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    Phosphorus supply affects long-term carbon accumulation in mid-latitude ombrotrophic peatlands

    1.Loisel, J. et al. A database and synthesis of northern peatland soil properties and Holocene carbon and nitrogen accumulation. Holocene 24, 1028–1042 (2014).
    Google Scholar 
    2.Loisel, J. et al. Insights and issues with estimating northern peatland carbon stocks and fluxes since the Last Glacial Maximum. Earth Sci. Rev. 165, 59–80 (2017).CAS 

    Google Scholar 
    3.Yu, Z., Loisel, J., Brosseau, D. P., Beilman, D. W. & Hunt, S. J. Global peatland dynamics since the Last Glacial Maximum. Geophys. Res. Lett. 37, L13402 (2010).4.Scharlemann, J. P., Tanner, E. V., Hiederer, R. & Kapos, V. Global soil carbon: understanding and managing the largest terrestrial carbon pool. Carbon Manag. 5, 81–91 (2014).CAS 

    Google Scholar 
    5.Chambers, F. M., Barber, K. E., Maddy, D. & Brew, J. A 5500-year proxy-climate and vegetation record from blanket mire at Talla Moss, Borders, Scotland. The Holocene 7, 391–399 (1997).
    Google Scholar 
    6.Charman, D. J., Blundell, A., Chiverrell, R. C., Hendon, D. & Langdon, P. G. Compilation of non-annually resolved Holocene proxy climate records: stacked Holocene peatland palaeo-water table reconstructions from northern Britain. Quat. Sci. Rev. 25, 336–350 (2006).
    Google Scholar 
    7.Swindles, G. T. et al. Widespread drying of European peatlands in recent centuries. Nat. Geosci. 12, 922–928 (2019).CAS 

    Google Scholar 
    8.van der Linden, M. & van Geel, B. Late Holocene climate change and human impact recorded in a south Swedish ombrotrophic peat bog. Palaeogeogr. Palaeoclimatol. Palaeoecol. 240, 649–667 (2006).
    Google Scholar 
    9.Clymo, R. S. The limits to peat bog growth. Philos. Trans. R. Soc. B Biol. Sci. 303, 605–654 (1984).
    Google Scholar 
    10.Hessen, D. O., Ågren, G. I., Anderson, T. R., Elser, J. J. & de Ruiter, P. C. Carbon sequestration in ecosystems: the role of stoichiometry. Ecology 85, 1179–1192 (2004).
    Google Scholar 
    11.Damman, A. W. H. Distribution and movement of elements in ombrotrophic peat bogs. Oikos 30, 480–495 (1978).CAS 

    Google Scholar 
    12.Malmer, N. Patterns in the growth and the accumulation of inorganic constituents in the Sphagnum cover on ombrotrophic bogs in Scandinavia. Oikos 53, 105–120 (1988).CAS 

    Google Scholar 
    13.Wang, R. et al. Global forest carbon uptake due to nitrogen and phosphorus deposition from 1850 to 2100. Glob. Change Biol. 23, 4854–4872 (2017).
    Google Scholar 
    14.Du, E. et al. Imbalanced phosphorus and nitrogen deposition in China’s forests. Atmos. Chem. Phys. 16, 8571–8579 (2016).CAS 

    Google Scholar 
    15.Du, E. et al. Global patterns of terrestrial nitrogen and phosphorus limitation. Nat. Geosci. 13, 221–226 (2020).CAS 

    Google Scholar 
    16.Bragazza, L. et al. Atmospheric nitrogen deposition promotes carbon loss from peat bogs. Proc. Natl. Acad. Sci. USA 103, 19386–19389 (2006).CAS 

    Google Scholar 
    17.Bragazza, L. et al. High nitrogen deposition alters the decomposition of bog plant litter and reduces carbon accumulation. Glob. Change Biol. 18, 1163–1172 (2012).
    Google Scholar 
    18.Aerts, R., Wallén, B. & Malmer, N. Growth-limiting nutrients in Sphagnum-dominated bogs subject to low and high atmospheric nitrogen supply. J. Ecol. 80, 131–140 (1992).
    Google Scholar 
    19.Brahney, J., Mahowald, N., Ward, D. S., Ballantyne, A. P. & Neff, J. C. Is atmospheric phosphorus pollution altering global alpine Lake stoichiometry? Glob. Biogeochem. Cycles 29, 1369–1383 (2015).20.Charman, D. J. et al. Drivers of Holocene peatland carbon accumulation across a climate gradient in northeastern North America. Quat. Sci. Rev. 121, 110–119 (2015).
    Google Scholar 
    21.Charman, D. J. et al. Climate-related changes in peatland carbon accumulation during the last millennium. Biogeosciences 10, 929–944 (2013).
    Google Scholar 
    22.Beilman, D. W., MacDonald, G. M., Smith, L. C. & Reimer, P. J. Carbon accumulation in peatlands of West Siberia over the last 2000 years. Glob. Biogeochem. Cycles 23, GB1012 (2009).23.Wang, M., Moore, T. R., Talbot, J. & Richard, P. J. H. The cascade of C:N:P stoichiometry in an ombrotrophic peatland: from plants to peat. Environ. Res. Lett. 9, 024003 (2014).CAS 

    Google Scholar 
    24.Wang, M., Moore, T. R., Talbot, J. & Riley, J. L. The stoichiometry of carbon and nutrients in peat formation. Glob. Biogeochem. Cycles 29, 113–121 (2015).
    Google Scholar 
    25.Gorham, E. & Janssens, J. A. The distribution and accumulation of chemical elements in five peat cores from the mid-continent to the eastern coast of North America. Wetlands 25, 259–278 (2005).
    Google Scholar 
    26.Ratcliffe, J. L. et al. Rapid carbon accumulation in a peatland following Late Holocene tephra deposition, New Zealand. Quat. Sci. Rev. 246, 106505 (2020).
    Google Scholar 
    27.Kylander, M. E. et al. Mineral dust as a driver of carbon accumulation in northern latitudes. Sci. Rep. 8, 6876 (2018).28.Hughes, P. D. M. et al. The impact of high tephra loading on late-Holocene carbon accumulation and vegetation succession in peatland communities. Quat. Sci. Rev. 67, 160–175 (2013).
    Google Scholar 
    29.Limpens, J., Berendse, F. & Klees, H. How phosphorus availability affects the impact of nitrogen deposition on Sphagnum and vascular plants in bogs. Ecosystems 7, 793–804 (2004).CAS 

    Google Scholar 
    30.Fritz, C. et al. Nutrient additions in pristine Patagonian Sphagnum bog vegetation: can phosphorus addition alleviate (the effects of) increased nitrogen loads. Plant Biol. 14, 491–499 (2012).CAS 

    Google Scholar 
    31.White, J. R. & Reddy, K. R. Influence of phosphorus loading on organic nitrogen mineralization of everglades soils. Soil Sci. Soc. Am. J. 64, 1525 (2000).CAS 

    Google Scholar 
    32.Bledsoe, R. B., Goodwillie, C. & Peralta, A. L. Long-term nutrient enrichment of an oligotroph-dominated wetland increases bacterial diversity in bulk soils and plant rhizospheres. mSphere 5, e00035-20 (2020).
    Google Scholar 
    33.Lin, X. et al. Microbial community stratification linked to utilization of carbohydrates and phosphorus limitation in a boreal peatland at Marcell Experimental Forest, Minnesota, USA. Appl. Environ. Microbiol. 80, 3518–3530 (2014).
    Google Scholar 
    34.Sjögersten, S., Cheesman, A. W., Lopez, O. & Turner, B. L. Biogeochemical processes along a nutrient gradient in a tropical ombrotrophic peatland. Biogeochemistry 104, 147–163 (2011).
    Google Scholar 
    35.Cheesman, A. W., Turner, B. L. & Ramesh Reddy, K. Soil phosphorus forms along a strong nutrient gradient in a tropical ombrotrophic wetland. Soil Sci. Soc. Am. J. 76, 1496–1506 (2012).CAS 

    Google Scholar 
    36.Kivimäki, S. K., Sheppard, L. J., Leith, I. D. & Grace, J. Long-term enhanced nitrogen deposition increases ecosystem respiration and carbon loss from a Sphagnum bog in the Scottish Borders. Environ. Exp. Bot. 90, 53–61 (2013).
    Google Scholar 
    37.Moore, T. R., Knorr, K.-H., Thompson, L., Roy, C. & Bubier, J. L. The effect of long-term fertilization on peat in an ombrotrophic bog. Geoderma 343, 176–186 (2019).CAS 

    Google Scholar 
    38.Hill, B. H. et al. Ecoenzymatic stoichiometry and microbial processing of organic matter in northern bogs and fens reveals a common P-limitation between peatland types. Biogeochemistry 120, 203–224 (2014).CAS 

    Google Scholar 
    39.Vitousek, P. M. et al. Towards an ecological understanding of biological nitrogen fixation. In The Nitrogen Cycle at Regional to Global Scales (eds. Boyer, E. W. & Howarth, R. W.) 1–45 (Springer Netherlands, 2002).40.Larmola, T. et al. Methanotrophy induces nitrogen fixation during peatland development. Proc. Natl. Acad. Sci. USA 111, 734–739 (2014).CAS 

    Google Scholar 
    41.van den Elzen, E. et al. Symbiosis revisited: phosphorus and acid buffering stimulate N2 fixation but not Sphagnum growth. Biogeosciences 14, 1111–1122 (2017).
    Google Scholar 
    42.van den Elzen, E., Bengtsson, F., Fritz, C., Rydin, H. & Lamers, L. P. M. Variation in symbiotic N2 fixation rates among Sphagnum mosses. PLoS ONE 15, e0228383 (2020).
    Google Scholar 
    43.Toberman, H. et al. Dependence of ombrotrophic peat nitrogen on phosphorus and climate. Biogeochemistry 125, 11–20 (2015).CAS 

    Google Scholar 
    44.Basilier, K., Granhall, U., Stenström, T.-A. & Stenstrom, T.-A. Nitrogen fixation in wet minerotrophic moss communities of a subarctic mire. Oikos 31, 236 (1978).CAS 

    Google Scholar 
    45.Lin, X. et al. Microbial metabolic potential for carbon degradation and nutrient (nitrogen and phosphorus) acquisition in an ombrotrophic peatland. Appl. Environ. Microbiol. 80, 3531–3540 (2014).
    Google Scholar 
    46.Kox, M. A. R. et al. Effects of nitrogen fertilization on diazotrophic activity of microorganisms associated with Sphagnum magellanicum. Plant Soil 406, 83–100 (2016).CAS 

    Google Scholar 
    47.Bubier, J. L., Moore, T. R. & Bledzki, L. A. Effects of nutrient addition on vegetation and carbon cycling in an ombrotrophic bog. Glob. Change Biol. 13, 1168–1186 (2007).
    Google Scholar 
    48.Fritz, C., Lamers, L. P. M., Riaz, M., van den Berg, L. J. L. & Elzenga, T. J. T. M. Sphagnum mosses – masters of efficient N-uptake while avoiding intoxication. PLoS ONE 9, e79991 (2014).
    Google Scholar 
    49.Morris, P. J. et al. Global peatland initiation driven by regionally asynchronous warming. Proc. Natl. Acad. Sci. USA 115, 4851–4856 (2018).CAS 

    Google Scholar 
    50.Schillereff, D. N. et al. Long-term macronutrient stoichiometry of UK ombrotrophic peatlands. Sci. Total Environ. 572, 1561–1572 (2016).CAS 

    Google Scholar 
    51.Sjöström, J. K. et al. Paleodust deposition and peat accumulation rates – bog size matters. Chem. Geol. 554, 119795 (2020).
    Google Scholar 
    52.Kylander, M. E. et al. Potentials and problems of building detailed dust records using peat archives: an example from Store Mosse (the “Great Bog”), Sweden. Geochim. Cosmochim. Acta 190, 156–174 (2016).CAS 

    Google Scholar 
    53.Mahowald, N. et al. Global distribution of atmospheric phosphorus sources, concentrations and deposition rates, and anthropogenic impacts. Glob. Biogeochem. Cycles 22, 1–19 (2008).
    Google Scholar 
    54.Tipping, E. et al. Atmospheric deposition of phosphorus to land and freshwater. Environ. Sci.: Processes Impacts 16, 1608–1617 (2014).CAS 

    Google Scholar 
    55.Wang, R. et al. Significant contribution of combustion-related emissions to the atmospheric phosphorus budget. Nat. Geosci. 8, 48–54 (2015).CAS 

    Google Scholar 
    56.Newman, E. I. Phosphorus inputs to terrestrial ecosystems. J. Ecol. 83, 713–726 (1995).
    Google Scholar 
    57.Worrall, F., Moody, C. S., Clay, G. D., Burt, T. P. & Rose, R. The total phosphorus budget of a peat-covered catchment. J. Geophys. Res. Biogeosci. 121, 1814–1828 (2016).CAS 

    Google Scholar 
    58.Vitousek, P. M., Porder, S., Houlton, B. Z. & Chadwick, O. A. Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions. Ecol. Appl. 20, 5–15 (2010).
    Google Scholar 
    59.Bedford, B. L., Walbridge, M. R. & Aldous, A. Patterns in nutrient availability and plant diversity of temperate North American Wetlands. Ecology 80, 2151–2169 (1999).
    Google Scholar 
    60.Güsewell, S. N: P ratios in terrestrial plants: variation and functional significance: Tansley review. New Phytol. 164, 243–266 (2004).
    Google Scholar 
    61.Yan, J. et al. Preliminary investigation of phosphorus adsorption onto two types of iron oxide-organic matter complexes. J. Environ. Sci. 42, 152–162 (2016).CAS 

    Google Scholar 
    62.Barrow, N. J. Comparing two theories about the nature of soil phosphate. Eur. J. Soil Sci. 72, 679–685 (2021).CAS 

    Google Scholar 
    63.Bridgham, S. D., Pastor, J., Janssens, J. A., Chapin, C. & Malterer, T. J. Multiple limiting gradients in peatlands: a call for a new paradigm. Wetlands 16, 45–65 (1996).
    Google Scholar 
    64.Kuhry, P. & Vitt, D. H. Fossil carbon/nitrogen ratios as a measure of peat decomposition. Ecology 77, 271–275 (1996).
    Google Scholar 
    65.Kuhry, P., Halsey, L. A., Bayley, S. E. & Vitt, D. H. Peatland development in relation to Holocene climatic change in Manitoba and Saskatchewan (Canada). Can. J. Earth Sci. 29, 1070–1090 (1992).CAS 

    Google Scholar 
    66.Malmer, N. & Wallén, B. Input rates, decay losses and accumulation rates of carbon in bogs during the last millennium: internal processes and environmental changes. The Holocene 14, 111–117 (2004).
    Google Scholar 
    67.Malmer, N. & Holm, E. Variation in the C/N-quotient of peat in relation to decomposition rate and age determination with 210 Pb. Oikos 43, 171–182 (1984).CAS 

    Google Scholar 
    68.Larsson, A., Segerstrom, U., Laudon, H. & Nilsson, M. Holocene carbon and nitrogen accumulation rates and contemporary carbon export in discharge: a study from a boreal fen catchment. Holocene 27, 48 (2016), https://doi.org/10.1177/0959683616675936.69.Berendse, F. et al. Raised atmospheric CO2 levels and increased N deposition cause shifts in plant species composition and production in Sphagnum bogs. Glob. Change Biol. 7, 591–598 (2001).
    Google Scholar 
    70.Juutinen, S., Bubier, J. L. & Moore, T. R. Responses of vegetation and ecosystem CO2 exchange to 9 years of nutrient addition at Mer Bleue bog. Ecosystems 13, 874–887 (2010).CAS 

