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    Net greenhouse gas balance with cover crops in semi-arid irrigated cropping systems

    United Nations Framework Convention on Climate Change (UNFCCC). The Paris Agreement. https://unfccc.int/process-and-meetings/the-paris-agreement/the-paris-agreement (2015). Accessed on 16 Dec 2021.Tubiello, F. N. et al. The contribution of agriculture, forestry and other land use activities to global warming, 1990–2012. Glob. Change Biol. 21(7), 2655–2660 (2015).ADS 
    Article 

    Google Scholar 
    Frank, S. et al. Agricultural non-CO2 emission reduction potential in the context of the 15 °C target. Nat. Clim. Change 9(1), 66–72 (2019).ADS 
    CAS 
    Article 

    Google Scholar 
    Crippa, M. et al. Food systems are responsible for a third of global anthropogenic GHG emissions. Nat. Food 2, 198–209 (2021).CAS 
    Article 

    Google Scholar 
    Hong, C. et al. Global and regional drivers of land-use emissions in 1961–2017. Nature 589, 554–561 (2021).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Tubiello, F. N. et al. Greenhouse gas emissions from food systems: Building the evidence base. Environ. Res. Lett. 16, 065007 (2021).ADS 
    CAS 
    Article 

    Google Scholar 
    Smith, P. et al. Agriculture, forestry and other land use (AFOLU). In Climate Change 2014: Mitigation of Climate Change. Contribution of Working Group III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (eds Edenhofer, O. et al.) (Cambridge University Press, 2014).
    Google Scholar 
    Schlesinger, W. H. & Andrews, J. A. Soil respiration and the global carbon cycle. Biogeochemistry 78, 7–20 (2000).Article 

    Google Scholar 
    Smith, K. A. & Conen, F. Impacts of land management on fluxes of trace greenhouse gases. Soil Use Manage. 20, 245–253 (2004).
    Google Scholar 
    Foley, J. A. et al. Solutions for a cultivated planet. Nature 478, 337–342 (2011).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Jones, S. K. et al. Nitrous oxide emissions from managed grassland: A comparison of eddy covariance and static chamber measurements. Atmos. Meas. Tech. 4, 2179–2194 (2011).CAS 
    Article 

    Google Scholar 
    Chapuis‐Lardy, L., Wrage, N., Metay, A., Chotte, J. L. & Bernoux, M. Soils, a sink for N2O? A review. Glob. Change Biol. 13, 1–17 (2007).ADS 
    Article 

    Google Scholar 
    Sanz-Cobena, A. et al. Do cover crops enhance N2O, CO2 or CH4 emissions from soil in Mediterranean arable systems? Sci. Total Environ. 466, 164–174 (2014).ADS 
    PubMed 
    Article 
    CAS 

    Google Scholar 
    Kaye, J. P. & Quemada, M. Using cover crops to mitigate and adapt to climate change. A review. Agron. Sustain. Dev. 37(1), 1–17 (2017).Article 

    Google Scholar 
    Poeplau, C. & Don, A. Carbon sequestration in agricultural soils via cultivation of cover crops—A meta-analysis. Agric. Ecosyst. Environ. 200, 33–41 (2015).CAS 
    Article 

    Google Scholar 
    Guardia, G. et al. Effective climate change mitigation through cover cropping and integrated fertilization: A global warming potential assessment from a 10-year field experiment. J Clean. Prod. 241, 118307 (2019).CAS 
    Article 

    Google Scholar 
    Osipitan, O. A., Dille, J. A., Assefa, Y. & Knezevic, S. Z. Cover crop for early season weed suppression in crops: Systematic review and meta-analysis. Agron. J. 110(6), 2211–2221 (2018).Article 

    Google Scholar 
    Thapa, R., Mirsky, S. B. & Tully, K. L. Cover crops reduce nitrate leaching in agroecosystems: A global meta-analysis. J. Environ. Qual. 47(6), 1400–1411 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Snapp, S. S. et al. Evaluating cover crops for benefits, costs and performance within cropping system niches. Agron. J. 97, 322–332 (2005).Article 

    Google Scholar 
    Reicks, G. W. et al. Winter cereal rye cover crop decreased nitrous oxide emissions during early spring. Agron. J. 113, 3900–3909 (2021).CAS 
    Article 

    Google Scholar 
    Behnke, G. D. & Villamil, M. B. Cover crop rotations affect greenhouse gas emissions and crop production in Illinois, USA. Field Crops Res. 241, 107580 (2019).Article 

    Google Scholar 
    Blanco-Canqui, H., Holman, J. D., Schlegel, A. J., Tatarko, J. & Shaver, T. M. Replacing fallow with cover crops in a semi-arid soil: Effects on soil properties. Soil Sci. Soc. Am. J. 77, 1026–1034 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    Basche, A. D., Miguez, F. E., Kaspar, T. C. & Castellano, M. J. Do cover crops increase or decrease nitrous oxide emissions? A meta-analysis. J. Soil Water Conserv. 69, 471–482 (2014).Article 

    Google Scholar 
    Smith, P. et al. Greenhouse gas mitigation in agriculture. Philos. Trans. R. Soc. B 363, 789–813 (2008).CAS 
    Article 

    Google Scholar 
    Finney, D. M., White, C. M. & Kaye, J. P. Biomass production and carbon nitrogen ratio influence ecosystem services from cover crop mixtures. Agron. J. 108, 39–52 (2016).CAS 
    Article 

    Google Scholar 
    Drost, S. M., Rutgers, M., Wouterse, M., De Boer, W. & Bodelier, P. L. Decomposition of mixtures of cover crop residues increases microbial functional diversity. Geoderma 361, 114060 (2020).ADS 
    CAS 
    Article 

    Google Scholar 
    Thapa, V. R., Ghimire, R., Acosta-Martínez, V., Marsalis, M. A. & Schipanski, M. E. Cover crop biomass and species composition affect soil microbial community structure and enzyme activities in semi-arid cropping systems. Appl. Soil Ecol. 157, 103735 (2021).Article 

    Google Scholar 
    Muhammad, I. et al. Regulation of soil CO2 and N2O emissions by cover crops: A meta-analysis. Soil Till. Res. 192, 103–112 (2019).Article 

    Google Scholar 
    Sarkodie-Addo, J., Lee, H. C. & Baggs, E. M. Nitrous oxide emissions after application of inorganic fertilizer and incorporation of green manure residues. Soil Use Manage. 19, 331–339 (2006).Article 

    Google Scholar 
    Guardia, G. et al. Effect of cover crops on greenhouse gas emissions in an irrigated field under integrated soil fertility management. Biogeosciences 13, 5245–5257 (2016).ADS 
    CAS 
    Article 

    Google Scholar 
    Mitchell, D. C., Castellano, M. J., Sawyer, J. E. & Pantoja, J. Cover crop effects on nitrous oxide emissions: Role of mineralizable carbon. Soil Sci. Soc. Am. J. 77, 1765 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    Bodner, G., Mentler, A., Klik, A., Kaul, H. P. & Zechmeister-Boltenstern, S. Do cover crops enhance soil greenhouse gas losses during high emission moments under temperate Central Europe conditions? Die Bodenkult J. Land Manage. Food Environ. 68, 171–187 (2018).Article 
    CAS 

    Google Scholar 
    Álvaro-Fuentes, J., Easter, M. & Paustian, K. Climate change effects on organic carbon storage in agricultural soils of northeastern Spain. Agric. Ecosyst. Environ. 155, 87–94 (2012).Article 
    CAS 

    Google Scholar 
    Bronson, K. F. et al. Carbon and nitrogen pools of southern High Plains cropland and grassland soils. Soil Sci. Soc. Am. J. 68, 1695–1704 (2004).ADS 
    CAS 
    Article 

    Google Scholar 
    Zhou, X., Talley, M. & Luo, Y. Biomass, litter and soil respiration along a precipitation gradient in Southern Great Plains, USA. Ecosystems 12, 1369–1380 (2009).CAS 
    Article 

    Google Scholar 
    Poulter, B. et al. Contribution of semi-arid ecosystems to interannual variability of the global carbon cycle. Nature 509, 600–603 (2014).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Ahlström, A. et al. The dominant role of semi-arid ecosystems in the trend and variability of the land CO2 sink. Science 348, 895–899 (2015).ADS 
    PubMed 
    Article 
    CAS 

    Google Scholar 
    Huang, J., Yu, H., Guan, X., Wang, G. & Guo, R. Accelerated dryland expansion under climate change. Nat. Clim. Change 6, 166–171 (2016).ADS 
    Article 

    Google Scholar 
    Antosh, E., Idowu, J., Schutte, B. & Lehnhoff, E. Winter cover crops effects on soil properties and sweet corn yield in semi-arid irrigated systems. Agron. J. 112, 92–106 (2020).Article 

    Google Scholar 
    Paye, W. S. et al. Cover crop water use and corn silage production in semi-arid irrigated conditions. Agric. Water Manage. 260, 107275 (2022).Article 

    Google Scholar 
    Paye, W. S., Acharya, P. & Ghimire, R. Water productivity of forage sorghum in response to winter cover crops in semi-arid irrigated conditions. Field Crops Res. 283, 108552 (2022).Article 

    Google Scholar 
    Garba, I. I., Bell, L. W. & Williams, A. Cover crop legacy impacts on soil water and nitrogen dynamics, and on subsequent crop yields in drylands: A meta-analysis. Agron. Sustain. Dev. 42(3), 1–21 (2022).Article 
    CAS 

    Google Scholar 
    Gabriel, J. L., Muñoz-Carpena, R. & Quemada, M. The role of cover crops in irrigated systems: Water balance, nitrate leaching and soil mineral nitrogen accumulation. Agric. Ecosyst. Environ. 155, 50–61 (2012).CAS 
    Article 

    Google Scholar 
    Trost, B. et al. Irrigation, soil organic carbon and N2O emissions. A review. Agron. Sustain Dev. 33, 733–749 (2013).CAS 
    Article 

    Google Scholar 
    Nilahyane, A., Ghimire, R., Thapa, V. R. & Sainju, U. M. Cover crop effects on soil carbon dioxide emissions in a semiarid cropping system. Agrosyst. Geosci. Environ. 3, e20012 (2020).
    Google Scholar 
    Thapa, V. R., Ghimire, R., Duval, B. D. & Marsalis, M. A. Conservation systems for positive net ecosystem carbon balance in semi-arid drylands. Agrosyst. Geosci. Environ. 2, 1–8 (2019).Article 

    Google Scholar 
    Abdalla, M. et al. A critical review of the impacts of cover crops on nitrogen leaching, net greenhouse gas balance and crop productivity. Glob. Change Biol. 25(8), 2530–2543 (2019).ADS 
    Article 

    Google Scholar 
    Larionova, A. A., Sapronov, D. V., de Gerenyu, V. L., Kuznetsova, L. G. & Kudeyarov, V. N. Contribution of plant root respiration to the CO2 emission from soil. Eurasian Soil Sci. 39, 1127–1135 (2006).ADS 
    Article 

    Google Scholar 
    Hanson, P. J., Edwards, N. T., Garten, C. T. & Andrews, J. A. Separating root and soil microbial contributions to soil respiration: A review of methods and observations. Biogeochemistry 48, 115–146 (2000).CAS 
    Article 

    Google Scholar 
    Rochette, P., Flanagan, L. B. & Gregorich, E. G. Separating soil respiration into plant and soil components using analyses of the natural abundance of carbon-13. Soil Sci. Soc. Am. J. 63, 1207–1213 (1999).ADS 
    CAS 
    Article 

    Google Scholar 
    Sainju, U. M., Jabro, J. D. & Stevens, W. B. Soil carbon dioxide emission and carbon content as affected by irrigation, tillage, cropping system, and nitrogen fertilization. J. Environ. Qual. 37, 98–106 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    Mosier, A. R., Halvorson, A. D., Reule, C. A. & Liu, X. J. Net global warming potential and greenhouse gas intensity in irrigated cropping systems in northeastern Colorado. J. Environ. Qual. 35, 1584–1598 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    Fan, J. et al. Stover retention rather than no-till decreases the global warming potential of rainfed continuous maize cropland. Field Crops Res. 219, 14–23 (2018).Article 

    Google Scholar 
    USDA Soil Survey Staff. Web Soil Survey. http://websoilsurvey.sc.egov.usda.gov/App/WebSoilSurvey.aspx (2022). Accessed on 23 Jan 2022.Zibilske, L. M. Carbon mineralization. In Methods of Soil Analysis: Part 2. Microbiological and Biochemical Properties (eds Weaver, R. W. et al.). https://doi.org/10.2136/sssabookser5.2.c38 (Soil Science Society of America Journal, 1994).Chapter 

    Google Scholar 
    Sainju, U. M. Net global warming potential, and greenhouse gas intensity. Soil Sci. Soc. Am. J. 84, 1393–1404 (2020).ADS 
    CAS 
    Article 

    Google Scholar 
    Lal, R. Carbon emission from farm operations. Environ. Int. 30, 981–990 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    Haile-Mariam, S., Collins, H. P. & Higgins, S. S. Greenhouse gas fluxes from an irrigated sweet corn (Zea mays L.)–potato (Solanum tuberosum L.) rotation. J. Environ. Qual. 37(3), 759–771 (2008).CAS 
    PubMed 
    Article 

    Google Scholar  More

  • in

    Repatriation of a historical North Atlantic right whale habitat during an era of rapid climate change

    Descamps, S. et al. Diverging phenological responses of Arctic seabirds to an earlier spring. Glob. Change Biol. 25, 4081–4091 (2019).ADS 
    Article 

    Google Scholar 
    Ramp, C., Delarue, J., Palsbøll, P. J., Sears, R. & Hammond, P. S. Adapting to a warmer ocean—seasonal shift of baleen whale movements over three decades. PLoS ONE 10, e0121374 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Insley, S. J., Halliday, W. D., Mouy, X. & Diogou, N. Bowhead whales overwinter in the Amundsen Gulf and Eastern Beaufort Sea. R. Soc. Open Sci. 8, 1 (2021).Article 

