. I. & Head, J. W. Valley network-fed, open-basin lakes on Mars: distribution and implications for Noachian surface and subsurface hydrology. Icarus 198, 37–56 (2008).ADS 
    Article 

    Google Scholar 
    Tanaka, K. L. et al. Geologic Map of Mars: U.S. Geological Survey Scientific Investigations Map 3292, Scale 1000,000 (US Geological Survey, 2014); https://doi.org/10.3133/sim3292Sun, V. Z. & Stack, K. M. Geologic Map of Jezero Crater and the Nili Planum Region, Mars: U.S. Geological Survey Scientific Investigations Map 3464, Scale 1000 (US Geological Survey, 2020); https://doi.org/10.3133/sim3464Ward, P. The Medea Hypothesis (Princeton Univ. Press, 2009).Chopra, A. & Lineweaver, C. H. The Case for a Gaian bottleneck: the biology of habitability. Astrobiology 16, 7–22 (2016).ADS 
    Article 

    Google Scholar 
    Arney, G. et al. The Pale Orange Dot: The Spectrum and Habitability of Hazy Archean Earth. Astrobiology 16, 873–899 (2016).Batalha, N. et al. Testing the early Mars H2-CO2 greenhouse hypothesis with a 1-D photochemical model. Icarus 258, 337–349 (2015).ADS 
    Article 

    Google Scholar 
    Stüeken, E. E. et al. Isotopic evidence for biological nitrogen fixation by molybdenum-nitrogenase from 3.2 Gyr. Nature 520, 666–669 (2015).ADS 
    Article 

    Google Scholar 
    Cockell, C. S. et al. Minimum units of habitability and their abundance in the universe. Astrobiology 21, 481–489 (2021).ADS 
    Article 

    Google Scholar 
    Adams, D. et al. Nitrogen fixation at early Mars. Astrobiology 21, 968–980 (2021).ADS 
    Article 

    Google Scholar 
    Fergason, R. L., Hare, T. M. and Laura, J. HRSC and MOLA Blended Digital Elevation Model at 200m v2. Astrogeology PDS Annex (US Geological Survey, 2018); http://bit.ly/HRSC_MOLA_Blend_v0Sauterey, B. MarsEcosys v.1.0. Zenodo https://doi.org/10.5281/zenodo.6963348 (2022). More

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    Resolving malaria’s dry-season dilemma

    Seasonal fluctuations in animal population dynamics are among the most fundamental attributes of life on Earth. A long recognized but poorly understood example is the dramatic seasonal fluctuation in the abundance of malaria vectors in the semi-arid savannah and Sahel regions of Africa. In these regions, the vector mosquitoes largely disappear during a prolonged 3- to 8-month dry season, when lack of rain causes the aquatic larval habitats to disappear. As a result, malaria transmission plummets. When the rains return, the mosquito vectors rapidly reappear, leading to a resurgence of malaria transmission. How the vector populations are able to persist through the prolonged dry season and rapidly rebound with the onset of rains is referred to as the ‘dry-season malaria paradox’, and has remained an enduring mystery of malariology for nearly 100 years. Writing in Nature Ecology & Evolution, Faiman et al.1 help to resolve this mystery by using an innovative isotopic labelling strategy: they demonstrate that at least approximately 20% of the local population of the malaria vector Anopheles coluzzi in the West African Sahel survive the dry season locally by undergoing summer dormancy, known as aestivation. More

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    Oceanic vertical migrators in a warming world

    Seibel, B. A. & Birk, M. A. Nat. Clim. Change https://doi.org/10.1038/s41558-022-01491-6 (2022).Article 

    Google Scholar 
    Urban, M. C. et al. Science 353, aad8466 (2016).Article 

    Google Scholar 
    Pörtner, H. O. & Knust, R. Science 315, 95–97 (2007).Article 

    Google Scholar 
    Verberk, W. C. E. P., Bilton, D. T., Calosi, P. & Spicer, J. I. Ecology 92, 1565–1572 (2011).Article 

    Google Scholar 
    Rubalcaba, J. G., Verberk, W. C., Hendriks, A. J., Saris, B. & Woods, H. A. Proc. Natl Acad. Sci. USA 117, 31963–31968 (2020).CAS 
    Article 

    Google Scholar 
    Deutsch, C. et al. Proc. Natl Acad. Sci. USA 119, e2201345119 (2022).CAS 
    Article 

    Google Scholar 
    Stramma, L. et al. Nat. Clim. Change 2, 33–37 (2012).CAS 
    Article 

    Google Scholar 
    Vergés, A. et al. Proc. R. Soc. B 281, 20140846 (2014).Article 

    Google Scholar  More

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    Protecting the Amazon forest and reducing global warming via agricultural intensification