    Google Scholar 
    71.Lequy, É., Legout, A., Conil, S. & Turpault, M. P. Aeolian dust deposition rates in Northern French forests and inputs to their biogeochemical cycles. Atmos. Environ. 80, 281–289 (2013).CAS 

    Google Scholar 
    72.Harrison, J. A., Caraco, N. & Seitzinger, S. P. Global patterns and sources of dissolved organic matter export to the coastal zone: results from a spatially explicit, global model. Glob. Biogeochem. Cycles 19, GB4S04 (2005).73.Yu, Z. Holocene carbon flux histories of the world’s peatlands: global carbon-cycle implications. The Holocene 21, 761–774 (2011).
    Google Scholar 
    74.Schlesinger, W. H. & Bernhardt, E. S. Biogeochemistry. (Elsevier, Amsterdam, 2013).
    Google Scholar 
    75.Peñuelas, J. et al. Human-induced nitrogen–phosphorus imbalances alter natural and managed ecosystems across the globe. Nat. Commun. 4, 2934 (2013).76.Larmola, T. et al. Vegetation feedbacks of nutrient addition lead to a weaker carbon sink in an ombrotrophic bog. Glob. Change Biol. 19, 3729–3739 (2013).
    Google Scholar 
    77.Li, F. et al. Organic carbon linkage with soil colloidal phosphorus at regional and field scales: insights from size fractionation of fine particles. Environ. Sci. Technol. 55, 5815–5825 (2021).CAS 

    Google Scholar 
    78.Spohn, M. Increasing the organic carbon stocks in mineral soils sequesters large amounts of phosphorus. Glob. Change Biol. 26, 4169–4177 (2020).
    Google Scholar 
    79.Sjöström, J. Mid-Holocene Mineral Dust Deposition in Raised Bogs in Southern Sweden: Processes and Links. PhD thesis, Stockholm Univ. (2021).80.Gallego-Sala, A. V. et al. Latitudinal limits to the predicted increase of the peatland carbon sink with warming. Nat. Clim. Change 8, 907–913 (2018).CAS 

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

    Google Scholar 
    82.Dorrepaal, E. et al. Carbon respiration from subsurface peat accelerated by climate warming in the subarctic. Nature 460, 616–619 (2009).CAS 

    Google Scholar 
    83.Clymo, R. S. & Bryant, C. L. Diffusion and mass flow of dissolved carbon dioxide, methane, and dissolved organic carbon in a 7-m deep raised peat bog. Geochim. Cosmochim. Acta 72, 2048–2066 (2008).CAS 

    Google Scholar 
    84.Morris, P. J., Waddington, J. M., Benscoter, B. W. & Turetsky, M. R. Conceptual frameworks in peatland ecohydrology: looking beyond the two-layered (acrotelm-catotelm) model. Ecohydrology 4, 1–11 (2011).
    Google Scholar 
    85.Rydin, H. & Jeglum, J. The Biology of Peatlands (Oxford University Press, 2013).86.Limpens, J., Heijmans, M. M. P. D. & Berendse, F. The nitrogen cycle in boreal peatlands. Boreal Peatl. Ecosyst. 188, 195–230 (2006).CAS 

    Google Scholar 
    87.Biester, H., Knorr, K.-H., Schellekens, J., Basler, A. & Hermanns, Y.-M. Comparison of different methods to determine the degree of peat decomposition in peat bogs. Biogeosciences 11, 2691–2707 (2014).CAS 

    Google Scholar 
    88.Zaccone, C., Plaza, C., Ciavatta, C., Miano, T. M. & Shotyk, W. Advances in the determination of humification degree in peat since: Applications in geochemical and paleoenvironmental studies. Earth-Sci. Rev. 185, 163–178 (2018).CAS 

    Google Scholar 
    89.Alboukadel Kassambara. ggpubr: ‘ggplot2’ Based Publication Ready Plots. R package version 0.4.0. https://CRAN.R-project.org/package=ggpubr (CRAN, 2020).90.Legendre, P. & Oksanen, J. lmodel2: Model II Regression. R package version 1.7–3. https://CRAN.R-project.org/package=lmodel2 (CRAN, 2018).91.Wickham, H. ggplot2: Elegant Graphics for Data Analysis. (Springer-Verlag, New York, 2016).
    Google Scholar 
    92.Tipping, E. et al. Long-term increases in soil carbon due to ecosystem fertilization by atmospheric nitrogen deposition demonstrated by regional-scale modelling and observations. Sci. Rep. 7, 1890 (2017).CAS 

    Google Scholar 
    93.Bragazza, L. & Limpens, J. Dissolved organic nitrogen dominates in European bogs under increasing atmospheric N deposition. Glob. Biogeochem. Cycles 18, GB4018 (2004).94.Turunen, J., Roulet, N. T., Moore, T. R. & Richard, P. J. H. Nitrogen deposition and increased carbon accumulation in ombrotrophic peatlands in eastern Canada. Glob. Biogeochem. Cycles 18, 1–12 (2004).
    Google Scholar 
    95.Lund, M., Christensen, T. R., Mastepanov, M., Lindroth, A. & Ström, L. Effects of N and P fertilization on the greenhouse gas exchange in two northern peatlands with contrasting N deposition rates. Biogeosciences 6, 2135–2144 (2009).CAS 

    Google Scholar 
    96.Xu, J., Morris, P. J., Liu, J. & Holden, J. PEATMAP: refining estimates of global peatland distribution based on a meta-analysis. Catena 160, 134–140 (2018).
    Google Scholar  More

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    The significance of region-specific habitat models as revealed by habitat shifts of grey-faced buzzard in response to different agricultural schedules

    Study regionsWe conducted the field survey in the Kyushu of southern Japan (Fig. 2a,b). The rice-transplanting schedule in Kyushu, is generally late (in late June24) because it is necessary to delay rice-transplanting timing after the harvest of wheat as a back crop22,23. However, since the technique of early transplanting was established around 1960, early transplanting (in early April24) has been practiced instead of a back crop of wheat in some areas in Kyushu25,26, so the rice-transplanting schedules differ at the regional scale. We established two study regions with early-transplanting schedules (Karatsu in northern Kyushu; N33.4, E129.9 and Amakusa in central Kyushu; N32.5, E130.1), and two study regions with late-transplanting schedules (Itoshima in northern Kyushu; N33.6, E130.2 and Uki in central Kyushu; N32.6, E130.8) (Fig. 2c–f). Each study region is 10–20 km2, and the distances between the regions are 20–140 km. Climatic conditions between the regions are similar (Supplementary Table S3). The size of each region is much larger than the size of the typical territory of breeding buzzards (approximately 500 m radius from the nest18).Figure 2Map of (a) Japan and (b) the entire study regions, (c) Karatsu, (d) Amakusa, (e) Itoshima and (f) Uki. Squares represent study blocks. Light and dark grey areas indicate waterbodies and residential areas, respectively. Background map source is the black map of Japan (http://www.craftmap.box-i.net/japan/line.php) and the topographic data of Fundamental Geospatial Data developed by the Geospatial Information Authority of Japan (https://www.gsi.go.jp/kiban/).Full size imageBuzzards surveyWe examined the distribution of buzzards in 2019. Buzzards are migratory birds that breed in Japan, northeastern China, and the Russian Far East in summer, and overwinter in the Ryukyu Islands, Southeast Asia, and southern China27. In our study regions, buzzards start breeding in April, soon after returning from their wintering area. Buzzards incubate their eggs from late April until late May when they hatch. Once the eggs hatch, buzzards feed nestlings. Then nestlings start to fledge in late June, but the adults continue feeding their fledglings for several weeks. Buzzards migrate to their wintering grounds around October. The breeding season of buzzards thus overlaps largely with the rice production season, but there is a slight but significant differences in seasonality, i.e., paddies are already planted and flooded before hatching in early rice-transplanting schedules, while not yet flooded in late rice-transplanting schedules.Because breeding buzzards were thought to prefer mosaic landscapes of farmland and forest17,19, we established 62 study blocks that included edges between farmland and forest in each study region (Fig. 2c–f; northern-early: 17 central-early: 11 northern-late: 17 central-late: 17). The study blocks were 400 m square and located at least 700 m apart from each other, a distance determined from the knowledge that buzzards intensively use an area of 200 m from their nests18. To examine the presence/absence of breeding buzzards in each block, we conducted 2 days of 30-min observations during the breeding season (April to July). Using a pilot study, we determined that this observation time was enough to minimize the possibility of missing buzzards. We identified breeding individuals based on displays, feeding behaviors, and territorial behaviors.Land use surveyDuring the brood-rearing period (late June to early July) in 2019, we recorded the land use (forest, grassland, flooded paddies, non-flooded paddies) in each block. We then used these data to create a land use map in each block using QGIS3.16.228 and overlaying it on Google Earth aerial photographs in 2017.Prey species surveyWe surveyed the distribution of prey species in paddies and grasslands in the study regions in 2019 and 2020. Based on the previous studies on the feeding habits of buzzards17,18,19,20,21, we surveyed the distribution of frogs and orthopterans larger than 3 cm as prey of this size is considered their main prey. We established survey transects in paddies and grasslands in our study blocks. We conducted surveys twice each year during the brood-rearing period (late June to early July), when breeding buzzards need a large amount of prey. We walked along the transects and counted the number of prey species observed within 0.5-m of both sides. This survey method is suitable to assess prey availability29 because buzzards visually search for prey (e.g.20,30). A total of 148 20 m-transects were placed in paddies in 34 blocks and 157 15-m transects were placed in grasslands in 37 blocks, and each transect was surveyed in both or either 2019 and 2020. In the paddy transects, we recorded the height and coverage of vegetation, the ditch characteristics (none, concrete ditch, earthen ditch), the surrounding land use (10 m width from the transect: flooded paddy, non-flooded paddy, grassland, forest, stone wall, and road), and flooding or non-flooding in the paddy field adjacent to transects. In grassland transects, we recorded the height and coverage of vegetation and the grassland types on which the transect was located (abandoned land, orchard, farmland, bank, forest edge).Statistical analysisBuzzard modelTo investigate the habitat selection of buzzards, we used a generalized linear model with a binomial error distribution. We used the edge length between the landscape elements and forest as independent variables, because the edge length, rather than the area of the landscape elements, is known to be an important determinant for buzzard distribution19. We prepared a land use map and calculated the edge length between the landscape elements and forest by using the field calculator of QGIS, and values were standardized (mean = 0 and SD = 1).To explore the variation in habitat selection across regions with different transplanting schedules, we first used a model that included the interaction term of transplanting schedules and landscape elements as independent variables. The length of paddy-forest edges, grassland-forest edges, the transplanting schedules, the interaction term of the edge length and the transplanting schedules, and the study regions were included as independent variables (details of independent variables: Supplementary Table S4). The presence/absence of breeding buzzards was included as a dependent variable. We analyzed the full model and all sub-models containing different combinations of all independent variables, including the null model. We regarded models that had ΔAIC values (the difference between the AIC value of the focal model and that of the best-fit model) of  0.6) to avoid serious multicollinearity.We performed all analyses in R 4.0.333, using the glmmTMB packages34 for model fitting, the MuMIn package35 for model selection and averaging, and the ggplot236 for graphic illustration or results. More

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    Biogeochemical feedbacks to ocean acidification in a cohesive photosynthetic sediment

    1.Revelle, R. & Suess, H. E. Carbon dioxide exchange between atmosphere and ocean and the question of an increase of atmospheric CO2 during the past decades. Tellus 9, 18–27 (1957).ADS 
    CAS 

    Google Scholar 
    2.Frankignoulle, M. A complete set of buffer factors for acid/base CO2 system in seawater. J. Mar. Syst. 5, 111–118 (1994).
    Google Scholar 
    3.Egleston, E. S., Sabine, C. L. & Morel, F. M. M. Revelle revisited: Buffer factors that quantify the response of ocean chemistry to changes in DIC and alkalinity. Glob. Biogeochem. Cycles 24, GB1002 (2010).ADS 

    Google Scholar 
    4.Bates, N. et al. A time-series view of changing surface ocean chemistry due to ocean uptake of anthropogenic CO2 and ocean acidification. Oceanography 27(1), 126–141 (2014).MathSciNet 

    Google Scholar 
    5.Lauvset, S., Gruber, N., Landschützer, P., Olsen, A. & Tjiputra, J. Trends and drivers in global surface ocean pH over the past 3 decades. Biogeosciences 12(5), 1285–1298 (2015).ADS 

    Google Scholar 
    6.Ríos, A. F. et al. Decadal acidification in the Atlantic. Proc. Natl. Acad. Sci. 112(32), 9950–9955 (2015).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    7.Schulz, K. G. & Riebesell, U. Diurnal changes in seawater carbonate chemistry speciation at increasing atmospheric carbon dioxide. Mar. Biol. 160, 1889–1899 (2013).CAS 
    PubMed 

    Google Scholar 
    8.Provoost, P., van Heuven, S., Soetaert, K., Laane, R. W. P. M. & Middelburg, J. J. Seasonal and long-term changes in pH in the Dutch coastal zone. Biogeosciences 7, 3869–3878 (2010).ADS 
    CAS 

    Google Scholar 
    9.Hofmann, G. E. et al. High-frequency dynamics of ocean pH: A multi-ecosystem comparison. PLoS ONE 6, e28983 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    10.Borges, A. V. & Gypens, N. Carbonate chemistry in the coastal zone responds more strongly to eutrophication than ocean acidification. Limnol. Oceanogr. 55, 346–353 (2010).ADS 
    CAS 

    Google Scholar 
    11.Cai, W.-J. et al. Acidification of subsurface coastal waters enhanced by eutrophication. Nat. Geosci. 4, 766–770 (2011).ADS 
    CAS 

    Google Scholar 
    12.Sunda, W. G. & Cai, W.-J. Eutrophication induced CO2-acidification of subsurface coastal waters: Interactive effects of temperature, salinity, and atmospheric pCO2. Environ. Sci. Technol. 46, 10651–10659 (2012).ADS 
    CAS 
    PubMed 

    Google Scholar 
    13.Jury, C. P., Thomas, F. I. M., Atkinson, M. J. & Toonen, R. J. Buffer capacity, ecosystem feedbacks, and seawater chemistry under global change. Water 5, 1303–1325 (2013).CAS 

    Google Scholar 
    14.Hagens, M. et al. Biogeochemical processes and buffering capacity concurrently affect acidification in a seasonally hypoxic coastal marine basin. Biogeosciences 12, 1561–1583 (2015).ADS 

    Google Scholar 
    15.Santschi, P., Höhener, P., Benoit, G. & Buchholtz-ten, B. M. Chemical processes at the sediment–water interface. Mar. Chem. 30, 269–315 (1990).CAS 

    Google Scholar 
    16.Pawlik, J. R. Chemical ecology of the settlement of benthic marine invertebrates. Oceangr. Mar. Biol. Annu. Rev. 30, 273–335 (1992).
    Google Scholar 
    17.Marinelli, R. L. & Woodin, S. A. Experimental evidence for linkages between infaunal recruitment, disturbance, and sediment surface chemistry. Limnol. Oceanogr. 47(1), 221–229 (2002).ADS 
    CAS 

    Google Scholar 
    18.Clements, J. C. & Hunt, H. L. Marine animal behaviour in a high CO2 ocean. Mar. Ecol. Prog. Ser. 536, 259–279 (2015).ADS 
    CAS 