    Google Scholar 
    Heide-Jørgensen, M. P., Laidre, K. L., Quakenbush, L. T. & Citta, J. J. The Northwest Passage opens for bowhead whales. Biol. Lett. 8, 270–273 (2012).PubMed 
    Article 

    Google Scholar 
    Durant, J., Hjermann, D., Ottersen, G. & Stenseth, N. Climate and the match or mismatch between predator requirements and resource availability. Clim. Res. 33, 271–283 (2007).Article 

    Google Scholar 
    Staudinger, M. D. et al. It’s about time: A synthesis of changing phenology in the Gulf of Maine ecosystem. Fish. Oceanogr. 28, 532–566 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Miller-Rushing, A. J., Høye, T. T., Inouye, D. W. & Post, E. The effects of phenological mismatches on demography. Philos. Trans. R. Soc. B Biol. Sci. 365, 3177–3186 (2010).Article 

    Google Scholar 
    Edwards, M. & Richardson, A. J. Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430, 881–884 (2004).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Record, N. et al. Rapid climate-driven circulation changes threaten conservation of endangered North Atlantic right whales. Oceanography 32, 1 (2019).Article 

    Google Scholar 
    MacLeod, C. Global climate change, range changes and potential implications for the conservation of marine cetaceans: a review and synthesis. Endanger. Species Res. 7, 125–136 (2009).Article 

    Google Scholar 
    Learmonth, J. A. et al. Potential effects of climate change on marine mammals. Oceanogr. Mar. Biol. Annu. Rev. 44, 431–464 (2006).
    Google Scholar 
    Pinsky, M. L., Worm, B., Fogarty, M. J., Sarmiento, J. L. & Levin, S. A. Marine taxa track local climate velocities. Science 341, 1239–1242 (2013).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Pershing, A. J. et al. Slow adaptation in the face of rapid warming leads to collapse of the Gulf of Maine cod fishery. Science 350, 809–812 (2015).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Gulf of Maine Research Institute. Gulf of Maine Warming Update: 2021 the Hottest Year on Record. (2022).Saba, V. S. et al. Enhanced warming of the Northwest Atlantic Ocean under climate change. J. Geophys. Res. Oceans 121, 118–132 (2016).ADS 
    Article 

    Google Scholar 
    Friedland, K. D. et al. Trends and change points in surface and bottom thermal environments of the US Northeast Continental Shelf Ecosystem. Fish. Oceanogr. 29, 396–414 (2020).Article 

    Google Scholar 
    Nye, J., Link, J., Hare, J. & Overholtz, W. Changing spatial distribution of fish stocks in relation to climate and population size on the Northeast United States continental shelf. Mar. Ecol. Prog. Ser. 393, 111–129 (2009).ADS 
    Article 

    Google Scholar 
    Kress, S. W., Shannon, P. & O’Neal, C. Recent changes in the diet and survival of Atlantic puffin chicks in the face of climate change and commercial fishing in midcoast Maine, USA. FACETS 1, 27–43 (2017).Article 

    Google Scholar 
    Davis, G. E. et al. Exploring movement patterns and changing distributions of baleen whales in the western North Atlantic using a decade of passive acoustic data. Glob. Change Biol. 26, 4812–4840 (2020).ADS 
    Article 

    Google Scholar 
    Pace, R. M., Corkeron, P. J. & Kraus, S. D. State-space mark-recapture estimates reveal a recent decline in abundance of North Atlantic right whales. Ecol. Evol. 7, 8730–8741 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Meyer-Gutbrod, E. L. & Greene, C. H. Uncertain recovery of the North Atlantic right whale in a changing ocean. Glob. Change Biol. 24, 455–464 (2018).ADS 
    Article 

    Google Scholar 
    Sorochan, K. A. et al. North Atlantic right whale (Eubalaena glacialis) and its food: (II) interannual variations in biomass of Calanus spp. on western North Atlantic shelves. J. Plankton Res. 41, 687–708 (2019).Article 

    Google Scholar 
    Friedland, K. D. et al. Spring bloom dynamics and zooplankton biomass response on the US Northeast Continental Shelf. Cont. Shelf Res. 102, 47–61 (2015).ADS 
    Article 

    Google Scholar 
    Meyer-Gutbrod, E., Greene, C., Davies, K. & Johns, D. Ocean regime shift is driving collapse of the North Atlantic right whale population. Oceanography 34, 22–31 (2021).Article 

    Google Scholar 
    Knowlton, A., Hamilton, P., Marx, M., Pettis, H. & Kraus, S. Monitoring North Atlantic right whale Eubalaena glacialis entanglement rates: A 30 yr retrospective. Mar. Ecol. Prog. Ser. 466, 293–302 (2012).ADS 
    Article 

    Google Scholar 
    Davies, K. T. A. & Brillant, S. W. Mass human-caused mortality spurs federal action to protect endangered North Atlantic right whales in Canada. Mar. Policy 104, 157–162 (2019).Article 

    Google Scholar 
    Kraus, S. D. & Rolland, R. M. Right whales in the urban ocean. in The urban whale: North Atlantic right whales at the crossroads 1–38 (Harvard University Press, 2010). https://doi.org/10.2307/j.ctv1pnc1q9.Winn, H. E., Price, C. A. & Sorensen, P. W. The distributional biology of the right whale (Eubalaena glacialis) in the western North Atlantic. Rep. Int. Whal. Comm. Spec. 10, 129–138 (1986).
    Google Scholar 
    Mayo, C. A. & Marx, M. K. Surface foraging behaviour of the North Atlantic right whale, Eubalaena glacialis, and associated zooplankton characteristics. Can. J. Zool. 68, 2214–2220 (1990).Article 

    Google Scholar 
    Mayo, C. A. et al. Distribution, demography, and behavior of North Atlantic right whales (Eubalaena glacialis) in Cape Cod Bay, Massachusetts, 1998–2013. Mar. Mammal Sci. 34, 979–996 (2018).Article 

    Google Scholar 
    Pendleton, D. E. et al. Regional-scale mean copepod concentration indicates relative abundance of North Atlantic right whales. Mar. Ecol. Prog. Ser. 378, 211–225 (2009).ADS 
    Article 

    Google Scholar 
    Kenney, R. D., Winn, H. E. & Macaulay, M. C. Cetaceans in the Great South Channel, 1979–1989: right whale (Eubalaena glacialis). Cont. Shelf Res. 15, 385–414 (1995).ADS 
    Article 

    Google Scholar 
    Brown, M. W. et al. Recovery strategy for the North Atlantic right whale (Eubalaena glacialis) in Atlantic Canadian waters. in Species at risk act recovery strategy series (Fisheries and Oceans Canada, 2009).Weinrich, M. T., Kenney, R. D. & Hamilton, P. K. Right whales (Eubalaena glacialis) on Jeffreys Ledge: a habitat of unrecognized importance?. Mar. Mammal Sci. 16, 326–337 (2000).Article 

    Google Scholar 
    Cole, T. et al. Evidence of a North Atlantic right whale Eubalaena glacialis mating ground. Endanger. Species Res. 21, 55–64 (2013).Article 

    Google Scholar 
    Ganley, L., Brault, S. & Mayo, C. What we see is not what there is: estimating North Atlantic right whale Eubalaena glacialis local abundance. Endanger. Species Res. 38, 101–113 (2019).Article 

    Google Scholar 
    Simard, Y., Roy, N., Giard, S. & Aulanier, F. North Atlantic right whale shift to the Gulf of St. Lawrence in 2015, revealed by long-term passive acoustics. Endanger. Species Res. 40, 271–284 (2019).Article 

    Google Scholar 
    Leiter, S. et al. North Atlantic right whale Eubalaena glacialis occurrence in offshore wind energy areas near Massachusetts and Rhode Island, USA. Endanger. Species Res. 34, 45–59 (2017).Article 

    Google Scholar 
    Stone, K. M. et al. Distribution and abundance of cetaceans in a wind energy development area offshore of Massachusetts and Rhode Island. J. Coast. Conserv. 21, 527–543 (2017).Article 

    Google Scholar 
    Vanderlaan, A., Taggart, C., Serdynska, A., Kenney, R. & Brown, M. Reducing the risk of lethal encounters: Vessels and right whales in the Bay of Fundy and on the Scotian Shelf. Endanger. Species Res. 4, 283–297 (2008).Article 

    Google Scholar 
    National Marine Fisheries Service. Endangered and threatened species; critical habitat for endangered North Atlantic right whale. Fed. Regist. 80, 9314–9345 (2015).
    Google Scholar 
    National Marine Fisheries Service. Taking of marine mammals incidental to commercial fishing operations; Atlantic large whale take reduction plan regulations; Atlantic coastal fisheries cooperative management act provisions; American lobster fishery. Fed. Regist. 85, 86878–86900 (2020).
    Google Scholar 
    Reeves, R. R., Breiwick, J. M. & Mitchell, E. D. History of whaling and estimated kill of right whales, Balaena glacialis, in the Northeastern United States, 1620–1924. Mar. Fish. Rev. 36, 1 (1999).
    Google Scholar 
    Allen, G. M. The whalebone whales of New England. Mem. Boston Soc. Nat. Hist. 8, 107–322 (1915).ADS 

    Google Scholar 
    CETAP (Cetacean and Turtle Assessment Program). A characterization of marine mammals and turtles in the mid- and North- Atlantic areas of the U.S. Outer Continental Shelf, final report. (1982).Kenney, R. D. & Vigness-Raposa, K. J. Marine mammals and sea turtles of Narragansett Bay, Block Island Sound, Rhode Island Sound, and nearby waters: An analysis of existing data for the Rhode Island Ocean Special Area Management Plan. in Rhode Island Ocean Special Area Management Plan; Volume 2 Appendix A: Technical Reports for the Rhode Island Ocean Special Area Management Plan. 701–1037 (Rhode Island Coastal Resources Management Council, Wakefield, RI, 2010).Pendleton, D. et al. Weekly predictions of North Atlantic right whale Eubalaena glacialis habitat reveal influence of prey abundance and seasonality of habitat preferences. Endanger. Species Res. 18, 147–161 (2012).MathSciNet 
    Article 

    Google Scholar 
    Kraus, S. D., Kenney, R. D. & Thomas, L. A framework for studying the effects of offshore wind development on marine mammals and turtles. (2019). Report prepared for the Massachusetts Clean Energy Center, Boston, MA, and the Bureau of Ocean Energy Management, Office of Renewable Energy Programs, Sterling, VA. Anderson Cabot Center for Ocean Life, New England Aquarium, Boston, MA. 48 pp.Quintana-Rizzo, E. et al. Residency, demographics, and movement patterns of North Atlantic right whales Eubalaena glacialis in an offshore wind energy development area in southern New England, USA. Endanger. Species Res. 45, 251–268 (2021).Article 

    Google Scholar 
    Taylor, J. K. D., Kenney, R. D., LeRoi, D. J. & Kraus, S. D. Automated vertical photography for detecting pelagic species in multitaxon aerial surveys. Mar. Technol. Soc. J. 48, 36–48 (2014).Article 

    Google Scholar 
    Hamilton, P. K., Knowlton, A. R. & Marx, M. K. Right whales tell their own stories: the photo-identification catalog. in The urban whale: North Atlantic right whales at the crossroads 75–104 (Harvard University Press, 2010).Buckland, S. T., Anderson, D. R., Burnham, K. P. & Laake, J. L. Distance sampling: Estimating abundance of biological populations Vol. 50 (Chapman and Hall, 1993).MATH 
    Book 

    Google Scholar 
    R: The R Project for Statistical Computing. https://www.r-project.org/.Miller, D. L., Rexstad, E., Thomas, L., Marshall, L. & Laake, J. L. Distance Sampling in R. J. Stat. Softw. 89, 1–28 (2019).Article 

    Google Scholar 
    Eberhardt, L. L., Chapman, D. G. & Gilbert, J. R. A review of marine mammal census methods. Wildl. Monogr. 1, 3–46 (1979).
    Google Scholar 
    Durant, S. M. et al. Long-term trends in carnivore abundance using distance sampling in Serengeti National Park, Tanzania: Serengeti carnivore trends. J. Appl. Ecol. 48, 1490–1500 (2011).Article 

    Google Scholar 
    Reeves, R. R. & Mitchell, E. The Long Island, New York, right whale fishery: 1650–1924. Rep. Int. Whal. Comm. 10, 201–220 (1986).
    Google Scholar 
    Davis, G. E. et al. Long-term passive acoustic recordings track the changing distribution of North Atlantic right whales (Eubalaena glacialis) from 2004 to 2014. Sci. Rep. 7, 13460 (2017).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Jackson, J. et al. Have whales returned to a historical hotspot of industrial whaling? The pattern of southern right whale Eubalaena australis recovery at South Georgia. Endanger. Species Res. 43, 323–339 (2020).Article 

    Google Scholar 
    Carroll, E. L. et al. Reestablishment of former wintering grounds by New Zealand southern right whales. Mar. Mammal Sci. 30, 206–220 (2014).Article 

    Google Scholar 
    Charlton, C. et al. Southern right whales (Eubalaena australis) return to a former wintering calving ground: Fowlers Bay, South Australia. Mar. Mammal Sci. 35, 1438–1462 (2019).Article 

    Google Scholar 
    Garrigue, C. et al. Searching for humpback whales in a historical whaling hotspot of the Coral Sea, South Pacific. Endanger. Species Res. 42, 67–82 (2020).Article 

    Google Scholar 
    Clapham, P. J., Aguilar, A. & Hatch, L. T. Determining spatial and temporal scales for management: lessons from whaling. Mar. Mammal Sci. 24, 183–201 (2008).Article 

    Google Scholar 
    Watkins, W. A. & Schevill, W. E. Right whale feeding and baleen rattle. J. Mammal. 57, 58–66 (1976).Article 

    Google Scholar 
    Beardsley, R. C. et al. Spatial variability in zooplankton abundance near feeding right whales in the Great South Channel.. Deep Sea Res Part II Top. Stud. Oceanogr. 43, 1601–1625 (1996).ADS 
    Article 