    Study regions and recent trends in land use changeOur analysis focuses on four biomes (referred to as regions in the rest of the text), accounting for nearly all soybean area in Brazil: the Pampa, the Atlantic Forest, the Cerrado and the Amazon (Supplementary Section 1). Soybean production is negligible in the Pantanal and the Caatinga, so these two regions were excluded from our analysis. We focused on soybean-based systems in Brazil, either those that include one crop per year (single soybean) or those including a second-crop maize. In the latter system, soybean is sown in September–October, and maize is sown right after the soybean harvest in late January–February. Single soybean is common in the Pampa, where the drier climate does not allow double cropping. In contrast, higher precipitation allows double cropping in the Amazon, the Cerrado and most of the Atlantic Forest (Supplementary Section 2).Recent trends in yield, area and production for soybean and second-crop maize were derived from official statistics for the 2007–2019 period16. We fitted linear models to derive the annual rate of yield improvement and harvested area for soybean and second-crop maize, separately for each region (Fig. 1 and Extended Data Fig. 1). Land use change arising from soybean expansion was estimated using data from the MapBiomas project (v.5.0)10 (Supplementary Table 1). Our estimation of land use change accounted for the time lag between land conversion and the beginning of soybean production, which can include transitional stages such as the cultivation of upland rice or short-term pasture-based livestock systems42. To account for this, we looked at the new land brought into soybean production during the 2008–2019 period, and we analysed how much of this land was under a different land use type (forest, savannah, grassland, pasture or other crops) in 2000 (Extended Data Fig. 2).Estimation of yield potential and yield gapsWe used results on yield potential for Brazil that we generated through the Global Yield Gap Atlas project43 using well-validated process-based crop models and the best available sources of weather, soil and management data. Briefly, we selected 32 sites to portray the distribution of the soybean harvested area within the country, following protocols that ensure representativeness and a reasonable coverage of the national crop area44. The 32 sites collectively accounted for half of the soybean harvested area in Brazil. These sites were located within agro-climatic zones accounting for 86% of the national soybean production and accounted for 72–92% of the soybean area in each region. Following protocols that gave preference to measured data at a high level of spatial and temporal resolution45, we collected databases on weather, soil, management and crop yields for soybean for each site, and also for second-crop maize at those sites where double-cropping is practised (Supplementary Tables 2 and 3 and Supplementary Section 3).Yield potential was simulated for widespread cultivars in each region using the CROPGRO soybean model embedded in DSSAT v.4.546 and the Hybrid-Maize model47. Both models simulate crop growth and development on a daily time step. Growth rates are determined by simulating both CO2 assimilation and respiration, with partitioning coefficients to different organs dependent on developmental stage. The model phenological coefficients were calibrated to portray the crop cycle of the most dominant cultivars in each region in Brazil. We used generic default coefficients for growth-related model internal parameters such as photosynthesis, respiration, leaf area expansion, light interception, biomass partitioning and grain filling. In all cases, simulations of yield potential assumed the absence of insect pests, weeds and diseases and no nutrient limitations. In simulating yield potential, both models account for solar radiation, photoperiod, temperature, and the timing and amount of rainfall as well as soil properties influencing crop water balance.We first evaluated the CROPGRO and Hybrid-Maize models on the ability to reproduce measured phenology and yields across 40 well-managed experiments located across the four regions. The models showed satisfactory performance at reproducing the measured values (Extended Data Fig. 3). We then simulated soybean yield potential for the dominant agricultural soils at each site (usually two or three), as determined from the soil maps generated by the Radambrasil project48. The simulations were based on long-term (1999–2018) measured daily weather data retrieved from the Brazilian Institute of Meteorology49. Soybean yield potential was simulated for each year of the time series. We also simulated yield potential for second-crop maize for those sites where double-cropping is practised. To do so, we used sowing dates and cultivar maturities that maximize the overall productivity of the soybean–maize system; these sowing dates and cultivar maturities are within the current ranges in each region21,28. To estimate the average yield potential for each site, we weighted the simulated values for each soil type by soil area fraction at each site. In all cases, the simulations assumed no limitations to crop growth due to nutrient deficiencies or incidence of biotic stresses such as weeds, insect pests and pathogens. The results were upscaled from site to region and then to country following van Bussel et al.44. Briefly, the average yield potential for each region was estimated by averaging the simulated yields across the sites located within each region, weighing sites according to their share of the soybean area within each region. A similar approach was followed to upscale yield potential from region to the national level. Details on crop modelling, data sources and upscaling are provided in Supplementary Section 3.The average farmer yield was calculated separately for soybean and second-crop maize on the basis of the average yield reported over the 2012–2017 period for the municipalities that overlap with each site, weighing municipalities on the basis of their share of the soybean or maize area within each site16. Including more years before 2012 would have led to a biased estimate of average actual yield due to the technological yield trend in Brazil. Average farmer yields were estimated at the region and country levels following the same upscaling approach as for yield potential. Finally, the exploitable yield gap was calculated as the difference between attainable yield and average farmer yield. The attainable yield was calculated as 80% of the simulated yield potential, which is considered a reasonable yield for farmers with adequate access to inputs, markets and technical information (Supplementary Section 2).Assessing scenarios of intensification and land use changeWe explored three scenarios with different soybean and maize yields and areas by 2035 and assessed their outcomes in terms of production, land use change and GWP (Supplementary Table 4). A 15-year future timespan is long enough to facilitate the implementation of long-term policies, investments and technologies devoted to closing the exploitable yield gap and to implement land-use policies, but it is short enough to minimize long-term effects from climate change on crop yields and cropping systems. In the BAU scenario, historical (2007–2019) trends of soybean and second-crop maize area and yield (Extended Data Fig. 1) remain unchanged in all regions between the baseline year (2019) and the final year (2035). Likewise, soybean area expands following the same pattern of land use change observed during 2008–2019 (Extended Data Fig. 2).To explore the available opportunity for increasing production on the existing production area, we considered an NCE scenario in which there is no physical expansion of cropland while full closure of the exploitable yield gap occurs in the regions where the current yield gaps are small (the Pampa and the Atlantic Forest), and 50% closure of the exploitable yield gap takes place in regions where the current yield gaps are large (the Amazon and the Cerrado) (Supplementary Table 4). These rates are comparable to historical yield gains in the Pampa and the Atlantic Forest. A scenario of full yield closure in the Amazon and the Cerrado would have been unrealistic, as it would have required rates of yield improvement that are three to four times higher than historical rates, much higher than those in the Pampa and the Atlantic Forest, and well beyond those reported for main soybean-producing countries. In the case of second-crop maize, we assumed full closure of the exploitable yield gap by 2035 because historical rates of yield improvement are adequate to reach that yield level. Regarding second-crop maize area, we projected the proportion of double-cropping to increase from the current 47% (Amazon), 39% (Cerrado) and 31% (Atlantic Forest) to 100%, 70% and 50%, respectively, as determined on the basis of the degree of water limitation in each region (Supplementary Section 4).Finally, we explored a third scenario of intensification plus target area expansion (INT), in which identical yield gain rates and the adoption of double-cropping equivalent to those in the NCE scenario were assumed, but with physical expansion of the soybean–maize system allowed in low-C ecosystems (that is, pastures and grasslands). In this scenario, soybean expansion is limited to 5% of existing pastures and grasslands in the Pampa, the Atlantic Forest and the Cerrado (total of 5.7 Mha) as a result of a parallel intensification in the pasture-based livestock sector that frees up land for soybean production. The latter would require an increase of current stocking rates, not only for freeing up 5% of the area for soybean cultivation but also to meet the projected 7% beef production increase during the study period (2020–2035)17. Hence, an overall 12% increase in stocking rates would be required within our 15-year timeframe, which is a reasonable target as reported in previous studies and based on current trends in stocking rates16,29,32,33.Another assumption is that the yield potential of pasture and grasslands converted for soybean production is similar to that in existing soybean areas in each region. Cropland expansion into grassland and pastures was allowed in all regions except for the Amazon to prevent ‘leaking’ effects and the impact of road development on land clearing50,51. Similarly, the conversion of area cultivated with food crops for soybean production was not allowed to avoid the negative impact of indirect land use change52.Estimation of GWP and gross incomeWe estimated GHG emissions, including carbon dioxide (CO2), methane (CH4) and nitrous oxides (N2O), associated with land conversion (GHGLUC) and crop production (GHGPROD) for the baseline year (2019) and for the three scenarios by year 2035 (BAU, NCE and INT). GHGLUC includes emissions associated with changes in C stocks from aboveground and belowground biomass when land is converted for soybean production (GHGBIO), as well as GHG emissions derived from changes in soil organic C (GHGSOC). For each land use type, annual GHGBIO was estimated on the basis of the difference between C stocks of the land use type that was converted for production (Supplementary Table 5) and, depending on the scenario and region, the average C stocks of the new cropping system53,54,55:$${mathrm{GHG}}_{{mathrm{BIO}}} = {sum} {left( {{mathrm{TDM}}_i-{mathrm{TDM}}_{{mathrm{crop}}}} right) times A_i}$$
    (1)
    where i is the land cover type, TDM is the total dry matter (tC ha−1) in land cover type i and in cropland (crop), and Ai is the annual area converted from land use type i for soybean cultivation (Supplementary Table 4). C stocks for single soybean and soybean–second-crop maize systems were assumed at 2 and 5 tC ha−1, respectively53,54,55. Changes in SOC stocks were estimated following the Intergovernmental Panel on Climate Change 2019 guidelines54, available country-specific emission factors56 and the SOC values estimated for each region57,58:$${mathrm{GHG}}_{{mathrm{SOC}}} = {sum} {left( {{mathrm{SOC}}_{{mathrm{REF}},i} times F_{{mathrm{LU}}}} right) times A_i}$$
    (2)
    where SOCREF is the SOC stock for mineral soils in the upper 30 cm for the reference condition (tC ha−1)57 in land cover type i (Supplementary Table 5), and FLU is the stock change factor for SOC land-use systems for a particular land use (Supplementary Table 4). Because no-till is the predominant soil management strategy in Brazil59, we used FLU = 0.96 for natural vegetation converted to no-till annual crop production, and FLU = 1.16 for pasture and grassland converted to no-till annual crop production56. Because we wanted to assess the full impact of the three scenarios (BAU, NCE and INT) on GWP, we assigned all GHGBIO and GHGSOC derived from land conversion to the first year after land conversion and expressed them as CO2 equivalents by multiplying changes in C stocks by 3.67.Annual GHG emissions derived from soybean and second-crop maize production (GHGPROD) were calculated for each scenario and included those derived from manufacturing, packaging and transportation of agricultural inputs, fossil fuel use for field operations, soil N2O emissions derived from the application of nitrogen (N) fertilizer, and domestic grain transportation. For the baseline year (2019), annual GHG emissions from N, phosphorous (P) and potassium (K) fertilizers and other inputs (lime, pesticides and fuel) were calculated on the basis of current average input rates for soybean and second-crop maize in each region as derived from the crop management data collected for each region (Supplementary Table 6 and Supplementary Section 3.4). To calculate GHG emissions associated with manufacturing, packaging and transportation of N, P and K fertilizers and lime, we used specific updated emissions factors for South America60, selecting those fertilizer sources that are most commonly used for soybean and second-crop maize production: urea (N), monoammonium phosphate (P) and potassium chloride (K). Our calculations also included the extra lime application that is needed to correct soil acidity in converted areas. Emission factors associated with seed production, pesticides and diesel were derived from ref. 61. Soil N2O emissions derived from N fertilizer application were calculated assuming an N2O emission factor of 1% of the applied N fertilizer on the basis of the country-specific emission factor62. Emissions derived from domestic grain transportation for each region were estimated using the GHGs per ton of grain as reported by previous studies for each region63. We assumed that inputs other than nutrient fertilizer will not change relative to the baseline in the BAU scenario. In the INT scenario, applied inputs were calculated on the basis of those reported for current high-yield fields where the yield gap is small. We estimated fertilizer nutrient rates for the three scenarios following a nutrient-balance approach that depends on the projected yield for each scenario (Supplementary Table 6 and Supplementary Section 3.4).GHGPROD in the baseline year (2019) and for the three scenarios in 2035 (BAU, NCE and INT) was estimated for each region by multiplying the emissions per unit of area by the annual soybean harvested area, summing them to estimate GHG emissions at the national level. Overall 100-year GWP was estimated as the sum of GHGLUC and GHGPROD, both expressed as CO2e to account for the higher warming potential of CH4 and N2O, which are 25 and 298 times the intensity of CO2 on a per mass basis, respectively. The gross income was estimated for each scenario by multiplying the annual crop production by the average price for soybean and maize grain during the past ten years (US$453 and US$184 per t for soybean and maize, respectively1). Finally, to combine the environmental and economic impacts into one metric, we calculated the GWP intensity as the ratio between GWP and gross income.Reporting summaryFurther information on research design is available in the Nature Research Reporting Summary linked to this article. More

