More stories

  • in

    French crop yield, area and production data for ten staple crops from 1900 to 2018 at county resolution

    Crop dataCrop area (in hectare, ha, for sown areas) and production (in kg) statistics on departmental level from 1900 until 1988 were collected from books of national agricultural statistics (‘Statistique agricole annuelle’ or ‘Annuaire de statistique agricole’) compiled by the French Ministry of Agriculture; detailed references are provided in the supplementary information. Numbers were manually digitized from photocopied versions of the original paper documents. Data from 1989 to 2018 were derived from digital statistics from the Agreste database (‘Statistique agricole annuelle’ compiled by the Service de la Statistique et de la Prospective (SSP), Secrétariat Général du Ministère de l’Agriculture, de l’Agroalimentaire et de la Forêt (MAAF), France); details are provided in the supplementary information. Yields were calculated from total production and sown area for each department to avoid apparently often incorrect yield values printed in the old statistics books. Yields are given in kilogram per hectare (kg/ha, for sown area) for dry mass with 10–16% moisture content, depending on the crop.Data are available for ten crops: soft wheat (spring and winter separately), durum wheat, maize, oats (spring and winter), rapeseed (spring and winter), barley (spring and winter), potatoes, sugarbeet, sunflower and wine. The split into spring and winter crops eventually results in 18 distinct crop-cultivar types. Time frames with available data and the correspondence between French and English names are provided in Table 1.Table 1 Data set description for yields on department level.Full size tableThe shapes of French departments have changed over time. We use the 96 mainland (Metropolitan France) departments in their current form and subsume historical values to modern departments as follows. Corsica was one single department until 1975 but then split into Corse-du-Sud and Haute-Corse. Data for Corsica until 1975 were split equally (area, production) or copied (yield) to both new departments. Seine and Seine-et-Oise were two departments until 1967, but then subdivided into seven new departments on 1 January 1968. To account for this, we consider the values of the seven new departments (Essonne, Hauts-de-Seine, Paris, Seine-Saint-Denis, Val-de-Marne, Val-d’Oise, Yvelines) only from 1968 on and unite the two old departments into one counter-factual (“Seine_SeineOise” in the data tables) until 1967.Multiple cropping per year within this set of crops is accounted for by separate area data, but is practically nonexistent in France6.Quality filtersSome yield values had to be considered as outliers, also after checking for digitizing errors. There were four criteria for defining an outlier. First, absolute yield values larger than a physiologically currently unreachable threshold were removed; threshold values were 15 t/ha for barley and durum wheat, 200 t/ha for sugarbeet and potatoes, 20 t/ha for maize, oats and wheat, 10 t/ha for rape and sunflower and 200 hl/ha for wine. These thresholds were chosen to eliminate visually obvious outliers likely due to mismatches between area and production records. The values are set slightly above current maximum attained yields, thus remaining permissive and removing only obvious errors in this first step. Additionally, all yield values for winter rape in 1944, spring rape in 1968 and spring barley in 1980 were removed due to wrongly reported values in the yearbooks. This first step removed in total 167 yield data points. Second, the top 1% of yield values across all departments per decade were removed. Third, values above or below the mean +/− four times the standard deviation of each crop-department time series (for yield, area and production separately) were removed. Fourth, and finally, a similar variance filter as in the third step was applied within each decade of a single time series, filtering values above or below decadal mean +/− two (for yield) or three (area, production) decadal standard deviations. The latter three filters removed, on average, 3.6% of the yield and 0.2% of the area or production data, respectively (Table 1). There were, as a median, 43 yield outliers per department (out of 1,260 data points on average), with a range of 4 (department Hauts de Seine) and 255 (Nord) and an interquartile range of 35–50 outliers. Outliers were masked as missing values to avoid introducing a bias from any correction. In the accompanying data sets we provide two version of the full data set, one without any corrections (“RAW”) and one where the filters described above have been applied (“FILTERED”).ValidationNationally aggregated area, production and yield data from our data set were validated with national data from 1961 to 2018 provided by the FAO (http://faostat3.fao.org/home/E). Area and production data for crops with separate spring and winter data were summed on department level to test agreement with area and production data digitized for the ‘total’ crop. More

  • in

    Climate drives long-term change in Antarctic Silverfish along the western Antarctic Peninsula

    1.DeWitt, H. H. The character of the midwater fish fauna of the Ross Sea, Antarctica. Antarctic Ecol. 1, 305–314 (1970).
    Google Scholar 
    2.Guglielmo, L., Granata, A. & Greco, S. Distribution and abundance of postlarval and juvenile Pleuragramma antarcticum (Pisces, Nototheniidae) off Terra Nova Bay (Ross Sea, Antarctica). Polar Biol. 19, 37–51 (1997).
    Google Scholar 
    3.La Mesa, M. & Eastman, J. T. Antarctic silverfish: life strategies of a key species in the high-Antarctic ecosystem. Fish Fisheries 13, 241–266 (2012).
    Google Scholar 
    4.La Mesa, M., Eastman, J. T. & Vacchi, M. The role of notothenioid fish in the food web of the Ross Sea shelf waters: a review. Polar Biol. 27, 321–338 (2004).
    Google Scholar 
    5.Pinkerton, M. H., Bradford-Grieve, J. M. & Hanchet, S. M. A balanced model of the food web of the Ross Sea, Antarctica. CCAMLR Sci. 17, 1–31 (2010).
    Google Scholar 
    6.Caccavo, J. A. et al. Along-shelf connectivity and circumpolar gene flow in Antarctic silverfish (Pleuragramma antarctica). Sci. Rep. 8, 1–16 (2018).
    Google Scholar 
    7.Beers, J. M. & Jayasundara, N. Antarctic notothenioid fish: what are the future consequences of ‘losses’ and ‘gains’ acquired during long-term evolution at cold and stable temperatures? J. Exp. Biol. 218, 1834–1845 (2015).PubMed 

    Google Scholar 
    8.Bilyk, K. T. & DeVries, A. L. Heat tolerance and its plasticity in Antarctic fishes. Compar. Biochem. Physiol. A Mol. Integr. Physiol. 158, 382–390 (2011).
    Google Scholar 
    9.Sandersfeld, T., Davison, W., Lamare, M. D., Knust, R. & Richter, C. Elevated temperature causes metabolic trade-offs at the whole-organism level in the Antarctic fish Trematomus bernacchii. J. Exp. Biol. 218, 2373–2381 (2015).PubMed 

    Google Scholar 
    10.Cook, A. J. et al. Ocean forcing of glacier retreat in the western Antarctic Peninsula. Science 353, 283–286 (2016).CAS 
    PubMed 

    Google Scholar 
    11.Stammerjohn, S. E. & Scambos, T. A. Warming reaches the South Pole. Nat. Clim. Change 10, 710–711 (2020).
    Google Scholar 
    12.Henley, S. F. et al. Variability and change in the west Antarctic Peninsula marine system: research priorities and opportunities. Prog. Oceanogr. 173, 208–237 (2019).
    Google Scholar 
    13.Mintenbeck, K. & Torres, J. J. in The Antarctic silverfish: a keystone species in a changing ecosystem, 253–286 (Springer, 2017).14.Vacchi, M. et al. A nursery area for the Antarctic silverfish Pleuragramma antarcticum at Terra Nova Bay (Ross Sea): first estimate of distribution and abundance of eggs and larvae under the seasonal sea-ice. Polar Biol. 35, 1573–1585 (2012).
    Google Scholar 
    15.Vacchi, M., La Mesa, M., Dalu, M. & Macdonald, J. Early life stages in the life cycle of Antarctic silverfish, Pleuragramma antarcticum in Terra Nova Bay, Ross Sea. Antartic Sci. 16, 299–305 (2004).
    Google Scholar 
    16.Kellermann, A. K. Midwater fish ecology. Found. Ecol. Res. West Antarctic Peninsula 70, 231–256 (1996).
    Google Scholar 
    17.La Mesa, M., Riginella, E., Mazzoldi, C. & Ashford, J. Reproductive resilience of ice-dependent Antarctic silverfish in a rapidly changing system along the Western Antarctic Peninsula. Mar. Ecol. 36, 235–245 (2015).
    Google Scholar 
    18.Parker, M. L. et al. Assemblages of micronektonic fishes and invertebrates in a gradient of regional warming along the Western Antarctic Peninsula. J. Mar. Syst. 152, 18–41 (2015).
    Google Scholar 
    19.Ross, R. M. et al. Trends, cycles, interannual variability for three pelagic species west of the Antarctic Peninsula 1993–2008. Mar. Ecol. Prog. Ser. 515, 11–32 (2014).
    Google Scholar 
    20.Koubbi, P. et al. Spatial distribution and inter-annual variations in the size frequency distribution and abundances of Pleuragramma antarcticum larvae in the Dumont d’Urville Sea from 2004 to 2010. Polar Sci. 5, 225–238 (2011).
    Google Scholar 
    21.Davis, L. B., Hofmann, E. E., Klinck, J. M., Piñones, A. & Dinniman, M. S. Distributions of krill and Antarctic silverfish and correlations with environmental variables in the western Ross Sea, Antarctica. Mar. Ecol. Prog. Ser. 584, 45–65 (2017).CAS 

    Google Scholar 
    22.La Mesa, M. et al. Influence of environmental conditions on spatial distribution and abundance of early life stages of Antarctic silverfish, Pleuragramma antarcticum (Nototheniidae), in the Ross Sea. Antarctic Sci. 22, 243 (2010).
    Google Scholar 
    23.Raphael, M. N. et al. The Amundsen Sea low: variability, change, and impact on Antarctic climate. Bull. Am. Meteorol. Soc. 97, 111–121 (2016).
    Google Scholar 
    24.Fogt, R. L., Wovrosh, A. J., Langen, R. A. & Simmonds, I. The characteristic variability and connection to the underlying synoptic activity of the Amundsen-Bellingshausen Seas Low. J. Geophys. Res. Atmos. https://doi.org/10.1029/2011JD017337 (2012).25.Hosking, J. S., Orr, A., Marshall, G. J., Turner, J. & Phillips, T. The influence of the Amundsen–Bellingshausen Seas low on the climate of West Antarctica and its representation in coupled climate model simulations. J. Clim. 26, 6633–6648 (2013).
    Google Scholar 
    26.Hosking, J. S., Orr, A., Bracegirdle, T. J. & Turner, J. Future circulation changes off West Antarctica: sensitivity of the Amundsen Sea Low to projected anthropogenic forcing. Geophys. Res. Lett. 43, 367–376 (2016).
    Google Scholar 
    27.Hobbs, W. R. et al. A review of recent changes in Southern Ocean sea ice, their drivers and forcings. Glob. Planet. Change 143, 228–250 (2016).
    Google Scholar 
    28.Stammerjohn, S. E. et al. Seasonal sea ice changes in the Amundsen Sea, Antarctica, over the period of 1979–2014. Elementa Sci. Anthropocene 3, 000055 (2015).29.Holland, M. M., Landrum, L., Raphael, M. N. & Kwok, R. The regional, seasonal, and lagged influence of the Amundsen Sea Low on Antarctic sea ice. Geophys. Res. Lett. 45, 11–227 (2018).
    Google Scholar 
    30.Thoma, M., Jenkins, A., Holland, D. & Jacobs, S. Modelling circumpolar deep water intrusions on the Amundsen Sea continental shelf, Antarctica. Geophys. Res. Lett. https://doi.org/10.1029/2008GL034939 (2008).31.Dotto, T. S. et al. Control of the oceanic heat content of the Getz‐Dotson Trough, Antarctica, by the Amundsen Sea Low. J. Geophys. Res. Oceans 125, e2020JC016113 (2020).32.Holland, P. R., Bracegirdle, T. J., Dutrieux, P., Jenkins, A. & Steig, E. J. West Antarctic ice loss influenced by internal climate variability and anthropogenic forcing. Nat. Geosci. 12, 718–724 (2019).CAS 

    Google Scholar 
    33.Dinniman, M. S., Klinck, J. M. & Hofmann, E. E. Sensitivity of circumpolar deep water transport and Ice Shelf Basal Melt along the West Antarctic Peninsula to changes in the winds. J. Clim. 25, 4799–4816 (2012).
    Google Scholar 
    34.Dinniman, M. S., Klinck, J. M. & Smith, W. O. A model study of circumpolar deep water on the West Antarctic Peninsula and Ross Sea continental shelves. Deep Sea Res. II Top. Stud. Oceanogr. 58, 1508–1523 (2011).CAS 

    Google Scholar 
    35.Nakayama, Y., Menemenlis, D., Zhang, H., Schodlok, M. & Rignot, E. Origin of circumpolar deep water intruding onto the Amundsen and Bellingshausen Sea continental shelves. Nat. Commun. 9, 3403 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    36.Spence, P. et al. Rapid subsurface warming and circulation changes of Antarctic coastal waters by poleward shifting winds. Geophys. Res. Lett. 41, 4601–4610 (2014).
    Google Scholar 
    37.Greaves, B. L. et al. The Southern Annular Mode (SAM) influences phytoplankton communities in the seasonal ice zone of the Southern Ocean. Biogeosciences 17, 3815–3835 (2020).CAS 