    Google Scholar 
    Wishner, K. F. et al. Copepod patches and right whales in the Great South Channel off New England. Bull. Mar. Sci. 43, 825–844 (1988).ADS 

    Google Scholar 
    Baumgartner, M., Cole, T., Clapham, P. & Mate, B. North Atlantic right whale habitat in the lower Bay of Fundy and on the SW Scotian Shelf during 1999–2001. Mar. Ecol. Prog. Ser. 264, 137–154 (2003).ADS 
    Article 

    Google Scholar 
    Moore, M. J. & van der Hoop, J. M. The painful side of trap and fixed net fisheries: Chronic entanglement of large whales. J. Mar. Biol. 2012, 1–4 (2012).Article 

    Google Scholar  More

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    Drivers and trends of global soil microbial carbon over two decades

    Predictors of microbial carbon stocksWe used a machine learning modeling approach to predict soil microbial carbon from a set of environmental covariates. To account for stochastic variability, we ran a set of models to assess the importance of environmental factors, which showed that the contribution of each variable to the model fit differed between runs, with some overlap between a number of them (Fig. 2b). Mean annual temperature was always the most important variable, with soil organic carbon and soil pH following. Clay content, precipitation, land-cover type, nitrogen content, and sand content contributed roughly equally to explaining variations in microbial carbon. Finally, NDVI and elevation had the lowest variable importance. Coniferous forests had the highest and most variable predicted values of microbial carbon (Supplementary Figs. 1, 2), which can be explained by high soil organic matter and a thick litter layer26. Tropical forests also had fairly high values of microbial carbon, while shrublands and croplands had the lowest values26. We used partial prediction response curves to evaluate the direction and range of effect of the predictor variables (Supplementary Figs. 1, 2). In agreement with the variable importance measure, variables that scored high often showed strong effects on the predicted microbial carbon values, while variables with a low variable importance score (e.g., elevation, NDVI, and sand content) only showed smaller responses. The only exception was for precipitation, which had a relatively high variable importance, although the response curves only showed a weak effect of precipitation for forests and grasslands, with limited effect on other land-cover types (Supplementary Fig. 2). The importance of precipitation might also indicate that this relationship involves interactions with other variables7,28. Overall, the differences in microbial carbon between land-cover types showed mostly similar patterns across the range of variables. Soil organic carbon and nitrogen content had a positive and mostly linear effect on microbial carbon (Supplementary Fig. 1). In contrast, clay content, soil pH, and mean temperature had non-linear relationships, with high microbial carbon in the low range of these variables and a rapid decrease that reached an asymptote at low microbial carbon values for the higher portion of the range. Soil pH patterns showed a decrease in microbial carbon for values between 4.1 and 5.8, and a constant pattern between 5.8 and 8.6. Contrary to our expectations, we did not find a parabolic effect of soil pH on microbial carbon26. Instead, our model predicted higher values in very acidic soils with a pH below 5.2, which are rare globally and almost only found in central Amazonia. Similarly, locations with a clay content lower than 16.9% had higher values in microbial carbon, and then stabilized until 51.0%.Fig. 2: Microbial carbon stock spatial predictions and temporal trends.a Microbial carbon stock predictions for 2013. b Variable importance from 100 random forest model runs, calculated by the mean decrease in accuracy after variable permutation. Variables were ordered by the median variable importance. SOC soil organic carbon, NDVI normalized difference vegetation index. Center line, median; box limits, upper and lower quartiles; whiskers, 1.5× interquartile range; points, outliers. c Relative microbial carbon stocks rate of change in percentage per year.Full size imageMean temperature showed an interesting shift with much higher microbial carbon values with a mean annual temperature below zero, but had otherwise a limited effect on microbial carbon values in the rest of the range above zero up to 28.9 °C. Based on partial predictions (Supplementary Figs. 1–2), microbial carbon decreased monotonically with an increase in temperature (with all other variables fixed to their median), with the relationship being mostly stable for parts of the range. We observed an especially sharp decrease at around 0°C, which is in agreement with the patterns observed in the data. The reason for sites with a mean annual temperature below the freezing point to have higher microbial carbon stocks is not fully understood. This could be due to a regime shift in which microbial communities are in a semi-dormant state for a major part of the year35. Moreover, it could also be in part explained by the soil organic carbon content that follows a similar trend and accumulates in higher latitude soils9, thus promoting higher microbial carbon stocks. Within these cold, high organic carbon soils, large microbial populations can be maintained, due to the low temperature that reduces metabolic requirements35. In contrast, at higher temperatures, metabolic activity increases and requires more resources and nutrients to maintain microorganisms alive. Experimental evidence is divided about the effects of warming on microbial carbon18,36, highlighting the strong context-dependency of this relationship, although global observations show a clear pattern, where low-temperature sites have higher soil microbial carbon stocks. Despite this uncertainty, there is a strong indication that a warming soil would tend to lose organic carbon17,37, and subsequent patterns in microbial carbon can also be expected, because of the dependency on organic substrate9,26,38. These dynamics were observed in Melillo et al.39, where the warming of sites in a mid-latitude forest ecosystem led to a decrease in soil carbon, followed by a decrease in microbial carbon12.Even with predictions being made for each grid location separately, microbial carbon values showed distinctive patterns and transitions over the globe (Fig. 2a). While temporal changes took place, broad spatial patterns were relatively constant over the range of years studied (Supplementary Movie 1). The highest microbial carbon stock values ranging from 1.50 to 7.00 t ha−1 were found at high latitudes in the Northern Hemisphere in areas of coniferous forest. Tropical humid regions also showed high microbial carbon values between 0.50 and 1.50 t ha−1 in the Amazon Rainforest and Central Africa. The main regions with low microbial carbon below 0.30 t ha−1 were in Eastern South America, areas directly south of the Sahara Desert, East Africa, and most of Australia, all of which mostly correspond to shrublands. Cropland areas as seen in India were also predicted with low microbial carbon values ranging from 0.06 to 0.38 t ha−1. A strong latitudinal gradient was visible for North America and Eurasia, with the highest microbial carbon stocks at high latitude, medium values in temperate ecosystems, and decreasing values towards the Equator. Positive coastal effects can also be observed, mostly on the Eastern South American and Australian coasts. In total, we estimated that there is 4.34 Gt of microbial carbon in the 5 to 15 cm layer for the predicted areas. Using the coefficient of variation calculated from the variability assessment set of models, we found that predictions made for the Amazon Basin, Northern Canada, and South-East Russia were more variable than for other regions (Supplementary Fig. 3a). Especially Western Europe, Central North America, and South-East Asia, however, showed high stability in the predictions between model runs.Drivers of changeThe analysis of the rate of change of microbial carbon stocks over time revealed that large regions of the globe experienced important changes in soil microbial carbon stocks between 1992 and 2013, with contrasting patterns across areas, and overall larger regions showed a decrease rather than an increase in microbial carbon stocks (Fig. 2c and Supplementary Fig. 3b). To account for spatial differences in microbial carbon stocks, we calculated the relative rate of change in percentage for each location (Fig. 2c). When considering all predictable regions together, microbial carbon stocks in the 5–15 cm layer showed a decrease of 7.09 Mt per year, summing to 148.80 Mt between 1992 and 2013, or 3.4% of the global microbial carbon pool predicted (Supplementary Fig. 4a; p = 0.038). The main regions with a microbial carbon loss higher than 0.7 kg ha−1 y−1 were in Northern Canada and a large continuous region in North-Eastern Europe. These northern regions accounted for an important part of the global loss in microbial carbon stocks, with large areas that had both a high soil microbial carbon stock and a fast decrease (Figs. 3 and 4). Other areas of high loss were in the Amazon basin, Western Argentina, the USA East Coast, Southern South Africa, and South-East Russia. The main continuous region of microbial carbon increase above 0.7 kg ha−1 y−1 was in central Russia, with smaller regions present in India, Europe, Central North America, and parts of Africa. Besides these general patterns, predictions vary at the local scale, and they consider the effects of parameters including soil properties, elevation, and land-cover type, which change between neighbor locations and affect the observed patterns. This is especially visible in the Americas, where both increases and decreases happen side-by-side.Fig. 3: Status of microbial carbon stocks between 1992 and 2013.Bivariate plot comparing the relative microbial carbon stock rate of change (% per year) with the amount of microbial carbon stock. The status groups were allocated using quantile distributions.Full size imageFig. 4: Distribution and classification of point values from the locations in Fig. 3.The assignment of points into the 9 groups was performed using quantile distributions. Areas in dark red are especially vulnerable to climate and land-cover change.Full size imagePatterns in the relative rate of change have a lot in common with that of absolute change, with a few notable differences (Fig. 2c and Supplementary Fig. 3b). Both positive and negative stock changes in tropical and subtropical regions are more prominent in relative terms, as these regions typically have low microbial carbon stocks. Similarly, regions in Central Russia with high microbial carbon stocks show less decrease in relative terms. To assess how stable these trends are over time, we show the p values of the rate of change for the 22 years (Supplementary Fig. 3c). The largest region with low p values is associated with more significant trends in Western Russia, and corresponds to an area with a fast loss of microbial carbon. India and Central Russia show high p values, and are informative of high variability compared to the strength of the signal. Considering that only up to 22 data points are available for each grid location and that especially climatic conditions vary considerably from year to year, p values are only provided as a complementary assessment. We can summarize the global situation by combining the two maps of microbial carbon stocks and relative rate of change to categorize and define vulnerable locations that experienced a high loss of microbial carbon (Figs. 3 and 4), and where the provision of soil functions is potentially at risk.It is informative to look at regional trends, by grouping grid locations using the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES) sub-regions, and assessing regional-scale changes in microbial carbon stocks (Fig. 5, Supplementary Table 1). The main regions that contributed to microbial carbon loss were North America with a decrease of 62.49 Mt of microbial carbon and Eastern Europe with 60.88 Mt over the studied period, although both trends had high yearly variability and were non-significant. The region with the highest increase was North-East Asia with a gain of 4.49 Mt, but this change was also non-significant. The Caribbean was the only region to show a significant increase in soil microbial carbon stocks over time (+2.1% over 22 y, p = 0.017), while significant decreases in stocks were found in North Africa (−4.1%, p  More

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    Resistance evolution can disrupt antibiotic exposure protection through competitive exclusion of the protective species

    Laxminarayan R, Duse A, Wattal C, Zaidi AKM, Wertheim HFL, Sumpradit N, et al. Antibiotic resistance—the need for global solutions. Lancet Infect Dis. 2013;13:1057–98.PubMed 
    Article 

    Google Scholar 
    Murray CJ, Ikuta KS, Sharara F, Swetschinski L, Robles Aguilar G, Gray A, et al. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet. 2022;399:629–55.CAS 
    Article 

    Google Scholar 
    O’Neil J. Antimicrobial resistance: tackling a crisis for the health and wealth of nations. The review on antimicrobial resistance. 2014. https://amr-review.org/sites/default/files/AMRReviewPaper-Tacklingacrisisforthehealthandwealthofnations_1.pdf.Pang Z, Raudonis R, Glick BR, Lin T-J, Cheng Z. Antibiotic resistance in Pseudomonas aeruginosa: mechanisms and alternative therapeutic strategies. Biotechnol Adv. 2019;37:177–92.CAS 
    PubMed 
    Article 

    Google Scholar 
    Vandeplassche E, Tavernier S, Coenye T, Crabbé A. Influence of the lung microbiome on antibiotic susceptibility of cystic fibrosis pathogens. Eur Respir Rev. 2019;28:190041.PubMed 
    Article 

    Google Scholar 
    Wheatley R, Diaz Caballero J, Kapel N, de Winter FHR, Jangir P, Quinn A, et al. Rapid evolution and host immunity drive the rise and fall of carbapenem resistance during an acute Pseudomonas aeruginosa infection. Nat Commun. 2021;12:2460.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Adamowicz EM, Flynn J, Hunter RC, Harcombe WR. Cross-feeding modulates antibiotic tolerance in bacterial communities. ISME J. 2018;12:2723–35.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Allison DG, Matthews MJ. Effect of polysaccharide interactions on antibiotic susceptibility of Pseudomonas aeruginosa. J Appl Bacteriol. 1992;73:484–8.CAS 
    PubMed 
    Article 

    Google Scholar 
    Beaudoin T, Yau YCW, Stapleton PJ, Gong Y, Wang PW, Guttman DS, et al. Staphylococcus aureus with Pseudomonas aeruginosa biofilm enhances tobramycin resistance. Npj Biofilms Microbiomes. 2017;3:25.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bottery MJ, Matthews JL, Wood AJ, Johansen HK, Pitchford JW, Friman V-P. Inter-species interactions alter antibiotic efficacy in bacterial communities. ISME J. 2022;16:812–21.CAS 
    PubMed 
    Article 

    Google Scholar 
    Elias S, Banin E. Multi-species biofilms: living with friendly neighbors. FEMS Microbiol Rev. 2012;36:990–1004.CAS 
    PubMed 
    Article 

    Google Scholar 
    Hoffman LR, Deziel E, D’Argenio DA, Lepine F, Emerson J, McNamara S, et al. Selection for Staphylococcus aureus small-colony variants due to growth in the presence of Pseudomonas aeruginosa. Proc Natl Acad Sci USA. 2006;103:19890–5.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Molina-Santiago C, Daddaoua A, Fillet S, Duque E, Ramos J-L. Interspecies signalling: Pseudomonas putida efflux pump TtgGHI is activated by indole to increase antibiotic resistance: Antibiotic resistance. Environ Microbiol. 2014;16:1267–81.CAS 
    PubMed 
    Article 

    Google Scholar 
    Orazi G, O’Toole GA. Pseudomonas aeruginosa alters Staphylococcus aureus sensitivity to vancomycin in a biofilm model of cystic fibrosis infection. mBio. 2017;8:e00873–17. https://doi.org/10.1128/mBio.00873-17.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Perlin MH, Clark DR, McKenzie C, Patel H, Jackson N, Kormanik C, et al. Protection of Salmonella by ampicillin-resistant Escherichia coli in the presence of otherwise lethal drug concentrations. Proc R Soc B Biol Sci. 2009;276:3759–68.CAS 
    Article 