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    Isotopic evidence that aestivation allows malaria mosquitoes to persist through the dry season in the Sahel

    Adamou, A. et al. The contribution of aestivating mosquitoes to the persistence of Anopheles gambiae in the Sahel. Malar. J. 10, 151 (2011).PubMed 
    PubMed Central 

    Google Scholar 
    Huestis, D. L. et al. Seasonal variation in metabolic rate, flight activity and body size of Anopheles gambiae in the Sahel. J. Exp. Biol. 215, 2013–2021 (2012).PubMed 
    PubMed Central 

    Google Scholar 
    Huestis, D. L. et al. Variation in metabolic rate of Anopheles gambiae and A. arabiensis in a Sahelian village. J. Exp. Biol. 214, 2345–2353 (2011).PubMed 
    PubMed Central 

    Google Scholar 
    Lehmann, T. et al. Aestivation of the African malaria mosquito, Anopheles gambiae in the Sahel. Am. J. Trop. Med. Hyg. 83, 601–606 (2010).PubMed 
    PubMed Central 

    Google Scholar 
    Yaro, A. S. et al. Dry season reproductive depression of Anopheles gambiae in the Sahel. J. Insect Physiol. 58, 1050–1059 (2012).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Omer, S. M. & Cloudsley-Thompson, J. L. Survival of female Anopheles gambiae Giles through a 9-month dry season in Sudan. Bull. World Health Organ. 42, 319 (1970).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Omer, S. M. & Cloudsley-Thompson, J. L. Dry season biology of Anopheles gambiae Giles in the Sudan. Nature 217, 879–880 (1968).
    Google Scholar 
    Holstein, M. H. Biology of Anopheles gambiae (1954). World Health Organization.Andrade, C. M. et al. Increased circulation time of Plasmodium falciparum underlies persistent asymptomatic infection in the dry season. Nat. Med. 26, 1929–1940 (2020).CAS 
    PubMed 

    Google Scholar 
    Coulibaly, D. et al. Spatio-temporal dynamics of asymptomatic malaria: bridging the gap between annual malaria resurgences in a Sahelian environment. Am. J. Trop. Med. Hyg. 27, 1761–1769 (2017).
    Google Scholar 
    Gillies, M. & Wilkes, T. A study of the age-composition of populations of Anopheles gambiae Giles and A. funestus Giles in north-eastern Tanzania. Bull. Entomol. Res. 56, 237–262 (1965).CAS 
    PubMed 

    Google Scholar 
    Gillies, M. T. & De Meillon, B. The Anophelinae of Africa south of the Sahara (Ethiopian Zoogeographical Region) (Johannesburg: South African Institute for Medical Research, 1968).Dao, A. et al. Signatures of aestivation and migration in Sahelian malaria mosquito populations. Nature 516, 387–390 (2014).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Thomson, J. G. Malaria in Nyasaland. Proc. R. Soc. Med. 28, 391–404 (1934).
    Google Scholar 
    Huestis, D. L. et al. Windborne long-distance migration of malaria mosquitoes in the Sahel. Nature 574, 404–408 (2019).CAS 
    PubMed 

    Google Scholar 
    Lambert, B., North, A., Burt, A. & Godfray, H. C. J. The use of driving endonuclease genes to suppress mosquito vectors of malaria in temporally variable environments. Malar. J. 17, 154 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    Verhulst, N. O., Loonen, J. A. C. M. & Takken, W. Advances in methods for colour marking of mosquitoes. Parasit. Vectors 6, 200 (2013).PubMed 
    PubMed Central 

    Google Scholar 
    Hagler, J. R. & Jackson, C. G. Methods for marking insects: current techniques and future prospects. Annu. Rev. Entomol. 46, 511–543 (2001).CAS 
    PubMed 