    Google Scholar 
    38.Steinberg, D. K. et al. Long-term (1993–2013) changes in macrozooplankton off the Western Antarctic Peninsula. Deep Sea Res. I Oceanogr. Res. Papers 101, 54–70 (2015).
    Google Scholar 
    39.La, H. S. et al. Zooplankton and micronekton respond to climate fluctuations in the Amundsen Sea polynya, Antarctica. Sci. Rep. 9, 10087 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    40.Granata, A., Zagami, G., Vacchi, M. & Guglielmo, L. Summer and spring trophic niche of larval and juvenile Pleuragramma antarcticum in the Western Ross Sea, Antarctica. Polar Biol. 32, 369–382 (2009).
    Google Scholar 
    41.Bhaskaran, K., Gasparrini, A., Hajat, S., Smeeth, L. & Armstrong, B. Time series regression studies in environmental epidemiology. Int. J. Epidemiol. 42, 1187–1195 (2013).PubMed 
    PubMed Central 

    Google Scholar 
    42.Ghigliotti, L. et al. Reproductive features of the Antarctic silverfish (Pleuragramma antarctica) from the western Ross Sea. Polar Biol. 40, 199–211 (2017).
    Google Scholar 
    43.Chapman, E. W., Hofmann, E. E., Patterson, D. L., Ribic, C. A. & Fraser, W. R. Marine and terrestrial factors affecting Adélie ­penguin Pygoscelis adeliae chick growth and recruitment off the western Antarctic Peninsula. Mar. Ecol. Prog. Ser. 436, 273–289 (2011).
    Google Scholar 
    44.Coggins, J. H. J. & McDonald, A. J. The influence of the Amundsen Sea Low on the winds in the Ross Sea and surroundings: Insights from a synoptic climatology. J. Geophys. Res. Atmos. 120, 2167–2189 (2015).
    Google Scholar 
    45.Assmann, K. M. et al. Variability of circumpolar deep water transport onto the Amundsen Sea Continental shelf through a shelf break trough. J. Geophys. Res. Oceans 118, 6603–6620 (2013).
    Google Scholar 
    46.Moffat, C., Owens, B. & Beardsley, R. C. On the characteristics of circumpolar deep water intrusions to the west Antarctic Peninsula Continental Shelf. J. Geophys. Res. Oceans https://doi.org/10.1029/2008JC004955 (2009).47.Dahlke, F. T., Wohlrab, S., Butzin, M. & Pörtner, H.-O. Thermal bottlenecks in the life cycle define climate vulnerability of fish. Science 369, 65–70 (2020).CAS 
    PubMed 

    Google Scholar 
    48.Regan, H. C., Holland, P. R., Meredith, M. P. & Pike, J. Sources, variability and fate of freshwater in the Bellingshausen Sea, Antarctica. Deep Sea Res I Oceanogr. Res. Pap. 133, 59–71 (2018).
    Google Scholar 
    49.Holland, P. R. et al. Modeled trends in Antarctic sea ice thickness. J. Clim. 27, 3784–3801 (2014).
    Google Scholar 
    50.Hoppmann, M. et al. Platelet ice, the Southern Ocean’s hidden ice: a review. Ann. Glaciol. 61, 341–368 (2020).
    Google Scholar 
    51.Arrigo, K. R. Sea ice ecosystems. Annu. Rev. Mar. Sci 6, 439–467 (2014).
    Google Scholar 
    52.Veazey, A. L., Jeffries, M. O. & Morris, K. Small-scale variability of physical properties and structural characteristics of Antarctic fast ice. Ann. Glaciol. 20, 61–66 (1994).
    Google Scholar 
    53.Garrison, D. L., Ackley, S. F. & Buck, K. R. A physical mechanism for establishing algal populations in frazil ice. Nature 306, 363–365 (1983).CAS 

    Google Scholar 
    54.Quetin, L. B. & Ross, R. M. in Smithsonian at the Poles: Contributions to International Polar Year Science (eds Krupnik, I., Lang, M. A. & Miller, S. E.) 285–298 (IPY, 2009).55.Meredith, M. P. & King, J. C. Rapid climate change in the ocean west of the Antarctic Peninsula during the second half of the 20th century. Geophys. Res. Lett. https://doi.org/10.1029/2005GL024042 (2005).56.Turner, J. et al. Absence of 21st century warming on Antarctic Peninsula consistent with natural variability. Nature 535, 411–415 (2016).CAS 
    PubMed 

    Google Scholar 
    57.Rintoul, S. R. et al. Choosing the future of Antarctica. Nature 558, 233–241 (2018).CAS 
    PubMed 

    Google Scholar 
    58.Turner, J., Phillips, T., Hosking, J. S., Marshall, G. J. & Orr, A. The Amundsen Sea low. Int. J. Climatol. 33, 1818–1829 (2013).
    Google Scholar 
    59.Ding, Q., Steig, E. J., Battisti, D. S. & Küttel, M. Winter warming in West Antarctica caused by central tropical Pacific warming. Nat. Geosci. 4, 398–403 (2011).CAS 

    Google Scholar 
    60.Moline, M. A., Claustre, H., Frazer, T. K., Schofield, O. & Vernet, M. Alteration of the food web along the Antarctic Peninsula in response to a regional warming trend. Glob. Change Biol. 10, 1973–1980 (2004).
    Google Scholar 
    61.Gleiber, M. Long-Term Change in Copepod Community Structure in the Western Antarctic Peninsula: Linkage to Climate and Implications for Carbon Cycling. Dissertations, Theses, and Masters Projects, College of William and Mary, Virginia Institute of Marine Science (2014).62.Wöhrmann, A. P., Hagen, W. & Kunzmann, A. Adaptations of the Antarctic silverfish Pleuragramma antarcticum(Pisces: Nototheniidae) to pelagic life in high-Antarctic waters. Mar. Ecol. Prog. Ser. 151, 205–218 (1997).
    Google Scholar 
    63.Venables, H. J., Clarke, A. & Meredith, M. P. Wintertime controls on summer stratification and productivity at the western Antarctic Peninsula. Limnol. Oceanogr. 58, 1035–1047 (2013).
    Google Scholar 
    64.Meredith, M. P. et al. Variability in the freshwater balance of northern Marguerite Bay, Antarctic Peninsula: results from δ18O. Deep Sea Res. II Top. Stud. Oceanogr. 55, 309–322 (2008).
    Google Scholar 
    65.Slosarczyk, W. Attempts at a quantitative estimate by trawl sampling of distribution of postlarval and juvenile notothenioids (Pisces, Perciformes) in relation to environmental conditions in the Antarctic Peninsula region during SIBEX 1983–84. Mem Natl Inst Polar Res Spec Issue. 40, 299–315 (1986).
    Google Scholar 
    66.Varsamos, S., Nebel, C. & Charmantier, G. Ontogeny of osmoregulation in postembryonic fish: a review. Compar. Biochem. Physiol. A Mol. Integr. Physiol. 141, 401–429 (2005).
    Google Scholar 
    67.Gille, S. T., McKee, D. C. & Martinson, D. G. Temporal changes in the Antarctic circumpolar current: implications for the Antarctic Continental Shelves. Oceanography 29, 96–105 (2016).
    Google Scholar 
    68.Thompson, D. W. J. et al. Signatures of the Antarctic ozone hole in Southern Hemisphere surface climate change. Nat. Geosci. 4, 741–749 (2011).CAS 

    Google Scholar 
    69.Allen, M. et al. Technical summary: global warming of 1.5 °C. An IPCC Special Report on the impacts of global warming of 1.5 °C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty. https://www.ipcc.ch/site/assets/uploads/sites/2/2018/12/SR15_TS_High_Res.pdf (2019).70.Screen, J. A., Bracegirdle, T. J. & Simmonds, I. Polar climate change as manifest in atmospheric circulation. Curr. Clim. Change Rep. 4, 383–395 (2018).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    71.Gao, M. et al. Historical fidelity and future change of Amundsen Sea Low under 1.5 °C–4 °C global warming in CMIP6. Atmos. Res. 255, 105533 (2021).
    Google Scholar 
    72.Emslie, S. D. & McDaniel, J. D. Adélie penguin diet and climate change during the middle to late Holocene in northern Marguerite Bay, Antarctic Peninsula. Polar Biol. 25, 222–229 (2002).
    Google Scholar 
    73.Fraser, W. R. & Trivelpiece, W. Z. Factors controlling the distribution of seabirds: winter-summer heterogeneity in the distribution of Adélie penguin populations. In Foundations for Ecological Research West of the Antarctic Peninsula 257–272 (American Geophysical Union, 1996).74.Cimino, M. A., Lynch, H. J., Saba, V. S. & Oliver, M. J. Projected asymmetric response of Adélie penguins to Antarctic climate change. Sci. Rep. 6, 28785 (2016).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    75.Ainley, D. G. et al. Post-fledging survival of Adélie penguins at multiple colonies: chicks raised on fish do well. Mar. Ecol. Prog. Ser. 601, 239–251 (2018).
    Google Scholar 
    76.Ruck, K. E., Steinberg, D. K. & Canuel, E. A. Regional differences in quality of krill and fish as prey along the Western Antarctic Peninsula. Mar. Ecol. Prog. Ser. 509, 39–55 (2014).CAS 

    Google Scholar 
    77.Ainley, D. G. et al. Decadal trends in abundance, size and condition of Antarctic toothfish in McMurdo Sound, Antarctica, 1972–2011. Fish Fisheries 14, 343–363 (2013).
    Google Scholar 
    78.Eastman, J. T. Pleuragramma antarcticum (Pisces, Nototheniidae) as food for other fishes in McMurdo Sound, Antarctica. Polar Biol. 4, 155–160 (1985).
    Google Scholar 
    79.Hanchet, S. et al. The Antarctic toothfish (Dissostichus mawsoni): biology, ecology, and life history in the Ross Sea region. Hydrobiologia 761, 397–414 (2015).
    Google Scholar 
    80.Pinkerton, M., Hanchet, S. & Bradford-Grieve, J. Finding the role of Antarctic toothfish in the Ross Sea ecosystem. Water Atmos. 15, 20–21 (2007).
    Google Scholar 
    81.Hanchet, S. M. & Rickard, G. J. A hypothetical life cycle for Antarctic toothfish (Dissostichus mawsoni) in the Ross Sea region. CCAMLR Sci. 15, 35–53 (2008).
    Google Scholar 
    82.Fuiman, L., Davis, R. & Williams, T. Behavior of midwater fishes under the Antarctic ice: observations by a predator. Mar. Biol. 140, 815–822 (2002).
    Google Scholar 
    83.Casaux, R., Baroni, A. & Ramón, A. The diet of the Weddell Seal Leptonychotes weddellii at the Danco Coast, Antarctic Peninsula. Polar Biol. 29, 257–262 (2006).
    Google Scholar 
    84.Ponganis, P. J. & Stockard, T. K. Short note: the Antarctic toothfish: how common a prey for Weddell seals? Antarctic Sci. 19, 441–442 (2007).
    Google Scholar 
    85.Rumolo, P. et al. The diet of Weddell seals (Leptonychotes weddellii) in Terra Nova Bay using stable isotope analysis. Eur. Zool. J. 87, 94–104 (2020).
    Google Scholar 
    86.Hubold, G. & Ekau, W. Feeding patterns of post-larval and juvenile notothenioids in the southern Weddell Sea (Antarctica). Polar Biol. 10, 255–260 (1990).87.Moreno, C., Rueda, T. & Asencio, G. The trophic niche of Pleuragramma antarcticum in the Bransfield Strait, Antarctica: quantitative comparison with other areas of the Southern Ocean. Ser. Cient. INACH 35, 101–117 (1986).88.Gleiber, M. R., Steinberg, D. K. & Schofield, O. M. E. Copepod summer grazing and fecal pellet production along the Western Antarctic Peninsula. J. Plankton Res. 38, 732–750 (2016).CAS 

    Google Scholar 
    89.Garzio, L., Steinberg, D., Erickson, M. & Ducklow, H. Microzooplankton grazing along the Western Antarctic Peninsula. Aquat. Microb. Ecol. 70, 215–232 (2013).
    Google Scholar 
    90.Hobbie, J. E. Scientific accomplishments of the Long Term Ecological Research Program: an introduction. Bioscience 53, 17–20 (2003).
    Google Scholar 
    91.Hughes, B. B. et al. Long-term studies contribute disproportionately to ecology and policy. Bioscience 67, 271–281 (2017).
    Google Scholar 
    92.Hilton, E. J., Watkins-Colwell, G. J. & Huber, S. K. The expanding role of natural history collections. Ichthyol. Herpetol. 109, 379–391 (2021).
    Google Scholar 
    93.Hoey, J. A. et al. Using multiple natural tags provides evidence for extensive larval dispersal across space and through time in summer flounder. Mol. Ecol. 29, 1421–1435 (2020).CAS 
    PubMed 

    Google Scholar 
    94.Houde, E. D. Emerging from Hjort’s shadow. J. Northw. Atl. Fish. Sci 41, 53–70 (2008).
    Google Scholar 
    95.Ducklow, H. W. et al. Marine pelagic ecosystems: the West Antarctic Peninsula. Philos. Trans. R. Soc. B Biol. Sci. 362, 67–94 (2007).
    Google Scholar 
    96.Smith, R. C. et al. The Palmer LTER: a long-term ecological research program at Palmer Station, Antarctica. Oceanography 8, 77–86 (1995).
    Google Scholar 
    97.Kellermann, A. K. Identification key and catalogue of larval Antarctic fishes. Ber. Polarforsch 1–138 (1990).98.Stammerjohn, S. E., Martinson, D. G., Smith, R. C. & Iannuzzi, R. A. Sea ice in the western Antarctic Peninsula region: spatio-temporal variability from ecological and climate change perspectives. Deep Sea Res. II Top. Stud. Oceanogr. 55, 2041–2058 (2008).
    Google Scholar 
    99.Hurrell, J. W. Decadal trends in the North Atlantic oscillation: regional temperatures and precipitation. Science 269, 676–679 (1995).CAS 
    PubMed 