    Google Scholar 
    19.Vopel, K., Laverock, B., Cary, C. & Pilditch, C. A. Effects of warming and CO2 enrichment on O2 consumption, porewater oxygenation and pH of subtidal silt sediment. Aquat. Sci. 83, 8 (2021).CAS 

    Google Scholar 
    20.Green, M. A., Jones, M. E., Boudreau, C. L., Moore, R. L. & Westman, B. A. Dissolution mortality of juvenile bivalves in coastal marine deposits. Limnol. Oceanogr. 49(3), 727–734 (2004).ADS 

    Google Scholar 
    21.Green, M. A., Waldbusser, G., Reilly, S., Emerson, K. & O’Donnell, S. Death by dissolution: Sediment saturation state as a mortality factor for juvenile bivalves. Limnol. Oceanogr. 54(4), 1037–1047 (2009).ADS 
    CAS 

    Google Scholar 
    22.Green, M. A., Waldbusser, G. G., Hubazc, L., Cathcart, E. & Hall, J. Carbonate mineral saturation state as the recruitment cue for settling bivalves in marine muds. Estuaries Coasts 36, 18–27 (2013).CAS 

    Google Scholar 
    23.Clements, J. C., Woodard, K. D. & Hunt, H. L. Porewater acidification alters the burrowing behavior and post-settlement dispersal of juvenile soft-shell clams (Mya arenaria). J. Exp. Mar. Biol. Ecol. 477, 103–111 (2016).
    Google Scholar 
    24.Ries, J. B., Ghazaleh, M. N., Connolly, B., Westfield, I. & Castillo, K. D. Impacts of seawater saturation state (ΩA = 0.4–4.6) and temperature (10, 25 °C) on the dissolution kinetics of whole-shell biogenic carbonates. Geochim. Cosmochim. Acta 192, 318–337 (2016).ADS 
    CAS 

    Google Scholar 
    25.Nimer, N. A., Brownlee, C. & Merrett, M. J. Extracellular carbonic anhydrase facilitates carbon dioxide availability for photosynthesis in the marine dinoflagellate Prorocentrum micans. Plant Physiol. 120, 105–112 (1999).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    26.Hopkinson, B. M., Meile, C. & Shen, C. Quantification of extracellular carbonic anhydrase activity in two marine diatoms and investigation of its role. Plant Physiol. 162, 1142–1152 (2013).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    27.Tachibana, M. et al. Localization of putative carbonic anhydrase in two marine diatoms, Phaeodactylum tricornutum and Thalassiosira pseudonana. Photosynth. Res. 109, 205–221 (2011).CAS 
    PubMed 

    Google Scholar 
    28.Samukawa, M., Shen, C., Hopkinson, B. M. & Matsuda, Y. Localization of putative carbonic anhydrases in the marine diatom, Thalassiosira pseudonana. Photosynth. Res. 121, 235–249 (2014).CAS 
    PubMed 

    Google Scholar 
    29.Matsuda, Y., Hopkinson, B. M., Nakajima, K., Dupont, C. L. & Tsuji, Y. Mechanisms of carbon dioxide acquisition and CO2 sensing in marine diatoms: A gateway to carbon metabolism. Philos. Trans. R. Soc. B 372, 20160403 (2017).
    Google Scholar 
    30.Milligan, A. J. & Morel, F. M. M. A proton buffering role for silica in diatoms. Science 297, 1848–1850 (2002).ADS 
    CAS 
    PubMed 

    Google Scholar 
    31.Subhas, A. V. et al. Catalysis and chemical mechanisms of calcite dissolution in seawater. Proc. Natl. Acad. Sci. 114, 8175–8180 (2017).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    32.Middelburg, J. J., Soetaert, K. & Hagens, M. Ocean alkalinity, buffering and biogeochemical processes. Rev. Geophys. 58, e2019RG000681 (2020).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    33.Soetaert, K., Hofmann, A. F., Middelburg, J. J., Meysman, F. J. R. & Greenwood, J. The effect of biogeochemical processes on pH. Mar. Chem. 105, 30–51 (2007).CAS 

    Google Scholar 
    34.Zhu, Q., Aller, R. C. & Fan, Y. Two-dimensional pH distributions and dynamics in bioturbated marine sediments. Geochim. Cosmochim. Acta 70, 4933–4949 (2006).ADS 
    CAS 

    Google Scholar 
    35.Vopel, K., Del-Río, C. & Pilditch, C. A. Effects of CO2 enrichment on benthic primary production and inorganic nitrogen fluxes in two coastal sediments. Sci. Rep. 8, 1035 (2018).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    36.Jeffrey, S. W. & Humphrey, G. F. New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem. Physiol. Pflanzen 167, 191–194 (1975).CAS 

    Google Scholar 
    37.Dickson, A. G., Sabine, C. L. & Christian, J. R. Guide to best practices for ocean CO2 measurements: PICES Special Publication 3. http://cdiac.ornl.gov/oceans/Handbook_2007.html (2007).38.Lewis, E. & Wallace, D. W. R. Program Developed for CO2 System Calculations. ORNL/CDIAC-105 (Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy, 1998).
    Google Scholar 
    39.Dickson, A. G. Standard potential of the reaction: AgCl(s) + 12H2(g) = Ag(s) + HCL(aq), and the standard acidity constant of the ion HSO4− in synthetic sea water from 273.15 to 318.15 K. J. Chem. Thermodyn. 22, 113–127 (1990).CAS 

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

    Google Scholar 
    41.Dickson, A. G. & Millero, F. J. A comparison of the equilibrium constants for the dissolution of carbonic acid in seawater media. Deep Sea Res. 34(10), 1733–1743 (1987).ADS 
    CAS 

    Google Scholar 
    42.Berg, P. N., Risgaard-Petersen, N. & Rysgaard, S. Interpretation of measured concentration profiles in sediment pore water. Limnol. Oceanogr. 43, 1500–1510 (1998).ADS 
    CAS 

    Google Scholar 
    43.Revsbech, N. P., Nielsen, L. P. & Ramsing, N. B. A novel microsensor for determination of apparent diffusivity in sediments. Limnol. Oceanogr. 43, 986–992 (1998).ADS 
    CAS 

    Google Scholar 
    44.Vopel, K., Pilditch, C. A., Wilson, P. & Ellwood, M. J. Oxidation of surface sediment: Effects of disturbance depth and seawater flow speed. Mar. Ecol. Prog. Ser. 392, 43–55 (2009).ADS 
    CAS 

    Google Scholar 
    45.Broecker, W. S. & Peng, T.-H. Gas exchange rates between air and sea. Tellus 26(1–2), 21–35 (1974).ADS 
    CAS 

    Google Scholar 
    46.Cussler, E. L. Diffusion: Mass Transfer in Fluid Systems (Cambridge University Press, 2009).
    Google Scholar 
    47.Li, Y.-H. & Gregory, S. Diffusion of ions in sea water and in deep-sea sediments. Geochim. Cosmochim. Acta 38(5), 703–714 (1974).ADS 
    CAS 

    Google Scholar 
    48.Ullman, W. J. & Aller, R. C. Diffusion coefficients in nearshore marine sediments. Limnol. Oceanogr. 27(3), 552–556 (1982).ADS 
    CAS 

    Google Scholar 
    49.Jørgensen, B. B. & Revsbech, N. P. Diffusive boundary layers and the oxygen uptake of sediments and detritus. Limnol. Oceanogr. 30(1), 111–122 (1985).ADS 

    Google Scholar 
    50.Rasmussen, H. & Jørgensen, B. B. Microelectrode studies of seasonal oxygen uptake in a coastal sediment: Role of molecular diffusion. Mar. Ecol. Prog. Ser. 81, 289–303 (1992).ADS 
    CAS 

    Google Scholar 
    51.Nordstrom, D. K., Jenne, E. A. & Ball, J. W. Redox equilibria of iron in acid mine waters. In Chemical Modeling in Aqueous Systems. American Chemical Society Symposium Series Vol. 93 (ed. Jenne, E. A.) 57–79 (American Chemical Society, 1979).
    Google Scholar 
    52.Dushoff, J., Kain, M. P. & Bolker, B. M. I can see clearly now: Reinterpreting statistical significance. Methods Ecol. Evol. 10, 756–759 (2019).
    Google Scholar  More

  • in

    Cost-effective surveillance of invasive species using info-gap theory

    1.Jenkins, P. T. Free trade and exotic species introductions. Conserv. Biol. 10, 300–302 (1996).Article 

    Google Scholar 
    2.Sharov, A. A. Bioeconomics of managing the spread of exotic pest species with barrier zones. Risk Anal. 24, 879–892 (2004).Article 

    Google Scholar 
    3.Lodge, D. M. et al. Biological invasions: Recommendations for U.S. policy and management. Ecol. Appl. 16, 2035–2054 (2006).Article 

    Google Scholar 
    4.Yemshanov, D. et al. Optimizing surveillance strategies for early detection of invasive alien species. Ecol. Econ. 162, 87–99 (2019).Article 

    Google Scholar 
    5.Hauser, C. E. & Mccarthy, M. A. Streamlining “search and destroy”: Cost-effective surveillance for invasive species management. Ecol. Lett. 12, 683–692 (2009).Article 

    Google Scholar 
    6.Gottwald, T. R., da Graça, J. V. & Bassanezi, R. B. Citrus Huanglongbing: The pathogen and its impact. Plant Health Prog. https://doi.org/10.1094/PHP-2007-0906-01-RV (2007).Article 

    Google Scholar 
    7.Anderson, D. P. et al. Bio-economic optimisation of surveillance to confirm broadscale eradications of invasive pests and diseases. Biol. Invasions 19, 2869–2884 (2017).Article 

    Google Scholar 
    8.Russell, J. C., Binnie, H. R., Oh, J., Anderson, D. P. & Samaniego-Herrera, A. Optimizing confirmation of invasive species eradication with rapid eradication assessment. J. Appl. Ecol. 54, 160–169 (2017).Article 

    Google Scholar 
    9.Moffitt, L. J., Stranlund, J. K. & Osteen, C. D. Robust detection protocols for uncertain introductions of invasive species. J. Environ. Manag. 89, 293–299 (2008).Article 

    Google Scholar 
    10.Knight, F. H. Risk, Uncertainty, and Profit (Houghton Mifflin Company, 1921).11.Ben-Haim, Y. Uncertainty, probability and information-gaps. Reliab. Eng. Syst. Saf. 85, 249–266 (2004).Article 

    Google Scholar 
    12.Johnson, D. R. & Geldner, N. B. Contemporary decision methods for agricultural, environmental, and resource management and policy. Annu. Rev. Resour. Econ. 11, 19–41 (2019).Article 

    Google Scholar 
    13.Baker, C. M. & Bode, M. Recent advances of quantitative modeling to support invasive species eradication on islands. Conserv. Sci. Pract. 3, e246. https://doi.org/10.1111/csp2.246 (2021).Article 

    Google Scholar 
    14.Bertsimas, D. & Sim, M. The price of robustness. Oper. Res. 52, 35–53 (2004).MathSciNet 
    Article 

    Google Scholar 
    15.Ben-Haim, Y. & Demertzis, M. Decision making in times of knightian uncertainty: An info-gap perspective. Economics 10, 1–29 (2016).Article 

    Google Scholar 
    16.Ben-Haim, Y. Management of invasive species: Info-gap perspectives. in Invasive Species: Risk Assessment and Management (eds. Robinson, A., Walshe, T., Burgman, M. A., Nunn, M.) 266–286 (Cambridge University Press, 2017).17.Davidovitch, L. et al. Info-gap theory and robust design of surveillance for invasive species: The case study of Barrow Island. J. Environ. Manag. 90, 2785–2793 (2009).Article 

    Google Scholar 
    18.Rout, T. M., Thompson, C. J. & McCarthy, M. A. Robust decisions for declaring eradication of invasive species. J. Appl. Ecol. 46, 782–786 (2009).Article 

    Google Scholar 
    19.Foxcroft, L. C. Developing thresholds of potential concern for invasive alien species: Hypotheses and concepts. Koedoe. https://doi.org/10.4102/koedoe.v51i1.157 (2009).Article 

    Google Scholar 
    20.Pitt, J. P. W. Modelling the Spread of Invasive Species Across Heterogeneous Landscapes. (Lincoln University, 2008).21.Mehta, S. V., Haight, R. G., Homans, F. R., Polasky, S. & Venette, R. C. Optimal detection and control strategies for invasive species management. Ecol. Econ. 61, 237–245 (2007).Article 

    Google Scholar 
    22.Mcdonald-madden, E., Peter, W. J. B. & Possingham, H. P. Making robust decisions for conservation with restricted money and knowledge. J. Appl. Ecol. 45, 1630–1638 (2008).Article 

    Google Scholar 
    23.Rout, T. M., Moore, J. L. & Mccarthy, M. A. Prevent, search or destroy? A partially observable model for invasive species management. J. Appl. Ecol. 51, 804–813 (2014).Article 

    Google Scholar 
    24.Yemshanov, D. et al. Robust surveillance and control of invasive species using a scenario optimization approach. Ecol. Econ. 133, 86–98 (2017).Article 

    Google Scholar 
    25.Rödder, D., Solé, M. & Böhme, W. Predicting the potential distributions of two alien invasive Housegeckos (Gekkonidae: Hemidactylus frenatus, Hemidactylus mabouia). North-West. J. Zool. 4, 236–246 (2008).
    Google Scholar 
    26.Hoskin, C. J. The invasion and potential impact of the Asian House Gecko (Hemidactylus frenatus) in Australia. Austral. Ecol. 36, 240–251 (2011).Article 

    Google Scholar 
    27.García-Díaz, P., Ross, J. V., Vall-llosera, M. & Cassey, P. Low detectability of alien reptiles can lead to biosecurity management failure: A case study from Christmas Island (Australia). NeoBiota 45, 75–92 (2019).Article 

    Google Scholar 
    28.Scott, J. K. et al. Zero-tolerance biosecurity protects high-conservation-value island nature reserve. Sci. Rep. 7, 772–779 (2017).ADS 
    Article 

    Google Scholar 
    29.Commonwealth Government of Australia. Approval—Gorgon Gas Development (EPBC Reference: 2008/4178). (2009).30.Jarrad, F. C. et al. Improved design method for biosecurity surveillance and early detection of non-indigenous rats. N. Z. J. Ecol. 35, 132–144 (2011).
    Google Scholar 
    31.Metlay, D. From tin roof to torn wet blanket: Predicting and observing ground water movement at a proposed nuclear waste site. in Prediction: Science, Decision Making, and the Future of Nature (eds. Sarewitz, D. R., Byerly, R., Pielke, R. A.). 276–319. (Island Press, 2000).32.Wintle, B. & Burgman, M. Expert Elicitation for Barrow Island Surveillance System Revision, Project Report. (2015).33.Vanderduys, E. & Kutt, A. Is the Asian house gecko, Hemidactylus frenatus, really a threat to Australia’s biodiversity?. Aust. J. Zool. 60, 361–367 (2013).Article 

    Google Scholar 
    34.McGinnis, S. M. & Stebbins, R. C. A Field Guide to Western Reptiles and Amphibians. 4th edn. (Houghton Mifflin Harcourt, 2018).35.Whittle, P., Jarrad, F., Edwards, K. & Mengersen, K. Design of the quarantine surveillance for non-indigenous species of invertebrates on Barrow Island. Rec. West. Aust. Mus. Suppl. 83, 113–130 (2013).Article 

    Google Scholar 
    36.Ben-Haim, Y. Info-gap Decision Theory: Decisions Under Severe Uncertainty. 2nd edn. (Academic Press, 2006).37.MathWorks. MATLAB R2018b. (MathWorks, 2018).38.Bogich, T. L., Liebhold, A. M. & Shea, K. To sample or eradicate? A cost minimization model for monitoring and managing an invasive species. J. Appl. Ecol. 45, 1134–1142 (2008).Article 