    Google Scholar 
    Hamer, G. L. et al. Dispersal of adult culex mosquitoes in an urban West Nile virus hotspot: a mark–capture study incorporating stable isotope enrichment of natural larval habitats. PLoS Negl. Trop. Dis. 8, e2768 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    Hamer, G. L. et al. Evaluation of a stable isotope method to mark naturally-breeding larval mosquitoes for adult dispersal studies. J. Med. Entomol. 49, 61–70 (2012).CAS 
    PubMed 

    Google Scholar 
    Opiyo, M. A. et al. Using stable isotopes of carbon and nitrogen to mark wild populations of Anopheles and Aedes mosquitoes in south-eastern Tanzania. PLoS ONE 11, e0159067 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Hood-Nowotny, R., Mayr, L. & Knols, B. Use of carbon-13 as a population marker for Anopheles arabiensis in a sterile insect technique (SIT) context. Malar. J. 5, 6 (2006).PubMed 
    PubMed Central 

    Google Scholar 
    Hood-Nowotny, R. & Knols, B. G. J. Stable isotope methods in biological and ecological studies of arthropods. Entomol. Exp. Appl. 124, 3–16 (2007).CAS 

    Google Scholar 
    Hood-Nowotny, R. et al. Intrinsic and synthetic stable isotope marking of tsetse flies. J. Insect Sci. 11, 79 (2011).PubMed 
    PubMed Central 

    Google Scholar 
    Atzrodt, J., Derdau, V., Kerr, W. J. & Reid, M. Deuterium- and tritium-labelled compounds: applications in the life sciences. Angew. Chem. Int. Ed. 57, 1758–1784 (2018).CAS 

    Google Scholar 
    Copia, L., Wassenaar, L. I., Terzer-Wassmuth, S., Belachew, D. L. & Araguas-Araguas, L. J. Comparative evaluation of 2H- versus 3H-based enrichment factor determination on the uncertainty and accuracy of low-level tritium analyses of environmental waters. Appl. Radiat. Isot. 176, 109850 (2021).CAS 
    PubMed 

    Google Scholar 
    Begon, M., Harper, J. & Townsend, C. Ecology: Individuals, Populations and Communities (Blackwell Science, 1996).Faiman, R. et al. Marking mosquitoes in their natural larval sites using 2H-enriched water: a promising approach for tracking over extended temporal and spatial scales. Methods Ecol. Evol. 10, 1274–1285 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    Florkin, M. Chemical Zoology: Arthropoda Part B (Academic Press, 2014).Hackman, R. H. & Goldberg, M. Studies on chitin VI. The nature of alpha-and beta-chitins. Aust. J. Biol. Sci. 18, 935–946 (1965).CAS 
    PubMed 

    Google Scholar 
    Faiman, R. et al. Quantifying flight aptitude variation in wild Anopheles gambiae in order to identify long-distance migrants. Malar. J. 19, 263 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    Huestis, D. L. & Lehmann, T. Ecophysiology of Anopheles gambiae s.l.: persistence in the Sahel. Infect. Genet. Evol. 28, 648–661 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    Lehmann, T. et al. Seasonal variation in spatial distributions of Anopheles gambiae in a Sahelian village: evidence for aestivation. J. Med. Entomol. 51, 27–38 (2014).PubMed 

    Google Scholar 
    Costantini, C. et al. Density, survival and dispersal of Anopheles gambiae complex mosquitoes in a West African Sudan savanna village. Med. Vet. Entomol. 10, 203–219 (1996).CAS 
    PubMed 

    Google Scholar 
    Toure, Y. T. et al. Mark–release–recapture experiments with Anopheles gambiae s.l. in Banambani Village, Mali, to determine population size and structure. Med. Vet. Entomol. 12, 74–83 (1998).CAS 
    PubMed 

    Google Scholar 
    Faiman, R. et al. A novel fluorescence and DNA combination for versatile, long-term marking of mosquitoes. Methods Ecol. Evol. https://doi.org/10.1111/2041-210X.13592 (2021).Brattström, O., Bensch, S., Wassenaar, L. I., Hobson, K. A. & Åkesson, S. Understanding the migration ecology of European red admirals Vanessa atalanta using stable hydrogen isotopes. Ecography 33, 720–729 (2010).
    Google Scholar 
    Hobson, K. A., Jinguji, H., Ichikawa, Y., Kusack, J. W. & Anderson, R. C. Long-distance migration of the globe skimmer dragonfly to Japan revealed using stable hydrogen (δ 2H) isotopes. Environ. Entomol. 50, 247–255 (2020).
    Google Scholar 
    Schilling, E. G. et al. Phenological and isotopic evidence for migration as a life history strategy in Aeshna canadensis (family: Aeshnidae) dragonflies. Ecol. Entomol. 46, 209–219 (2021).
    Google Scholar 
    Girard, P., Hillaire-Marcel, C. & Oga, M. S. Determining the recharge mode of Sahelian aquifers using water isotopes. J. Hydrol. 197, 189–202 (1997).CAS 

    Google Scholar 
    Gutiérrez-Expósito, C., Ramírez, F., Afán, I., Forero, M. & Hobson, K. A. Toward a deuterium feather isoscape for sub-Saharan Africa: progress, challenges and the path ahead. PLoS ONE https://doi.org/10.1371/journal.pone.0135938 (2015).Lutz, A., Thomas, J. M. & Panorska, A. Environmental controls on stable isotope precipitation values over Mali and Niger, West Africa. Environ. Earth Sci. 62, 1749–1759 (2011).CAS 