    Google Scholar 
    100.Hosking, J. S. & National Center for Atmospheric Research Staff. (eds) The Climate Data Guide: Amundsen Sea Low indices. https://climatedataguide.ucar.edu/climate-data/amundsen-sea-low-indices (2020).101.O’Brien, R. M. A caution regarding rules of thumb for variance inflation factors. Qual. Quant. 41, 673–690 (2007).
    Google Scholar 
    102.Gareth, J., Daniela, W., Trevor, H. & Robert, T. An Introduction to Statistical Learning: With Applications in R (Spinger, 2013).103.Shono, H. Application of the Tweedie distribution to zero-catch data in CPUE analysis. Fisheries Res. 93, 154–162 (2008).
    Google Scholar 
    104.R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2020).105.Denes, F. V., Silveira, L. F. & Beissinger, S. R. Estimating abundance of unmarked animal populations: accounting for imperfect detection and other sources of zero inflation. Methods Ecol. Evol. 6, 543–556 (2015).
    Google Scholar 
    106.Zuur, A. F. & Ieno, E. N. Beginner´s Guide to Zero-inflated Models with R (Highland Statistics Ltd., 2016).107.Barnett, A. G., Koper, N., Dobson, A. J., Schmiegelow, F. & Manseau, M. Using information criteria to select the correct variance–covariance structure for longitudinal data in ecology. Methods Ecol. Evol. 1, 15–24 (2010).
    Google Scholar 
    108.Clark, I. Statistics or geostatistics? Sampling error or nugget effect? J. Southern African Inst. Mining Metall. 110, 307–312 (2010).
    Google Scholar 
    109.Gschlößl, S. & Czado, C. Modelling count data with overdispersion and spatial effects. Stat. Papers 49, 531–552 (2008).
    Google Scholar 
    110.Brooks, M. E. et al. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J. 9, 378–400 (2017).
    Google Scholar 
    111.Aho, K., Derryberry, D. & Peterson, T. Model selection for ecologists: the worldviews of AIC and BIC. Ecology 95, 631–636 (2014).PubMed 

    Google Scholar 
    112.Lüdecke, D. ggeffects: Tidy data frames of marginal effects from regression models. JOSS 3, 772 (2018).
    Google Scholar 
    113.Francq, B. G., Lin, D. & Hoyer, W. Confidence, prediction, and tolerance in linear mixed models. Stat. Med. 38, 5603–5622 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    114.Spineli, L. M. & Pandis, N. Prediction interval in random-effects meta-analysis. Am. J. Orthod. Dentofacial Orthop. 157, 586–588 (2020).PubMed 

    Google Scholar 
    115.Comiso, J. C. Variability and trends in Antarctic surface temperatures from in situ and satellite infrared measurements. J. Clim. 13, 1674–1696 (2000).
    Google Scholar 
    116.Comiso, J. C. & Nishio, F. Trends in the sea ice cover using enhanced and compatible AMSR-E, SSM/I, and SMMR data. J. Geophys. Res. Oceans https://doi.org/10.1029/2007JC004257 (2008).117.Hersbach, H. et al. ERA5 monthly averaged data on single levels from 1979 to present. https://doi.org/10.24381/CDS.F17050D7 (2019).118.Reynolds, R. W., Rayner, N. A., Smith, T. M., Stokes, D. C. & Wang, W. An improved in situ and satellite SST analysis for climate. J. Clim. 15, 1609–1625 (2002).
    Google Scholar  More

  • in

    Environmental structure impacts microbial composition and secondary metabolism

    1.Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL, et al. Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol. 2006;4:102–12.CAS 
    PubMed 

    Google Scholar 
    2.Caswell H, Cohen JE. Disturbance, interspecific interaction and diversity in metapopulations. Biol J Linn Soc. 1991;42:193–218.
    Google Scholar 
    3.Tolker-Nielsen T, Molin S. Spatial organization of microbial biofilm communities. Microb Ecol. 2000;40:75–84.CAS 
    PubMed 

    Google Scholar 
    4.Yanni D, Márquez-Zacarías P, Yunker PJ, Ratcliff WC. Drivers of spatial structure in social microbial communities. Curr Biol. 2019;29:R545–50.CAS 
    PubMed 

    Google Scholar 
    5.Ho A, Angel R, Veraart AJ, Daebeler A, Jia Z, Kim SY, et al. Biotic interactions in microbial communities as modulators of biogeochemical processes: methanotrophy as a model system. Front Microbiol. 2016;7:1–11.
    Google Scholar 
    6.Falkowski PG, Fenchel T, Delong EF. The microbial engines that drive earth’s biogeochemical cycles. Science. 2008;320:1034–9.CAS 
    PubMed 

    Google Scholar 
    7.Overmann J, van Gemerden H. Microbial interactions involving sulfur bacteria: Implications for the ecology and evolution of bacterial communities. FEMS Microbiol Rev. 2000;24:591–9.CAS 
    PubMed 

    Google Scholar 
    8.García-Bayona L, Comstock LE. Bacterial antagonism in host-associated microbial communities. Science. 2018;361:1–11.
    Google Scholar 
    9.Coyte KZ, Schluter J, Foster KR. The ecology of the microbiome: Networks, competition, and stability. Science. 2015;350:663–6.CAS 
    PubMed 

    Google Scholar 
    10.Wang X, Li X, Ling J. Streptococcus gordonii LuxS/autoinducer-2 quorum-sensing system modulates the dual-species biofilm formation with Streptococcus mutans. J Basic Microbiol. 2017;57:605–16.CAS 
    PubMed 

    Google Scholar 
    11.Hotterbeekx A, Kumar-Singh S, Goossens H, Malhotra-Kumar S. In vivo and In vitro interactions between Pseudomonas aeruginosa and Staphylococcus spp. Front Cell Infect Microbiol. 2017;7:1–13.
    Google Scholar 
    12.Dal Co A, van Vliet S, Kiviet DJ, Schlegel S, Ackermann M. Short-range interactions govern the dynamics and functions of microbial communities. Nat Ecol Evol. 2020;4:366–75. https://doi.org/10.1038/s41559-019-1080-2.Article 
    PubMed 

    Google Scholar 
    13.Justice NB, Sczesnak A, Hazen TC, Arkin AP. Environmental selection, dispersal, and organism interactions shape community assembly in high-throughput enrichment culturing. Appl Environ Microbiol. 2017;83:1–16.
    Google Scholar 
    14.Hilker M. New synthesis: parallels between biodiversity and chemodiversity. J Chem Ecol. 2014;40:225–6.CAS 
    PubMed 

    Google Scholar 
    15.Raguso R, Agrawal A, Douglas A, Jander G, Kessler A, Poveda K, et al. The raison d’être of chemical ecology. Ecology. 2015;96:617–30.PubMed 

    Google Scholar 
    16.Tilman D. Competition and biodiversity in spatially structured habitats. Ecology. 1994;75:2–16.
    Google Scholar 
    17.Geyrhofer L, Brenner N. Coexistence and cooperation in structured habitats. BMC Ecol. 2020;20:1–15. https://doi.org/10.1186/s12898-020-00281-y.Article 

    Google Scholar 
    18.Wakano JY, Nowak MA, Hauert C. Spatial dynamics of ecological public goods. Proc Natl Acad Sci USA. 2009;106:7910–4.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    19.Nemergut DR, Schmidt SK, Fukami T, O’Neill SP, Bilinski TM, Stanish LF, et al. Patterns and processes of microbial community assembly. Microbiol Mol Biol Rev. 2013;77:342–56.PubMed 
    PubMed Central 

    Google Scholar 
    20.Lowery NV, Ursell T. Structured environments fundamentally alter dynamics and stability of ecological communities. Proc Natl Acad Sci USA. 2019;116:379–88.CAS 

    Google Scholar 
    21.Lee JZ, Craig Everroad R, Karaoz U, Detweiler AM, Pett-Ridge J, Weber PK, et al. Metagenomics reveals niche partitioning within the phototrophic zone of a microbial mat. PLoS ONE. 2018;13:1–19.
    Google Scholar 
    22.Quinn RA, Comstock W, Zhang T, Morton JT, da Silva R, Tran A, et al. Niche partitioning of a pathogenic microbiome driven by chemical gradients. Sci Adv. 2018;4:1–12.
    Google Scholar 
    23.Fenchel T, Finlay B. Oxygen and the spatial structure of microbial communities. Biol Rev. 2008;83:553–69.PubMed 

    Google Scholar 
    24.Esteban DJ, Hysa B, Bartow-McKenney C. Temporal and spatial distribution of the microbial community of winogradsky columns. PLoS ONE. 2015;10:1–21.
    Google Scholar 
    25.Azam F. Microbial control of oceanic carbon flux: The plot thickens. Science. 1998;280:694–6.CAS 

    Google Scholar 
    26.McNally L, Brown SP. Building the microbiome in health and disease: niche construction and social conflict in bacteria. Philos Trans R Soc B Biol Sci. 2015;370:1–8.
    Google Scholar 
    27.Schreiber F, Ackermann M. Environmental drivers of metabolic heterogeneity in clonal microbial populations. Curr Opin Biotechnol. 2020;62:202–11. https://doi.org/10.1016/j.copbio.2019.11.018.CAS 
    Article 
    PubMed 

    Google Scholar 
    28.Lopez D, Vlamakis H, Kolter R. Biofilms. Cold Spring Harbor Perspectives in Biology. 2010;2:1–11.
    Google Scholar 
    29.Picketts STA, Cadenasso ML. Landscape ecology: spatial heterogeneity in ecological systems. NCASI Techn Bull. 1999;2:420.
    Google Scholar 
    30.Chao L, Levin BR. Structured habitats and the evolution of anticompetitor toxins in bacteria. Proc Natl Acad Sci USA. 1981;78:6324–8.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    31.Rainey PB, Travisano M. Adaptive radiation in a heterogeneous environment. Nature. 1998;394:69–72.CAS 
    PubMed 

    Google Scholar 
    32.Cardinale BJ. Biodiversity improves water quality through niche partitioning. Nature. 2011;472:86–91.CAS 
    PubMed 

    Google Scholar 
    33.Loreau M, Naeem S, Inchausti P, Bengtsson J, Grime JP, Hector A, et al. Ecology: biodiversity and ecosystem functioning: current knowledge and future challenges. Science. 2001;294:804–8.CAS 
    PubMed 

    Google Scholar 
    34.Wellborn GA, Langerhans RB. Ecological opportunity and the adaptive diversification of lineages. Ecol Evol. 2015;5:176–95.PubMed 

    Google Scholar 
    35.Czárán TL, Hoekstra RF. Killer-sensitive coexistence in metapopulations of micro-organisms. Proc R Soc B Biol Sci. 2003;270:1373–8.
    Google Scholar 
    36.West SA, Griffin AS, Gardner A, Diggle SP. Social evolution theory for microorganisms. Nat Rev Microbiol. 2006;4:597–607.CAS 
    PubMed 

    Google Scholar 
    37.Wagner M, Loy A, Nogueira R, Purkhold U, Lee N, Daims H. Microbial community composition and function in wastewater treatment plants. Antonie Van Leeuwenhoek. 2002;81:665–80.CAS 
    PubMed 

    Google Scholar 
    38.Johnson DR, Lee TK, Park J, Fenner K, Helbling DE. The functional and taxonomic richness of wastewater treatment plant microbial communities are associated with each other and with ambient nitrogen and carbon availability. Environ Microbiol. 2015;17:4851–60.CAS 
    PubMed 

    Google Scholar 
    39.Liébana R, Arregui L, Santos A, Murciano A, Marquina D, Serrano S. Unravelling the interactions among microbial populations found in activated sludge during biofilm formation. FEMS Microbiol Ecol. 2016;92:1–13.
    Google Scholar 
    40.Reasoner DJ, Geldreich EE. A new medium for the enumeration and subculture of bacteria from potable water. Appl Environ Microbiol. 1985;49:1–7.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    41.Parada AE, Needham DM, Fuhrman JA. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol. 2015;18:1403–14.PubMed 

    Google Scholar 
    42.Junkins EN, Stevenson BS. Using plate-wash PCR and high-throughput sequencing to measure cultivated diversity for natural product discovery efforts. Front Microbiol. 2021;12:1–14.
    Google Scholar 
    43.Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 2011;17:10–12.
    Google Scholar 
    44.Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    45.Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:590–6.
    Google Scholar 
    46.Yilmaz P, Parfrey LW, Yarza P, Gerken J, Pruesse E, Quast C, et al. The SILVA and “all-species Living Tree Project (LTP)” taxonomic frameworks. Nucleic Acids Res. 2014;42:643–8.
    Google Scholar 
    47.Davis NM, Proctor DM, Holmes SP, Relman DA, Callahan BJ. Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data. Microbiome. 2018;6:1–14.
    Google Scholar 
    48.Wright ES. DECIPHER: Harnessing local sequence context to improve protein multiple sequence alignment. BMC Bioinformatics. 2015;16:1–14. https://doi.org/10.1186/s12859-015-0749-z.CAS 
    Article 