    Google Scholar 
    Ryan RP, Fouhy Y, Garcia BF, Watt SA, Niehaus K, Yang L, et al. Interspecies signalling via the Stenotrophomonas maltophilia diffusible signal factor influences biofilm formation and polymyxin tolerance in Pseudomonas aeruginosa. Mol Microbiol. 2008;68:75–86.CAS 
    PubMed 
    Article 

    Google Scholar 
    Sherrard LJ, McGrath SJ, McIlreavey L, Hatch J, Wolfgang MC, Muhlebach MS, et al. Production of extended-spectrum β -lactamases and the potential indirect pathogenic role of Prevotella isolates from the cystic fibrosis respiratory microbiota. Int J Antimicrob Agents. 2016;47:140–5.CAS 
    PubMed 
    Article 

    Google Scholar 
    Tognon M, Köhler T, Gdaniec BG, Hao Y, Lam JS, Beaume M, et al. Co-evolution with Staphylococcus aureus leads to lipopolysaccharide alterations in Pseudomonas aeruginosa. ISME J. 2017;11:2233–43.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Adamowicz EM, Muza M, Chacón JM, Harcombe WR. Cross-feeding modulates the rate and mechanism of antibiotic resistance evolution in a model microbial community of Escherichia coli and Salmonella enterica. PLOS Pathog. 2020;16:e1008700.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bottery MJ, Pitchford JW, Friman V-P. Ecology and evolution of antimicrobial resistance in bacterial communities. ISME J. 2021;15:939–48.PubMed 
    Article 

    Google Scholar 
    Estrela S, Brown SP. Community interactions and spatial structure shape selection on antibiotic resistant lineages. PLOS Comput Biol. 2018;14:e1006179.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Klümper U, Recker M, Zhang L, Yin X, Zhang T, Buckling A, et al. Selection for antimicrobial resistance is reduced when embedded in a natural microbial community. ISME J. 2019;13:2927–37.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Scheuerl T, Hopkins M, Nowell RW, Rivett DW, Barraclough TG, Bell T. Bacterial adaptation is constrained in complex communities. Nat Commun. 2020;11:754.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Sorg RA, Lin L, van Doorn GS, Sorg M, Olson J, Nizet V, et al. Collective resistance in microbial communities by intracellular antibiotic deactivation. PLOS Biol. 2016;14:e2000631.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Kulczycki LL, Kostuch M, Bellanti JA. A clinical perspective of cystic fibrosis and new genetic findings: relationship of CFTR mutations to genotype-phenotype manifestations. Am J Med Genet. 2003;116A:262–7.PubMed 
    Article 

    Google Scholar 
    Flume PA, Mogayzel PJ, Robinson KA, Rosenblatt RL, Quittell L, Marshall BC. Cystic fibrosis pulmonary guidelines: pulmonary complications: hemoptysis and pneumothorax. Am J Respir Crit Care Med. 2010;182:298–306.PubMed 
    Article 

    Google Scholar 
    Belkin RA, Henig NR, Singer LG, Chaparro C, Rubenstein RC, Xie SX, et al. Risk factors for death of patients with cystic fibrosis awaiting lung transplantation. Am J Respir Crit Care Med. 2006;173:659–66.PubMed 
    Article 

    Google Scholar 
    Martin C, Hamard C, Kanaan R, Boussaud V, Grenet D, Abély M, et al. Causes of death in French cystic fibrosis patients: the need for improvement in transplantation referral strategies! J Cyst Fibros. 2016;15:204–12.PubMed 
    Article 

    Google Scholar 
    Döring G, Conway SP, Heijerman HGM, Hodson ME, Høiby N, Smyth A, et al. Antibiotic therapy against Pseudomonas aeruginosa in cystic fibrosis: a European consensus. Eur Respir J. 2000;16:749.PubMed 
    Article 

    Google Scholar 
    Marshall B, Faro A, Brown W, Elbert A, Fink A, Cromwell E, et al. Patient registry, annual data report. Bethesda, Maryland: Cystic Fibrosis Foundation; 2020. https://www.cff.org/sites/default/files/2021-11/Patient-Registry-Annual-Data-Report.pdf.Vongthilath R, Richaud Thiriez B, Dehillotte C, Lemonnier L, Guillien A, Degano B, et al. Clinical and microbiological characteristics of cystic fibrosis adults never colonized by Pseudomonas aeruginosa: analysis of the French CF registry. PLOS ONE. 2019;14:e0210201.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Zolin A, Orenti A, Jung A, van Rens J. ECFSPR annual report 2019. Denmark: European Cystic Fibrosis Society Patient Registry; 2021. https://www.ecfs.eu/sites/default/files/general-content-files/working-groups/ecfs-patient-registry/ECFSPR_Report_2019_v1_16Feb2022.pdf.Conrad D, Haynes M, Salamon P, Rainey PB, Youle M, Rohwer F. Cystic fibrosis therapy: a community ecology perspective. Am J Respir Cell Mol Biol. 2013;48:150–6.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Filkins LM, Graber JA, Olson DG, Dolben EL, Lynd LR, Bhuju S, et al. Coculture of Staphylococcus aureus with Pseudomonas aeruginosa drives S. aureus towards fermentative metabolism and reduced viability in a cystic fibrosis model. J Bacteriol. 2015;197:2252–64.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Zhao J, Schloss PD, Kalikin LM, Carmody LA, Foster BK, Petrosino JF, et al. Decade-long bacterial community dynamics in cystic fibrosis airways. Proc Natl Acad Sci USA. 2012;109:5809–14.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ballestero S, Vírseda I, Escobar H, Suárez L, Baquero F. Stenotrophomonas maltophilia in cystic fibrosis patients. Eur J Clin Microbiol Infect Dis. 1995;14:728–9.CAS 
    PubMed 
    Article 

    Google Scholar 
    Gladman G, Connor PJ, Williams RF, David TJ. Controlled study of Pseudomonas cepacia and Pseudomonas maltophilia in cystic fibrosis. Arch Dis Child. 1992;67:192–5.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Goss CH. Association between Stenotrophomonas maltophilia and lung function in cystic fibrosis. Thorax. 2004;59:955–9.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Parkins MD, Floto RA. Emerging bacterial pathogens and changing concepts of bacterial pathogenesis in cystic fibrosis. J Cyst Fibros. 2015;14:293–304.CAS 
    PubMed 
    Article 

    Google Scholar 
    Goss CH, Otto K, Aitken ML, Rubenfeld GD. Detecting Stenotrophomonas maltophilia does not reduce survival of patients with cystic fibrosis. Am J Respir Crit Care Med. 2002;166:356–61.PubMed 
    Article 

    Google Scholar 
    Alonso A, Martínez JL. Multiple antibiotic resistance in Stenotrophomonas maltophilia. Antimicrob Agents Chemother. 1997;41:1140–2.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Zhang L, Li XZ, Poole K. Multiple antibiotic resistance in Stenotrophomonas maltophilia: involvement of a multidrug efflux system. Antimicrob Agents Chemother. 2000;44:287–93.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Abda EM, Krysciak D, Krohn-Molt I, Mamat U, Schmeisser C, Förstner KU, et al. Phenotypic heterogeneity affects Stenotrophomonas maltophilia K279a colony morphotypes and β-lactamase expression. Front Microbiol. 2015;6:1373.Okazaki A, Avison MB. Induction of L1 and L2 β-lactamase production in Stenotrophomonas maltophilia is dependent on an AmpR-type regulator. Antimicrob Agents Chemother. 2008;52:1525–8.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Walsh TR, Hall L, Assinder SJ, Nichols WW, Cartwright SJ, MacGowan AP, et al. Sequence analysis of the L1 metallo-β-lactamase from Xanthomonas maltophilia. Biochim Biophys Acta. 1994;1218:199–201.CAS 
    PubMed 
    Article 

    Google Scholar 
    Yang Z, Liu W, Cui Q, Niu W, Li H, Zhao X, et al. Prevalence and detection of Stenotrophomonas maltophilia carrying metallo-I2-lactamase blaL1 in Beijing, China. Front Microbiol. 2014;5:692.Kataoka D, Fujiwara H, Kawakami T, Tanaka Y, Tanimoto A, Ikawa S, et al. The indirect pathogenicity of Stenotrophomonas maltophilia. Int J Antimicrob Agents. 2003;22:601–6.CAS 
    PubMed 
    Article 

    Google Scholar 
    Winstanley C, O’Brien S, Brockhurst MA. Pseudomonas aeruginosa evolutionary adaptation and diversification in cystic fibrosis chronic lung infections. Trends Microbiol. 2016;24:327–37.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    McGuigan L, Callaghan M. The evolving dynamics of the microbial community in the cystic fibrosis lung. Environ Microbiol. 2015;17:16–28.PubMed 
    Article 

    Google Scholar 
    Wistrand-Yuen E, Knopp M, Hjort K, Koskiniemi S, Berg OG, Andersson DI. Evolution of high-level resistance during low-level antibiotic exposure. Nat Commun. 2018;9:1599.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Mahrt N, Tietze A, Künzel S, Franzenburg S, Barbosa C, Jansen G, et al. Bottleneck size and selection level reproducibly impact evolution of antibiotic resistance. Nat Ecol Evol. 2021;5:1233–1242.Govaert L, Altermatt F, De Meester L, Leibold MA, McPeek MA, Pantel JH, et al. Integrating fundamental processes to understand eco‐evolutionary community dynamics and patterns. Funct Ecol. 2021;35:2138–55.Article 

    Google Scholar 
    Palmer KL, Aye LM, Whiteley M. Nutritional cues control Pseudomonas aeruginosa multicellular behavior in cystic fibrosis sputum. J Bacteriol. 2007;189:8079–87.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Souza Barbosa F, Capra Pezzi L, Tsao M, Oliveira TF, Manoela Dias Macedo S, Schapoval EES, et al. Stability and degradation products of imipenem applying High‐Resolution Mass Spectrometry: an analytical study focused on solutions for infusion. Biomed Chromatogr. 2018;33:4471.Verpooten G, Verbist L, Buntinx A, Entwistle L, Jones K, Broe M. The pharmacokinetics of imipenem (thienamycin-formamidine) and the renal dehydropeptidase inhibitor cilastatin sodium in normal subjects and patients with renal failure. Br J Clin Pharmacol. 1984;18:183–93.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Li H, Luo Y-F, Williams BJ, Blackwell TS, Xie C-M. Structure and function of OprD protein in Pseudomonas aeruginosa: from antibiotic resistance to novel therapies. Int J Med Microbiol. 2012;302:63–8.CAS 
    PubMed 
    Article 

    Google Scholar 
    Kousser C, Clark C, Sherrington S, Voelz K, Hall RA. Pseudomonas aeruginosa inhibits Rhizopus microsporus germination through sequestration of free environmental iron. Sci Rep. 2019;9:5714.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Schalk IJ, Guillon L. Pyoverdine biosynthesis and secretion in Pseudomonas aeruginosa: implications for metal homeostasis: pyoverdine biosynthesis. Environ Microbiol. 2013;15:1661–73.CAS 
    PubMed 
    Article 

    Google Scholar 
    Duan X, Pan Y, Cai Z, Liu Y, Zhang Y, Liu M, et al. rpoS-mutation variants are selected in Pseudomonas aeruginosa biofilms under imipenem pressure. Cell Biosci. 2021;11:138.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Zhu K, Chen S, Sysoeva TA, You L. Universal antibiotic tolerance arising from antibiotic-triggered accumulation of pyocyanin in Pseudomonas aeruginosa. PLOS Biol. 2019;17:e3000573.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    El-Fouly MZ, Sharaf AM, Shahin AAM, El-Bialy HA, Omara AMA. Biosynthesis of pyocyanin pigment by Pseudomonas aeruginosa. J Radiat Res Appl Sci. 2015;8:36–48.CAS 
    Article 

    Google Scholar 
    Baron SS, Rowe JJ. Antibiotic action of pyocyanin. Antimicrob Agents Chemother. 1981;20:814–20.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kimura M, Ohta T. The average number of generations until fixation of a mutant gene in a finite population. Genetics. 1969;61:763–71.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Meirelles LA, Perry EK, Bergkessel M, Newman DK. Bacterial defenses against a natural antibiotic promote collateral resilience to clinical antibiotics. PLOS Biol. 2021;19:e3001093.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hall JPJ, Harrison E, Brockhurst MA. Competitive species interactions constrain abiotic adaptation in a bacterial soil community. Evol Lett. 2018;2:580–9.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Scanlan PD, Hall AR, Blackshields G, Friman V-P, Davis MR, Goldberg JB, et al. Coevolution with bacteriophages drives genome-wide host evolution and constrains the acquisition of abiotic-beneficial mutations. Mol Biol Evol. 2015;32:1425–35.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Finkel SE. Long-term survival during stationary phase: evolution and the GASP phenotype. Nat Rev Microbiol. 2006;4:113–20.CAS 
    PubMed 
    Article 

    Google Scholar 
    Gefen O, Fridman O, Ronin I, Balaban NQ. Direct observation of single stationary-phase bacteria reveals a surprisingly long period of constant protein production activity. Proc Natl Acad Sci. 2014;111:556–61.CAS 
    PubMed 
    Article 

    Google Scholar 
    Fang Z, Zhang L, Huang Y, Qing Y, Cao K, Tian G, et al. OprD mutations and inactivation in imipenem-resistant Pseudomonas aeruginosa isolates from China. Infect Genet Evol. 2014;21:124–8.CAS 
    PubMed 
    Article 

    Google Scholar 
    Hirabayashi A, Kato D, Tomita Y, Iguchi M, Yamada K, Kouyama Y, et al. Risk factors for and role of OprD protein in increasing minimal inhibitory concentrations of carbapenems in clinical isolates of Pseudomonas aeruginosa. J Med Microbiol. 2017;66:1562–72.CAS 
    PubMed 
    Article 

    Google Scholar 
    Huang H, Jeanteur D, Pattus F, Hancock REW. Membrane topology and site-specific mutagenesis of Pseudomonas aeruginosa porin OprD. Mol Microbiol. 1995;16:931–41.CAS 
    PubMed 
    Article 