    Google Scholar 
    Risi, C. et al. Understanding the Sahelian water budget through the isotopic composition of water vapor and precipitation. J. Geophys. Res. Atmos. 115, 1–23 (2010).
    Google Scholar 
    Tremoy, G. et al. A 1-year long δ18O record of water vapor in Niamey (Niger) reveals insightful atmospheric processes at different timescales. Geophys. Res. Lett. 39, 1–5 (2012).
    Google Scholar 
    Terzer‐Wassmuth, S., Wassenaar, L. I., Welker, J. M., Araguás-Araguás, L. J. Improved high‐resolution global and regionalized isoscapes of δ18O, δ2H and d‐excess in precipitation. Hydrol. Process. 35 (2021).Hobson, K. A. et al. A multi-isotope (δ13C, δ15N, δ2H) feather isoscape to assign Afrotropical migrant birds to origins. Ecosphere 3, art44 (2012).
    Google Scholar 
    Diuk-Wasser, M. A. et al. Effect of rice cultivation patterns on malaria vector abundance in rice-growing villages in Mali. Am. J. Trop. Med. Hyg. 76, 869–874 (2007).PubMed 

    Google Scholar 
    Sogoba, N. et al. Malaria transmission dynamics in Niono, Mali: the effect of the irrigation systems. Acta Trop. 101, 232–240 (2007).PubMed 

    Google Scholar 
    Florio, J. et al. Diversity, dynamics, direction, and magnitude of high-altitude migrating insects in the Sahel. Sci. Rep. 10, 20523 (2020).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wilkins, E. E., Howell, P. I. & Benedict, M. Q. IMP PCR primers detect single nucleotide polymorphisms for Anopheles gambiae species identification, Mopti and Savanna rDNA types, and resistance to dieldrin in Anopheles arabiensis. Malar. J. 5, 125 (2006).PubMed 
    PubMed Central 

    Google Scholar 
    Wassenaar, L. I. & Hobson, K. A. Comparative equilibration and online technique for determination of non-exchangeable hydrogen of keratins for use in animal migration studies. Isotopes Environ. Health Stud. 39, 211–217 (2003).CAS 
    PubMed 

    Google Scholar 
    Chesson, L. A., Podlesak, D. W., Cerling, T. E. & Ehleringer, J. R. Evaluating uncertainty in the calculation of non-exchangeable hydrogen fractions within organic materials. Rapid Commun. Mass Spectrom. 23, 1275–1280 (2009).CAS 
    PubMed 

    Google Scholar 
    Schimmelmann, A. Determination of the concentration and stable isotopic composition of nonexchangeable hydrogen in organic matter. Anal. Chem. 63, 2456–2459 (1991).CAS 

    Google Scholar 
    Speakman, J. Doubly Labelled Water: Theory and Practice (Chapman & Hall, 1997).Base SAS 9.4 Procedures Guide (SAS Institute, 2015).Cade, B. S. & N, B. R. A gentle introduction to quantile regression for ecologists. Front. Ecol. Environ. 1, 412–420 (2003).
    Google Scholar 
    SAS/STAT® 15.1 User’s Guide (SAS Institute, 2018).Mcclintock, B. T. et al. Uncovering ecological state dynamics with hidden Markov models. Ecol. Lett. 23, 1878–1903 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    Issam, M., Naulet, N., Martin, M. L. & Martin, G. J. A site-specific and multielement approach to the determination of liquid–vapor isotope fractionation parameters: the case of alcohols. J. Phys. Chem. 94, 8303–8309 (1990).
    Google Scholar 
    Linderstrøm-Lang, C. U. & Vaslow, F. Isotope effect on the vapor pressures of water–ethanol and deuterium oxide–ethanol-d mixtures. J. Phys. Chem. 72, 2645–2650 (1968).
    Google Scholar 
    Ventura, M. & Jeppesen, E. Effects of fixation on freshwater invertebrate carbon and nitrogen isotope composition and its arithmetic correction. Hydrobiologia 632, 297–308 (2009).CAS 

    Google Scholar  More

  • in

    Unique thermal sensitivity imposes a cold-water energetic barrier for vertical migrators

    Robison, B. H. Conservation of deep pelagic biodiversity. Conserv. Biol. 23, 847–858 (2009).
    Google Scholar 
    Fernandez-Alamo, M. A. & Färber-Lorda, J. Zooplankton and the oceanography of the eastern tropical Pacific: a review. Prog. Oceanogr. 69, 318–359 (2006).
    Google Scholar 
    Bianchi, D., Galbraith, E. D., Carozza, D. A., Mislan, K. A. S. & Stock, C. A. Intensification of open-ocean oxygen depletion by vertically migrating animals. Nat. Geosci. 6, 545–548 (2013).CAS 

    Google Scholar 
    Steinberg, D. K. & Landry, M. R. Zooplankton and the ocean carbon cycle. Annu. Rev. Mar. Sci. 9, 413–444 (2017).
    Google Scholar 
    Kiko, R. & Hauss, H. On the estimation of zooplankton-mediated active fluxes in oxygen minimum zones regions. Front. Mar. Sci. https://doi.org/10.3389/fmars.2019.00741 (2019).Longhurst, A., Bedo, A., Harrison, W., Head, E. & Sameoto, D. Vertical flux of respiratory carbon by oceanic diel migrant biota. Deep Sea Res. Part I 37, 685–694 (1990).CAS 

    Google Scholar 
    Elder, L. E. & Seibel, B. A. The thermal stress response to diel vertical migration in the hyperiid amphipod, Phronima sedentaria. Comp. Biochem. Physiol. A 187, 20–26 (2015).CAS 