    Google Scholar 
    49.Wright ES. Using DECIPHER v2.0 to analyze big biological sequence data in R. R J. 2016;8:352–9.
    Google Scholar 
    50.Schliep KP. phangorn: phylogenetic analysis in R. Bioinformatics. 2011;27:592–3.CAS 
    PubMed 

    Google Scholar 
    51.McMurdie PJ, Holmes S. Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE. 2013;8:1–11.
    Google Scholar 
    52.Willis A, Bunge J. Estimating diversity via frequency ratios. Biometrics. 2015;71:1042–9.PubMed 

    Google Scholar 
    53.Pielou EC. The measurement of diversity in different types of biological collections. J Theor Biol. 1966;13:131–44.
    Google Scholar 
    54.Levene H. Robust tests for equality of variances. In: Olkin I, editor. Contributions to probability and statistics: essays in honor of Harold Hotelling. Stanford University Press, Palo Alto, California, USA; 1960. p. 278–92.55.Fox J, Weisberg S. An R companion to applied regression. 3rd ed. Thousand Oaks, CA: Sage; 2019.56.Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol. 2005;71:8228–35.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    57.Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: community ecology package. R Package; 2019.58.Martin BD, Witten D, Willis AD. Modeling microbial abundances and dysbiosis with beta-binomial regression. Ann Appl Stat. 2020;14:94–115.PubMed 
    PubMed Central 

    Google Scholar 
    59.Chambers MC, MacLean B, Burke R, Amodei D, Ruderman DL, Neumann S, et al. A cross-platform toolkit for mass spectrometry and proteomics. Nat Biotechnol. 2012;30:918–20.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    60.Pluskal T, Castillo S, Villar-Briones A, Orešič M. MZmine 2: modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data. BMC Bioinformatics. 2010;11:1–11.61.Myers OD, Sumner SJ, Li S, Barne S, Du X. One step forward for reducing false positive and false negative compound identifications from mass spectrometry metabolomics data: new algorithms for constructing extracted ion chromatograms and detecting chromatographic peaks. Anal Chem. 2017;89:8696–703.CAS 
    PubMed 

    Google Scholar 
    62.Wang M, Carver JJ, Phelan VV, Sanchez LM, Garg N;, Peng Y, et al. Sharing and community curation of mass spectrometry data with GNPS. Nat Biotechnol. 2017;34:828–37.
    Google Scholar 
    63.Nothias LF, Petras D, Schmid R, Dührkop K, Rainer J, Sarvepalli A, et al. Feature-based molecular networking in the GNPS analysis environment. Nat Methods. 2020;17:905–8. https://doi.org/10.1038/s41592-020-0933-6.CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    64.Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: a software environment for integrated models. Genome Res. 2003;13:2498–504. http://ci.nii.ac.jp/naid/110001910481/.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    65.R Core Team. R: a language and environment for R Foundation for Statistical Computing. 2018. https://www.r-project.org/.66.Bates D, Mächler M, Bolker BM, Walker SC. Fitting linear mixed-effects models using lme4. J Stat Softw. 2015;67:1–48.
    Google Scholar 
    67.Djoumbou Feunang Y, Eisner R, Knox C, Chepelev L, Hastings J, Owen G, et al. ClassyFire: automated chemical classification with a comprehensive, computable taxonomy. J Cheminform. 2016;8:1–20.
    Google Scholar 
    68.O’Brien J, Wright GD. An ecological perspective of microbial secondary metabolism. Curr Opin Biotechnol. 2011;22:552–8. https://doi.org/10.1016/j.copbio.2011.03.010.CAS 
    Article 
    PubMed 

    Google Scholar 
    69.Thierbach S, Wienhold M, Fetzner S, Hennecke U. Synthesis and biological activity of methylated derivatives of the Pseudomonas metabolites HHQ, HQNO and PQS. Beilstein J Org Chem. 2019;15:187–93.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    70.Morales-Soto N, Dunham SJB, Baig NF, Ellis JF, Madukoma CS, Bohn PW, et al. Spatially dependent alkyl quinolone signaling responses to antibiotics in Pseudomonas aeruginosa swarms. J Biol Chem. 2018;293:9544–52.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    71.Heeb S, Fletcher MP, Chhabra SR, Diggle SP, Williams P, Cámara M. Quinolones: from antibiotics to autoinducers. FEMS Microbiol Rev. 2011;35:247–74.CAS 
    PubMed 

    Google Scholar 
    72.Grollman AP. Inhibitors of protein biosynthesis. II. Mode of action of anisomycin. J Biolog Chem. 1967;242:3226–33. https://doi.org/10.1016/S0021-9258(18)95953-3.CAS 
    Article 

    Google Scholar 
    73.Sobin BA, Tanner FW Jr. Anisomycin, a new anti-protozoan antibiotic. J Am Chem Soc. 1954;76:4053–4053.CAS 

    Google Scholar 
    74.Gross H, Stockwell VO, Henkels MD, Nowak-Thompson B, Loper JE, Gerwick WH. The genomisotopic approach: a systematic method to isolate products of orphan biosynthetic gene clusters. Chem Biol. 2007;14:53–63.CAS 
    PubMed 

    Google Scholar 
    75.Jang JY, Yang SY, Kim YC, Lee CW, Park MS, Kim JC, et al. Identification of orfamide A as an insecticidal metabolite produced by Pseudomonas protegens F6. J Agric Food Chem. 2013;61:6786–91.CAS 
    PubMed 

    Google Scholar 
    76.Ma Z, Geudens N, Kieu NP, Sinnaeve D, Ongena M, Martins JC, et al. Biosynthesis, chemical structure, and structure-activity relationship of orfamide lipopeptides produced by Pseudomonas protegens and related species. Front Microbiol. 2016;7:1–16.
    Google Scholar 
    77.Figueira V, Vaz-Moreira I, Silva M, Manaia CM. Diversity and antibiotic resistance of Aeromonas spp. in drinking and waste water treatment plants. Water Res. 2011;45:5599–611.CAS 
    PubMed 

    Google Scholar 
    78.Skwor T, Stringer S, Haggerty J, Johnson J, Duhr S, Johnson M, et al. Prevalence of potentially pathogenic antibiotic-resistant Aeromonas spp. in treated urban wastewater effluents versus recipient riverine populations: a 3-year comparative study. Appl Environ Microbiol. 2020;86:1–16.
    Google Scholar 
    79.Janda JM, Abbott SL. The genus Aeromonas: taxonomy, pathogenicity, and infection. Clin Microbiol Rev. 2010;23:35–73.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    80.Rema T, Lawrence JR, Dynes JJ, Hitchcock AP, Korber DR. Microscopic and spectroscopic analyses of chlorhexidine tolerance in Delftia acidovorans biofilms. Antimicrob Agents Chemother. 2014;58:5673–86.PubMed 
    PubMed Central 

    Google Scholar 
    81.Assanta MA, Roy D, Lemay MJ, Montpetit D. Attachment of Arcobacter butzleri, a new waterborne pathogen, to water distribution pipe surfaces. J Food Protect. 2002;65:1240–7.
    Google Scholar 
    82.Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science. 1999;284:1318–22.CAS 
    PubMed 

    Google Scholar 
    83.Harrison F, Paul J, Massey RC, Buckling A. Interspecific competition and siderophore-mediated cooperation in Pseudomonas aeruginosa. ISME J. 2008;2:49–55.PubMed 

    Google Scholar 
    84.Inglis RF, Roberts PG, Gardner A, Buckling A. Spite and the scale of competition in Pseudomonas aeruginosa. Am Nat. 2011;178:276–85.PubMed 

    Google Scholar 
    85.van der Meij A, Worsley SF, Hutchings MI, van Wezel GP. Chemical ecology of antibiotic production by Actinomycetes. FEMS Microbiol Rev. 2017;41:392–416.PubMed 

    Google Scholar 
    86.Traxler MF, Kolter R. Natural products in soil microbe interactions and evolution. Nat Prod Rep. 2015;32:956–70.CAS 
    PubMed 

    Google Scholar 
    87.Kinkel LL, Schlatter DC, Xiao K, Baines AD. Sympatric inhibition and niche differentiation suggest alternative coevolutionary trajectories among Streptomycetes. ISME J. 2014;8:249–56. https://doi.org/10.1038/ismej.2013.175. [Internet]Available fromCAS 
    Article 
    PubMed 

    Google Scholar 
    88.Pacala SW, Levin SA. Biologically generated spatial pattern and the coexistence of competing species. In: Tilman D, Kareiva P, editors. Spatial ecology: the role of space in population dynamics and interspecific interactions; Princeton University Press, Princeton, New Jersey, USA; 1997.89.Zhou J, Ning D. Stochastic community assembly: does it matter in microbial ecology? Microbiol Mol Biol Rev. 2017;81:1–32.
    Google Scholar 
    90.Haig SJ, Quince C, Davies RL, Dorea CC, Collinsa G. The relationship between microbial community evenness and function in slow sand filters. mBio. 2015;6:1–12.
    Google Scholar 
    91.Wittebolle L, Marzorati M, Clement L, Balloi A, Daffonchio D, Heylen K, et al. Initial community evenness favours functionality under selective stress. Nature. 2009;458:623–6.CAS 
    PubMed 

    Google Scholar 
    92.Davies J, Ryan KS. Introducing the parvome: bioactive compounds in the microbial world. ACS Chem Biol. 2012;7:252–9.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    93.Bassler BL, Losick R. Bacterially speaking. Cell. 2006;125:237–46.CAS 
    PubMed 

    Google Scholar 
    94.Venturi V. Regulation of quorum sensing in Pseudomonas. FEMS Microbiol Rev. 2006;30:274–91.CAS 
    PubMed 

    Google Scholar 
    95.Granato ET, Meiller-Legrand TA, Foster KR. The evolution and ecology of bacterial warfare. Curr Biol. 2019;29:R521–37. https://doi.org/10.1016/j.cub.2019.04.024.CAS 
    Article 
    PubMed 

    Google Scholar 
    96.Estrela S, Brown SP. Community interactions and spatial structure shape selection on antibiotic resistant lineages. PLoS Comput Biol. 2018;14:1–21.CAS 

    Google Scholar 
    97.Hibbing ME, Fuqua C, Parsek MR, Peterson SB. Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol. 2010;8:15–25.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    98.Garcia-Garcera M, Rocha EPC. Community diversity and habitat structure shape the repertoire of extracellular proteins in bacteria. Nat Commun. 2020;11:1–11. https://doi.org/10.1038/s41467-020-14572-x.CAS 
    Article 

    Google Scholar  More

  • in

    Global and regional health and food security under strict conservation scenarios

    1.Butchart, S. H. M. et al. Global biodiversity: indicators of recent declines. Science 328, 1164–1168 (2010).CAS 
    Article 

    Google Scholar 
    2.Buchanan, G. M., Butchart, S. H. M., Chandler, G. & Gregory, R. D. Assessment of national-level progress towards elements of the Aichi Biodiversity Targets. Ecol. Indic. 116, 106497 (2020).Article 

    Google Scholar 
    3.Butchart, S. H. M. et al. in Global Assessment Report of the Intergovernmental Science–Policy Platform on Biodiversity and Ecosystem Services (eds Berkes, F. & Brooks, T. M.) Ch. 3 (IPBES Secretariat, 2019); https://doi.org/10.5281/zenodo.38320534.Maxwell, S. L. et al. Area-based conservation in the twenty-first century. Nature 586, 217–227 (2020).CAS 
    Article 

    Google Scholar 
    5.Locke, H. Nature needs half: a necessary and hopeful new agenda for protected areas. Nat. N. S. W. 58, 7–17 (2014).
    Google Scholar 
    6.Dinerstein, E. et al. An ecoregion-based approach to protecting half the terrestrial realm. Bioscience 67, 534–545 (2017).Article 

    Google Scholar 
    7.Dinerstein, E. et al. A global deal for nature: guiding principles, milestones, and targets. Sci. Adv. 5, eaaw2869 (2019).CAS 
    Article 

    Google Scholar 
    8.Mehrabi, Z., Ellis, E. C. & Ramankutty, N. The challenge of feeding the world while conserving half the planet. Nat. Sustain. 1, 409–412 (2018).Article 

    Google Scholar 
    9.Kok, M. T. J. et al. Assessing ambitious nature conservation strategies within a 2 degree warmer and food-secure world. Preprint at bioRxiv https://doi.org/10.1101/2020.08.04.236489 (2020).10.Rosa, I. M. D. et al. Multiscale scenarios for nature futures. Nat. Ecol. Evol. 1, 1416–1419 (2017).Article 

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

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

    Google Scholar 
    13.Rabin, S. S. et al. Impacts of future agricultural change on ecosystem service indicators. Earth Syst. Dynam. 11, 357–376 (2019).Article 

    Google Scholar 
    14.Springmann, M. et al. Global and regional health effects of future food production under climate change: a modelling study. Lancet 387, 1937–1946 (2016).Article 

    Google Scholar 
    15.Springmann, M. et al. Health and nutritional aspects of sustainable diet strategies and their association with environmental impacts: a global modelling analysis with country-level detail. Lancet Planet. Health 2, e451–e461 (2018).Article 