    Google Scholar 
    39.Epanchin-Niell, R. S., Haight, R. G., Berec, L., Kean, J. M. & Liebhold, A. M. Optimal surveillance and eradication of invasive species in heterogeneous landscapes. Ecol. Lett. 15, 803–812 (2012).Article 

    Google Scholar 
    40.Trebitz, A. S. et al. Early detection monitoring for aquatic non-indigenous species: Optimizing surveillance, incorporating advanced technologies, and identifying research needs. J. Environ. Manag. 202, 299–310 (2017).CAS 
    Article 

    Google Scholar 
    41.Molina, R., Horton, T., Trappe, J. & Marcot, B. Addressing uncertainty: How to conserve and manage rare or little-known fungi. Fungal Ecol. 4, 134–146 (2011).Article 

    Google Scholar  More

  • in

    Pleistocene allopatric differentiation followed by recent range expansion explains the distribution and molecular diversity of two congeneric crustacean species in the Palaearctic

    1.Paillard, D. The timing of Pleistocene glaciations from a simple multiple-state climate model. Nature 391, 378–381 (1998).ADS 

    Google Scholar 
    2.Hewitt, G. M. Genetic consequences of climatic oscillations in the Quaternary. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 359, 183–195 (2004).CAS 

    Google Scholar 
    3.Hewitt, G. The genetic legacy of the quaternary ice ages. Nature 405, 907–913 (2000).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    4.Taberlet, P., Fumagalli, L., Wust-Saucy, A.-G. & Cosson, J.-F. Comparative phylogeography and postglacial colonization routes in Europe. Mol. Ecol. 7, 453–464 (1998).CAS 
    PubMed 

    Google Scholar 
    5.Incagnone, G., Marrone, F., Barone, R., Robba, L. & Naselli-Flores, L. How do freshwater organisms cross the ‘dry ocean’? A review on passive dispersal and colonization processes with a special focus on temporary ponds. Hydrobiologia 750, 103–123 (2015).
    Google Scholar 
    6.Schmitt, T. & Varga, Z. Extra-Mediterranean refugia: The rule and not the exception?. Front Zool 9, 22 (2012).PubMed 
    PubMed Central 

    Google Scholar 
    7.Hewitt, G. M. Speciation, hybrid zones and phylogeography—Or seeing genes in space and time. Mol. Ecol. 10, 537–549 (2001).CAS 
    PubMed 

    Google Scholar 
    8.Habel, J. C., Drees, C., Schmitt, T. & Assmann, T. Review refugial areas and postglacial colonizations in the Western Palearctic. In Relict Species (eds Habel, J. C. & Assmann, T.) 189–197 (Springer, 2010).
    Google Scholar 
    9.Hewitt, G. Some genetic consequences of ice ages, and their role in divergence and speciation. Biol. J. Lin. Soc. 58, 247–276 (1996).
    Google Scholar 
    10.Marrone, F., Lo Brutto, S. & Arculeo, M. Molecular evidence for the presence of cryptic evolutionary lineages in the freshwater copepod genus Hemidiaptomus G.O. Sars, 1903 (Calanoida, Diaptomidae). Hydrobiologia 644, 115–125 (2010).CAS 

    Google Scholar 
    11.Husemann, M., Schmitt, T., Zachos, F. E., Ulrich, W. & Habel, J. C. Palaearctic biogeography revisited: Evidence for the existence of a North African refugium for Western Palaearctic biota. J. Biogeogr. 41, 81–94 (2014).
    Google Scholar 
    12.García-Vázquez, D., Bilton, D. T., Foster, G. N. & Ribera, I. Pleistocene range shifts, refugia and the origin of widespread species in western Palaearctic water beetles. Mol. Phylogenet. Evol. 114, 122–136 (2017).PubMed 

    Google Scholar 
    13.Perktas, U., Barrowclough, G. F. & Groth, J. G. Phylogeography and species limits in the green woodpecker complex (Aves: Picidae): Multiple Pleistocene refugia and range expansion across Europe and the Near East. Biol. J. Lin. Soc. 104, 710–723 (2011).
    Google Scholar 
    14.Stewart, J. R. & Lister, A. M. Cryptic northern refugia and the origins of the modern biota. Trends Ecol. Evol. 16, 608–613 (2001).
    Google Scholar 
    15.Stewart, J. R., Lister, A. M., Barnes, I. & Dalén, L. Refugia revisited: Individualistic responses of species in space and time. Proc. R. Soc. B Biol. Sci. 277, 661–671 (2010).
    Google Scholar 
    16.Sworobowicz, L., Mamos, T., Grabowski, M. & Wysocka, A. Lasting through the ice age: The role of the proglacial refugia in the maintenance of genetic diversity, population growth, and high dispersal rate in a widespread freshwater crustacean. Freshw. Biol. 65, 1028–1046 (2020).CAS 

    Google Scholar 
    17.Provan, J. & Bennett, K. D. Phylogeographic insights into cryptic glacial refugia. Trends Ecol. Evol. 23, 564–571 (2008).PubMed 

    Google Scholar 
    18.Antal, L. et al. Phylogenetic evidence for a new species of Barbus in the Danube River basin. Mol. Phylogenet. Evol. 96, 187–194 (2016).CAS 
    PubMed 

    Google Scholar 
    19.Copilaş-Ciocianu, D., Fišer, C., Borza, P. & Petrusek, A. Is subterranean lifestyle reversible? Independent and recent large-scale dispersal into surface waters by two species of the groundwater amphipod genus Niphargus. Mol. Phylogenet. Evol. 119, 37–49 (2018).PubMed 

    Google Scholar 
    20.Říčanová, Š et al. Multilocus phylogeography of the European ground squirrel: Cryptic interglacial refugia of continental climate in Europe. Mol. Ecol. 22, 4256–4269 (2013).PubMed 

    Google Scholar 
    21.Vörös, J., Mikulíček, P., Major, Á., Recuero, E. & Arntzen, J. W. Phylogeographic analysis reveals northerly refugia for the riverine amphibian Triturus dobrogicus (Caudata: Salamandridae). Biol. J. Linn. Soc. 119, 974–991 (2016).
    Google Scholar 
    22.Wielstra, B. et al. Tracing glacial refugia of Triturus newts based on mitochondrial DNA phylogeography and species distribution modeling. Front. Zool. 10, 13 (2013).PubMed 
    PubMed Central 

    Google Scholar 
    23.Hutchison, D. W. & Templeton, A. R. Correlation of pairwise genetic and geographic distance measures: Inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 53, 1898–1914 (1999).PubMed 

    Google Scholar 
    24.Schmitt, T. Molecular biogeography of Europe: Pleistocene cycles and postglacial trends. Front. Zool. 4, 11 (2007).PubMed 
    PubMed Central 

    Google Scholar 
    25.Ewart, K. M. et al. Phylogeography of the iconic Australian red-tailed black-cockatoo (Calyptorhynchus banksii) and implications for its conservation. Heredity 125, 85–100 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    26.Hutama, A. et al. Identifying spatially concordant evolutionary significant units across multiple species through DNA barcodes: Application to the conservation genetics of the freshwater fishes of Java and Bali. Glob. Ecol. Conserv. 12, 170–187 (2017).
    Google Scholar 
    27.Médail, F. & Baumel, A. Using phylogeography to define conservation priorities: The case of narrow endemic plants in the Mediterranean Basin hotspot. Biol. Cons. 224, 258–266 (2018).
    Google Scholar 
    28.Previšić, A., Walton, C., Kučinić, M., Mitrikeski, P. T. & Kerovec, M. Pleistocene divergence of Dinaric Drusus endemics (Trichoptera, Limnephilidae) in multiple microrefugia within the Balkan Peninsula. Mol. Ecol. 18, 634–647 (2009).PubMed 

    Google Scholar 
    29.Brendonck, L. & Riddoch, B. J. Wind-borne short-range egg dispersal in anostracans (Crustacea: Branchiopoda). Biol. J. Linn. Soc. 67, 87–95 (1999).
    Google Scholar 
    30.Horváth, Z., Vad, C. F. & Ptacnik, R. Wind dispersal results in a gradient of dispersal limitation and environmental match among discrete aquatic habitats. Ecography 39, 726–732 (2016).PubMed 

    Google Scholar 
    31.Brochet, A. L. et al. Field evidence of dispersal of branchiopods, ostracods and bryozoans by teal (Anas crecca) in the Camargue (southern France). Hydrobiologia 637, 255 (2009).
    Google Scholar 
    32.Figuerola, J. & Green, A. J. Dispersal of aquatic organisms by waterbirds: A review of past research and priorities for future studies. Freshw. Biol. 47, 483–494 (2002).
    Google Scholar 
    33.Vanschoenwinkel, B. et al. Dispersal of freshwater invertebrates by large terrestrial mammals: A case study with wild boar (Sus scrofa) in Mediterranean wetlands. Freshw. Biol. 53, 2264–2273 (2008).
    Google Scholar 
    34.Brendonck, L., Rogers, D. C., Olesen, J., Weeks, S. & Hoeh, W. R. Global diversity of large branchiopods (Crustacea : Branchiopoda) in freshwater. Hydrobiologia 595, 167–176 (2008).
    Google Scholar 
    35.Dumont, H. J. & Negrea, S. V. Introduction to the Class Branchiopoda. (Backhuys Publishers, 2002).36.Belk, D. Global status and trends in ephemeral pool invertebrate conservation: Implications for Californian fairy shrimp. In Ecology, Conservation, and Management of Vernal Pool Ecosystems—Proceedings from a 1996 conference 147–150 (California Native Plant Society, 1998).37.Jocque, M., Vanschoenwinkel, B. & Brendonck, L. Anostracan monopolisation of early successional phases in temporary waters?. Fundam. Appl. Limnol. 176, 127–132 (2010).
    Google Scholar 
    38.Lukić, D., Horváth, Z., Vad, C. F. & Ptacnik, R. Food spectrum of Branchinecta orientalis—Are anostracans omnivorous top consumers of plankton in temporary waters?. J. Plankton Res. 40, 436–445 (2018).
    Google Scholar 
    39.Lukić, D., Ptacnik, R., Vad, C. F., Pόda, C. & Horváth, Z. Environmental constraint of intraguild predation: Inorganic turbidity modulates omnivory in fairy shrimps. Freshw. Biol. 65, 226–239 (2020).
    Google Scholar 
    40.Waterkeyn, A., Grillas, P., Anton-Pardo, M., Vanschoenwinkel, B. & Brendonck, L. Can large branchiopods shape microcrustacean communities in Mediterranean temporary wetlands?. Mar. Freshw. Res. 62, 46–53 (2011).CAS 

    Google Scholar 
    41.Brendonck, L. & De Meester, L. Egg banks in freshwater zooplankton: Evolutionary and ecological archives in the sediment. Hydrobiologia 491, 65–84 (2003).
    Google Scholar 
    42.Hairston, N. G., Brunt, R. A. V., Kearns, C. M. & Engstrom, D. R. Age and survivorship of diapausing eggs in a sediment egg bank. Ecology 76, 1706–1711 (1995).
    Google Scholar 
    43.Lukić, D. et al. High genetic variation and phylogeographic relations among Palearctic fairy shrimp populations reflect persistence in multiple southern refugia during Pleistocene ice ages and postglacial colonisation. Freshw. Biol. 64, 1896–1907 (2019).
    Google Scholar 
    44.Marrone, F., Alfonso, G., Naselli-Flores, L. & Stoch, F. Diversity patterns and biogeography of Diaptomidae (Copepoda, Calanoida) in the Western Palearctic. Hydrobiologia 800, 45–60 (2017).CAS 

    Google Scholar 
    45.Vanschoenwinkel, B. et al. Toward a global phylogeny of the “living fossil’’ crustacean order of the Notostraca. PLos ONE 7, e34998 (2012).46.Boileau, M. & Hebert, P. Genetic consequences of passive dispersal in pond-dwelling Copepods. Evolution 45, 721–733 (1991).PubMed 

    Google Scholar 
    47.Deng, Z., Chen, Y., Ma, X., Hu, W. & Yin, M. Dancing on the top: Phylogeography and genetic diversity of high-altitude freshwater fairy shrimps (Branchiopoda, Anostraca) with a focus on the Tibetan Plateau. Hydrobiologia 848, 2611–2626 (2021).CAS 

    Google Scholar 
    48.Ketmaier, V. et al. Mitochondrial DNA regionalism and historical demography in the extant populations of Chirocephalus kerkyrensis (Branchiopoda: Anostraca). PLoS ONE 7, e30082 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    49.Korn, M. et al. Phylogeny, molecular ecology and taxonomy of southern Iberian lineages of Triops mauritanicus (Crustacea: Notostraca). Org. Divers. Evol. 10, 409–440 (2010).
    Google Scholar 
    50.Stoch, F., Korn, M., Turki, S., Naselli-Flores, L. & Marrone, F. The role of spatial environmental factors as determinants of large branchiopod distribution in Tunisian temporary ponds. Hydrobiologia 782, 37–51 (2016).
    Google Scholar 
    51.Lindholm, M., d’Auriac, M. A., Thaulow, J. & Hobaek, A. Dancing around the pole: Holarctic phylogeography of the Arctic fairy shrimp Branchinecta paludosa (Anostraca, Branchiopoda). Hydrobiologia 772, 189–205 (2016).CAS 

    Google Scholar 
    52.Vörös, J., Alcobendas, M., Martínez-Solano, I. & García-París, M. Evolution of Bombina bombina and Bombina variegata (Anura: Discoglossidae) in the Carpathian Basin: A history of repeated mt-DNA introgression across species. Mol. Phylogenet. Evol. 38, 705–718 (2006).PubMed 

    Google Scholar 
    53.Zharov, A. A. et al. Pleistocene branchiopods (Cladocera, Anostraca) from Transbaikalian Siberia demonstrate morphological and ecological stasis. Water 12, 3063 (2020).
    Google Scholar 
    54.Velonà, A., Luchetti, A., Scanabissi, F. & Mantovani, B. Genetic variability and reproductive modalities in European populations of Triops cancriformis (Crustacea, Branchiopoda, Notostraca). Ital. J. Zool. 76, 366–375 (2009).
    Google Scholar 
    55.Vanschoenwinkel, B., Gielen, S., Vandewaerde, H., Seaman, M. & Brendonck, L. Relative importance of different dispersal vectors for small aquatic invertebrates in a rock pool metacommunity. Ecography 31, 567–577 (2008).
    Google Scholar 
    56.Hulsmans, A., Moreau, K., Meester, L. D., Riddoch, B. J. & Brendonck, L. Direct and indirect measures of dispersal in the fairy shrimp Branchipodopsis wolfi indicate a small scale isolation-by-distance pattern. Limnol. Oceanogr. 52, 676–684 (2007).ADS 

    Google Scholar 
    57.Vanschoenwinkel, B., Vries, C. D., Seaman, M. & Brendonck, L. The role of metacommunity processes in shaping invertebrate rock pool communities along a dispersal gradient. Oikos 116, 1255–1266 (2007).
    Google Scholar 
    58.Sánchez, M. I., Green, A. J., Amat, F. & Castellanos, E. M. Transport of brine shrimps via the digestive system of migratory waders: Dispersal probabilities depend on diet and season. Mar. Biol. 151, 1407–1415 (2007).
    Google Scholar 
    59.Horváth, Z. et al. Eastern spread of the invasive Artemia franciscana in the Mediterranean Basin, with the first record from the Balkan Peninsula. Hydrobiologia 822, 229–235 (2018).
    Google Scholar 
    60.Muñoz, J., Amat, F., Green, A. J., Figuerola, J. & Gómez, A. Bird migratory flyways influence the phylogeography of the invasive brine shrimp Artemia franciscana in its native American range. PeerJ 1, e200 (2013).PubMed 
    PubMed Central 