    Google Scholar 
    Tremblay, N., Gomez-Gutierrez, J., Zenteno-Savin, T., Robinson, C. J. & Sanchez-Velascoa, L. Role of oxidative stress in seasonal and daily vertical migration of three krill species in the Gulf of California. Limnol. Oceanogr. 55, 2570–2584 (2010).CAS 

    Google Scholar 
    Lopes, A. R. et al. Oxidative stress in deep scattering layers: heat shock response and antioxidant enzymes activities of myctophid fishes thriving in oxygen minimum zones. Deep Sea Res. Part I 82, 10–16 (2013).CAS 

    Google Scholar 
    Seibel, B. A., Schneider, J., Kaartvedt, S., Wishner, K. F. & Daly, K. L. Hypoxia tolerance and metabolic suppression in oxygen minimum zone euphausiids: implications for ocean deoxygenation and biogeochemical cycles. Integr. Comp. Biol. https://doi.org/10.1093/icb/icw091 (2016).Seibel, B. A. et al. Metabolic suppression during protracted exposure to hypoxia in the jumbo squid, Dosidicus gigas, living in an oxygen minimum zone. J. Exp. Biol. 217, 2710–2716 (2014).
    Google Scholar 
    Wishner, K. F. et al. Ocean deoxygenation and zooplankton: very small oxygen differences matter. Sci. Adv. 4, eaau5180 (2018).CAS 

    Google Scholar 
    Koslow, J. A., Goericke, R., Lara-Lopez, A. & Watson, W. Impact of declining intermediate-water oxygen on deepwater fishes in the California Current. Mar. Ecol. Prog. Ser. 436, 207–218 (2011).
    Google Scholar 
    Oschlies, A. A committed fourfold increase in ocean oxygen loss. Nat. Commun. 12, 2307 (2021).CAS 

    Google Scholar 
    Wishner, K. F., Seibel, B. A. & Outram, D. Ocean deoxygenation and copepods: coping with oxygen minimum zone variability. Biogeosciences 17, 2315–2339 (2020).
    Google Scholar 
    Stramma, L. et al. Expansion of oxygen minimum zones may reduce available habitat for tropical pelagic fishes. Nat. Clim. Change 2, 33–37 (2012).CAS 

    Google Scholar 
    Köhn, E. E., Münnich, M., Vogt, M., Desmmet, F. & Gruber, N. Strong habitat compression by extreme shoaling events of hypoxic waters in the Eastern Pacific. J. Geophys. Res. Oceans 127, e2022JC018429 (2022).
    Google Scholar 
    Poloczanska, E. S. et al. Global imprint of climate change on marine life. Nat. Clim. Change 3, 919–925 (2013).
    Google Scholar 
    Pinsky, M. L., Selden, R. L. & Kitchel, Z. J. Climate-driven shifts in marine species ranges: scaling from organisms to communities. Annu. Rev. Mar. Sci. 12, 153–179 (2020).
    Google Scholar 
    Cavole, L. M. et al. Biological impacts of the 2013–2015 warm-water anomaly in the northeast Pacific: winners, losers, and the future. Oceanography 29, 273–285 (2016).
    Google Scholar 
    Lavaniegosa, B. E., Jiménez-Herrera, M. A. & Ambriz-Arreola, I. Unusually low euphausiid biomass during the warm years of 2014–2016 in the transition zone of the California Current. Deep Sea Res. Part II 1, 69–170 (2019).
    Google Scholar 
    Lilly, L. E. & Ohman, M. D. Euphausiid spatial displacements and habitat shifts in the southern California Current system in response to El Niño variability. Prog. Oceanogr. 193, 102544 (2021).
    Google Scholar 
    Zeidberg, L. D. & Robison, B. H. Invasive range expansion by the Humboldt squid, Dosidicus gigas, in the eastern North Pacific. Proc. Natl Acad. Sci. USA 104, 12948–12950 (2007).CAS 

    Google Scholar 
    Szesciorka, A. R. et al. Timing is everything: drivers of interannual variability in blue whale migration. Sci. Rep. 10, 7710 (2020).CAS 

    Google Scholar 
    Hoving, H.-J. et al. Extreme plasticity in life‐history strategy allows a migratory predator (jumbo squid) to cope with a changing climate. Glob. Change Biol. 19, 2089–2103 (2013).
    Google Scholar 
    Boscolo-Galazzo, F. et al. Temperature controls carbon cycling and biological evolution in the ocean twilight zone. Science 371, 1148–1152 (2021).CAS 

    Google Scholar 
    Deutsch, C., Ferrel, A., Seibel, B. A., Pörtner, H.-O. & Huey, R. B. Climate change tightens a metabolic constraint on marine habitats. Science 348, 1132–1135 (2015).CAS 

    Google Scholar 
    Seibel, B. A. & Deutsch, C. Oxygen supply capacity in animals evolves to meet maximum demand at the current oxygen partial pressure regardless of size or temperature. J. Exp. Biol. 223, jeb210492 (2020).
    Google Scholar 
    Deutsch, C., Penn, J. L. & Seibel, B. A. Diverse hypoxia and thermal tolerances shape biogeography of marine animals. Nature 585, 557–562 (2020).CAS 

    Google Scholar 
    Childress, J. J. Are there physiological and biochemical adaptations of metabolism in deep-sea animals? Trends Ecol. Evol. 10, 30–36 (1995).CAS 