    Google Scholar 
    16.Dinerstein, E. et al. A “Global Safety Net” to reverse biodiversity loss and stabilize Earth’s climate. Sci. Adv. 6, eabb2824 (2020).Article 

    Google Scholar 
    17.Locke, H. et al. Three global conditions for biodiversity conservation and sustainable use: an implementation framework. Natl Sci. Rev. https://doi.org/10.1093/nsr/nwz136 (2019).18.Waldron, A. et al. Protecting 30% of the Planet for Nature: Costs, Benefits and Economic Implications (Campaign for Nature, 2020).19.Strassburg, B. B. N. et al. Global priority areas for ecosystem restoration. Nature 586, 724–729 (2020).CAS 
    Article 

    Google Scholar 
    20.O’Neill, B. C. et al. The roads ahead: narratives for Shared Socioeconomic Pathways describing world futures in the 21st century. Glob. Environ. Change 42, 169–180 (2015).21.Riahi, K. et al. The Shared Socioeconomic Pathways and their energy, land use, and greenhouse gas emissions implications: an overview. Glob. Environ. Change 42, 153–168 (2017).22.Tauli-Corpuz, V., Alcorn, J., Molnar, A., Healy, C. & Barrow, E. Cornered by PAs: adopting rights-based approaches to enable cost-effective conservation and climate action. World Dev. 130, 104923 (2020).Article 

    Google Scholar 
    23.Kashwan, P. V., Duffy, R., Massé, F., Asiyanbi, A. P. & Marijnen, E. From racialized neocolonial global conservation to an inclusive and regenerative conservation. Environ. Sci. Policy Sustain. Dev. 63, 4–19 (2021).Article 

    Google Scholar 
    24.The State of Food Security and Nutrition in the World 2017: Building Resilience for Peace and Food Security (FAO, 2017).25.Schleicher, J. et al. Protecting half of the planet could directly affect over one billion people. Nat. Sustain. 2, 1094–1096 (2019).Article 

    Google Scholar 
    26.Allan, J. R. et al. The minimum land area requiring conservation attention to safeguard biodiversity. Preprint at bioRxiv https://doi.org/10.1101/839977 (2021).27.Brockington, D. & Wilkie, D. Protected areas and poverty. Phil. Trans. R. Soc. B 370, 20140271 (2015).28.Protected Planet Report 2020 (UNEP–WCMC and IUCN, 2021).29.Naidoo, R. et al. Evaluating the impacts of protected areas on human well-being across the developing world. Sci. Adv. 5, eaav3006 (2019).CAS 
    Article 

    Google Scholar 
    30.Dutta, A., Allan, J., Shimray, G., General, S. & Pact, A. I. P. RE: “A ‘Global Safety Net’ to reverse biodiversity loss and stabilize Earth’s climate”. Sci. Adv. 6, eabb2824 (2020).Article 

    Google Scholar 
    31.Simmons, B. A., Nolte, C. & McGowan, J. Tough questions for the “30 × 30” conservation agenda. Front. Ecol. Environ. 19, 322–323 (2021).Article 

    Google Scholar 
    32.Jung, M. et al. Areas of global importance for conserving terrestrial biodiversity, carbon and water. Nat. Ecol. Evol. https://doi.org/10.1038/s41559-021-01528-7 (2021).33.The IUCN Red List of Threatened Species Version 2019.2 (IUCN, 2019).34.The World Database of Key Biodiversity Areas (KBA Partnership, 2019); www.keybiodiversityareas.org35.Mogg, S., Fastre, C. & Visconti, P. Targeted expansion of protected areas to maximise the persistence of terrestrial mammals. Preprint at bioRxiv https://doi.org/10.1101/608992 (2019).36.Gurobi Optimizer Reference Manual (Gurobi Optimization, 2019).37.Hanson, J. O. et al. prioritizr: Systematic Conservation Prioritization in R. R package version 5.0.3 https://CRAN.R-project.org/package=prioritizr (2020).38.Hurtt, G., Chini, L., Frolking, S. & Sahajpal, R. Land-Use Harmonization (LUH2) (Global Ecology Laboratory, Univ. Maryland, 2017).39.Protected Planet: The World Database on Protected Areas (WDPA) (UNEP-WCMC and IUCN, accessed April 2019); www.protectedplanet.net40.Dellink, R., Chateau, J., Lanzi, E. & Magné, B. Long-term economic growth projections in the Shared Socioeconomic Pathways. Glob. Environ. Change 42, 200–214 (2017).41.Jones, B. & O’Neill, B. C. Spatially explicit global population scenarios consistent with the Shared Socioeconomic Pathways. Environ. Res. Lett. 11, 84003 (2016).42.van Vuuren, D. P. et al. The representative concentration pathways: an overview. Climatic Change 109, 5–31 (2011).Article 

    Google Scholar 
    43.Engström, K. et al. Assessing uncertainties in global cropland futures using a conditional probabilistic modelling framework. Earth Syst. Dynam. 7, 893–915 (2016).44.Alexander, P. et al. Drivers for global agricultural land use change: the nexus of diet, population, yield and bioenergy. Glob. Environ. Change 35, 138–147 (2015).Article 

    Google Scholar 
    45.Popp, A. et al. Land-use transition for bioenergy and climate stabilization: model comparison of drivers, impacts and interactions with other land use based mitigation options. Climatic Change 123, 495–509 (2014).Article 

    Google Scholar 
    46.GBD Results Tool (IHME, 2020); http://ghdx.healthdata.org/gbd-results-tool47.KC, S. & Lutz, W. The human core of the Shared Socioeconomic Pathways: population scenarios by age, sex and level of education for all countries to 2100. Glob. Environ. Change 42, 181–192 (2017). More

  • in

    Low tropical diversity during the adaptive radiation of early land plants

    1.Gaston, K. J. Global patterns of biodiversity. Nature 405, 220–227 (2000).CAS 
    Article 

    Google Scholar 
    2.Friis, E. M., Crane, P. R. & Pedersen, K. R. Early Flowers and Angiosperm Evolution (Cambridge Univ. Press, 2011).3.Blomenkemper, P. et al. A hidden cradle of plant evolution in Permian tropical lowlands. Science 362, 1414–1416 (2018).CAS 
    Article 

    Google Scholar 
    4.Kenrick, P. & Crane, P. R. The Origin and Early Diversification of Land Plants: A Cladistic Study (Smithsonian Institution Scholarly Press, 1997).5.Puttick, M. N. et al. The interrelationships of land plants and the nature of the nature of the ancestral embryophyte. Curr. Biol. 28, 733–745 (2018).CAS 
    Article 

    Google Scholar 
    6.Morris, J. L. et al. The timescale of early land plant evolution. Proc. Natl Acad. Sci. USA 115, 2274–2283 (2018).Article 

    Google Scholar 
    7.Wellman, C. H., Steemans, P. & Vecoli, M. in Early Palaeozoic Biogeography and Palaeogeography (eds Harper, D. & Servais, T.) Ch. 29 (Geological Society of London, 2014).8.Edwards, D. et al. Piecing together the eophytes—a new group of ancient plants containing cryptospores. New Phytol. 233, 1440–1455 (2021).Article 

    Google Scholar 
    9.Gray, J. The microfossil record of early land plants; advances in understanding of early terrestrialization, 1970–1984. Philos. Trans. R. Soc. Lond. B 309, 167–195 (1985).Article 

    Google Scholar 
    10.Wellman, C. H. Cryptospores from the type area for the Caradoc Series (Ordovician) in southern Britain. Palaeontology 55, 103–136 (1996).
    Google Scholar 
    11.Torsvik, T. H. & Cocks, L. R. M. Earth History and Palaeogeography (Cambridge Univ. Press, 2017).12.Harland, W. B. The Geology of Svalbard (Geological Society of London, 1997).13.Davies, N. S., Berry, C. M., Marshall, J. E. A., Wellman, C. H. & Lindemann, F.-J. The Devonian landscape factory: plant–sediment interactions in the Old Red Sandstone of Svalbard and the rise of vegetation as a biogeomorphic agent. J. Geol. Soc. Lond. https://doi.org/10.1144/jgs2020-225 (2021).14.Blieck, A., Goujet, D. & Janvier, P. The vertebrate stratigraphy of the Lower Devonian (Red Bay Group and Wood Bay Formation) of Spitsbergen. Mod. Geol. 11, 197–217 (1987).
    Google Scholar 
    15.Blom, H. & Goujet, D. Thelodont scales from the Lower Devonian Red Bay Group, Spitsbergen. Palaeontology 45, 795–820 (2002).Article 

    Google Scholar 
    16.Pernègre, V. N. & Blieck, A. A revised heterostrachan-cased ichthyostratigraphy of the Wood Bay Formation (Lower Devonian, Spitsbergen), and correlation with Russian Arctic archipelagos. Geodiversitas 38, 5–20 (2016).Article 

    Google Scholar 
    17.Wellman, C. H. & Richardson, J. B. Sporomorph assemblages from the ‘Lower Old Red Sandstone’ of Lorne Scotland. Spec. Pap. Palaeontol. 55, 41–101.18.Richardson J. B. Taxonomy and classification of some new Early Devonian cryptospores from England. Spec. Pap. Palaeontol. 55, 7–40 (1996).19.Steemans, P. Etude palynostratgraphique du Devonian Inferieur dans l’Ouest de l’Europe. Mém. Soc. Géol. Minér. Bretagne 27, 1–453 (1989).
    Google Scholar 
    20.Rodriguez, R. M. Palinologia de las Formaciones del Silurico Superior-Devonico Inferior de la Cordillera Cantabrica, Noroeste de España (Institución Fray Bernardino de Sahagún, de la Excelentísima Diputación provincial de León y del Servicio de Publicaciones de la Universidad de León, 1983).21.Richardson, J. B., Rodriguez, R. M. & Sutherland, S. J. E. Palynological zonation of Mid-Palaeozoic sequences from the Cantabrian Mountains, NW Spain: implications for inter-regional and interfacies correlation of the Ludfor/Pridoli and Silurian/Devonian boundaries, and plant dispersal patterns. Bull. Nat. Hist. Mus. Lond. 57, 115–162 (2001).
    Google Scholar 
    22.Rubinstein, C. & Steemans, P. Miospore assemblages from the Silurian–Devonian boundary, in borehole A1–61, Ghadames Basin, Libya. Rev. Palaeobot. Palynol. 118, 397–412 (2002).Article 

    Google Scholar 
    23.Spina, A. & Vecoli, M. Palynostratigraphy and vegetational change in the Siluro-Devonian of the Ghadamis basin, North Africa. Palaeogeog. Palaeoclimatol. Palaeoecol. 282, 1–18 (2009).Article 

    Google Scholar 
    24.Hao, S. G. & Gensel, P. G. in Plants Invade the Land (eds Gensel, P. G. & Edwards, D.) 103–119 (Columbia Univ. Press, 2001).25.Wellman, C. H. et al. Spore assemblages from the Lower Devonian Xujiachong Formation from Qujing, Yunnan, China. Palaeontology 55, 583–611 (2012).Article 

    Google Scholar 
    26.Hao, S. & Xue, J. The Early Devonian Posongchong Flora of Yunnan (Science Press, 2013).27.Edwards, D., & Li, C.-S. Further insights into the Lower Devonian terrestrial vegetation of Sichuan Province, China. Rev. Palaeobot. Palynol. 253, 37–48 (2018).Article 

    Google Scholar 
    28.Gao, L. Early Devonian spore and acritarchs from the Guijiatum Formation of Qujing, China. Bull. Inst. Geol. Chin. Acad. Sci. 9, 125–136 (1984).
    Google Scholar 
    29.Tian, J. et al. Late Silurian to early Devonian palynomorphs from Qujing, Yunnan, southwest China. Acta Geol. Sin. 85, 559–568 (2011).Article 

    Google Scholar 
    30.Høeg, O. A. The Downtonian and Dittonian flora of Spitsbergen. Skr. Svalbard Ishavet 83, 1–229 (1942).
    Google Scholar 
    31.Morris, J. L., Edwards, D. & Richardson, J. B. in Transformative Paleobotany (eds Krings, M. et al.) 49–67 (Academic Press, 2018).32.McSweeney, F. R., Shimeta, J. & Buckeridge, J. St. J. S. Two new genera of early Tracheophyta (Zosterophyllaceae) from the upper Silurian–Lower Devonian of Victoria, Australia. Alcheringa https://doi.org/10.1080/03115518.2020.1744725 (2020).33.Xue, J. H. et al. Silurian–Devonian terrestrial revolution in South China: taxonomy, diversity, and character evolution of vascular plants in a paleogeographically isolated low-latitude region. Earth Sci. Rev. 180, 92–125 (2018).Article 

    Google Scholar 
    34.Hao, S. G. et al. Zosterophyllum Penhallow around the Silurian–Devonian boundary of northeastern Yunnan, China. Int. J. Plant Sci. 168, 477–489 (2007).Article 

    Google Scholar 
    35.Hao, S. G. et al. Earliest rooting system and root: shoot ratio from a new Zosterophyllum plant. New Phytol. 185, 217–225 (2009).Article 

    Google Scholar 
    36.Xue, J.-Z. Two zosterophyll plants from the Lower Devonian (Lochkovian) Xitun Formation of northeastern Yunnan, China. Acta Geol. Sin. 83, 504–512 (2009).Article 