    Google Scholar 
    61.Muñoz, J. et al. Phylogeography and local endemism of the native Mediterranean brine shrimp Artemia salina (Branchiopoda: Anostraca). Mol. Ecol. 17, 3160–3177 (2008).PubMed 

    Google Scholar 
    62.Sánchez, M. I., Hortas, F., Figuerola, J. & Green, A. J. Comparing the potential for dispersal via waterbirds of a native and an invasive brine shrimp. Freshw. Biol. 57, 1896–1903 (2012).
    Google Scholar 
    63.Viana, D. S., Santamaría, L., Michot, T. C. & Figuerola, J. Migratory strategies of waterbirds shape the continental-scale dispersal of aquatic organisms. Ecography 36, 430–438 (2013).
    Google Scholar 
    64.Green, A. J. et al. Dispersal of invasive and native brine shrimps Artemia (Anostraca) via waterbirds. Limnol. Oceanogr. 50, 737–742 (2005).ADS 

    Google Scholar 
    65.Kappas, I. et al. Molecular and morphological data suggest weak phylogeographic structure in the fairy shrimp Streptocephalus torvicornis (Branchiopoda, Anostraca). Hydrobiologia 801, 21–32 (2017).CAS 

    Google Scholar 
    66.Rogers, D. C. Larger hatching fractions in avian dispersed anostracan eggs (Branchiopoda). J. Crustac. Biol. 34, 135–143 (2014).
    Google Scholar 
    67.Angeler, D. G., Viedma, O., Sánchez-Carrillo, S. & Alvarez-Cobelas, M. Conservation issues of temporary wetland Branchiopoda (Anostraca, Notostraca: Crustacea) in a semiarid agricultural landscape: What spatial scales are relevant?. Biol. Cons. 141, 1224–1234 (2008).
    Google Scholar 
    68.Horváth, Z., Vad, C. F., Vörös, L. & Boros, E. Distribution and conservation status of fairy shrimps (Crustacea: Anostraca) in the astatic soda pans of the Carpathian basin: the role of local and spatial factors. J. Limnol. 72, 103–116 (2013).
    Google Scholar 
    69.Svensson, L., Mullarney, K. & Zetterström, D. Collins Bird Guide 2nd edn. (HarperCollins Publishers Ltd., 2009).
    Google Scholar 
    70.Horváth, Z., Vad, C. F., Vörös, L. & Boros, E. The keystone role of anostracans and copepods in European soda pans during the spring migration of waterbirds. Freshw. Biol. 58, 430–440 (2013).
    Google Scholar 
    71.Gill, J. L. Ecological impacts of the late Quaternary megaherbivore extinctions. New Phytol. 201, 1163–1169 (2014).PubMed 

    Google Scholar 
    72.Neretina, A. N. et al. Crustacean remains from the Yuka mammoth raise questions about non-analogue freshwater communities in the Beringian region during the Pleistocene. Sci. Rep. 10, 859 (2020).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    73.Chang, D. et al. The evolutionary and phylogeographic history of woolly mammoths: A comprehensive mitogenomic analysis. Sci. Rep. 7, 44585 (2017).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    74.Lister, A. M., Sher, A. V., van Essen, H. & Wei, G. The pattern and process of mammoth evolution in Eurasia. Quatern. Int. 126–128, 49–64 (2005).
    Google Scholar 
    75.Vanschoenwinkel, B. et al. Passive external transport of freshwater invertebrates by elephant and other mud-wallowing mammals in an African savannah habitat. Freshw. Biol. 56, 1606–1619 (2011).
    Google Scholar 
    76.Waterkeyn, A., Pineau, O., Grillas, P. & Brendonck, L. Invertebrate dispersal by aquatic mammals: A case study with nutria Myocastor coypus (Rodentia, Mammalia) in Southern France. Hydrobiologia 654, 267–271 (2010).
    Google Scholar 
    77.Belk, D. & Brtek, J. Checklist of the Anostraca. Hydrobiologia 298, 315–353 (1995).
    Google Scholar 
    78.Marrone, F., Korn, M., Stoch, F., Naselli Flores, L. & Turki, S. Updated checklist and distribution of large branchiopods (Branchiopoda: Anostraca, Notostraca, Spinicaudata) in Tunisia. Biogeogr. J. Integr. Biogeogr. 31, 27–53 (2016).79.Mura, G. & Brtek, J. Revised key to families and genera of the Anostraca with notes on their geographical distribution. Crustaceana 73, 1037–1088 (2000).
    Google Scholar 
    80.Atashbar, B., Agh, N., Van Stappen, G., Mertens, J. & Beladjal, L. Combined effect of temperature and salinity on hatching characteristics of three fairy shrimp species (Crustacea: Anostraca). J. Limnol. 73, 574–583 (2014).
    Google Scholar 
    81.Eder, E., Hödl, W. & Gottwald, R. Distribution and phenology of large branchiopods in Austria. Hydrobiologia 359, 13–22 (1997).
    Google Scholar 
    82.Šćiban, M., Marković, A., Lukić, D. & Miličić, D. Autumn populations of Branchinecta orientalis G. O. Sars, 1903 and Chirocephalus diaphanus Prevost, 1803 (Crustacea, Branchiopoda) in the Central European Lowlands (Pannonian Plain, Serbia). North-West. J. Zool. 10, 435–437 (2014).
    Google Scholar 
    83.Alonso, M. A survey of the Spanish Euphyllopoda. Miscelania Zool. 9, 179–208 (1985).
    Google Scholar 
    84.Petkovski, S. On the presence of the genus Branchinecta Verrill, 1869 (Crustacea, Anostraca) in Yugoslavia. Hydrobiologia 226, 17–27 (1991).
    Google Scholar 
    85.Dimentman, C. The rainpool ecosystems of Israel: Geographical distribution of freshwater Anostraca (Crustacea). Israel J. Ecol. Evol. 30, 1–15 (1981).
    Google Scholar 
    86.Eid, E. K. New records of large branchiopods from northern Jordan (Crustacea: Branchiopoda). Zool. Middle East 46, 116–117 (2009).
    Google Scholar 
    87.Mura, G., Ozkutuk, S. R., Aygen, C. & Cottarelli, V. New data on the taxonomy and distribution of anostracan fauna from Turkey. J. Biol. Res. 15, 17–23 (2011).
    Google Scholar 
    88.Rogers, D. C., Quinney, D. L., Weaver, J. & Olesen, J. A new giant species of predatory fairy shrimp from Idaho, USA (Branchiopoda: Anostraca). J. Crustac. Biol. 26, 1–12 (2006).
    Google Scholar 
    89.Rodríguez-Flores, P. C., Jiménez-Ruiz, Y., Forró, L., Vörös, J. & García-París, M. Non-congruent geographic patterns of genetic divergence across European species of Branchinecta (Anostraca: Branchinectidae). Hydrobiologia 801, 47–57 (2017).
    Google Scholar 
    90.Atashbar, B., Agh, N., Van Stappen, G. & Beladjal, L. Diversity and distribution patterns of large branchiopods (Crustacea: Branchiopoda) in temporary pools (Iran). J. Arid. Environ. 111, 27–34 (2014).ADS 

    Google Scholar 
    91.Belk, D. & Esparza, C. E. Anostraca of the Indian Subcontinent. Hydrobiologia 298, 287–293 (1995).
    Google Scholar 
    92.Brtek, J. & Thiéry, A. The geographic distribution of the European Branchiopods (Anostraca, Notostraca, Spinicaudata, Laevicaudata). Hydrobiologia 298, 263–280 (1995).
    Google Scholar 
    93.Horn, W. & Paul, M. Occurrence and distribution of the Eurasian Branchinecta orientalis (Anostraca) in Central Asia (Northwest Mongolia, Uvs Nuur Basin) and in other holarctic areas. Lauterbornia 49, 81–91 (2004).
    Google Scholar 
    94.Marrone, F., Alonso, M., Pieri, V., Augugliaro, C. & Stoch, F. The crustacean fauna of Bayan Onjuul area (Tov Province, Mongolia) (Crustacea: Branchiopoda, Copepoda, Ostracoda). North West. J. Zool. 11, 288–295 (2015).
    Google Scholar 
    95.Mura, G. & Takami, G. A. A contribution to the knowledge of the anostracan fauna of Iran. Hydrobiologia 441, 117–121 (2000).
    Google Scholar 
    96.Naganawa, H. et al. Does the dispersal of fairy shrimps (Branchiopoda, Anostraca) reflect the shifting geographical distribution of freshwaters since the late Mesozoic?. Limnology https://doi.org/10.1007/s10201-019-00589-9 (2019).Article 

    Google Scholar 
    97.Padhye, S. M., Kulkarni, M. R. & Dumont, H. J. Diversity and zoogeography of the fairy shrimps (Branchiopoda: Anostraca) on the Indian subcontinent. Hydrobiologia 801, 117–128 (2017).
    Google Scholar 
    98.Petkovski, S. Taksonomsko-morfološka i zoogeografsko-ekološka studija Anostraca (Crustacea: Branchiopoda) jugoslovenskih zemalja. (Prirodno-matematički fakultet, Novi Sad, 1993).99.Pretus, J. L. A commented check-list of the Balearic Branchiopoda (Crustacea). Limnetica 6, 157–164 (1990).
    Google Scholar 
    100.van den Broeck, M., Waterkeyn, A., Rhazi, L. & Brendonck, L. Distribution, coexistence, and decline of Moroccan large branchiopods. J. Crustacean Biol. 35, 355–365 (2015).
    Google Scholar 
    101.Hijmans, R. J., Philips, S., Leathwick, J. & Elith, J. Package ‘dismo’. 9, 1–68 (2017).102.R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. (2014).103.Hijmans, R. J., Cameron, S. E. & Parra, J. L. Climate Date from Worldclim (2004).104.Alfonso, G. & Marrone, F. Branchiopoda Anostraca, Notostraca, Spinicaudata. In Checklist of the Italian fauna (in press).105.Defaye, D., Rabet, N. & Thiéry, A. Atlas et bibliographie des crustaces branchiopodes (Anostraca, Notostraca, Spinicaudata) de France metropolitaine. Collection patrimoines naturels (1998).106.Song, H., Buhay, J. E., Whiting, M. F. & Crandall, K. A. Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. PNAS 105, 13486–13491 (2008).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    107.Hall, T. A. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. Ser. 41, 95–98 (1999).CAS 

    Google Scholar 
    108.Aguilar, A. et al. High intraspecific genetic divergence in the versatile fairy shrimp Branchinecta lindahli with a comment on cryptic species in the genus Branchinecta (Crustacea: Anostraca). Hydrobiologia 801, 59–69 (2017).
    Google Scholar 
    109.Jeffery, N. W., Elías-Gutiérrez, M. & Adamowicz, S. J. Species diversity and phylogeographical affinities of the Branchiopoda (Crustacea) of Churchill, Manitoba, Canada. PLoS ONE 6, e18364 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    110.Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T. & Calcott, B. PartitionFinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol. Biol. Evol. 34, 772–773 (2017).CAS 
    PubMed 

    Google Scholar 
    111.Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549 (2018).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    112.Drummond, A. J., Suchard, M. A., Xie, D. & Rambaut, A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973 (2012).113.Huelsenbeck, J. P. & Ronquist, F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755 (2001).CAS 
    PubMed 

    Google Scholar 
    114.Ronquist, F. & Huelsenbeck, J. P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574 (2003).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    115.Ronquist, F. et al. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012).116.Bandelt, H. J., Forster, P. & Röhl, A. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16, 37–48 (1999).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    117.Leigh, J. W. & Bryant, D. popart: Full-feature software for haplotype network construction. Methods Ecol. Evol. 6, 1110–1116 (2015).
    Google Scholar 
    118.Xia, X. & Kumar, S. DAMBE7: New and improved tools for data analysis in molecular biology and evolution. Mol. Biol. Evol. 35, 1550–1552 (2018).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    119.Xia, X. & Lemey, P. Assessing substitution saturation with DAMBE. In The phylogenetic Handbook 615–630 (Cambridge University Press, 2009).120.Xia, X., Xie, Z., Salemi, M., Chen, L. & Wang, Y. An index of substitution saturation and its application. Mol. Phylogenet. Evol. 26, 1–7 (2003).CAS 
    PubMed 

    Google Scholar 
    121.Kimura, M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111–120 (1980).ADS 
    CAS 
    PubMed 

    Google Scholar 
    122.Rozas, J. et al. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol. Biol. Evol. 34, 3299–3302 (2017).CAS 

    Google Scholar 
    123.Nychka, D. et al. fields: Tools for Spatial Data (2020).124.Oksanen, J. et al. vegan: Community ecology package. – R package ver. 2.0-4. http://CRAN.R-project.org/package=vegan. (2012). More

  • in

    Transcriptional responses of Trichodesmium to natural inverse gradients of Fe and P availability

    1.Falkowski PG. Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean. Nature. 1997;387:272–5.CAS 

    Google Scholar 
    2.Zehr JP. Nitrogen fixation by marine cyanobacteria. Trends Microbiol. 2011;19:162–73.CAS 
    PubMed 

    Google Scholar 
    3.Capone DG, Zehr JP, Paerl HW, Bergman B, Carpenter EJ. Trichodesmium a globally significant marine cyanobacterium. Science (80-). 1997;276:1221–9.CAS 

    Google Scholar 
    4.Bergman B, Sandh G, Lin S, Larsson J, Carpenter EJ. Trichodesmium – a widespread marine cyanobacterium with unusual nitrogen fixation properties. FEMS Microbiol Rev. 2013;37:286–302. 37(3):286–302CAS 
    PubMed 

    Google Scholar 
    5.Capone DG, Burns JA, Montoya JP, Subramaniam A, Mahaffey C, Gunderson T, et al. Nitrogen fixation by Trichodesmium spp.: An important source of new nitrogen to the tropical and subtropical North Atlantic Ocean. Glob Biogeochem Cycles. 2005;19:1–17.
    Google Scholar 
    6.Mahaffey C, Michaels AF, Capone DG. The conundrum of marine N2 fixation. Am J Sci. 2005;305:546–95.CAS 

    Google Scholar 
    7.Moore C, Mills MM, Achterberg EP, Geider RJ, Laroche J, Lucas MI, et al. Large-scale distribution of Atlantic nitrogen fixation controlled by iron availability. Nat Geosci. 2009;2:867–71.CAS 

    Google Scholar 
    8.Dyhrman ST, Webb EA, Anderson DM, Moffett JW, Waterbury JB. Cell-specific detection of phosphorus stress in Trichodesmium from the Western North Atlantic. Limnol Oceanogr. 2002;47:1832–6.
    Google Scholar 
    9.Snow JT, Schlosser C, Woodward EMS, Mills MM, Achterberg EP, Mahaffey C, et al. Environmental controls on the biogeography of diazotrophy and Trichodesmium in the Atlantic Ocean. Glob Biogeochem Cycles. 2015;29:865–84.CAS 

    Google Scholar 
    10.Jickells TD, An ZS, Andersen KK, Baker AR, Bergametti C, Brooks N, et al. Global iron connections between desert dust, ocean biogeochemistry, and climate. Science. 2005;308:67–71.CAS 
    PubMed 