    Google Scholar 
    Seibel, B. A. & Drazen, J. C. The rate of metabolism in marine animals: environmental constraints, ecological demands and energetic opportunities. Philos. Trans. R. Soc. B. 362, 2061–2078 (2007).CAS 

    Google Scholar 
    Seibel, B. A. et al. Oxygen supply capacity breathes new life into the critical oxygen partial pressure (Pcrit). J. Exp. Biol. 224, jeb242210 (2021).
    Google Scholar 
    Childress, J. J. & Seibel, B. A. Life at stable low oxygen: adaptations of animals to oceanic oxygen minimum layers. J. Exp. Biol. 201, 1223–1232 (1998).CAS 

    Google Scholar 
    Garcia, H. E., et al. World Ocean Atlas 2018, Volume 3: Dissolved Oxygen, Apparent Oxygen Utilization, and Oxygen Saturation (NOAA/NESDIS, 2019).Locarnini, R. A., et. al. World Ocean Atlas 2018, Volume 1: Temperature (NOAA/NESDIS, 2019).Maas, A. E., Frazar, S., Outram, D., Seibel, B. A. & Wishner, K. F. Fine-scale vertical distribution of macroplankton and micronekton in an eastern tropical North Pacific in association with an oxygen minimum zone. J. Plankton Res. 36, 1557–1575 (2014).
    Google Scholar 
    Rosa, R. & Seibel, B. A. Synergistic effect of climate-related variables suggests future physiological impairment in a top oceanic predator. Proc. Natl Acad. Sci. USA 52, 20776–20780 (2008).
    Google Scholar 
    Halsey, L. G., Killen, S. S., Clark, T. D. & Norin, T. Exploring key issues of aerobic scope interpretation in ectotherms: absolute versus factorial. Rev. Fish. Biol. Fish. 28, 405–415 (2018).
    Google Scholar 
    Peterson, C. C., Nagy, K. A. & Diamond, J. Sustained metabolic scope. Proc. Natl Acad. Sci. USA 87, 2324–2328 (1990).CAS 

    Google Scholar 
    Seibel, B. A., Luu, B. E., Tessier, S. N., Towanda, T. & Storey, K. B. Metabolic suppression in the pelagic crab, Pleuroncodes planipes, in oxygen minimum zones. Comp. Biochem. Physiol. A 224, 88–97 (2018).CAS 

    Google Scholar 
    Hadj-Moussa, H., Logan, S. M., Seibel, B. A. & Storey, K. B. Potential role for microRNA in regulating hypoxia-induced metabolic suppression in the jumbo squid? BBA Gene Regul. Mech. 1861, 586–593 (2018).CAS 

    Google Scholar 
    Torres, J. J. & Childress, J. J. Relationship of oxygen consumption to swimming speed in Euphausia pacifica. Mar. Biol. 74, 79–86 (1983).
    Google Scholar 
    Cohen, J. H. & Forward, R. B. Jr. Zooplankton diel vertical migration—a review of proximate control. Oceanogr. Mar. Biol. Annu. Rev. 47, 77–110 (2009).
    Google Scholar 
    Gilly, W. F. et al. Locomotion and behavior of Humboldt squid, Dosidicus gigas, in relation to natural hypoxia in the Gulf of California, Mexico. J. Exp. Biol. 215, 3175–3190 (2012).
    Google Scholar 
    Jaffe, J. S., Ohman, M. D. & De Robertis, A. Sonar estimates of daytime activity levels of Euphausia pacifica in Saanich inlet. Can. J. Fish. Aquat. Sci. 56, 2000–2010 (1999).
    Google Scholar 
    Klevjer, T. A. & Kaartvedt, S. Krill (Meganyctiphanes norvegica) swim faster at night. Limnol. Oceanogr. 56, 765–774 (2011).
    Google Scholar 
    Backus, R. H. et al. Ceratoscopelus maderensis: pecuiiar sound-scattering layer identified with this myctophid fish. Science 160, 991–993 (1968).CAS 

    Google Scholar 
    Barham, E. G. in Proceedings of an International Symposium on Biological Sound Scattering in the Ocean (ed. Farquhar, G. B.) 100–118 (Superintendent of Documents, 1971).Sanders, N. K. & Childress, J. J. A comparison of the respiratory function of the haemocyanins of vertically migrating and non-migrating pelagic, deep-sea Oplophorid shrimps. J. Exp. Biol. 152, 167–187 (1990).
    Google Scholar 
    Seibel, B. A. Critical depth in the jumbo squid, Dosidicus gigas (Ommastrephidae), living in oxygen minimum zones II. Blood-oxygen binding. Deep Sea Res. Part II 95, 139–144 (2013).CAS 

    Google Scholar 
    Pörtner, H.-O., Bock, C. & Mark, F. C. Oxygen- and capacity-limited thermal tolerance: bridging ecology and physiology. J. Exp. Biol. 220, 2685–2696 (2017).
    Google Scholar 
    Laffoley, D. & Baxter, J. M. Ocean Deoxygenation: Everyone’s Problem—Causes, Impacts, Consequences and Solutions (IUCN, 2019).Birk, M. A. Respirometry: Tools for Conducting and Analyzing Respirometry Experiments. R version 1.4.0 http://cran.r-project.org/package=respirometry (2021).Huang, B. et al. Improvements of the daily optimum interpolation sea surface temperature (DOISST) Version 2.1. J. Clim. 34, 2923–2939 (2021).
    Google Scholar  More