    Google Scholar 
    37.Xue, J.-Z. Lochkovian plants from the Xitun Formation of Yunnan, China and their palaeophytogeographical significance. Geol. Mag. 149, 333–344 (2012).Article 

    Google Scholar 
    38.Sun, Y. et al. Lethally high temperatures during the early Triassic greenhouse. Science 6105, 366–370 (2012).Article 

    Google Scholar 
    39.Meng, X. Y. & Gai, Z. K. Falxcornus, a new genus of Tridensaspidae (Galeaspida, stem-Gnathostomata) from the Lower Devonian in Qujing, Yunnan, China. Hist. Biol. https://doi.org/10.1080/08912963.2021.1952198 (2021).40.Traverse, A. Paleopalynology 2nd edn (Springer, 2007). More

  • in

    Temperature sensitivity of woody nitrogen fixation across species and growing temperatures

    1.Hungate, B. A., Dukes, J. S., Shaw, M. R., Luo, Y. & Field, C. B. Nitrogen and climate change. Science 302, 1512–1513 (2003).CAS 
    Article 

    Google Scholar 
    2.Wieder, W. R., Cleveland, C. C., Smith, W. K. & Todd-Brown, K. Future productivity and carbon storage limited by terrestrial nutrient availability. Nat. Geosci. 8, 441–444 (2015).CAS 
    Article 

    Google Scholar 
    3.Sulman, B. N. et al. Diverse mycorrhizal associations enhance terrestrial C storage in a global model. Glob. Biogeochem. Cycles 33, 501–523 (2019).CAS 
    Article 

    Google Scholar 
    4.Wieder, W. R., Cleveland, C. C., Lawrence, D. M. & Bonan, G. B. Effects of model structural uncertainty on carbon cycle projections: biological nitrogen fixation as a case study. Environ. Res. Lett. 10, 044016 (2015).5.Shi, M., Fisher, J. B., Brzostek, E. R. & Phillips, R. P. Carbon cost of plant nitrogen acquisition: global carbon cycle impact from an improved plant nitrogen cycle in the Community Land Model. Glob. Change Biol. 22, 1299–1314 (2016).Article 

    Google Scholar 
    6.Meyerholt, J., Zaehle, S. & Smith, M. J. Variability of projected terrestrial biosphere responses to elevated levels of atmospheric CO2 due to uncertainty in biological nitrogen fixation. Biogeosciences 13, 1491–1518 (2016).CAS 
    Article 

    Google Scholar 
    7.Fisher, J. B. et al. Carbon cost of plant nitrogen acquisition: a mechanistic, globally applicable model of plant nitrogen uptake, retranslocation, and fixation. Glob. Biogeochem. Cycles 24, GB1014 (2010).8.Wang, Y. P. & Houlton, B. Z. Nitrogen constraints on terrestrial carbon uptake: Implications for the global carbon-climate feedback. Geophys. Res. Lett. 36, L24403 (2009).9.Houlton, B. Z., Wang, Y.-P., Vitousek, P. M. & Field, C. B. A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454, 327–330 (2008).CAS 
    Article 

    Google Scholar 
    10.Steidinger, B. S. et al. Climatic controls of decomposition drive the global biogeography of forest-tree symbioses. Nature 569, 404–408 (2019).CAS 
    Article 

    Google Scholar 
    11.van Velzen, R., Doyle, J. J. & Geurts, R. A resurrected scenario: single gain and massive loss of nitrogen-fixing nodulation. Trends Plant Sci. 24, 49–57 (2018).Article 

    Google Scholar 
    12.Mills, B. et al. Modelling the long-term carbon cycle, atmospheric CO2, and Earth surface temperature from late Neoproterozoic to present day. Gondwana Res. 67, 172–186 (2018).Article 

    Google Scholar 
    13.Fowler, D. et al. The global nitrogen cycle in the twenty-first century. Philos. Trans. R. Soc. B 368, 20130164 (2013).14.Rogers, A. et al. A roadmap for improving the representation of photosynthesis in Earth system models. New Phytol. 213, 22–42 (2017).Article 

    Google Scholar 
    15.Prévost, D., Antoun, H. & Bordeleau, L. M. Effects of low temperatures on nitrogenase activity in sainfoin (Onobrychis viciifolia) nodulated by Arctic rhizobia. FEMS Microbiol. Lett. 45, 205–210 (1987).Article 

    Google Scholar 
    16.Rainbird, R. M., Atkins, C. A. & Pate, J. S. Effect of temperature on nitrogenase functioning in cowpea nodules. Plant Physiol. 73, 392–394 (1983).CAS 
    Article 

    Google Scholar 
    17.Dalton, D. A. & Zobel, D. B. Ecological aspects of nitrogen fixation by Purshia tridentata. Plant Soil 48, 57–80 (1977).CAS 
    Article 

    Google Scholar 
    18.Waughman, G. J. The effect of temperature on nitrogenase activity. J. Exp. Bot. 28, 949–960 (1977).CAS 
    Article 

    Google Scholar 
    19.Wheeler, C. T. The causation of the diurnal changes in nitrogen fixation in the nodules of Alnus glutinosa. New Phytol. 70, 487–495 (1971).Article 

    Google Scholar 
    20.Schomberg, H. H. & Weaver, R. W. Nodulation, nitrogen fixation, and early growth of arrowleaf clover in response to root temperature and starter nitrogen. Agron. J. 84, 1046 (1992).CAS 
    Article 

    Google Scholar 
    21.Kou-Giesbrecht, S. & Menge, D. N. L. Nitrogen-fixing trees increase soil nitrous oxide emissions: a meta-analysis. Ecology 102, e03415 (2021).22.Bytnerowicz, T. A., Min, E., Griffin, K. L. & Menge, D. N. L. Repeatable, continuous and real‐time estimates of coupled nitrogenase activity and carbon exchange at the whole‐plant scale. Methods Ecol. Evol. 10, 960–970 (2019).Article 

    Google Scholar 
    23.Menge, D. N. L., Lichstein, J. W. & Ángeles-Pérez, G. Nitrogen fixation strategies can explain the latitudinal shift in nitrogen-fixing tree abundance. Ecology 95, 2236–2245 (2014).Article 

    Google Scholar 
    24.Staccone, A. et al. A spatially explicit, empirical estimate of tree-based biological nitrogen fixation in forests of the United States. Glob. Biogeochem. Cycles 32, e2019GB006241 (2020).25.Cierjacks, A. et al. Biological flora of the British Isles: Robinia pseudoacacia. J. Ecol. 101, 1623–1640 (2013).Article 

    Google Scholar 
    26.Benson, D. R. & Dawson, J. O. Recent advances in the biogeography and genecology of symbiotic Frankia and its host plants. Physiol. Plant. 130, 318–330 (2007).CAS 
    Article 

    Google Scholar 
    27.Fick, S. E. & Hijmans, R. J. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315 (2017).Article 

    Google Scholar 
    28.Kumarathunge, D. P. et al. Acclimation and adaptation components of the temperature dependence of plant photosynthesis at the global scale. New Phytol. 222, 768–784 (2019).CAS 
    Article 

    Google Scholar 
    29.Heskel, M. A. et al. Convergence in the temperature response of leaf respiration across biomes and plant functional types. Proc. Natl Acad. Sci. USA 113, 3832–3837 (2016).CAS 
    Article 

    Google Scholar 
    30.Kou-Giesbrecht, S. et al. A novel representation of biological nitrogen fixation and competitive dynamics between nitrogen-fixing and non-fixing plants in a land model (GFDL LM4.1-BNF). Biogeosciences 18, 4143–4183 (2021).CAS 
    Article 

    Google Scholar 
    31.Hardy, R. W. F., Holsten, R. D., Jackson, E. K. & Burns, R. C. The acetylene-ethylene assay for N2 fixation: laboratory and field evaluation. Plant Physiol. 43, 1185–1207 (1968).CAS 
    Article 

    Google Scholar 
    32.Cassar, N., Bellenger, J. P., Jackson, R. B., Karr, J. & Barnett, B. A. N2 fixation estimates in real-time by cavity ring-down laser absorption spectroscopy. Oecologia 168, 335–342 (2012).Article 

    Google Scholar 
    33.Taylor, B. N., Chazdon, R. L. & Menge, D. N. L. Successional dynamics of nitrogen fixation and forest growth in regenerating Costa Rican rainforests. Ecology 100, e02637 (2019).34.Kok, B. A Critical Consideration of the Quantum Yield of Chlorella-Photosynthesis (W. Junk, 1948).35.Liang, L. L. et al. Macromolecular rate theory (MMRT) provides a thermodynamics rationale to underpin the convergent temperature response in plant leaf respiration. Glob. Change Biol. 24, 1538–1547 (2018).Article 

    Google Scholar 
    36.Gunderson, C. A., O’hara, K. H., Campion, C. M., Walker, A. V. & Edwards, N. T. Thermal plasticity of photosynthesis: the role of acclimation in forest responses to a warming climate. Glob. Change Biol. 16, 2272–2286 (2010).Article 

    Google Scholar 
    37.Medlyn, B. E. et al. Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data. Plant Cell Environ. 25, 1167–1179 (2002).CAS 
    Article 

    Google Scholar 
    38.Slot, M. & Winter, K. In situ temperature relationships of biochemical and stomatal controls of photosynthesis in four lowland tropical tree species. Plant Cell Environ. 40, 3055–3068 (2017).CAS 
    Article 

    Google Scholar 
    39.Murphy, B. K. & Stinziano, J. R. A derivation error that affects carbon balance models exists in the current implementation of the modified Arrhenius function. New Phytol. 6, 2371–2381 (2021).40.Yan, W. & Hunt, L. A. An equation for modelling the temperature response of plants using only the cardinal temperatures. Ann. Bot. 84, 607–614 (1999).Article 

    Google Scholar 
    41.Farquhar, G. D. & Busch, F. A. Changes in the chloroplastic CO2 concentration explain much of the observed Kok effect: a model. New Phytol. 214, 570–584 (2017).CAS 
    Article 

    Google Scholar 
    42.Farquhar, G. D., Von Caemmerer, S. & Berry, J. A. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90 (1980).CAS 
    Article 

    Google Scholar 
    43.Duursma, R. A. Plantecophys – an R package for analysing and modelling leaf gas exchange data. PLoS ONE 10, e0143346 (2015).44.Bernacchi, C. J., Singsaas, E. L., Pimentel, C., Portis, A. R. Jr & Long, S. P. Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant Cell Environ. 24, 253–260 (2001).CAS 
    Article 

    Google Scholar 
    45.De Kauwe, M. G. et al. A test of the ‘one-point method’ for estimating maximum carboxylation capacity from field-measured, light-saturated photosynthesis. New Phytol. 210, 1130–1144 (2016).Article 

    Google Scholar 
    46.Bolker, B. M. & R. Core Team. bbmle: Tools for General Maximum Likelihood Estimation (R Foundation for Statistical Computing, 2014).47.Burnham, K. P. & Anderson, D. R. Multimodel inference: understanding AIC and BIC in model selection. Sociol. Methods Res. 33, 261–304 (2004).Article 

    Google Scholar 
    48.Bolker, B. M. Ecological Models and Data in R (Princeton Univ. Press, 2008).49.Venables, W. & Ripley, B. Modern Applied Statistics with S (Springer, 2002).50.Bytnerowicz, T. A. tbytnero/Bytnerowicz-Akana-Griffin-Menge-N-fix-Temp: Bytnerowicz_Akana_Griffin_Menge_2022_Nature_Plants https://doi.org/10.5281/zenodo.5764790 (2021). More

  • in

    Species delimitation and mitonuclear discordance within a species complex of biting midges

    1.De Queiroz, K. Species concepts and species delimitation. Syst. Biol. 56, 879–886. https://doi.org/10.1080/10635150701701083 (2007).Article 
    PubMed 

    Google Scholar 
    2.Coyne, J. A. & Orr, H. A. Speciation (Sinauer Associates Inc, 2004).
    Google Scholar 
    3.Endler, J. A. Gene flow and population differentiation: studies of clines suggest that differentiation along environmental gradients may be independent of gene flow. Science 179, 243–250 (1973).CAS 
    PubMed 
    ADS 

    Google Scholar 
    4.Mayr, E. Systematics and the Origin of Species, from the Viewpoint of a Zoologist (Harvard University Press, 1999).
    Google Scholar 
    5.Richardson, J. L., Urban, M. C., Bolnick, D. I. & Skelly, D. K. Microgeographic adaptation and the spatial scale of evolution. Trends Ecol. Evol. 29, 165–176 (2014).PubMed 

    Google Scholar 
    6.Nosil, P. Ernst Mayr and the integration of geographic and ecological factors in speciation. Biol. J. Lin. Soc. 95, 26–46 (2008).
    Google Scholar 
    7.Kisel, Y. & Barraclough, T. G. Speciation has a spatial scale that depends on levels of gene flow. Am. Nat. 175, 316–334 (2010).PubMed 

    Google Scholar 
    8.Leliaert, F. et al. DNA-based species delimitation in algae. Eur. J. Phycol. 49, 179–196 (2014).
    Google Scholar 
    9.Carstens, B. C., Pelletier, T. A., Reid, N. M. & Satler, J. D. How to fail at species delimitation. Mol. Ecol. 22, 4369–4383 (2013).PubMed 