    Google Scholar 
    11.Schlosser CA, Strzepek K, Gao X, Fant C, Blanc É, Paltsev S, et al. The future of global water stress: an integrated assessment. Earth’s Future. 2014;2:341–61.
    Google Scholar 
    12.Wu J, Sunda W, Boyle EA, Karl DM. Phosphate depletion in the Western North Atlantic. Ocean Sci. 2000;289:759–62.CAS 

    Google Scholar 
    13.Mather RL, Reynolds SE, Wolff GA, Williams RG, Torres-Valdes S, Woodward EMS, et al. Phosphorus cycling in the North and South Atlantic Ocean subtropical gyres. Nat Geosci. 2008;1:439–43.CAS 

    Google Scholar 
    14.Ward BA, Dutkiewicz S, Moore CM, Follows MJ. Iron, phosphorus, and nitrogen supply ratios define the biogeography of nitrogen fixation. Limnol Oceanogr. 2013;58:2059–75.CAS 

    Google Scholar 
    15.Mills MM, Moore CM, Langlois R, Milne A, Achterberg E, Nachtigall K, et al. Nitrogen and phosphorus co-limitation of bacterial productivity and growth in the oligotrophic subtropical North Atlantic. Limnol Oceanogr. 2008;53:824–34.CAS 

    Google Scholar 
    16.Garcia NS, Fu F, Sedwick PN, Hutchins DA. Iron deficiency increases growth and nitrogen-fixation rates of phosphorus-deficient marine cyanobacteria. ISME J. 2015;9:238–45.CAS 
    PubMed 

    Google Scholar 
    17.Walworth NG, Fu FX, Webb EA, Saito MA, Moran D, McLlvin MR, et al. Mechanisms of increased Trichodesmium fitness under iron and phosphorus co-limitation in the present and future ocean. Nat Commun. 2016;7:1–11.
    Google Scholar 
    18.Walworth NG, Fu FX, Lee MD, Cai X, Saito MA, Webb EA, et al. Nutrient-colimited Trichodesmium as a nitrogen source or sink in a future ocean. Appl Environ Microbiol. 2018;84:1–14.CAS 

    Google Scholar 
    19.Held NA, Webb EA, McIlvin MM, Hutchins DA, Cohen NR, Moran DM, et al. Co-occurrence of Fe and P stress in natural populations of the marine diazotroph Trichodesmium. Biogeosciences 2020;17:2537–51.
    Google Scholar 
    20.Polyviou D, Baylay AJ, Hitchcock A, Robidart J, Moore CM, Bibby TS. Desert dust as a source of iron to the globally important diazotroph Trichodesmium. Front Microbiol. 2018;8:2683.PubMed 
    PubMed Central 

    Google Scholar 
    21.Snow JT, Polyviou D, Skipp P, Chrismas NA, Hitchcock A, Geider R, et al. Quantifying Integrated Proteomic Responses to Iron Stress in the Globally Important Marine Diazotroph Trichodesmium. PLOS ONE 2015;10:e0142626.22.Frischkorn KR, Haley ST, Dyhrman ST. Transcriptional and proteomic choreography under phosphorus deficiency and re-supply in the N2 fixing cyanobacterium Trichodesmium erythraeum. Front Microbiol. 2019;10:330. 2012;6:1728–39PubMed 
    PubMed Central 

    Google Scholar 
    23.Rouco M, Frischkorn KR, Haley ST, Alexander H, Dyhrman ST. Transcriptional patterns identify resource controls on the diazotroph Trichodesmium in the Atlantic and Pacific oceans. ISME J. 2018;12:1486–95.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    24.Shi T, Sun Y, Falkowski PG. Effects of iron limitation on the expression of metabolic genes in the marine cyanobacterium Trichodesmium erythraeum IMS101. Environ Microbiol. 2007;9:2945–56.CAS 
    PubMed 

    Google Scholar 
    25.Saito MA, Bertrand EM, Dutkiewicz S, Bulygin VV, Moran DM, Monteiro FM, et al. Iron conservation by reduction of metalloenzyme inventories in the marine diazotroph Crocosphaera watsonii. Proc Natl Acad Sci USA 2011;108:2184–9.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    26.La Roche J, Boyd PW, McKay RML, Geider RJ. Flavodoxin as an in situ marker for iron stress in phytoplankton. Nature. 1996;382:802–5.
    Google Scholar 
    27.De la Cerda B, Castielli O, Durán RV, Navarro JA, Hervás M, De la Rosa MA. A proteomic approach to iron and copper homeostasis in cyanobacteria. Brief Funct Genom Proteom. 2007;6:322–9.
    Google Scholar 
    28.Chappell PD, Webb EA. A molecular assessment of the iron stress response in the two phylogenetic clades of Trichodesmium. Environ Microbiol. 2010;12:13–27.CAS 
    PubMed 

    Google Scholar 
    29.Polyviou D, Machelett MM, Hitchcock A, Baylay AJ, MacMillan F, Mark Moore C, et al. Structural and functional characterization of IdiA/FutA (Tery_3377), an iron-binding protein from the ocean diazotroph Trichodesmium erythraeum. J Biol Chem. 2018;293:18099–109.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    30.Berman-Frank I, Lundgren P, Chen YB, Küpper H, Kolber Z, Bergman B, et al. Segregation of nitrogen fixation and oxygenic photosynthesis in the marine cyanobacterium Trichodesmium. Science. 2001;294:1534–7.CAS 
    PubMed 

    Google Scholar 
    31.Berman-Frank I, Lundgren P, Falkowski P. Nitrogen fixation and photosynthetic oxygen evolution in cyanobacteria. Res Microbiol. 2003;154:157–64.CAS 
    PubMed 

    Google Scholar 
    32.Sandh G, Ran L, Xu L, Sundqvist G, Bulone V, Bergman B. Comparative proteomic profiles of the marine cyanobacterium Trichodesmium erythraeum IMS101 under different nitrogen regimes. Proteomics. 2011;11:406–19.CAS 
    PubMed 

    Google Scholar 
    33.Orchard ED, Webb EA, Dyhrman ST. Molecular analysis of the phosphorus starvation response in Trichodesmium spp. Environ Microbiol. 2009;11:2400–11.CAS 
    PubMed 

    Google Scholar 
    34.Dyhrman ST, Ruttenberg KC. Presence and regulation of alkaline phosphatase activity in eukaryotic phytoplankton from the coastal ocean: Implications for dissolved organic phosphorus remineralization. Limnol Oceanogr. 2006;51:1381–90.CAS 

    Google Scholar 
    35.Karl DM. Nutrient dynamics in the deep blue sea. Trends Microbiol. 2002;10:410–8.CAS 
    PubMed 

    Google Scholar 
    36.Polyviou D, Hitchcock A, Baylay AJ, Moore CM, Bibby TS. Phosphite utilization by the globally important marine diazotroph Trichodesmium. Environ Microbiol Rep. 2015;7:824–30.CAS 
    PubMed 

    Google Scholar 
    37.Obata H, Karatani H, Matsui M, Nakayama E. Fundamental studies for chemical speciation of iron in seawater with an improved analytical method. Marine Chemistry. 1997;56:97–106.38.Kunde K, Wyatt NJ, González-Santana D, Tagliabue A, Mahaffey C, Lohan MC. Iron Distribution in the Subtropical North Atlantic: The Pivotal Role of Colloidal Iron. Glob Biogeochem Cycles. 2019;33:1532–47.CAS 

    Google Scholar 
    39.Woodward EMS, Rees AP. Nutrient distributions in an anticyclonic eddy in the northeast Atlantic Ocean, with reference to nanomolar ammonium concentrations. Deep Res Part II Top Stud Oceanogr. 2001;48:775–93.CAS 

    Google Scholar 
    40.Davis CE, Blackbird S, Wolff G, Woodward M, Mahaffey C. Seasonal organic matter dynamics in a temperate shelf sea. Prog Oceanogr. 2019;177:101925.
    Google Scholar 
    41.Lomas MW, Burke AL, Lomas DA, Bell DW, Shen C, Dyhrman ST, et al. Sargasso Sea phosphorus biogeochemistry: an important role for dissolved organic phosphorus (DOP). Biogeosci Discuss. 2009;6:10137–75.
    Google Scholar 
    42.Klawonn I, Lavik G, Böning P, et al. Simple approach for the preparation of 15−15N2-enriched water for nitrogen fixation assessments: evaluation, application and recommendations. Front Microbiol. 2015;6:769.PubMed 
    PubMed Central 

    Google Scholar 
    43.Frischkorn KR, Haley ST, Dyhrman ST. Coordinated gene expression between Trichodesmium and its microbiome over day-night cycles in the North Pacific Subtropical Gyre. ISME J. 2018;12:997–1007.PubMed 
    PubMed Central 

    Google Scholar 
    44.Tang W, Cerdán-García E, Berthelot H, Polyviou D, Wang S, Baylay A, et al. New insights into the distributions of nitrogen fixation and diazotrophs revealed by high-resolution sensing and sampling methods. ISME J. 2020;14:2514–26.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    45.Zehr JP, McReynolds LA. Use of degenerate oligonucleotides for amplification of the nifH gene from the marine cyanobacterium Trichodesmium thiebautii. Appl Environ Microbiol. 1989;55:2522–6.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    46.Zani S, Mellon MT, Collier JL, Zehr JP. Expression of nifH genes in natural microbial assemblages in Lake George, New York, detected by reverse transcriptase PCR. Appl Environ Microbiol. 2000;66:3119–24.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    47.Turk KA, Rees AP, Zehr JP, Pereira N, Swift P, Shelley R, et al. Nitrogen fixation and nitrogenase (nifH) expression in tropical waters of the eastern North Atlantic. ISME J. 2011;5:1201–12.CAS 
    PubMed 

    Google Scholar 
    48.Hitchen J, Sooknanan R, Khanna A. ScriptSeq V2 Library Preparation Method: A Rapid and Efficient Method for Preparing Directional RNA-Seq Libraries. J Biomol Tech. 2012;23:S33–S34.PubMed Central 

    Google Scholar 
    49.Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. Embnet J. 2011;17:10–2.
    Google Scholar 
    50.Nurk S, Meleshko D, Korobeynikov A, Pevzner PA. MetaSPAdes: a new versatile metagenomic assembler. Genome Res. 2017;27:824–34.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    51.Wu Y-W, Tang Y-H, Tringe SG, Simmons BA, Singer SW. MaxBin: an automated binning method to recover individual genomes from metagenomes using. Microbiome. 2014;2:4904–9.
    Google Scholar 
    52.Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: Assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25:1043–55.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    53.Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357–9.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    54.Hyatt D, Chen GL, LoCascio PF, Land ML, Frank W, Larimer LJH. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinforma. 2010;11:1–11.
    Google Scholar 
    55.Enright AJ, Van Dongen S, Ouzounis CA. An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res. 2002;30:1575–84.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    56.Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, et al. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res. 2014;42:D206–14.CAS 
    PubMed 

    Google Scholar 
    57.Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015;12:59–60.CAS 
    PubMed 

    Google Scholar 
    58.Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. correspondence QIIME allows analysis of high- throughput community sequencing data Intensity normalization improves color calling in SOLiD sequencing. Nat Publ Gr. 2010;7:335–6.CAS 

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

    Google Scholar 
    60.Edgar RC. UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10:996–8.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    61.Westreich ST, Treiber ML, Mills DA, Korf I, Lemay DG. SAMSA2: a standalone metatranscriptome analysis pipeline. BMC Bioinforma. 2018;19:1–11.
    Google Scholar 
    62.Bolger AM, Lohse M, Usadel B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    63.Kopylova E, Noé L, Touzet H. SortMeRNA: Fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics 2012;28:3211–7.CAS 

    Google Scholar 
    64.Zhang J, Kobert K, Flouri T, Stamatakis A. PEAR: A fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics. 2014;30:614–20.CAS 
    PubMed 

    Google Scholar 
    65.Tatusova T, Ciufo S, Fedorov B, O’Neill K, Tolstoy I. RefSeq microbial genomes database: new representation and annotation strategy. Nucleic Acids Res. 2014;42:D553–9.66.Kim D, Paggi JM, Park C, Bennett C, Salzberg SL. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol. 2019;37:907–15.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    67.Liao Y, Smyth GK, Shi W. FeatureCounts: an efficient general-purpose program for assigning sequence reads to genomic features. Bioinformatics 2014;30:923–30.CAS 

    Google Scholar 
    68.Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:1–21.
    Google Scholar 
    69.Wu S, Mi T, Zhen Y, Yu K, Wang F, Yu Z. A Rise in ROS and EPS Production: New Insights into the Trichodesmium erythraeum Response to Ocean Acidification. J Phycol. 2021;57:172–82.CAS 
    PubMed 

    Google Scholar 
    70.Sedwick PN, Church TM, Bowie AR, Marsay CM, Ussher SJ, Achilles KM, et al. Iron in the Sargasso Sea (Bermuda Atlantic Time-series Study region) during summer: Eolian imprint, spatiotemporal variability, and ecological implications. Global Biogeochem Cycles. 2005;19:GB4006.71.Hatta M, Measures CI, Wu J, Roshan S, Fitzsimmons JN, Sedwick P, et al. An overview of dissolved Fe and Mn distributions during the 2010-2011 U.S. GEOTRACES north Atlantic cruises: GEOTRACES GA03. Deep Res Part II Top Stud Oceanogr. 2015;116:117–29.CAS 

    Google Scholar 
    72.Mahaffey C, Reynolds S, Davis CE, Lohan MC. Alkaline phosphatase activity in the subtropical ocean: insights from nutrient, dust and trace metal addition experiments. Front Mar Sci. 2014;1:73.
    Google Scholar 
    73.Church MJ, Mahaffey C, Letelier RM, Lukas R, Zehr JP, Karl DM. Physical forcing of nitrogen fixation and diazotroph community structure in the North Pacific subtropical gyre. Global Biogeochem Cycles. 2009;23:GB2020.74.Zehr JP, Capone DG. Changing perspectives in marine nitrogen fixation. Science. 2020;368:eaay9514.75.Benavides M, Moisander PH, Daley MC, Bode A, Arístegui J. Longitudinal variability of diazotroph abundances in the subtropical North Atlantic Ocean. J Plankton Res. 2016;38:662–72.CAS 

    Google Scholar 
    76.Luo YW, Doney SC, Anderson LA, Benavides M, Berman-Frank I, Bode A, et al. Database of diazotrophs in global ocean: Abundance, biomass and nitrogen fixation rates. Earth Syst Sci Data. 2012;4:47–73.
    Google Scholar 
    77.Moisander PH, Beinart RA, Voss M, Zehr JP. Diversity and abundance of diazotrophic microorganisms in the South China Sea during intermonsoon. ISME J. 2008;2:954–67.CAS 
    PubMed 

    Google Scholar 
    78.Moisander PH, Serros T, Paerl RW, Beinart RA, Zehr JP. Gammaproteobacterial diazotrophs and nifH gene expression in surface waters of the South Pacific Ocean. ISME J 2014;8:1962–73.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    79.Robidart JC, Church MJ, Ryan JP, et al. Ecogenomic sensor reveals controls on N2-fixing microorganisms in the North Pacific Ocean. ISME J. 2014;8:1175–85.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    80.Stenegren M, Caputo A, Berg C, Bonnet S, Foster R. Distribution and drivers of symbiotic and free-living diazotrophic cyanobacteria in the western tropical South Pacific. Biogeosciences 2018;15:1559–78.CAS 

    Google Scholar 
    81.Langlois R, Großkopf T, Mills M, Takeda S, LaRoche J. Widespread Distribution and Expression of Gamma A (UMB), an Uncultured, Diazotrophic, γ-Proteobacterial nifH Phylotype. PLoS ONE. 2015;10:e0128912.PubMed 
    PubMed Central 