    Google Scholar 
    Fournier D, Richardot C, Müller E, Robert-Nicoud M, Llanes C, Plésiat P, et al. Complexity of resistance mechanisms to imipenem in intensive care unit strains of Pseudomonas aeruginosa. J Antimicrob Chemother. 2013;68:1772–80.CAS 
    PubMed 
    Article 

    Google Scholar 
    Kao C-Y, Chen S-S, Hung K-H, Wu H-M, Hsueh P-R, Yan J-J, et al. Overproduction of active efflux pump and variations of OprD dominate in imipenem-resistant Pseudomonas aeruginosa isolated from patients with bloodstream infections in Taiwan. BMC Microbiol. 2016;16:107.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Ocampo-Sosa AA, Cabot G, Rodríguez C, Roman E, Tubau F, Macia MD, et al. Alterations of OprD in carbapenem-intermediate and -susceptible strains of Pseudomonas aeruginosa isolated from patients with bacteremia in a Spanish multicenter study. Antimicrob Agents Chemother. 2012;56:1703–13.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Shu J-C, Kuo A-J, Su L-H, Liu T-P, Lee M-H, Su I-N, et al. Development of carbapenem resistance in Pseudomonas aeruginosa is associated with OprD polymorphisms, particularly the amino acid substitution at codon 170. J Antimicrob Chemother. 2017;72:2489–95.CAS 
    PubMed 
    Article 

    Google Scholar 
    Pernet E, Guillemot L, Burgel P-R, Martin C, Lambeau G, Sermet-Gaudelus I, et al. Pseudomonas aeruginosa eradicates Staphylococcus aureus by manipulating the host immunity. Nat Commun. 2014;5:5105.CAS 
    PubMed 
    Article 

    Google Scholar 
    Briaud P, Camus L, Bastien S, Doléans-Jordheim A, Vandenesch F, Moreau K. Coexistence with Pseudomonas aeruginosa alters Staphylococcus aureus transcriptome, antibiotic resistance and internalization into epithelial cells. Sci Rep. 2019;9:16564.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Khare A, Tavazoie S. Multifactorial competition and resistance in a two-species bacterial system. PLOS Genet. 2015;11:e1005715.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Mashburn LM, Jett AM, Akins DR, Whiteley M. Staphylococcus aureus serves as an iron source for Pseudomonas aeruginosa during in vivo coculture. J Bacteriol. 2005;187:554–66.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Cirz RT, O’Neill BM, Hammond JA, Head SR, Romesberg FE. Defining the Pseudomonas aeruginosa SOS response and its role in the global response to the antibiotic ciprofloxacin. J Bacteriol. 2006;188:7101–10.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    García-Contreras R, Nuñez-López L, Jasso-Chávez R, Kwan BW, Belmont JA, Rangel-Vega A, et al. Quorum sensing enhancement of the stress response promotes resistance to quorum quenching and prevents social cheating. ISME J. 2015;9:115–25.PubMed 
    Article 
    CAS 

    Google Scholar 
    Moradali MF, Ghods S, Rehm BHA. Pseudomonas aeruginosa lifestyle: a paradigm for adaptation, survival, and persistence. Front Cell Infect Microbiol 2017;7:39.Vogt SL, Green C, Stevens KM, Day B, Erickson DL, Woods DE, et al. The stringent response is essential for Pseudomonas aeruginosa virulence in the rat lung agar bead and Drosophila melanogaster feeding models of infection. Infect Immun. 2011;79:4094–104.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Baron SS, Terranova G, Rowe JJ. Molecular mechanism of the antimicrobial action of pyocyanin. Curr Microbiol. 1989;18:223–30.CAS 
    Article 

    Google Scholar 
    Castañeda-Tamez P, Ramírez-Peris J, Pérez-Velázquez J, Kuttler C, Jalalimanesh A, Saucedo-Mora MÁ, et al. Pyocyanin restricts social cheating in Pseudomonas aeruginosa. Front Microbiol. 2018;9:1348.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Fontoura R, Spada JC, Silveira ST, Tsai SM, Brandelli A. Purification and characterization of an antimicrobial peptide produced by Pseudomonas sp. strain 4B. World J Microbiol Biotechnol. 2009;25:205–13.CAS 
    Article 

    Google Scholar 
    Hassan HM, Fridovich I. Mechanism of the antibiotic action pyocyanine. J Bacteriol. 1980;141:156–63.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Machan ZA, Pitt TL, White W, Watson D, Taylor GW, Cole PJ, et al. Interaction between Pseudomonas aeruginosa and Staphylococcus aureus: description of an antistaphylococcal substance. J Med Microbiol. 1991;34:213–7.CAS 
    PubMed 
    Article 

    Google Scholar 
    Raji El Feghali PA, Nawas T. Pyocyanin: a powerful inhibitor of bacterial growth and biofilm formation. Madridge J Case Rep Stud. 2018;3:101–7.Article 

    Google Scholar 
    Saha S, Thavasi R, Jayalakshmi S. Phenazine pigments from Pseudomonas aeruginosa and their application as antibacterial agent and food colourants. Res J Microbiol. 2008;3:122–8.CAS 
    Article 

    Google Scholar 
    Schiessl KT, Hu F, Jo J, Nazia SZ, Wang B, Price-Whelan A, et al. Phenazine production promotes antibiotic tolerance and metabolic heterogeneity in Pseudomonas aeruginosa biofilms. Nat Commun. 2019;10:762.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Jagmann N, Brachvogel H-P, Philipp B. Parasitic growth of Pseudomonas aeruginosa in co-culture with the chitinolytic bacterium Aeromonas hydrophila: parasitic growth of Pseudomonas aeruginosa. Environ Microbiol. 2010;12:1787–802.CAS 
    PubMed 
    Article 

    Google Scholar 
    Noto MJ, Burns WJ, Beavers WN, Skaar EP. Mechanisms of pyocyanin toxicity and genetic determinants of resistance in Staphylococcus aureus. J Bacteriol. 2017;199:00221–17.Venkataraman A, Rosenbaum MA, Perkins SD, Werner JJ, Angenent LT. Metabolite-based mutualism between Pseudomonas aeruginosa PA14 and Enterobacter aerogenes enhances current generation in bioelectrochemical systems. Energy Environ Sci. 2011;4:4550.CAS 
    Article 

    Google Scholar 
    Waite RD, Qureshi MR, Whiley RA. Modulation of behaviour and virulence of a high alginate expressing Pseudomonas aeruginosa strain from cystic fibrosis by oral commensal bacterium Streptococcus anginosus. PLOS ONE. 2017;12:e0173741.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Whooley MA, McLoughlin AJ. The regulation of pyocyanin production in Pseudomonas aeruginosa. Eur J Appl Microbiol Biotechnol. 1982;15:161–6.CAS 
    Article 

    Google Scholar 
    Elbargisy RM. Optimization of nutritional and environmental conditions for pyocyanin production by urine isolates of Pseudomonas aeruginosa. Saudi J Biol Sci. 2021;28:993–1000.CAS 
    PubMed 
    Article 

    Google Scholar 
    Gupta S, Laskar N, Kadouri DE. Evaluating the effect of oxygen concentrations on antibiotic sensitivity, growth, and biofilm formation of human pathogens. Microbiol Insights. 2016;9. https://doi.org/10.4137/MBI.S40767.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Worlitzsch D, Tarran R, Ulrich M, Schwab U, Cekici A, Meyer KC, et al. Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J Clin Investig. 2002;109:317–25.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Skurnik D, Roux D, Cattoir V, Danilchanka O, Lu X, Yoder-Himes DR, et al. Enhanced in vivo fitness of carbapenem-resistant oprD mutants of Pseudomonas aeruginosa revealed through high-throughput sequencing. Proc Natl Acad Sci USA. 2013;110:20747–52.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Higgins S, Heeb S, Rampioni G, Fletcher MP, Williams P, Cámara M. Differential regulation of the phenazine biosynthetic operons by quorum sensing in Pseudomonas aeruginosa PAO1-N. Front Cell Infect Microbiol. 2018;8:252.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Dragoš A, Martin M, Falcón García C, Kricks L, Pausch P, Heimerl T, et al. Collapse of genetic division of labour and evolution of autonomy in pellicle biofilms. Nat Microbiol. 2018;3:1451–60.PubMed 
    Article 
    CAS 

    Google Scholar 
    Cuthbertson L, Walker AW, Oliver AE, Rogers GB, Rivett DW, Hampton TH, et al. Lung function and microbiota diversity in cystic fibrosis. Microbiome. 2020;8:45.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rogers GB, Carroll MP, Serisier DJ, Hockey PM, Jones G, Bruce KD. Characterization of bacterial community diversity in cystic fibrosis lung infections by use of 16S ribosomal DNA terminal restriction fragment length polymorphism profiling. J Clin Microbiol. 2004;42:5176–83.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Workentine ML, Sibley CD, Glezerson B, Purighalla S, Norgaard-Gron JC, Parkins MD, et al. Phenotypic heterogeneity of Pseudomonas aeruginosa populations in a cystic fibrosis patient. PLoS ONE. 2013;8:e60225.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Valdezate S. Persistence and variability of Stenotrophomonas maltophilia in cystic fibrosis patients, Madrid, 1991-8. Emerg Infect Dis. 2001;7:113–22.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Dalbøge CS, Hansen CR, Pressler T, Høiby N, Johansen HK. Chronic pulmonary infection with Stenotrophomonas maltophilia and lung function in patients with cystic fibrosis. J Cyst Fibros. 2011;10:318–25.PubMed 
    Article 

    Google Scholar 
    Jeon YD, Jeong WY, Kim MH, Jung IY, Ahn MY, Ann HW, et al. Risk factors for mortality in patients with Stenotrophomonas maltophilia bacteremia. Medicine. 2016;95:e4375.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Sherrard LJ, Tunney MM, Elborn JS. Antimicrobial resistance in the respiratory microbiota of people with cystic fibrosis. Lancet Lond Engl. 2014;384:703–13.CAS 
    Article 

    Google Scholar 
    Choi K-H, Schweizer HP. Mini-Tn7 insertion in bacteria with single attTn7 sites: example Pseudomonas aeruginosa. Nat Protoc. 2006;1:153–61.CAS 
    PubMed 
    Article 

    Google Scholar 
    Jelsbak L, Johansen HK, Frost A-L, Thøgersen R, Thomsen LE, Ciofu O, et al. Molecular epidemiology and dynamics of Pseudomonas aeruginosa populations in lungs of cystic fibrosis patients. Infect Immun. 2007;75:2214–24.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Yeung ATY, Parayno A, Hancock REW. Mucin promotes rapid surface motility in Pseudomonas aeruginosa. mBio. 2012;3:300073–12.Kirchner S, Fothergill JL, Wright EA, James CE, Mowat E, Winstanley C. Use of artificial sputum medium to test antibiotic efficacy against Pseudomonas aeruginosa in conditions more relevant to the cystic fibrosis lung. J Vis Exp. 2012;64:3857.Hill DB, Long RF, Kissner WJ, Atieh E, Garbarine IC, Markovetz MR, et al. Pathological mucus and impaired mucus clearance in cystic fibrosis patients result from increased concentration, not altered pH. Eur Respir J. 2018;52:1801297.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Benoni G, Cuzzolin L, Bertrand C, Puchetti V, Velo G. Imipenem kinetics in serum, lung tissue and pericardial fluid in patients undergoing thoracotomy. J Antimicrob Chemother. 1987;20:725–8.CAS 
    PubMed 
    Article 

    Google Scholar 
    Radhakrishnan M, Jaganath A, Rao GSU, Kumari HBV. Nebulized imipenem to control nosocomial pneumonia caused by Pseudomonas aeruginosa. J Crit Care. 2008;23:148–50.CAS 
    PubMed 
    Article 

    Google Scholar 
    Wenzler E, Fraidenburg DR, Scardina T, Danziger LH. Inhaled antibiotics for gram-negative respiratory infections. Clin Microbiol Rev. 2016;29:581–632.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    The European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters.Version 12.0, 2022. http://www.eucast.org.Kang D, Revtovich AV, Chen Q, Shah KN, Cannon CL, Kirienko NV. Pyoverdine-dependent virulence of Pseudomonas aeruginosa isolates from cystic fibrosis patients. Front Microbiol. 2019;10:2048.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Martin LW, Reid DW, Sharples KJ, Lamont IL. Pseudomonas siderophores in the sputum of patients with cystic fibrosis. BioMetals. 2011;24:1059–67.CAS 
    PubMed 
    Article 

    Google Scholar 
    Caldwell CC, Chen Y, Goetzmann HS, Hao Y, Borchers MT, Hassett DJ, et al. Pseudomonas aeruginosa exotoxin pyocyanin causes cystic fibrosis airway pathogenesis. Am J Pathol. 2009;175:2473–88.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    O’Loughlin CT, Miller LC, Siryaporn A, Drescher K, Semmelhack MF, Bassler BL. A quorum-sensing inhibitor blocks Pseudomonas aeruginosa virulence and biofilm formation. Proc Natl Acad Sci USA. 2013;110:17981–6.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Sass G, Nazik H, Penner J, Shah H, Ansari SR, Clemons KV, et al. Studies of Pseudomonas aeruginosa mutants indicate pyoverdine as the central factor in inhibition of Aspergillus fumigatus biofilm. J Bacteriol. 2018;200:00345–17.Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19:455–77.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30:2068–9.CAS 
    PubMed 
    Article 

    Google Scholar 
    Deatherage DE, Barrick JE. Identification of mutations in laboratory-evolved microbes from next-generation sequencing data using breseq. In: Sun L, Shou W, editors. Engineering and Analyzing Multicellular Systems. New York, NY: Springer New York; 2014. p. 165–88.Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, et al. Integrative genomics viewer. Nat Biotechnol. 2011;29:24–6.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Thorvaldsdottir H, Robinson JT, Mesirov JP. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform. 2013;14:178–92.CAS 
    PubMed 
    Article 

    Google Scholar  More

  • in

    Clearance and persistence of Escherichia coli in the freshwater mussel Unio mancus