    Google Scholar 
    10.Schlick-Steiner, B. C. et al. Integrative taxonomy: a multisource approach to exploring biodiversity. Annu. Rev. Entomol. 55, 421–438 (2010).CAS 
    PubMed 

    Google Scholar 
    11.Capblancq, T., Mavárez, J., Rioux, D. & Després, L. Speciation with gene flow: evidence from a complex of alpine butterflies (Coenonympha, Satyridae). Ecol. Evol. 9, 6444–6457 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    12.Pedraza-Marrón, C. d. R. et al. Genomics overrules mitochondrial DNA, siding with morphology on a controversial case of species delimitation. Proc. R. Soc. B 286, 20182924 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    13.Hinojosa, J. C. et al. A mirage of cryptic species: genomics uncover striking mitonuclear discordance in the butterfly Thymelicus sylvestris. Mol. Ecol. 28, 3857–3868 (2019).PubMed 

    Google Scholar 
    14.Nygren, A. et al. A mega-cryptic species complex hidden among one of the most common annelids in the North East Atlantic. PLoS ONE 13, e0198356 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    15.Thielsch, A., Knell, A., Mohammadyari, A., Petrusek, A. & Schwenk, K. Divergent clades or cryptic species? Mito-nuclear discordance in a Daphnia species complex. BMC Evol. Biol. 17, 1–9 (2017).
    Google Scholar 
    16.Eyer, P. A. & Hefetz, A. Cytonuclear incongruences hamper species delimitation in the socially polymorphic desert ants of the Cataglyphis albicans group in Israel. J. Evol. Biol. 31, 1828–1842 (2018).CAS 
    PubMed 

    Google Scholar 
    17.Borkent, A. Biology of Disease Vectors. 2nd edn, i–xxiii + 1–785 (Elsevier Academic Press, 2004).18.Mellor, P., Boorman, J. & Baylis, M. Culicoides biting midges: their role as arbovirus vectors. Annu. Rev. Entomol. 45, 307–340 (2000).CAS 
    PubMed 

    Google Scholar 
    19.Rushton, J. & Lyons, N. Economic impact of Bluetongue: a review of the effects on production. Veterinaria italiana 51, 401–406 (2015).PubMed 

    Google Scholar 
    20.Tabachnick, W. J. Culicoides vriipennis and Bluetongue-Virus eidemiology in the United States. Annu. Rev. Entomol. 41, 23–43. https://doi.org/10.1146/annurev.en.41.010196.000323 (1996).CAS 
    Article 
    PubMed 

    Google Scholar 
    21.Wirth, W. W. & Jones, R. H. The North American Subspecies of Culicoides variipennis (Diptera, Heleidae). U. S. Dep. Agric. Tech. Bull 1170, 1–35 (1957).
    Google Scholar 
    22.Holbrook, F. R. et al. Sympatry in the Culicoides variipennis Complex (Diptera: Ceratopogonidae): a Taxonomic Reassessment. J. Med. Entomol. 37, 65–76. https://doi.org/10.1603/0022-2585-37.1.65 (2000).CAS 
    Article 
    PubMed 

    Google Scholar 
    23.Hopken, M. W. Pathogen Vectors at the Wildlife-Livestock Interface: Molecular Approaches to Elucidating Culicoides (Diptera: Ceratopogonidae) Biology (University of Colorado, 2016).
    Google Scholar 
    24.Shults, P. A Study of the Taxonomy, Ecology, and Systematics of Culicoides Species (Diptera: Ceratopogonidae) Including those Associated with Deer Breeding Facilities in Southeast Texas (Texas A&M University, 2015).
    Google Scholar 
    25.Velten, R. K. & Mullens, B. A. Field morphological variation and laboratory hybridization of Culicoides variipennis sonorensis and C. v. occidentalis (Diptera:Ceratopogonidae) in southern California. J. Med. Entomol. 34, 277–284 (1997).CAS 
    PubMed 

    Google Scholar 
    26.Fontaine, M. C. et al. Extensive introgression in a malaria vector species complex revealed by phylogenomics. Science 347, 1258522 (2015).PubMed 

    Google Scholar 
    27.Bolnick, D. I. & Otto, S. P. The magnitude of local adaptation under genotype-dependent dispersal. Ecol. Evol. 3, 4722–4735 (2013).PubMed 
    PubMed Central 

    Google Scholar 
    28.Slatkin, M. Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47, 264–279 (1993).PubMed 

    Google Scholar 
    29.Pante, E. et al. Species are hypotheses: avoid connectivity assessments based on pillars of sand. Mol. Ecol. 24, 525–544 (2015).PubMed 

    Google Scholar 
    30.Jacquet, S. et al. Colonization of the Mediterranean basin by the vector biting midge species Culicoides imicola: an old story. Mol. Ecol. 24, 5707–5725. https://doi.org/10.1111/mec.13422 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    31.Onyango, M. G. et al. Genotyping of whole genome amplified reduced representation libraries reveals a cryptic population of Culicoides brevitarsis in the Northern Territory, Australia. BMC Genomics 17, 769. https://doi.org/10.1186/s12864-016-3124-1 (2016).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    32.Onyango, M. G. et al. Delineation of the population genetic structure of Culicoides imicola in East and South Africa. Parasit. Vectors 8, 660. https://doi.org/10.1186/s13071-015-1277-4 (2015).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    33.Mignotte, A. et al. High dispersal capacity of Culicoides obsoletus (Diptera: Ceratopogonidae), vector of bluetongue and Schmallenberg viruses, revealed by landscape genetic analyses. Parasit. Vectors 14, 1–14 (2021).
    Google Scholar 
    34.Sanders, C. J. & Carpenter, S. Assessment of an immunomarking technique for the study of dispersal of Culicoides biting midges. Infect. Genet. Evol. 28, 583–587 (2014).PubMed 

    Google Scholar 
    35.Kluiters, G., Swales, H. & Baylis, M. Local dispersal of palaearctic Culicoides biting midges estimated by mark-release-recapture. Parasit. Vectors 8, 86 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    36.Ducheyne, E. et al. Quantifying the wind dispersal of Culicoides species in Greece and Bulgaria. Geospat. Health 10, 177–189 (2007).
    Google Scholar 
    37.Purse, B. V. et al. Climate change and the recent emergence of bluetongue in Europe. Nat. Rev. Microbiol. 3, 171–181 (2005).CAS 
    PubMed 

    Google Scholar 
    38.Jacquet, S. et al. Range expansion of the Bluetongue vector, Culicoides imicola, in continental France likely due to rare wind-transport events. Sci. Rep. https://doi.org/10.1038/srep27247 (2016).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    39.Rundle, H. D. & Nosil, P. Ecological speciation. Ecol. Lett. 8, 336–352 (2005).
    Google Scholar 
    40.Wang, I. J. & Bradburd, G. S. Isolation by environment. Mol. Ecol. 23, 5649–5662 (2014).PubMed 

    Google Scholar 
    41.Shults, P. A Study of Culicoides Biting Midges in the Subgenus Monoculicoides: Population Genetics, Taxonomy, Systematics, and Control. Ph.D. thesis, Texas A&M University (2021).42.Jewiss-Gaines, A., Barelli, L. & Hunter, F. F. First records of Culicoides sonorensis (Diptera: Ceratopogonidae), a known vector of bluetongue virus, Southern Ontario. J. Med. Entomol. 54, 757–762. https://doi.org/10.1093/jme/tjw215 (2017).CAS 
    Article 
    PubMed 

    Google Scholar 
    43.Chan, K. M. & Levin, S. A. Leaky prezygotic isolation and porous genomes: rapid introgression of maternally inherited DNA. Evolution 59, 720–729 (2005).CAS 
    PubMed 

    Google Scholar 
    44.Harrison, R. G. Hybrid zones: windows on evolutionary process. Oxf. Surv. Evol. Biol. 7, 69–128 (1990).
    Google Scholar 
    45.Harrison, R. G. Animal mitochondrial DNA as a genetic marker in population and evolutionary biology. Trends Ecol. Evol. 4, 6–11 (1989).CAS 
    PubMed 

    Google Scholar 
    46.Després, L. One, Two or More Species? Mitonuclear Discordance and Species Delimitation. Molecular ecology 28(17), 3845–3847 (2019).PubMed 

    Google Scholar 
    47.Janes, J. K. et al. The K= 2 conundrum. Mol. Ecol. 26, 3594–3602 (2017).PubMed 

    Google Scholar 
    48.De Meester, L., Vanoverbeke, J., Kilsdonk, L. J. & Urban, M. C. Evolving perspectives on monopolization and priority effects. Trends Ecol. Evol. 31, 136–146 (2016).PubMed 

    Google Scholar 
    49.Ballard, J. W. O., Chernoff, B. & James, A. C. Divergence of mitochondrial DNA is not corroborated by nuclear DNA, morphology, or behavior in Drosophila simulans. Evolution 56, 527–545 (2002).PubMed 

    Google Scholar 
    50.Behura, S., Sahu, S., Mohan, M. & Nair, S. Wolbachia in the Asian rice gall midge, Orseolia oryzae (Wood-Mason): Correlation between host mitotypes and infection status. Insect Mol. Biol. 10, 163–171 (2001).CAS 
    PubMed 

    Google Scholar 
    51.Covey, H. et al. Cryptic Wolbachia (Rickettsiales: Rickettsiaceae) detection and prevalence in Culicoides (Diptera: Ceratopogonidae) midge populations in the United States. J. Med. Entomol. 57, 1262–1269. https://doi.org/10.1093/jme/tjaa003 (2020).Article 
    PubMed 

    Google Scholar 
    52.Pagès, N., Muñoz-Muñoz, F., Verdún, M., Pujol, N. & Talavera, S. First detection of Wolbachia-infected Culicoides (Diptera: Ceratopogonidae) in Europe: Wolbachia and Cardinium infection across Culicoides communities revealed in Spain. Parasit. Vectors 10, 582. https://doi.org/10.1186/s13071-017-2486-9 (2017).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    53.Pilgrim, J. et al. Cardinium symbiosis as a potential confounder of mtDNA based phylogeographic inference in Culicoides imicola (Diptera: Ceratopogonidae), a vector of veterinary viruses. Parasit. Vectors 14, 100. https://doi.org/10.1186/s13071-020-04568-3 (2021).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    54.Hare, M. P. Prospects for nuclear gene phylogeography. Trends Ecol. Evol. 16, 700–706 (2001).
    Google Scholar 
    55.Onyango, M. G. et al. Assessment of population genetic structure in the arbovirus vector midge, Culicoides brevitarsis (Diptera: Ceratopogonidae), using multi-locus DNA microsatellites. Vet. Res. 46, 108. https://doi.org/10.1186/s13567-015-0250-8 (2015).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    56.Fonseca, D. M., Smith, J. L., Kim, H.-C. & Mogi, M. Population genetics of the mosquito Culex pipiens pallens reveals sex-linked asymmetric introgression by Culex quinquefasciatus. Infect. Genet. Evol. 9, 1197–1203 (2009).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    57.Goubert, C., Minard, G., Vieira, C. & Boulesteix, M. Population genetics of the Asian tiger mosquito Aedes albopictus, an invasive vector of human diseases. Heredity 117, 125–134 (2016).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    58.Lehmann, T. et al. Microgeographic structure of Anopheles gambiae in western Kenya based on mtDNA and microsatellite loci. Mol. Ecol. 6, 243–253 (1997).CAS 
    PubMed 

    Google Scholar 
    59.Chapuis, M.-P. & Estoup, A. Microsatellite null alleles and estimation of population differentiation. Mol. Biol. Evol. 24, 621–631. https://doi.org/10.1093/molbev/msl191 (2006).CAS 
    Article 
    PubMed 

    Google Scholar 
    60.Manni, M. et al. Molecular markers for analyses of intraspecific genetic diversity in the Asian Tiger mosquito, Aedes albopictus. Parasit. Vectors 8, 1–11 (2015).
    Google Scholar 
    61.Arntzen, J. W., Jehle, R., Bardakci, F., Burke, T. & Wallis, G. P. Asymmetric viability of reciprocal-cross hybrids between Crested and Marbled Newts (Triturus cristatus and T. marmoratus). Evolution 63, 1191–1202. https://doi.org/10.1111/j.1558-5646.2009.00611.x (2009).Article 
    PubMed 

    Google Scholar 
    62.Gibeaux, R. et al. Paternal chromosome loss and metabolic crisis contribute to hybrid inviability in Xenopus. Nature 553, 337. https://doi.org/10.1038/nature25188 (2018).CAS 
    Article 
    PubMed 
    PubMed Central 
    ADS 

    Google Scholar 
    63.Werren, J. H., Baldo, L. & Clark, M. E. Wolbachia: master manipulators of invertebrate biology. Nat. Rev. Microbiol. 6, 741 (2008).CAS 
    PubMed 

    Google Scholar 
    64.Servedio, M. R. & Kirkpatrick, M. The effects of gene flow on reinforcement. Evolution 51, 1764–1772. https://doi.org/10.1111/j.1558-5646.1997.tb05100.x (1997).Article 
    PubMed 

    Google Scholar 
    65.Howard, D. J. Reinforcement: origin, dynamics, and fate of an evolutionary hypothesis. Hybrid zones and the evolutionary process, 46–69 (1993).66.Yukilevich, R. Asymmetrical patterns of speciation uniquely support reinforcement in Drosophila. Evolution 66, 1430–1446. https://doi.org/10.1111/j.1558-5646.2011.01534.x (2012).Article 
    PubMed 