    Google Scholar 
    82.Ratten J-M, LaRoche J, Desai DK, et al. Sources of iron and phosphate affect the distribution of diazotrophs in the North Atlantic. Deep Sea Res Part II: Topical Stud Oceanogr. 2015;116:332–41.CAS 

    Google Scholar 
    83.Voss, M, Croot, P, Lochte, K, Mills, M, Peeken, I. Patterns of nitrogen fixation along 10°N in the tropical Atlantic. Geophys Res Lett. 2004;31:L23S09.84.Bibby TS, Nield J, Barber J. Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria. Nature. 2001;412:743–5.85.Richier S, Macey AI, Pratt NJ, Honey DJ, Moore CM, Bibby TS. Abundances of iron-binding photosynthetic and nitrogen-fixing proteins of Trichodesmium both in culture and in situ from the North Atlantic. PLoS ONE. 2012;7:e35571.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    86.Keren N, Aurora R, Pakrasi HB. Critical roles of bacterioferritins in iron storage and proliferation of cyanobacteria. Plant Physiol. 2004;135:1666–73.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    87.González A, Bes MT, Valladares A, Peleato ML, Fillat MF. FurA is the master regulator of iron homeostasis and modulates the expression of tetrapyrrole biosynthesis genes in Anabaena sp. PCC 7120. Environ Microbiol. 2012;14:3175–87.PubMed 

    Google Scholar 
    88.Sebastian M, Ammerman JW. The alkaline phosphatase PhoX is more widely distributed in marine bacteria than the classical PhoA. ISME J. 2009;3:563–72.CAS 
    PubMed 

    Google Scholar 
    89.Browning TJ, Achterberg EP, Yong JC, Rapp I, Utermann C, Engel A, et al. Iron limitation of microbial phosphorus acquisition in the tropical North Atlantic. Nat Commun. 2017;8:1–7.
    Google Scholar 
    90.Proudfoot M, Kuznetsova E, Brown G, Rao NN, Kitagawa M, Mori H, et al. General enzymatic screens identify three new nucleotidases in Escherichia coli: Biochemical characterization of SurE, YfbR, and YjjG. J Biol Chem. 2004;279:54687–94.CAS 
    PubMed 

    Google Scholar 
    91.Orchard ED, Benitez-Nelson CR, Pellechia PJ, Lomas MW, Dyhrman ST. Polyphosphate in Trichodesmium from the low-phosphorus Sargasso Sea. Limnol Oceanogr. 2010;55:2161–9.CAS 

    Google Scholar 
    92.Berman-Frank I, Cullen JT, Shaked Y, Sherrell RM, Falkowski PG. Iron availability, cellular iron quotas, and nitrogen fixation in Trichodesmium. Limnol Oceanogr. 2001;46:1249–60.CAS 

    Google Scholar 
    93.Schoffman H, Keren N. Function of the IsiA pigment–protein complex in vivo. Photosynth Res. 2019;141:343–53.CAS 
    PubMed 

    Google Scholar 
    94.Küpper H, Ferimazova N, Šetlík I, Berman-Frank I. Traffic lights in Trichodesmium. Regulation of photosynthesis for nitrogen fixation studied by chlorophyll fluorescence kinetic microscopy. Plant Physiol. 2004;135:2120–33.PubMed 
    PubMed Central 

    Google Scholar 
    95.Behrenfeld MJ, Milligan AJ. Photophysiological expressions of iron stress in phytoplankton. Ann Rev Mar Sci. 2013;5:217–46.PubMed 

    Google Scholar 
    96.Ho TY. Nickel limitation of nitrogen fixation in Trichodesmium. Limnol Oceanogr. 2013;58:112–20.CAS 

    Google Scholar 
    97.Tilman D. Resources: a graphical‐mechanistic approach to competition and predation. Am Nat. 1980;116:362–3.
    Google Scholar 
    98.Mills MM, Ridame C, Davey M, La Roche J, Geider RJ. Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic. Nature 2004;429:292–4.CAS 
    PubMed 

    Google Scholar 
    99.Saito MA, McIlvin MR, Moran DM, Goepfert TJ, DiTullio GR, Post AF, et al. Multiple nutrient stresses at intersecting Pacific Ocean biomes detected by protein biomarkers. Science 2014;345:1173–7.CAS 
    PubMed 

    Google Scholar 
    100.NASA Goddard Space Flight Center, Ocean Ecology Laboratory, Ocean Biology Processing Group. Moderate-resolution Imaging Spectroradiometer (MODIS) Aqua Chlorophyll Data. MODIS-Aqua Level 3 Mapped Chlorophyll Data Version R2018.0. NASA OB.DAAC, Greenbelt, MD, USA. Published online 2017. More

  • in

    The science of the host–virus network

    1.Jones, K. E. et al. Global trends in emerging infectious diseases. Nature 451, 990–993 (2008).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    2.Woolhouse, M. E. et al. Temporal trends in the discovery of human viruses. Proc. R. Soc. B 275, 2111–2115 (2008).PubMed 
    PubMed Central 

    Google Scholar 
    3.Smith, K. F. et al. Global rise in human infectious disease outbreaks. J. R. Soc. Interface 11, 20140950 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    4.Carlson, C. J. et al. Climate change will drive novel cross-species viral transmission. Preprint at bioRxiv https://doi.org/10.1101/2020.01.24.918755 (2020).5.Swei, A., Couper, L. I., Coffey, L. L., Kapan, D. & Bennett, S. Patterns, drivers, and challenges of vector-borne disease emergence. Vector Borne Zoonotic Dis. 20, 159–170 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    6.Belay, E. D. et al. Zoonotic disease programs for enhancing global health security. Emerg. Infect. Dis. 23, S65 (2017).PubMed Central 

    Google Scholar 
    7.Morse, S. S. et al. Prediction and prevention of the next pandemic zoonosis. Lancet 380, 1956–1965 (2012).PubMed 
    PubMed Central 

    Google Scholar 
    8.Carroll, D. et al. The global virome project. Science 359, 872–874 (2018).CAS 
    PubMed 

    Google Scholar 
    9.Carlson, C. J., Zipfel, C. M., Garnier, R. & Bansal, S. Global estimates of mammalian viral diversity accounting for host sharing. Nat. Ecol. Evol. 3, 1070–1075 (2019).PubMed 

    Google Scholar 
    10.Babayan, S. A., Orton, R. J. & Streicker, D. G. Predicting reservoir hosts and arthropod vectors from evolutionary signatures in RNA virus genomes. Science 362, 577–580 (2018).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    11.Han, B. A. et al. Undiscovered bat hosts of filoviruses. PLoS Negl. Trop. Dis. 10, e0004815 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    12.Schmidt, J. P. et al. Spatiotemporal fluctuations and triggers of Ebola virus spillover. Emerg. Infect. Dis. 23, 415 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    13.Guth, S., Visher, E., Boots, M. & Brook, C. E. Host phylogenetic distance drives trends in virus virulence and transmissibility across the animal–human interface. Phil. Trans. R. Soc. Biol. Sci. 374, 20190296 (2019).
    Google Scholar 
    14.Glennon, E. E. et al. Syndromic detectability of haemorrhagic fever outbreaks. Preprint at medRxiv https://doi.org/10.1101/2020.03.28.20019463 (2020).15.Pigott, D. M. et al. Local, national, and regional viral haemorrhagic fever pandemic potential in Africa: a multistage analysis. Lancet 390, 2662–2672 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    16.Palmer, S., Brown, D. & Morgan, D. Early qualitative risk assessment of the emerging zoonotic potential of animal diseases. BMJ 331, 1256–1260 (2005).PubMed 
    PubMed Central 

    Google Scholar 
    17.Grange, Z. L. et al. Ranking the risk of animal-to-human spillover for newly discovered viruses. Proc. Natl Acad. Sci. USA 118, e2002324118 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    18.Carlson, C. J. From PREDICT to prevention, one pandemic later. Lancet Microbe 1, e6–e7 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    19.Holmes, E., Rambaut, A. & Andersen, K. Pandemics: spend on surveillance, not prediction. Nature 558, 180–182 (2018).CAS 
    PubMed 

    Google Scholar 
    20.Breiman, L. Statistical modeling: the two cultures (with comments and a rejoinder by the author). Stat. Sci. 16, 199–231 (2001).
    Google Scholar 
    21.Mouquet, N. et al. Predictive ecology in a changing world. J. Appl. Ecol. 52, 1293–1310 (2015).
    Google Scholar 
    22.Olival, K. J. et al. Host and viral traits predict zoonotic spillover from mammals. Nature 546, 646–650 (2017).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    23.Stephens, P. R. et al. Global mammal parasite database version 2.0. Ecology 98, 1476 (2017).PubMed 

    Google Scholar 
    24.Wardeh, M., Risley, C., McIntyre, M. K., Setzkorn, C. & Baylis, M. Database of host–pathogen and related species interactions, and their global distribution. Sci. Data 2, 150049 (2015).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    25.Shaw, L. P. et al. The phylogenetic range of bacterial and viral pathogens of vertebrates. Mol. Ecol. 29, 3361–3379 (2020).PubMed 

    Google Scholar 
    26.Gibb, R. et al. Data proliferation, reconciliation, and synthesis in viral ecology. BioScience https://doi.org/10.1093/biosci/biab080 (2021).27.Dallas, T., Park, A. W. & Drake, J. M. Predicting cryptic links in host–parasite networks. PLoS Comput. Biol. 13, e1005557 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    28.Poisot, T. et al. Imputing the mammalian virome with linear filtering and singular value decomposition. Preprint at https://arxiv.org/abs/2105.14973 (2021).29.Carlson, C. J. et al. The Global Virome in One Network (VIRION): an atlas of vertebrate–virus associations. Preprint at bioRxiv https://doi.org/10.1101/2021.08.06.455442 (2021).30.Albery, G. F., Eskew, E. A., Ross, N. & Olival, K. J. Predicting the global mammalian viral sharing network using phylogeography. Nat. Commun. 11, 2260 (2020).31.Davies, T. J. & Pedersen, A. B. Phylogeny and geography predict pathogen community similarity in wild primates and humans. Proc. R. Soc. B Biol. Sci. 275, 1695–1701 (2008).
    Google Scholar 
    32.Guy, C., Thiagavel, J., Mideo, N. & Ratcliffe, J. M. Phylogeny matters: revisiting ‘a comparison of bats and rodents as reservoirs of zoonotic viruses’. R. Soc. Open Sci. 6, 181182 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    33.Washburne, A. D. et al. Taxonomic patterns in the zoonotic potential of mammalian viruses. PeerJ 6, e5979 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    34.Plowright, R. K. et al. Pathways to zoonotic spillover. Nat. Rev. Microbiol. 15, 502 (2017).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    35.Stephens, P. R. et al. The macroecology of infectious diseases: a new perspective on global-scale drivers of pathogen distributions and impacts. Ecol. Lett. 19, 1159–1171 (2016).PubMed 

    Google Scholar 
    36.Longdon, B., Brockhurst, M. A., Russell, C. A., Welch, J. J. & Jiggins, F. M. The evolution and genetics of virus host shifts. PLoS Pathog. 10, e1004395 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    37.Farrell, M. J., Elmasri, M., Stephens, D. A. & Davies, T. J. Predicting missing links in global host–parasite networks. bioRxiv https://doi.org/10.1101/2020.02.25.965046 (2020).38.Gilbert, A. T. et al. Deciphering serology to understand the ecology of infectious diseases in wildlife. EcoHealth 10, 298–313 (2013).PubMed 

    Google Scholar 
    39.Becker, D. J., Seifert, S. N. & Carlson, C. J. Beyond infection: integrating competence into reservoir host prediction. Trends Ecol. Evol. 35, 1062–1065 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    40.Walsh, M. G., Mor, S. M., Maity, H. & Hossain, S. A preliminary ecological profile of Kyasanur Forest disease virus hosts among the mammalian wildlife of the Western Ghats, India. Ticks Tick Borne Dis. 11, 101419 (2020).PubMed 

    Google Scholar 
    41.Plowright, R. K. et al. Prioritizing surveillance of Nipah virus in India. PLoS Negl. Trop. Dis. 13, e0007393 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    42.Schmidt, J. P. et al. Ecological indicators of mammal exposure to Ebolavirus. Philos. Trans. R. Soc. B Biol. Sci. 374, 20180337 (2019).
    Google Scholar 
    43.Worsley-Tonks, K. E. et al. Using host traits to predict reservoir host species of rabies virus. PLoS Negl. Trop. Dis. 14, e0008940 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    44.Woolhouse, M. E. & Gowtage-Sequeria, S. Host range and emerging and reemerging pathogens. Emerg. Infect. Dis. 11, 1842 (2005).PubMed 
    PubMed Central 

    Google Scholar 
    45.Johnson, C. K. et al. Spillover and pandemic properties of zoonotic viruses with high host plasticity. Sci. Rep. 5, 14830 (2015).
    Google Scholar 
    46.Elena, S. F. & Sanjuán, R. Adaptive value of high mutation rates of RNA viruses: separating causes from consequences. J. Virol. 79, 11555–11558 (2005).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    47.Duffy, S. Why are RNA virus mutation rates so damn high? PLoS Biol. 16, e3000003 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    48.Grewelle, R. E. Larger viral genome size facilitates emergence of zoonotic diseases. Preprint at bioRxiv https://doi.org/10.1101/2020.03.10.986109 (2020).49.Mollentze, N. & Streicker, D. G. Viral zoonotic risk is homogenous among taxonomic orders of mammalian and avian reservoir hosts. Proc. Natl Acad. Sci. USA 117, 9423–9430 (2020).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    50.Walker, J. W., Han, B. A., Ott, I. M. & Drake, J. M. Transmissibility of emerging viral zoonoses. PLoS ONE 13, e0206926 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    51.Damas, J. et al. Broad host range of SARS-CoV-2 predicted by comparative and structural analysis of ACE2 in vertebrates. Proc. Natl Acad. Sci. USA https://doi.org/10.1073/pnas.2010146117 (2020).52.Zhang, Z. et al. Rapid identification of human-infecting viruses. Transbound. Emerg. Dis. 66, 2517–2522 (2019).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    53.Eng, C. L., Tong, J. C. & Tan, T. W. Predicting zoonotic risk of influenza A viruses from host tropism protein signature using random forest. Int. J. Mol. Sci. 18, 1135 (2017).PubMed Central 

    Google Scholar 
    54.Li, J. et al. Machine learning methods for predicting human-adaptive influenza A viruses based on viral nucleotide compositions. Mol. Biol. Evol. 37, 1224–1236 (2020).CAS 
    PubMed 

    Google Scholar 
    55.Kim, B., Niu, X., Hunter, D. R. & Cao, X. A dynamic additive and multiplicative effects model with application to the United Nations voting behaviors. Preprint at https://arxiv.org/abs/1803.06711 (2018).56.Becker, D. et al. Optimizing predictive models to prioritize viral discovery in zoonotic reservoirs. Lancet Microbe (in the press).57.Han, B. A., Schmidt, J. P., Bowden, S. E. & Drake, J. M. Rodent reservoirs of future zoonotic diseases. Proc. Natl Acad. Sci. USA 112, 7039–7044 (2015).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    58.Plourde, B. T. et al. Are disease reservoirs special? Taxonomic and life history characteristics. PLoS ONE 12, e0180716 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    59.Keesing, F. et al. Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468, 647–652 (2010).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    60.Albery, G. F. & Becker, D. J. Fast-lived hosts and zoonotic risk. Trends Parasitol. 37, 117–129 (2021).CAS 
    PubMed 