    Galvani, A. P., Bauch, C. T., Anand, M., Singer, B. H. & Levin, S. A. Human–environment interactions in population and ecosystem health. Proc. Natl. Acad. Sci. U. S. A. 113, 14502–14506 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    WHO Director-General. Health, environment and climate change. Draft WHO global strategy on health, environment and climate change: The transformation needed to improve lives and well-being sustainably through healthy environments. vol. 18 https://apps.who.int/gb/ebwha/pdf_files/WHA72/A72_15-en.pdf?ua=1 (2019).Queenan, K., Häsler, B. & Rushton, J. A One Health approach to antimicrobial resistance surveillance: Is there a business case for it?. Int. J. Antimicrob. Agents 48, 422–427 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Aslam, B. et al. Antibiotic resistance: A rundown of a global crisis. Infect. Drug Resist. 11, 1645–1658 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Walsh, T. R. A one-health approach to antimicrobial resistance. Nat. Microbiol. 3, 854–855 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Taylor, L. H., Latham, S. M. & Woolhouse, M. E. J. Risk factors for human disease emergence. Philos. Trans. R. Soc. B Biol. Sci. 356, 983–989 (2001).CAS 
    Article 

    Google Scholar 
    Kruse, H., Kirkemo, A. M. & Handeland, K. Wildlife as source of zoonotic infections. Emerg. Infect. Dis. 10, 2067–2072 (2004).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Evans, T. et al. Links between ecological integrity, emerging infectious diseases and other aspects of human health—An overview of the literature. https://wcs.org (2020).Rabinowitz, P. M., Cullen, M. R. & Lake, H. R. Wildlife as sentinels for human health hazards: A review of study designs. J. Environ. Med. 1, 217–223 (1999).Article 

    Google Scholar 
    Rabinowitz, P. M. et al. Animals as sentinels of human environmental health hazards: An evidence-based analysis. EcoHealth 2, 26–37 (2005).Article 

    Google Scholar 
    Fox, G. A. Wildlife as sentinels of human health effects in the Great Lakes-St. Lawrence basin. Environ. Health Perspect. 109, 853–861 (2001).PubMed 
    PubMed Central 

    Google Scholar 
    Burket, S. R. et al. Corbicula fluminea rapidly accumulate pharmaceuticals from an effluent dependent urban stream. Chemosphere 224, 873–883 (2019).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Ricciardi, A. & Rasmussen, J. B. Extinction rates of North American freshwater fauna. Conserv. Biol. 13, 1220–1222 (1999).Article 

    Google Scholar 
    Ismail, N. S. et al. Improvement of urban lake water quality by removal of Escherichia coli through the action of the bivalve Anodonta californiensis. Environ. Sci. Technol. 49, 1664–1672 (2015).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Ismail, N. S., Tommerdahl, J. P., Boehm, A. B. & Luthy, R. G. Escherichia coli reduction by bivalves in an impaired river impacted by agricultural land use. Environ. Sci. Technol. 50, 11025–11033 (2016).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Burge, C. A. et al. The use of filter-feeders to manage disease in a changing world. Integr. Comp. Biol. 56, 573–587 (2016).PubMed 
    Article 

    Google Scholar 
    Aceves, A. K., Johnson, P., Bullard, S. A., Lafrentz, S. & Arias, C. R. Description and characterization of the digestive gland microbiome in the freshwater mussel Villosa nebulosa (Bivalvia: Unionidae). J. Molluscan Stud. 84, 240–246 (2018).Article 

    Google Scholar 
    Gu, J. D. & Mitchell, R. Indigenous microflora and opportunistic pathogens of the freshwater zebra mussel, Dreissena polymorpha. Hydrobiologia 474, 81–90 (2002).Article 

    Google Scholar 
    Gomes, J. F. et al. Biofiltration using C. fluminea for E. coli removal from water: Comparison with ozonation and photocatalytic oxidation. Chemosphere 208, 674–681 (2018).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Burkhardt, W. & Calci, K. R. Selective accumulation may account for shellfish-associated viral illness. Appl. Environ. Microbiol. 66, 1375–1378 (2000).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Huyvaert, K. P. et al. Freshwater clams as bioconcentrators of avian influenza virus in water. Vector-Borne Zoonotic Dis. 12, 904–906 (2012).PubMed 
    Article 

    Google Scholar 
    Le Guyader, F. S. et al. Norwalk virus-specific binding to oyster digestive tissues. Emerg. Infect. Dis. 12, 931–936 (2006).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Palos Ladeiro, M., Aubert, D., Villena, I., Geffard, A. & Bigot, A. Bioaccumulation of human waterborne protozoa by zebra mussel (Dreissena polymorpha): Interest for water biomonitoring. Water Res. 48, 148–155 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    Palos Ladeiro, M., Bigot-Clivot, A., Aubert, D., Villena, I. & Geffard, A. Assessment of Toxoplasma gondii levels in zebra mussel (Dreissena polymorpha) by real-time PCR: An organotropism study. Environ. Sci. Pollut. Res. 22, 13693–13701 (2015).CAS 
    Article 

    Google Scholar 
    Mezzanotte, V. et al. Removal of enteric viruses and Escherichia coli from municipal treated effluent by zebra mussels. Sci. Total Environ. 539, 395–400 (2016).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Cope, W. G. et al. Differential exposure, duration, and sensitivity of unionoidean bivalve life stages to environmental contaminants. J. N. Am. Benthol. Soc. 27, 451–462 (2008).Article 

    Google Scholar 
    Diamond, J. M., Bressler, D. W. & Serveiss, V. B. Assessing relationships between human land uses and the decline of native mussels, fish, and macroinvertebrates in the Clinch and Powell river watershed, USA. Environ. Toxicol. Chem. 21, 1147–1155 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    Augspurger, T., Dwyer, F. J., Ingersoll, C. G. & Kane, C. M. Advances and opportunities in assessing contaminant sensitivity of freshwater mussel (Unionidae) early life stages. Environ. Toxicol. Chem. 26, 2025–2028 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    Lopes-Lima, M. & Seddon, M. B. Unio mancus. The IUCN Red List of Threatened Species 2014: e. T22737A42466471 (2014). https://doi.org/10.2305/IUCN.UK.2014-3.RLTS.T22737A42466471.en.Lydeard, C. et al. The global decline of nonmarine mollusks. Bioscience 54, 321–330 (2004).Article 

    Google Scholar 
    Strayer, D. L. et al. Changing perspectives on pearly Mussels, North America’s most imperiled. Animals 54, 429–439 (2004).
    Google Scholar 
    Araujo, R. et al. The naiads of the Iberian Peninsula. Iberus 27, 7–72 (2009).
    Google Scholar 
    Araujo, R. et al. Who wins in the weaning process? Juvenile feeding morphology of two freshwater mussel species. J. Morphol. 279, 4–16 (2018).PubMed 
    Article 

    Google Scholar 
    Hinzmann, M., Bessa, L. J., Teixeira, A., Da Costa, P. M. & Machado, J. Antimicrobial and antibiofilm activity of unionid mussels from the North of Portugal. J. Shellfish Res. 37, 121–129 (2018).Article 

    Google Scholar 
    Mo, C. & Neilson, B. Standardization of oyster soft tissue dry weight measurements. Water Res. 28, 243–246 (1994).CAS 
    Article 

    Google Scholar 
    Kryger, J. & Riisgård, H. U. Filtration rate capacities in 6 species of European freshwater bivalves. Oecologia 77, 34–38 (1988).ADS 
    PubMed 
    Article 

    Google Scholar 
    Ostrovsky, I., Gophen, M. & Kalikhman, I. Distribution, growth, production, and ecological significance of the clam Unio terminalis in Lake Kinneret, Israel. Hydrobiologia 271, 49–63 (1993).Article 

    Google Scholar 
    Møhlenberg, F. & Riisgård, H. U. Efficiency of particle retention in 13 species of suspension feeding bivalves. Ophelia 17, 239–246 (1978).Article 

    Google Scholar 
    Møhlenberg, F. & Riisgård, H. U. Filtration rate, using a new indirect technique, in thirteen species of suspension-feeding bivalves. Mar. Biol. 54, 143–147 (1979).Article 

    Google Scholar 
    Riisgård, H. U. On measurement of filtration rates in bivalves—The stony road to reliable data: Review and interpretation. Mar. Ecol. Prog. Ser. 211, 275–291 (2001).ADS 
    Article 

    Google Scholar 
    Mills, S. C. & Reynolds, J. D. Mussel ventilation rates as a proximate cue for host selection by bitterling, Rhodeus sericeus. Oecologia 131, 473–478 (2002).ADS 
    PubMed 
    Article 

    Google Scholar 
    Filgueira, R., Labarta, U. & Fernández-Reiriz, M. J. Effect of condition index on allometric relationships of clearance rate in Mytilus galloprovincialis Lamarck, 1819. Rev. Biol. Mar. Oceanogr. 43, 391–398 (2008).Article 

    Google Scholar 
    Silverman, H., Achberger, E. C., Lynn, J. W. & Dietz, T. H. Filtration and utilization of laboratory-cultured bacteria by Dreissena polymorpha, Corbicula fluminea, and Carunculina texasensis. Biol. Bull. 189, 308–319 (1995).CAS 
    PubMed 
    Article 

    Google Scholar 
    Maki, J. S., Patel, G. & Mitchell, R. Experimental pathogenicity of Aeromonas spp. for the Zebra mussel, Dreissena polymorpha. Curr. Microbiol. 36, 19–23 (1998).CAS 
    PubMed 
    Article 

    Google Scholar 
    Love, D. C., Lovelace, G. L. & Sobsey, M. D. Removal of Escherichia coli, Enterococcus fecalis, coliphage MS2, poliovirus, and hepatitis A virus from oysters (Crassostrea virginica) and hard shell clams (Mercinaria mercinaria) by depuration. Int. J. Food Microbiol. 143, 211–217 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    de Mesquita, M. M. F., Evison, L. M. & West, P. A. Removal of faecal indicator bacteria and bacteriophages from the common mussel (Mytilus edulis) under artificial depuration conditions. J. Appl. Bacteriol. 70, 495–501 (1991).PubMed 
    Article 

    Google Scholar  More

  • in

    Assessment of Eurasian lynx reintroduction success and mortality risk in north-west Poland

    Sunquist, M. E. & Sunquist, F. C. Family Felidae. In Handbook of the Mammals of the World Vol. 1 (eds Wilson, D. E. & Mittermeier, R. A.) 54–170 (Lynx Editions, 2009).
    Google Scholar 
    Breitenmoser, U. et al. Action plan for the conservation of the Eurasian Lynx (Lynx lynx) in Europe. Nat. Environ. 112, 1–70 (2000).
    Google Scholar 
    Linnell, J. D. C., Breitenmoser, U., Breitenmoser-Würsten, C., Odden, J. & von Arx, M. Recovery of Eurasian lynx in Europe: What part has reintroduction played? In Reintroduction of Top-Order Predators (eds Hayward, M. W. & Somers, M. J.) 72–91 (Blackwell Publishing, 2009).Chapter 

    Google Scholar 
    Schmidt, K., Ratkiewicz, M. & Konopiński, M. K. The importance of genetic variability and population differentiation in the Eurasian lynx Lynx lynx for conservation, in the context of habitat and climate change. Mammal Rev. 41, 112–124 (2011).Article 

    Google Scholar 
    von Arx, M. et al. Status and conservation of the Eurasian lynx (Lynx lynx) in Europe in 2001. KORA Bericht 19, 1–330 (2004).
    Google Scholar 
    Kaczensky, P. et al. Status, management and distribution of large carnivores—Bear, lynx, wolf and wolverine in Europe. Part 1 – Europe summaries. Report: 1–72. A Large Carnivore Initiative for Europe Report prepared for the European Commission (2013).Chapron, G. et al. Recovery of large carnivores in Europe’s modern human-dominated landscapes. Science 346, 1517–1519 (2014).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Franz, K. W. & Romanowski, J. Revisiting the reintroduced Eurasian lynx population in Kampinos National Park Poland. Eur. Zool. J. 88, 966–979. https://doi.org/10.1080/24750263.2021.1968046 (2021).Article 

    Google Scholar 
    Bieniek, M., Wolsan, M. & Okarma, H. Historical biogeography of the lynx in Poland. Acta Zool. Cracov. 41, 143–167 (1998).
    Google Scholar 
    Jędrzejewski, W., Nowak, S., Schmidt, K. & Jędrzejewska, B. Wilk i ryś w Polsce: Wyniki inwentaryzacji w 2001 roku. Kosmos 51, 491–499 (2002).
    Google Scholar 
    Mysłajek, R., Kwiatkowska, I., Diserens, T., Haidt, A. & Nowak, S. Occurrence of Eurasian lynx in western Poland after two decades of strict protection. CATnews 69, 12–13 (2019).
    Google Scholar 
    Schmidt, K. Program ochrony rysia Lynx lynx w Polsce – Project. Strategia ochrony Rysia Warunkująca Trwałość Populacji Gatunku w Polsce (Warsaw University of Life Sciences, 2011).
    Google Scholar 
    Kaczensky, P. et al. Status, management and distribution of large carnivores—Bear, lynx, wolf and wolverine in Europe. Part 2: Country Species Summaries. Report: 1–200. A Large Carnivore Initiative for Europe Report prepared for the European Commission (2013).Breitenmoser, U. et al. Lynx lynx (errata version published in 2017). The IUCN Red List of Threatened Species 2015: e.T12519A121707666. Accessed 30 Oct 2021 (2015).Vandel, J.-M., Stahl, P., Herrenschmidt, V. & Marboutin, E. Reintroduction of the lynx into the Vosges mountain massif: From animal survival and movements to population development. Biol. Conserv. 131, 370–385. https://doi.org/10.1016/j.biocon.2006.02.012 (2006).Article 

    Google Scholar 
    Zimmermann, F., Breitenmoser-Würsten, C. & Breitenmoser, U. Importance of dispersal for the expansion of a Eurasian lynx Lynx lynx population in a fragmented landscape. Oryx 41, 358–368. https://doi.org/10.1017/s0030605307000712 (2007).Article 