    Google Scholar 
    67.Downes, J. A. The Culicoides variipennis complex: a necessary re-alignment of nomenclature (Diptera: Ceratopogonidae). Can. Entomol. 110, 63–69 (1978).
    Google Scholar 
    68.Toews, D. P. & Brelsford, A. The biogeography of mitochondrial and nuclear discordance in animals. Mol. Ecol. 21, 3907–3930 (2012).CAS 
    PubMed 

    Google Scholar 
    69.Smith, H. & Mullens, B. A. Seasonal activity, size, and parity of Culicoides occidentalis (Diptera: Ceratopogonidae) in a coastal southern California salt marsh. J. Med. Entomol. 40, 352–355. https://doi.org/10.1603/0022-2585-40.3.352 (2003).Article 
    PubMed 

    Google Scholar 
    70.Linley, J. The effect of salinity on oviposition and egg hatching in Culicoides variipennis sonorensis (Diptera: Ceratopogonidae). J. Am. Mosq. Control Assoc. 2, 79–82 (1986).CAS 
    PubMed 

    Google Scholar 
    71.Gerry, A. C. & Mullens, B. A. Response of Male Culicoides variipennis sonorensis (Diptera: Ceratopogonidae) to carbon dioxide and observations of mating behavior on and near cattle. J. Med. Entomol. 35, 239–244. https://doi.org/10.1093/jmedent/35.3.239 (1998).CAS 
    Article 
    PubMed 

    Google Scholar 
    72.Nolan, D. V. et al. Rapid diagnostic PCR assays for members of the Culicoides obsoletus and Culicoides pulicaris species complexes, implicated vectors of bluetongue virus in Europe. Vet. Microbiol. 124, 82–94 (2007).CAS 
    PubMed 

    Google Scholar 
    73.Sebastiani, F. et al. Molecular differentiation of the Old World Culicoides imicola species complex (Diptera, Ceratopogonidae), inferred using random amplified polymorphic DNA markers. Mol. Ecol. 10, 1773–1786 (2001).CAS 
    PubMed 

    Google Scholar 
    74.Carlson, D. Identification of mosquitoes of Anopheles gambiae species complex A and B by analysis of cuticular components. Science 207, 1089–1091 (1980).CAS 
    PubMed 
    ADS 

    Google Scholar 
    75.Palacios, G. et al. Characterization of the Sandfly fever Naples species complex and description of a new Karimabad species complex (genus Phlebovirus, family Bunyaviridae). J. Gen. Virol. 95, 292 (2014).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    76.Rivas, G., Souza, N. & Peixoto, A. A. Analysis of the activity patterns of two sympatric sandfly siblings of the Lutzomyia longipalpis species complex from Brazil. Med. Vet. Entomol. 22, 288–290 (2008).CAS 
    PubMed 

    Google Scholar 
    77.Wilson, W. C. et al. Current status of bluetongue virus in the Americas. Bluetongue 10, 197–220 (2009).
    Google Scholar 
    78.Allen, S. E. et al. Epizootic Hemorrhagic Disease in White-Tailed Deer, Canada. Emerg. Infect. Dis. 25, 832–834. https://doi.org/10.3201/eid2504.180743 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    79.McGregor, B. L. et al. Field data implicating Culicoides stellifer and Culicoides venustus (Diptera: Ceratopogonidae) as vectors of epizootic hemorrhagic disease virus. Parasit. Vectors 12, 258. https://doi.org/10.1186/s13071-019-3514-8 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    80.Shults, P., Ho, A., Martin, E. M., McGregor, B. L. & Vargo, E. L. Genetic diversity of Culicoides stellifer (Diptera: Ceratopogonidae) in the Southeastern United States compared with sequences from Ontario, Canada. J. Med. Entomol. 57, 1324–1327. https://doi.org/10.1093/jme/tjaa025 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    81.Mallet, J. Hybridization as an invasion of the genome. Trends Ecol. Evol. 20, 229–237 (2005).PubMed 

    Google Scholar 
    82.Ciota, A. T., Chin, P. A. & Kramer, L. D. The effect of hybridization of Culex pipiens complex mosquitoes on transmission of West Nile virus. Parasit. Vectors 6, 1–4 (2013).
    Google Scholar 
    83.Meiswinkel, R., Gomulski, L., Delécolle, J., Goffredo, M. & Gasperi, G. The taxonomy of Culicoides vector complexes-unfinished business. Vet. Ital. 40, 151–159 (2004).CAS 
    PubMed 

    Google Scholar 
    84.Ewels, P., Magnusson, M., Lundin, S. & Käller, M. MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics (Oxford, England) 32, 3047–3048. https://doi.org/10.1093/bioinformatics/btw354 (2016).CAS 
    Article 

    Google Scholar 
    85.Andrews, S. Babraham bioinformatics-FastQC a quality control tool for high throughput sequence data. https://www.bioinformatics.babraham.ac.uk/projects/fastqc (2010).86.Rochette, N. C., Rivera-Colón, A. G. & Catchen, J. M. Stacks 2: Analytical methods for paired-end sequencing improve RADseq-based population genomics. Mol. Ecol. 28, 4737–4754 (2019).CAS 
    PubMed 

    Google Scholar 
    87.Morales-Hojas, R. et al. The genome of the biting midge Culicoides sonorensis and gene expression analyses of vector competence for bluetongue virus. BMC Genomics 19, 624. https://doi.org/10.1186/s12864-018-5014-1 (2018).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    88.Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics (Oxford, England) 25, 1754–1760 (2009).CAS 

    Google Scholar 
    89.Pante, E. et al. Use of RAD sequencing for delimiting species. Heredity 114, 450–459 (2015).CAS 
    PubMed 

    Google Scholar 
    90.Benestan, L. M. et al. Conservation genomics of natural and managed populations: building a conceptual and practical framework. Mol. Ecol. 25, 2967–2977 (2016).PubMed 

    Google Scholar 
    91.Lischer, H. E. & Excoffier, L. PGDSpider: an automated data conversion tool for connecting population genetics and genomics programs. Bioinformatics (Oxford, England) 28, 298–299 (2012).CAS 

    Google Scholar 
    92.Pina-Martins, F., Silva, D. N., Fino, J. & Paulo, O. S. Structure_threader: An improved method for automation and parallelization of programs structure, fastStructure and MavericK on multicore CPU systems. Mol. Ecol. Resour. 17, e268–e274 (2017).CAS 
    PubMed 

    Google Scholar 
    93.Raj, A., Stephens, M. & Pritchard, J. K. Variational Inference of Population Structure in Large SNP Datasets. bioRxiv 10, 001073 (2013).
    Google Scholar 
    94.R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.http://www.R-project.org/ (2013).95.Jombart, Thibaut, and Caitlin Collins. A tutorial for discriminant analysis of principal components (DAPC) using adegenet 2.0. 0. London: Imperial College London, MRC Centre for Outbreak Analysis and Modelling (2015).96.Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics (Oxford, England) 30, 1312–1313 (2014).CAS 

    Google Scholar 
    97.Leaché, A. D., Banbury, B. L., Felsenstein, J., De Oca, A.N.-M. & Stamatakis, A. Short tree, long tree, right tree, wrong tree: New acquisition bias corrections for inferring SNP phylogenies. Syst. Biol. 64, 1032–1047 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    98.Pattengale, N. D., Alipour, M., Bininda-Emonds, O. R., Moret, B. M. & Stamatakis, A. How many bootstrap replicates are necessary?. J. Comput. Biol. 17, 337–354 (2010).MathSciNet 
    CAS 
    PubMed 

    Google Scholar 
    99.Trifinopoulos, J., Nguyen, L.-T., von Haeseler, A. & Minh, B. Q. W-IQ-TREE: A fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res. 44, W232–W235 (2016).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    100.Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K., Von Haeseler, A. & Jermiin, L. S. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587–589 (2017).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    101.Nguyen, L.-T., Schmidt, H. A., Von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).CAS 
    PubMed 

    Google Scholar 
    102.Hoang, D. T., Chernomor, O., Von Haeseler, A., Minh, B. Q. & Vinh, L. S. UFBoot2: improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 35, 518–522 (2018).CAS 
    PubMed 

    Google Scholar 
    103.Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 30. Syst. Biol. 59, 307–321. https://doi.org/10.1093/sysbio/syq010 (2010).CAS 
    Article 
    PubMed 

    Google Scholar 
    104.Rousset, F. genepop’007: a complete re‐implementation of the genepop software for Windows and Linux. Molecular ecology resources 8(1), 103–106 (2008).
    Google Scholar 
    105.Rousset, F. Genetic differentiation between individuals. J Evol Biol 13, 58–62 (2000).
    Google Scholar 
    106.Loiselle, B. A., Sork, V. L., Nason, J. & Graham, C. Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am. J. Bot. 82, 1420–1425 (1995).
    Google Scholar 
    107.Hardy, O. & Vekemans, X. SPAGeDi 1.5. A program for Spatial Pattern Analysis of Genetic Diversity. User’s manual http://ebe.ulb.ac.be/ebe/SPAGeDi_files/SPAGeDi_1.5_Manual.pdf. Université Libre de Bruxelles, Brussells, Belgium.[Google Scholar] (2015).108.Jay, F., Sjödin, P., Jakobsson, M. & Blum, M. G. Anisotropic isolation by distance: the main orientations of human genetic differentiation. Mol. Biol. Evol. 30, 513–525 (2013).CAS 
    PubMed 

    Google Scholar 
    109.Piry, S. et al. Mapping Averaged Pairwise Information (MAPI): a new exploratory tool to uncover spatial structure. Methods Ecol. Evol. 7, 1463–1475 (2016).
    Google Scholar 
    110.Kearse, M. et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics (Oxford, England) 28, 1647–1649. https://doi.org/10.1093/bioinformatics/bts199 (2012).Article 

    Google Scholar 
    111.Hopken, M. W. Pathogen Vectors at The Wildlife-Livestock Interface: Molecular Approaches to Elucidating Culicoides (Diptera: Ceratopogonidae) Ph.D. thesis, Colorado State University (2016).112.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 
    113.Bandelt, H. J., Forster, P. & Rohl, A. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16, 37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036 (1999).CAS 
    Article 
    PubMed 

    Google Scholar  More

  • in

    Completely predatory development is described in a braconid wasp

    The presents study indicates that Bracon predatorius generally oviposits during early stages of gall development (Fig. 1d) on galls induced by Aceria doctersi mostly on tender leaves (Fig 1a–c) and rarely on petioles and stems13. The number of B. predatorius larvae in parasitized galls ranged from 1–27 (n=93). Eighty-five percent of the examined galls (n=109) were parasitized by B. predatorius. Different development stages of larvae (Fig. 1f,g) and pupae (Fig. 1i) of B. predatorius were found together in some large galls (n=31) (Fig. 1i), which suggests multiple oviposition at different stages of gall development. Dissection of leaf galls two hours after oviposition by B. predatorius always revealed only a single egg (n=8). No live A. doctersi individuals were found close to the parasitoid wasp pupae (Fig. 1h). Aceria doctersi galls parasitised by B. predatorius have also been found in Kodakara (Thrissur district, Kerala) about 100 km away from the type locality in Kozhikode.The larval stages of B. predatorius feed on both juvenile and adults of A. doctersi (Fig 2d–f, Supplementary Video 1) which usually remain close to the erineal hairs on which they feed16; no egg predation occurs. Young larvae of B. predatorius wriggle through in between erineal hairs (Supplementary Video 1). They use their sickle-shaped mandibles (Fig 3b–e) to hunt mites (Supplementary Video 1). Continuous outward and inward movement of mandibles of B. predatorius larvae occurs along with the wriggling movement (Supplementary Video 1). The final instar larvae of B. predatorius are the most active and they feed voraciously at the rate of 5–7 A. doctersi individuals/min (n=8) (Supplementary Video 1).Figure 2Predatory behaviour of Bracon predatorius Ranjith & Quicke sp. nov. (a–c) Relationships between presence/absence and number of B. predatorius, gall size and numbers of mites (median, upper and lower quartiles, 1.5 × interquartile range and outliers): (a) galls without Bracon predatorius (n = 16) are significantly smaller than those with one or more Bracon predatorius (n = 93) (t = 3.7592, DF = 97.265, p-value = 0.000291), (b) galls without Bracon predatorius contain significantly more mites than those with (t = 6.308, DF = 15.877, p-value = 0.0001), (c) mite number as a function of number of Bracon predatorius larvae (only in parasitised galls) with gall volume as co-variate (n = 93, adjusted R2 = 0.4657,F = 21.13 on 3 and 89DF, p-value = 0.0001), gall volume and interaction were non-significant. (d–f) Sequential images of predatory behaviour of Bracon predatorius.Full size imageFigure 3Final instar larval cephalic structure of Bracon predatorius Ranjith & Quicke sp. nov. (a–d) Slide microphotographs of larval head capsule and mandible (a) macerated head capsule in anterior view, (b) head capsule, in dorsal view, (c) head capsule (in part), ventral view, (d) right mandible, in dorsal view, (e) anterior view of living final instar larva of B. predatorius consuming mite.Full size imageUnattacked galls were significantly smaller than those containing B. predatorius (means 217 and 595 respectively; p More