    Google Scholar 
    61.Young, C. C. & Olival, K. J. Optimizing viral discovery in bats. PLoS ONE 11, e0149237 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    62.Albery, G. F. et al. Urban-adapted mammal species have more known pathogens. Preprint at bioRxiv https://doi.org/10.1101/2021.01.02.425084 (2021).63.Wille, M., Geoghegan, J. L. & Holmes, E. C. How accurately can we assess zoonotic risk? PLoS Biol. 19, e3001135 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    64.Gibb, R. et al. Mammal virus diversity estimates are unstable due to accelerating discovery effort. Preprint at bioRxiv https://doi.org/10.1101/2021.08.10.455791 (2021).65.Xu, G. J. et al. Comprehensive serological profiling of human populations using a synthetic human virome. Science 348, aaa0698 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    66.Geoghegan, J. L. & Holmes, E. C. Predicting virus emergence amid evolutionary noise. Open Biol. 7, 170189 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    67.Fischhoff, I. R., Castellanos, A. A., Rodrigues, J. P., Varsani, A. & Han, B. A. Predicting the zoonotic capacity of mammals to transmit SARS-CoV-2. Proc. R. Soc. B Biol. Sci. https://doi.org/10.1098/rspb.2021.1651 (2021).68.Hou, Y. et al. Angiotensin-converting enzyme 2 (ACE2) proteins of different bat species confer variable susceptibility to SARS-CoV entry. Arch. Virol. 155, 1563–1569 (2010).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    69.Thompson, A. J., de Vries, R. P. & Paulson, J. C. Virus recognition of glycan receptors. Curr. Opin. Virol. 34, 117–129 (2019).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    70.Kocher, J. F. et al. Bat caliciviruses and human noroviruses are antigenically similar and have overlapping histo-blood group antigen binding profiles. Mbio 9, e00869-18 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    71.Chiramel, A. I. et al. TRIM5α restricts flavivirus replication by targeting the viral protease for proteasomal degradation. Cell Rep. 27, 3269–3283 (2019).CAS 
    PubMed 

    Google Scholar 
    72.Young, F., Rogers, S. & Robertson, D. L. Predicting host taxonomic information from viral genomes: a comparison of feature representations. PLoS Comput. Biol. 16, e1007894 (2020).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    73.Baek, M. et al. Accurate prediction of protein structures and interactions using a three-track neural network. Science 373, 871–876 (2021).CAS 
    PubMed 

    Google Scholar 
    74.Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583–589 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    75.Truong, P., Garcia-Vallve, S. & Puigbo, P. An unsupervised algorithm for host identification in flaviviruses. Life https://doi.org/10.3390/life11050442 (2021).76.Mollentze, N., Babayan, S. & Streicker, D. Identifying and prioritizing potential human-infecting viruses from their genome sequences. PLoS Biol. 19, e3001390 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    77.Wang, W. et al. A network-based integrated framework for predicting virus–prokaryote interactions. NAR Genom. Bioinform. 2, lqaa044 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    78.Bartoszewicz, J. M., Seidel, A. & Renard, B. Y. Interpretable detection of novel human viruses from genome sequencing data. NAR Genom. Bioinform. 3, lqab004 (2021).PubMed 
    PubMed Central 

    Google Scholar 
    79.He, X. et al. Neural collaborative filtering. In Proc. 26th International Conference on World Wide Web 26, 173–182 (Republic and Canton of Geneva, Switzerland, 2017).80.Fout, A., Byrd, J., Shariat, B. & Ben-Hur, A. Protein interface prediction using graph convolutional networks. NIPS’17: Proc. 31st International Conference on Neural Information Processing Systems 31, 6533–6542 (2017).
    Google Scholar 
    81.Hamilton, W. L., Ying, R. & Leskovec, J. Representation learning on graphs: methods and applications. IEEE Data Eng. Bull. 40, 52–74 (2017).
    Google Scholar 
    82.Bergner, L. M. et al. Characterizing and evaluating the zoonotic potential of novel viruses discovered in vampire bats. Viruses 13, 252 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    83.Dietze, M. C. et al. Iterative near-term ecological forecasting: needs, opportunities, and challenges. Proc. Natl Acad. Sci. USA 115, 1424–1432 (2018).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    84.Schulz, J. E. et al. Serological evidence for henipa-like and filo-like viruses in Trinidad bats. J. Infect. Dis. 221, S375–S382 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    85.Brook, C. E. et al. Disentangling serology to elucidate henipa- and filovirus transmission in Madagascar fruit bats. J. Anim. Ecol. 88, 1001–1016 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    86.Seifert, S. N. et al. Rousettus aegyptiacus bats do not support productive Nipah virus replication. J. Infect. Dis. 221, S407–S413 (2020).CAS 
    PubMed 

    Google Scholar 
    87.Carlson, C. J. et al. The future of zoonotic risk prediction. Phil. Trans. R. Soc. B Biol. Sci. 376, 20200358 (2021).
    Google Scholar 
    88.Ge, X.-Y. et al. Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature 503, 535–538 (2013).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    89.Menachery, V. D. et al. A SARS-like cluster of circulating bat coronaviruses shows potential for human emergence. Nat. Med. 21, 1508–1513 (2015).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    90.Guan, Y. et al. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 302, 276–278 (2003).CAS 
    PubMed 

    Google Scholar 
    91.Woo, P. C. Y. et al. Characterization and complete genome sequence of a novel coronavirus, coronavirus HKU1, from patients with pneumonia. J. Virol. 79, 884–895 (2005).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    92.Li, W. et al. Bats are natural reservoirs of SARS-like coronaviruses. Science 310, 676–679 (2005).CAS 
    PubMed 

    Google Scholar 
    93.Wang, M. et al. SARS-CoV infection in a restaurant from palm civet. Emerg. Infect. Dis. 11, 1860–1865 (2005).PubMed 
    PubMed Central 

    Google Scholar 
    94.Hu, B. et al. Discovery of a rich gene pool of bat SARS-related coronaviruses provides new insights into the origin of SARS coronavirus. PLoS Pathog. 13, e1006698 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    95.Zhou, P. et al. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature 579, 270–273 (2020).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    96.Xiao, K. et al. Isolation of SARS-CoV-2-related coronavirus from Malayan pangolins. Nature 583, 286–289 (2020).CAS 
    PubMed 

    Google Scholar 
    97.Lam, T.-Y. et al. Identifying SARS-CoV-2-related coronaviruses in Malayan pangolins. Nature 583, 282–285 (2020).CAS 
    PubMed 

    Google Scholar 
    98.Wacharapluesadee, S. et al. Evidence for SARS-CoV-2 related coronaviruses circulating in bats and pangolins in Southeast Asia. Nat. Commun. 12, 972 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    99.Holmes, E. C. et al. The origins of SARS-CoV-2: a critical review. Cell 184, 4848–4856 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    100.Oude Munnink, B. B. et al. Transmission of SARS-CoV-2 on mink farms between humans and mink and back to humans. Science 371, 172–177 (2021).CAS 
    PubMed 

    Google Scholar 
    101.Chandler, J. C. et al. SARS-CoV-2 exposure in wild white-tailed deer (Odocoileus virginianus). Proc. Natl Acad. Sci. USA 118, e2114828118 (2021).PubMed 

    Google Scholar 
    102.Jia, P., Dai, S., Wu, T. & Yang, S. New approaches to anticipate the risk of reverse zoonosis. Trends Ecol. Evol. 36, 580–590 (2021).PubMed 
    PubMed Central 

    Google Scholar 
    103.Lednicky, J. A. et al. Isolation of a novel recombinant canine coronavirus from a visitor to Haiti: further evidence of transmission of coronaviruses of zoonotic origin to humans. Clin. Infect. Dis. https://doi.org/10.1093/cid/ciab924 (2021).104.Vlasova, A. N. et al. Novel canine coronavirus isolated from a hospitalized pneumonia patient, East Malaysia. Clin. Infect. Dis. https://doi.org/10.1093/cid/ciab456 (2021).105.Lednicky, J. A. et al. Emergence of porcine delta-coronavirus pathogenic infections among children in Haiti through independent zoonoses and convergent evolution. Preprint at medRxiv https://doi.org/10.1101/2021.03.19.21253391 (2021).106.Hay, A. J. & McCauley, J. W. The WHO global influenza surveillance and response system (GISRS)—a future perspective. Influenza Other Respir. Viruses 12, 551–557 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    107.Subbarao, K. et al. Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. Science 279, 393–396 (1998).CAS 
    PubMed 

    Google Scholar 
    108.Kandeel, A. et al. Zoonotic transmission of avian influenza virus (H5N1), Egypt, 2006–2009. Emerg. Infect. Dis. 16, 1101 (2010).PubMed 
    PubMed Central 

    Google Scholar 
    109.Ke, C. et al. Human infection with highly pathogenic avian influenza A (H7N9) virus, China. Emerg. Infect. Dis. 23, 1332 (2017).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    110.Gaidet, N. et al. Evidence of infection by H5N2 highly pathogenic avian influenza viruses in healthy wild waterfowl. PLoS Pathog. 4, e1000127 (2008).PubMed 
    PubMed Central 

    Google Scholar 
    111.Webster, R. G., Bean, W. J., Gorman, O. T., Chambers, T. M. & Kawaoka, Y. Evolution and ecology of influenza A viruses. Microbiol. Mol. Biol. Rev. 56, 152–179 (1992).CAS 

    Google Scholar 
    112.Pawar, S. D. et al. Avian influenza surveillance reveals presence of low pathogenic avian influenza viruses in poultry during 2009–2011 in the West Bengal State, India. Virol. J. 9, 151 (2012).PubMed 
    PubMed Central 

    Google Scholar 
    113.Parry, R., Wille, M., Turnbull, O. M., Geoghegan, J. L. & Holmes, E. C. Divergent influenza-like viruses of amphibians and fish support an ancient evolutionary association. Viruses 12, 1042 (2020).CAS 
    PubMed Central 

    Google Scholar 
    114.Campbell, P. J. et al. The M segment of the 2009 pandemic influenza virus confers increased neuraminidase activity, filamentous morphology, and efficient contact transmissibility to A/Puerto Rico/8/1934-based reassortant viruses. J. Virol. 88, 3802–3814 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    115.Carlson, C. Evolutionary surprise, artificial intelligence, and H5N8. The Verena Blog https://www.viralemergence.org/blog/evolutionary-surprise-artificial-intelligence-and-h5n8 (2021).116.Wardeh, M., Baylis, M. & Blagrove, M. S. Predicting mammalian hosts in which novel coronaviruses can be generated. Nat. Commun. 12, 780 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    117.Crossman, L. C. Leveraging deep learning to simulate coronavirus spike proteins has the potential to predict future zoonotic sequences. Preprint at bioRxiv https://doi.org/10.1101/2020.04.20.046920 (2020). More

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    Reply to: Spatial scale and the synchrony of ecological disruption

    1.Colwell, R. K. Spatial scale and the synchrony of ecological disruption. Nature https://doi.org/10.1038/s41586-021-03760-4 (2021).2.Trisos, C. H., Merow, C. & Pigot, A. L. The projected timing of abrupt ecological disruption from climate change. Nature 580, 496–501 (2020).ADS 
    CAS 
    Article 

    Google Scholar 
    3.Jorda, G. et al. Ocean warming compresses the three-dimensional habitat of marine life. Nat. Ecol. Evol. 4, 109–114 (2020).Article 

    Google Scholar 
    4.Hughes, T. P. et al. Global warming transforms coral reef assemblages. Nature 556, 492–496 (2018).ADS 
    CAS 
    Article 

    Google Scholar 
    5.Ricklefs, R. E. Disintegration of the ecological community. Am. Nat. 172, 741–750 (2008).Article 

    Google Scholar 
    6.Hurlbert, A. H. & Jetz, W. Species richness, hotspots, and the scale dependence of range maps in ecology and conservation. Proc. Natl Acad. Sci. USA 104, 13384–13389 (2007).ADS 
    CAS 
    Article 

    Google Scholar 
    7.Nadeau, C. P., Urban, M. C. & Bridle, J. R. Coarse climate change projections for species living in a fine-scaled world. Glob. Change Biol. 23, 12–24 (2017).ADS 
    Article 

    Google Scholar 
    8.Stewart, S. B. et al. Climate extreme variables generated using monthly time‐series data improve predicted distributions of plant species. Ecography 44, 626–639 (2021).Article 

    Google Scholar 
    9.Harris, R. M. B. et al. Biological responses to the press and pulse of climate trends and extreme events. Nat. Clim. Change 8, 579–587 (2018).ADS 
    Article 

    Google Scholar 
    10.McKechnie, A. E. & Wolf, B. O. The Physiology of Heat Tolerance in Small Endotherms. Physiology 34, 302–313 (2019).CAS 
    Article 

    Google Scholar 
    11.Valladares, F. et al. The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change. Ecol. Lett. 17, 1351–1364 (2014).Article 

    Google Scholar 
    12.Mahony, C. R. & Cannon, A. J. Wetter summers can intensify departures from natural variability in a warming climate. Nat. Commun. 9, 783 (2018).ADS 
    Article 

    Google Scholar 
    13.Molnár, P. K., Derocher, A. E., Thiemann, G. W. & Lewis, M. A. Predicting survival, reproduction and abundance of polar bears under climate change. Biol. Conserv. 143, 1612–1622 (2010).Article 

    Google Scholar 
    14.Lister, B. C. & Garcia, A. Climate-driven declines in arthropod abundance restructure a rainforest food web. Proc. Natl Acad. Sci. USA 115, E10397–E10406 (2018).CAS 
    Article 

    Google Scholar 
    15.Vergés, A. et al. Long-term empirical evidence of ocean warming leading to tropicalization of fish communities, increased herbivory, and loss of kelp. Proc. Natl Acad. Sci. USA 113, 13791–13796 (2016).Article 

    Google Scholar 
    16.Genin, A., Levy, L., Sharon, G., Raitsos, D. E. & Diamant, A. Rapid onsets of warming events trigger mass mortality of coral reef fish. Proc. Natl Acad. Sci. USA 117, 25378–25385 (2020).ADS 
    CAS 
    Article 

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

    Google Scholar 
    18.Ruthrof, K. X. et al. Subcontinental heat wave triggers terrestrial and marine, multi-taxa responses. Sci. Rep. 8, 13094 (2018).ADS 
    Article 

    Google Scholar 
    19.Wernberg, T. et al. Climate-driven regime shift of a temperate marine ecosystem. Science 353, 169–172 (2016).ADS 
    CAS 
    Article 

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

    Google Scholar 
    21.Spooner, F. E. B., Pearson, R. G. & Freeman, R. Rapid warming is associated with population decline among terrestrial birds and mammals globally. Glob. Change Biol. 24, 4521–4531 (2018).ADS 
    Article 

    Google Scholar 
    22.Wiens, J. J. Climate-related local extinctions are already widespread among plant and animal species. PLoS Biol. 14, e2001104 (2016).Article 

    Google Scholar 
    23.Sinervo, B. et al. Erosion of lizard diversity by climate change and altered thermal niches. Science 328, 894–899 (2010).ADS 
    CAS 
    Article 

    Google Scholar 
    24.Soroye, P., Newbold, T. & Kerr, J. Climate change contributes to widespread declines among bumble bees across continents. Science 367, 685–688 (2020).ADS 
    CAS 
    Article 

    Google Scholar 
    25.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).Article 

    Google Scholar 
    26.NOAA National Geophysical Data Center. 2009: ETOPO1 1 Arc-Minute Global Relief Model. NOAA National Centers for Environmental Information. Accessed 10.05.2021. More