    Google Scholar 
    Schmidt, K., Kowalczyk, R., Ozolins, J., Mannil, P. & Fickel, J. Genetic structure of the Eurasian lynx population in north-eastern Poland and the Baltic states. Conserv. Genet. 10, 497–501. https://doi.org/10.1007/s10592-008-9795-7 (2009).Article 

    Google Scholar 
    Ratkiewicz, M. et al. Long-range gene flow and the effects of climatic and ecological factors on genetic structuring in a large, solitary carnivore: The Eurasian Lynx. PLoS ONE 9, e115160. https://doi.org/10.1371/journal.pone.0115160 (2014).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Port, M. et al. Rise and fall of a Eurasian lynx (Lynx lynx) stepping-stone population in central Germany. Mammal Res. https://doi.org/10.1007/s13364-020-00527-6 (2020).Article 

    Google Scholar 
    Drouilly, M. & O’Riain, J. M. Rewilding the world’s large carnivores without neglecting the human dimension: A response to reintroducing the Eurasian lynx to southern Scotland, England and Wales. Biodivers. Conserv. 30, 917–923. https://doi.org/10.1007/s10531-021-02112-y (2021).Article 

    Google Scholar 
    Böer, M., Smielowski, J. & Tyrala, P. Reintroduction of the European lynx (Lynx lynx) to the Kampinoski National Park/Poland field experiment with zooborn individuals. Part I: Selection, adaptation and training. Der Zool. Garten 70, 304–312 (1994).
    Google Scholar 
    Jakimiuk, S. (ed.). Aktywna ochrona populacji nizinnej rysia w Polsce. 1–144 (WWF, Poland, 2015).Huck, M. et al. Habitat suitability, corridors and dispersal barriers for large carnivores in Poland. Acta Theriol. 55, 177–192 (2010).Article 

    Google Scholar 
    Niedziałkowska, M. et al. Environmental correlates of Eurasian lynx occurrence in Poland: Large scale census and GIS mapping. Biol. Conserv. 133, 63–69. https://doi.org/10.1016/j.biocon.2006.05.022 (2006).Article 

    Google Scholar 
    Schmidt, K., Kowalczyk, R., Ozolins, J., Männil, P. & Fickel, J. Genetic structure of the Eurasian lynx population in north-eastern Poland and the Baltic states. Conserv. Genet. 10, 497–501. https://doi.org/10.1007/s10592-008-9795-7 (2009).Article 

    Google Scholar 
    Tracz, M. et al. The return of lynx to northwestern Poland. CATnews 14, 43–44 (2021).
    Google Scholar 
    The Return of Lynx to north-west Poland. http://www.rysie.org/en/rysie-strona-glowna. Accessed on 31 Oct 2021.IUCN/SSC. Guidelines for Reintroductions and Other Conservation Translocations. Version 1.0. 1–57 (IUCN Species Survival Commission, 2013).Rueda, C., Jiménez, J., Palacios, M. J. & Margalida, A. Exploratory and territorial behavior in a reintroduced population of Iberian lynx. Sci. Rep. 11, 14148. https://doi.org/10.1038/s41598-021-93673-z (2021).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gusset, M. A framework for evaluating reintroduction success in carnivores: Lessons from African wild dogs. In Reintroduction of Top-Order Predators (eds Hayward, M. W. & Somers, M. J.) 307–320 (Blackwell Publishing, 2009).Chapter 

    Google Scholar 
    Breitenmoser, U. & Haller, H. Patterns of predation by reintroduced European Lynx in the Swiss Alps. J. Wildl. Manage. 57, 135–144 (1993).Article 

    Google Scholar 
    Drouilly, M. & O’Riain, M. J. Rewilding the world’s large carnivores without neglecting the human dimension. Biodivers. Conserv. 30, 917–923 (2021).Article 

    Google Scholar 
    Jędrzejewski, W. et al. Population dynamics (1869–1994), demography, and home ranges of the Lynx in Białowieza Primeval Forest (Poland and Belarus). Ecography 19, 122–138 (1996).Article 

    Google Scholar 
    Palmero, S. et al. Demography of a Eurasian lynx (Lynx lynx) population within a strictly protected area in Central Europe. Sci. Rep. 11, 19868. https://doi.org/10.1038/s41598-021-99337-2 (2021).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Maran, T., Põdra, M., Põlma, M. & Macdonald, D. The survival of captive-born animals in restoration programmes: Case study of the endangered European mink Mustela lutreola. Biol. Conserv. 142, 1685–1692 (2009).Article 

    Google Scholar 
    Moehrenschlager, A. & Macdonald, D. W. Movement and survival parameters of translocated and resident swift foxes Vulpes velox. Anim. Conserv. 6, 199–206 (2003).Article 

    Google Scholar 
    Böer, M., Reklewski, J., Śmiełowski, J. & Tyrała, P. Reintroduction of the European Lynx to the Kampinoski Nationalpark/Poland: A field experiment with zooborn individuals. Part III: Demographic development of the population from December 1993 until January 2000. Der Zool. Garten 70, 304–312 (2000).
    Google Scholar 
    Jule, K. R., Leaver, L. A. & Lea, E. G. L. The effects of captive experience on reintroduction survival in carnivores: A review and analysis. Biol. Conserv. 141, 355–363 (2008).Article 

    Google Scholar 
    Hellstedt, P. & Kallio, E. R. Survival and behaviour of captive-born weasels (Mustela nivalis nivalis) released in nature. J. Zool. 266, 37–44 (2005).Article 

    Google Scholar 
    Devineau, O. et al. Evaluating the Canada lynx reintroduction programme in Colorado: Patterns in mortality. J. Appl. Ecol. 47, 524–531 (2010).Article 

    Google Scholar 
    Lengger, J., Breitenmoser, U. & Sliwa, A. EAZA breeding programmes as sources for lynx reintroductions. CATnews 14, 76–77 (2021).
    Google Scholar 
    Reading, P. R. & Clark, T. W. Carnivore introductions: An interdisciplinary Examination. In Carnivore Behavior, Ecology and Evolution (ed. Gittleman, J. L.) 296–336 (Cornell University Press, 1996).
    Google Scholar 
    McCarthy, M. A., Armstrong, D. P. & Runge, M. C. Adaptive management of reintroduction. In Reintroduction Biology: Integrating Science and Management (eds Ewen, J. G. et al.) 256–289 (Wiley-Blackwell, 2012).Chapter 

    Google Scholar 
    Bremner-Harrison, S., Prodohl, P. A. & Elwood, R. W. Behavioural trait assessment as a release criterion: Boldness predicts early death in a reintroduction programme of captive-bred swift fox (Vulpes velox). Anim. Conserv. 7, 313–320 (2004).Article 

    Google Scholar 
    Harrington, L., Põdra, M., Macdonald, D. & Maran, T. Post-release movements of captive-born European mink Mustela lutreola. Endanger. Species Res. 24, 137–148 (2014).Article 

    Google Scholar 
    Andrén, H. et al. Survival rates and causes of mortality in Eurasian lynx (Lynx lynx) in multi-use landscapes. Biol. Conserv. 131, 23–32 (2006).Article 

    Google Scholar 
    Heurich, M. et al. Illegal hunting as a major driver of the source-sink dynamics of a reintroduced lynx population in Central Europe. Biol. Conserv. 224, 355–365 (2018).Article 

    Google Scholar 
    Schmidt-Posthaus, H., Breitenmoser, Ch., Posthaus, H., Bacciarini, L. & Breitenmoser, U. Causes of mortality in reintroduced Eurasian lynx in Switzerland. J. Wildl. Dis. 38, 84–92 (2002).PubMed 
    Article 

    Google Scholar 
    Kołodziej-Sobocińska, M., Zalewski, A. & Kowalczyk, R. Sarcoptic mange vulnerability in carnivores of the Białowieża Primeval Forest, Poland: underlying determinant factors. Ecol. Res. 29, 237–244 (2014).Article 

    Google Scholar 
    Holt, G. & Berg, C. Sarcoptic mange in red fox and other wild carnivores in Norway. Nor Veterinaertidsskr 102, 427–432 (1990).
    Google Scholar 
    Mörner, T. Sarcoptic mange in Swedish wildlife. Rev. Sci. Tech. Off. Int. Epiz. 11, 1115–1121 (1992).Article 

    Google Scholar 
    Ryser-Degiorgis, M. P. et al. Notoedric and sarcoptic mange in free-ranging lynx from Switzerland. J. Wildl. Dis. 38, 228–232 (2002).PubMed 
    Article 

    Google Scholar 
    Soulsbury, C. D. et al. The impact of sarcoptic mange Sarcoptes scabiei on the British fox Vulpes vulpes population. Mam. Rev. 37, 278–296 (2007).
    Google Scholar 
    Garrote, G., Fernández-López, J., López, G., Ruiz, G. & Simón, M. A. Prediction of Iberian lynx road–mortality in southern Spain: A new approach using the MaxEnt algorithm. Anim. Biodivers. Conserv. 41, 217–225 (2018).Article 

    Google Scholar 
    Bencin, H., Prange, S., Rose, Ch. & Popescu, V. Roadkill and space use data predict vehicle-strike hotspots and mortality rates in a recovering bobcat (Lynx rufus) population. Sci. Rep. 9, 15391 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Bouyer, Y. et al. Tolerance to anthropogenic disturbance by a large carnivore: The case of Eurasian lynx in south-eastern Norway. Anim. Conserv. https://doi.org/10.1111/acv.12168 (2014).Article 

    Google Scholar 
    López-Bao, J. V. et al. Eurasian lynx fitness shows little variation across Scandinavian human-dominated landscapes. Sci. Rep. 9, 8903 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Cimatti, M. et al. Large carnivore expansion in Europe is associated with human population density and land cover changes. Divers. Distrib. 27, 602–617 (2021).Article 

    Google Scholar 
    Wegner, M. (ed.). Statistical Yearbook of Zachodniopomorskie Voivodship. 1–213 (Statistical Office in Szczecin, 2020).Górny, M., Schmidt, K. & Kowalczyk, R. Analiza przydatności środowiska dla reintrodukcji rysia w północno-zachodniej Polsce oraz prognoza i perspektywy funkcjonowania populacji. Expert study under the project POIS.02.04.00–0143/16 “Return of the lynx to northwestern Poland”. 1–25.Woodford, M. H., Keet, D. F. & Bengis, R. G. Post-mortem Procedures for Wildlife Veterinarians and Field Biologists. 1–55 (IUCN Species Survival Commission (SSC) & Veterinary Specialist Group, Care for the Wild International, World Organisation for Animal Health (OIE), 2000).Fain, A. Ѐtude de la variabilitѐ de Sarcoptes scabiei avec une rѐvision des Sarcoptidae. Acta Zool. Pathol. Antverp 47, 1–196 (1968).
    Google Scholar 
    Kaplan, E. L. & Meier, P. Nonparametric estimation from incomplete observations. J. Am. Stat. Assoc. 53, 457–481 (2012).MathSciNet 
    MATH 
    Article 

    Google Scholar 
    Therneau, M., Lumley, T., Atkinson, E. & Crowson, C. Survival Analysis. R Package Version 3.2-13. http://CRAN.R-project.org/package=survival (2021).Kassambara, A., Kosinski, M., Biecek, P. & Scheipl, F. survminer. Drawing Survival Curves using ‘ggplot2’. R package version 0.4.9. http://CRAN.R-project.org/package=survminer (2021).Dardis, C. survMisc. Miscellaneous Functions for Survival Data. R package version 0.5.5. http://CRAN.R-project.org/package=survMisc (2018).R Core Team. R: A language and environment for statistical computing (R Foundation for Statistical Computing). https://www.R-project.org (2021).Snedecor, G. W. & Cochran, W. G. Statistical Methods 7th edn. (Iowa State University Press, 1980).MATH 

    Google Scholar 
    Cox, D. R. Regression models and life tables (with discussion). J. R. Stat. Soc. B. 34, 187–220 (1972).MATH 

    Google Scholar 
    Bradburn, M. J., Clark, T. G., Love, S. B. & Altman, D. G. Survival Analysis Part II: Multivariate data analysis: An introduction to concepts and methods. Br. J. Cancer. 89, 431–436 (2003).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Wald, A. Tests of statistical hypothesis concerning several parameters when the number of observations is large. Trans. Am. Math. Soc. 54, 426–482 (1943).MATH 
    Article 

    Google Scholar 
    Aitchison, J. & Silvey, S. D. Maximum likelihood estimation of parameters subject to restraints. Ann. Math. Stat. 29, 813–828 (1958).MathSciNet 
    MATH 
    Article 

    Google Scholar 
    Mantel, N. Evaluation of survival data and two new rank order statistics arising in its consideration. Cancer Chemother. Rep. 50, 163–170 (1966).CAS 
    PubMed 

    Google Scholar  More

  • in

    STEM learning communities promote friendships but risk academic segmentation

    Xie, Y., Fang, M. & Shauman, K. STEM education. Annu. Rev. Sociol. 41, 331–357 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Chen, X. STEM attrition: College students’ paths into and out of STEM fields. National Center for Education Statistics. Retrieved from http://ies.ed.gov/pubsearch/pubsinfo.asp?pubid=2014001rev. Accessed 22 September 2021.Huang G, Taddese N, Walter E (2000) Entry and persistence of women and minorities in college science and engineering education. National Center for Education Statistics. Retrieved from https://eric.ed.gov/?id=ED566411. Accessed 22 September 2021.Hurtado, S., Eagan, K., & Chang, M. Degrees of Success: Bachelor’s Degree Completion Rates among Initial STEM Majors (Higher Education Research Institute, Los Angeles, CA) (2010).National Science Foundation, Broadening Participation Working Group (2014) Pathways to broadening participation in response to the CEOSE 2011–2012 recommendation. National Science Foundation. Retrieved from https://www.nsf.gov/pubs/2015/nsf15037/nsf15037.pdf. Accessed 22 Sep 2021.James, S. M. & Singer, S. R. From the NSF: The National Science Foundation’s investments in broadening participation in science, technology, engineering, and mathematics education through research and capacity building. CBE Life Sci. Educ. 15(3), 1–8 (2016).Article 

    Google Scholar 
    Smith, B. L., MacGregor, J., Matthews, R. & Gabelnick, F. Learning communities: Reforming undergraduate education (Jossey-Bass, 2004).
    Google Scholar 
    Andrade, M. S. Learning communities: Examining positive outcomes. J. Coll. Stud. Ret. 9(1), 1–20 (2007).Article 

    Google Scholar 
    Maton, K. I., Pollard, S. A., McDougall Weise, T. V. & Hrabowski, F. A. Meyerhoff Scholars Program: A strengths-based, institution-wide approach to increasing diversity in science, technology, engineering, and mathematics. Mt Sinai J. Med. 79(5), 610–623 (2012).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Dagley, M., Georgiopoulos, M., Reece, A. & Young, C. Increasing retention and graduation rates through a STEM learning community. J. Coll. Stud. Ret. 18(2), 167–182 (2016).Article 

    Google Scholar 
    National Survey of Student Engagement (2015) Engagement Insights: Survey Findings on the Quality of Undergraduate Education—Annual Results 2015 (Bloomington, IN).Tinto, V. Leaving college: Rethinking the causes and cures of student attrition (University of Chicago Press, 1987).
    Google Scholar 
    Tinto, V. Learning better together: The impact of learning communities on student success. Higher Educ. Monogr. Ser. 1(8), 1–8 (2003).
    Google Scholar 
    Otto, S., Evins, M. A., Boyer-Pennington, M. & Brinthaupt, T. M. Learning communities in higher education: Best practices. Journal of Student Success and Retention 2(1), 1–20 (2015).
    Google Scholar 
    Boda, Z., Elmer, T., Vörös, A. & Stadtfeld, C. Short-term and long-term effects of a social network intervention on friendships among university students. Sci. Rep. 10(1), 1–2 (2020).Article 
    CAS 

    Google Scholar 
    Hotchkiss, J. L., Moore, R. E. & Pitts, M. M. Freshman learning communities, college performance, and retention. Educ. Econ. 14(2), 197–210 (2006).Article 

    Google Scholar 
    Whalen, D. F. & Shelley, M. C. Academic success for STEM and non-STEM majors. J. STEM Educ. 11(1), 45–60 (2010).
    Google Scholar 
    Xu, D., Solanki, S., McPartlan, P. & Sato, B. EASEing students into college: The impact of multidimensional support for underprepared students. Educ. Res. 47(7), 435–450 (2018).Article 

    Google Scholar 
    Jaffee, D., Carle, A., Phillips, R. & Paltoo, L. Intended and unintended consequences of first-year learning communities: An initial investigation. J. First-Year Exp. Stud. Trans. 20(1), 53–70 (2008).
    Google Scholar 
    Tinto, V. & Goodsell, A. Freshman interest groups and the first-year experience: Constructing student communities in a large university. J. First Year Exp. Stud. Trans. 6(1), 7–28 (1994).
    Google Scholar 
    Domizi, D. Student perceptions about their informal learning experiences in a first-year residential learning community. J. First Year Exp. Stud. Transit. 20(1), 97–110 (2008).
    Google Scholar 
    Lee, D. S. & Lemieux, T. Regression discontinuity designs in economics. J. Econ. Lit. 2, 281–355 (2010).Article 

    Google Scholar 
    Jacob, R., Zhu, P., Somers, M.A., & Bloom, H. A Practical Guide to Regression Discontinuity (MDRC, New York, NY, 2012).Hays, R. B. & Oxley, D. Social network development and functioning during a life transition. J. Pers. Soc. Psychol. 50(2), 305–313 (1986).CAS 
    PubMed 
    Article 

    Google Scholar 
    Freeman, T. M., Anderman, L. H. & Jensen, J. M. Sense of belonging in college freshmen at the classroom and campus levels. J. Exp. Educ. 75(3), 203–220 (2007).Article 

    Google Scholar 
    Zumbrunn, S., McKim, C., Buhs, E. & Hawley, L. R. Support, belonging, motivation, and engagement in the college classroom: A mixed method study. Instr. Sci. 42(5), 661–684 (2014).Article 

    Google Scholar 
    Hasan, S. & Bagde, S. The mechanics of social capital and academic performance in an Indian college. Am. Sociol. Rev. 78(6), 1009–1032 (2013).Article 

    Google Scholar 
    Stadtfeld, C., Vörös, A., Elmer, T., Boda, Z. & Raabe, I. J. Integration in emerging social networks explains academic failure and success. Proc. Natl. Acad. Sci. USA 116(3), 792–797 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Kraemer, B. A. The academic and social integration of Hispanic students into college. Rev. High Educ. 20(2), 163–179 (1997).Article 

    Google Scholar 
    Nora, A. Two-year colleges and minority students’ educational aspirations: Help or hindrance. Higher Educ. Handb. Theory Res. 9(3), 212–247 (1993).
    Google Scholar 
    McCabe, J.M. Connecting in College: How Friendship Networks Matter for Academic and Social Success (University of Chicago Press, Chicago, IL, 2016).Felten, P., & Lambert, L. M. Relationship-rich Education: How Human Connections Drive Success in College (Johns Hopkins University Press, Baltimore, MD, 2020).Hallinan, M. T. The peer influence process. Stud. Educ. Eval. 7(3), 285–306 (1981).Article 

    Google Scholar 
    Thomas, S. L. Ties that bind: A social network approach to understanding student integration and persistence. J. Higher Educ. 71(5), 591–615 (2000).
    Google Scholar 
    Turetsky, K. M., Purdie-Greenaway, V., Cook, J. E., Curley, J. P. & Cohen, G. L. A psychological intervention strengthens students’ peer social networks and promotes persistence in STEM. Sci. Adv. 6(45), 1–10 (2020).Article 

    Google Scholar 
    Dokuka, S., Valeeva, D. & Yudkevich, M. How academic achievement spreads: The role of distinct social networks in academic performance diffusion. PLoS ONE 15(7), 1–16 (2020).Article 
    CAS 

    Google Scholar 
    Epstein, J. L. & Karweit, N. (eds) Friends in school: Patterns of selection and influence in secondary schools (Academic Press, 1983).
    Google Scholar 
    Feld, S. L. The focused organization of social ties. AJS 86(5), 1015–1035 (1981).
    Google Scholar 
    Rivera, M. T., Soderstrom, S. B. & Uzzi, B. Dynamics of dyads in social networks: Assortative, relational, and proximity mechanisms. Annu. Rev. Sociol. 36, 91–115 (2010).Article 

    Google Scholar 
    Mollenhorst, G., Volker, B. & Flap, H. Changes in personal relationships: How social contexts affect the emergence and discontinuation of relationships. Soc. Netw. 37, 65–80 (2014).Article 

    Google Scholar 
    Thomas, R. J. Sources of friendship and structurally induced homophily across the life course. Sociol Perspect 62(6), 822–843 (2019).Article 

    Google Scholar 
    Kubitschek, W. N. & Hallinan, M. T. Tracking and students’ friendships. Soc. Psychol. Q 46, 1–5 (1998).Article 

    Google Scholar 
    Frank, K. A., Muller, C. & Mueller, A. S. The embeddedness of adolescent friendship nominations: The formation of social capital in emergent network structures. AJS 119(1), 216–253 (2013).PubMed 
    PubMed Central 

    Google Scholar 
    Kossinets, G. & Watts, D. J. Origins of homophily in an evolving social network. AJS 115(2), 405–450 (2009).
    Google Scholar 
    Wimmer, A. & Lewis, K. Beyond and below racial homophily: ERG models of a friendship network documented on Facebook. AJS 116(2), 583–642 (2010).PubMed 

    Google Scholar 
    Hallinan, M. T. & Sørensen, A. B. Ability grouping and student friendships. Am. Educ. Res. J. 51, 485–499 (1985).Article 

    Google Scholar 
    Leszczensky, L. & Pink, S. Ethnic segregation of friendship networks in school: Testing a rational-choice argument of differences in ethnic homophily between classroom-and grade-level networks. Soc. Netw. 42, 18–26 (2015).Article 

    Google Scholar 
    DiMaggio, P. & Garip, F. Network effects and social inequality. Annu. Rev. Sociol. 54, 93–118 (2012).Article 

    Google Scholar 
    Johnson, A. M. ‘“I can turn it on when i need to”’: Pre-college Integration, culture, and peer academic engagement among black and Latino/a engineering Students. Sociol. Educ. 56, 1–20 (2019).Article 

    Google Scholar 
    Perry, B. L., Pescosolido, B. A. & Borgatti, S. P. Egocentric network analysis: Foundations, methods, and models (Cambridge University Press, 2018).Book 

    Google Scholar 
    Wasserman, S. & Faust, K. Social network analysis: Methods and applications (Cambridge University Press, 1994).MATH 
    Book 

    Google Scholar 
    Hartup, W. W. & Stevens, N. Friendships and adaptation in the life course. Psychol. Bull. 121(3), 355 (1997).Article 

    Google Scholar 
    Vaquera, E. & Kao, G. Do you like me as much as I like you? Friendship reciprocity and its effects on school outcomes among adolescents. Soc. Sci. Res. 37(1), 55–72 (2008).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Imbens, G. W. & Lemieux, T. Regression discontinuity designs: A guide to practice. J. Econom. 142(2), 615–635 (2008).MathSciNet 
    MATH 
    Article 

    Google Scholar 
    Imbens, G. W. & Angrist, J. D. Identification and estimation of local average treatment effects. Econometrica 62(2), 467–475 (1994).MATH 
    Article 

    Google Scholar 
    Robins, G., Pattison, P., Kalish, Y. & Lusher, D. An introduction to exponential random graph (p*) models for social networks. Soc. Netw. 29(2), 173–191 (2007).Article 

    Google Scholar 
    Handcock, M. S., Hunter, D. R., Butts, C. T., Goodreau, S. M. & Morris, M. Statnet: Software tools for the representation, visualization, analysis and simulation of network data. J. Stat. Softw. 24(1), 1548–7660 (2008).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Calonico, S., Cattaneo, M. D. & Titiunik, R. Optimal data-driven regression discontinuity plots. J. Am. Stat. Assoc. 110(512), 1753–1769 (2015).MathSciNet 
    CAS 
    MATH 
    Article 

    Google Scholar 
    Duxbury, S. W. The problem of scaling in exponential random graph models. Sociol. Methods Res. https://doi.org/10.1177/0049124120986178:1-39 (2021).MathSciNet 
    Article 

    Google Scholar 
    McPherson, M., Smith-Lovin, L. & Cook, J. M. Birds of a feather: Homophily in social networks. Annu. Rev. Sociol. 27(1), 415–444 (2001).Article 

    Google Scholar 
    Kadushin, C. Understanding social networks: Theories, concepts, and findings (Oxford University Press, 2012).
    Google Scholar 
    Flashman, J. Academic achievement and its impact on friend dynamics. Sociol. Educ. 85(1), 61–80 (2012).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Carrell, S. E., Sacerdote, B. I. & West, J. E. From natural variation to optimal policy? The importance of endogenous peer group formation. Econometrica 81(3), 855–882 (2013).MathSciNet 
    MATH 
    Article 

    Google Scholar 
    Cox, A. B. Cohorts, ‘“siblings”,’ and mentors: Organizational structures and the creation of social capital. Sociol. Educ. 90(1), 47–63 (2017).Article 

    Google Scholar 
    Valente, T. W. Network interventions. Science 337(6090), 49–53 (2012).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Nunn, L. M. College belonging: How first-year and first-generation students navigate campus life (Rutgers University Press, 2021).Book 

    Google Scholar 
    Garlick, R. Academic peer effects with different group assignment policies: Residential tracking versus random assignment. Am. Econ. J. Appl. Econ. 10(3), 345–369 (2018).Article 

    Google Scholar 
    Carrell, S. E., Fullerton, R. L. & West, J. E. Does your cohort matter? Measuring peer effects in college achievement. J. Labor. Econ. 27(3), 439–464 (2009).Article 

    Google Scholar 
    Lomi, A., Snijders, T. A., Steglich, C. E. & Torló, V. J. Why are some more peer than others? Evidence from a longitudinal study of social networks and individual academic performance. Soc. Sci. Res. 40(6), 1506–1520 (2011).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Poldin, O., Valeeva, D. & Yudkevich, M. Which peers matter: How social ties affect peer-group effects. Res. High Educ. 57(4), 448–468 (2016).Article 

    Google Scholar 
    Raabe, I. J., Boda, Z. & Stadtfeld, C. The social pipeline: How friend influence and peer exposure widen the STEM gender gap. Sociol. Educ. 92(2), 105–123 (2019).Article 

    Google Scholar 
    Burt, R. S. Structural holes and good ideas. AJS 110(2), 349–399 (2004).
    Google Scholar 
    Oakes, J. Keeping track: How schools structure inequality (Yale University Press, 2005).
    Google Scholar 
    Park JJ et al. (2021) Who are you studying with? The role of diverse friendships in STEM and corresponding inequality. Res. High Educ. https://doi.org/10.1007/s11162-021-09638-8.Marsden, P. V. & Campbell, K. E. Measuring tie strength. Soc. Forces 63(2), 482–501 (1984).Article 

    Google Scholar 
    Mattie, H., Engø-Monsen, K., Ling, R. & Onnela, J. P. Understanding tie strength in social networks using a local “bow tie” framework. Sci. Rep. 8(1), 1–9 (2018).CAS 
    Article 

    Google Scholar 
    Sørensen, A. B. Organizational differentiation of students and educational opportunity. Sociol. Educ. 43(4), 355–376 (1970).Article 

    Google Scholar  More

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    Himalayas: create an international peace park

    After the successful protection of Himalayan areas on the border of China and Nepal, we propose that the two nations should create the world’s highest international peace park by combining the Qomolangma and Sagarmatha national parks. This would align with United Nations Sustainable Development Goal 17, to achieve sustainable development through international cooperation (see go.nature.com/3ixmini).
    Competing Interests
    The authors declare no competing interests. More