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    Prokaryotic responses to a warm temperature anomaly in northeast subarctic Pacific waters

    1.Collins, M. et al. SPM6 Extremes, abrupt changes and managing risks. In: IPCC Special Report on the Ocean and Cryosphere in a Changing Climate (eds. Pörtner, H.-O. et al.) 589-655 (In press, 2019).2.Hegerl, G. C., Hanlon, H. & Beierkuhnlein, C. Elusive extremes. Nat. Geosci. 4, 142–143 (2011).CAS 
    Article 

    Google Scholar 
    3.Bérard, A., Ben Sassi, M., Renault, P. & Gros, R. Severe drought-induced community tolerance to heat wave. An experimental study on soil microbial processes. J. Soils Sediment. 12, 513–518 (2012).Article 

    Google Scholar 
    4.Schimel, J., Balser, T. C. & Wallenstein, M. Microbial stress-response physiology and its implications for ecosystem function. Ecology 88, 1386–1394 (2007).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    5.Acosta-Martínez, V. et al. Predominant bacterial and fungal assemblages in agricultural soils during a record drought/heat wave and linkages to enzyme activities of biogeochemical cycling. Appl. Soil Ecol. 84, 69–82 (2014).Article 

    Google Scholar 
    6.Hobday, A. J. et al. A hierarchical approach to defining marine heatwaves. Prog. Oceanogr. 141, 227–238 (2016).Article 

    Google Scholar 
    7.Frölicher, T. L. & Laufkötter, C. Emerging risks from marine heat waves. Nat. Commun. 9, 650 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    8.Garrabou, J. et al. Mass mortality in Northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave. Glob. Change Biol. 15, 1090–1103 (2009).Article 

    Google Scholar 
    9.Wernberg, T. et al. An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nat. Clim. Change 3, 78–82 (2013).Article 

    Google Scholar 
    10.Bond, N. A., Cronin, M. F., Freeland, H. & Mantua, N. Causes and impacts of the 2014 warm anomaly in the NE Pacific. Geophys. Res. Lett. 9, 3414–3420 (2015).11.Freeland, H. & Ross, T. ‘The Blob’—or, how unusual were ocean temperatures in the Northeast Pacific during 2014-2018? Deep Sea Res. Part I: Oceanographic Res. Pap. 150, 103061 (2019).Article 

    Google Scholar 
    12.Lorenzo, E. D. & Mantua, N. Multi-year persistence of the 2014/15 North Pacific marine heatwave. Nat. Clim. Change 6, 1042–1047 (2016).Article 

    Google Scholar 
    13.Peña, M. A., Nemcek, N. & Robert, M. Phytoplankton responses to the 2014–2016 warming anomaly in the northeast subarctic Pacific Ocean. Limnol. Oceanogr. 64, 515–525 (2019).Article 

    Google Scholar 
    14.Yang, B., Emerson, S. R. & Peña, M. A. The effect of the 2013–2016 high temperature anomaly in the subarctic Northeast Pacific (the “Blob”) on net community production. Biogeosciences 15, 6747–6759 (2018).CAS 
    Article 

    Google Scholar 
    15.Cavole, L. et al. Biological impacts of the 2013–2015 warm-water anomaly in the Northeast Pacific: winners, losers, and the future. Oceanography 29, 273–285 (2016).16.Azam, F. et al. The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser. 10, 257–263 (1983).Article 

    Google Scholar 
    17.Sarmento, Hugo, Montoya, JoséM., Vázquez-Domínguez, Evaristo, Vaqué, Dolors & Gasol, JosepM. Warming effects on marine microbial food web processes: how far can we go when it comes to predictions? Philos. Trans. R. Soc. B: Biol. Sci. 365, 2137–2149 (2010).Article 

    Google Scholar 
    18.Joint, I. & Smale, D. A. Marine heatwaves and optimal temperatures for microbial assemblage activity. FEMS Microbiol Ecol 93, fiw243 (2017).19.Deschaseaux, E. O., Brien, J., Siboni, N., Petrou, K. & Seymour, J. R. Shifts in dimethylated sulfur concentrations and microbiome composition in the red-tide causing dinoflagellate Alexandrium minutum during a simulated marine heatwave. Biogeosciences 16, 4377–4391 (2019).CAS 
    Article 

    Google Scholar 
    20.Hawley, A. K. et al. Diverse Marinimicrobia bacteria may mediate coupled biogeochemical cycles along eco-thermodynamic gradients. Nat. Commun. 8, 1507 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    21.Allers, E. et al. Diversity and population structure of Marine Group A bacteria in the Northeast subarctic Pacific Ocean. ISME J. 7, 256–268 (2013).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    22.Roux, S. et al. Ecology and evolution of viruses infecting uncultivated SUP05 bacteria as revealed by single-cell- and meta-genomics. eLife 3, e03125 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    23.Wright, J. J. et al. Genomic properties of Marine Group A bacteria indicate a role in the marine sulfur cycle. ISME J. 8, 455–468 (2014).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    24.Sherry, N. D., Boyd, P. W., Sugimoto, K. & Harrison, P. J. Seasonal and spatial patterns of heterotrophic bacterial production, respiration, and biomass in the subarctic NE Pacific. Deep Sea Res. Part II Top. Stud. Oceanogr. 46, 2557–2578 (1999).25.Harrison, P. J. Station Papa Time Series: insights into ecosystem dynamics. J. Oceanogr. 58, 259–264 (2002).CAS 
    Article 

    Google Scholar 
    26.Mende, D. R. et al. Environmental drivers of a microbial genomic transition zone in the ocean’s interior. Nat. Microbiol. 2, 1367–1373 (2017).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    27.Pommier, T. et al. Global patterns of diversity and community structure in marine bacterioplankton. Mol. Ecol. 16, 867–880 (2007).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    28.Cram, J. A. et al. Seasonal and interannual variability of the marine bacterioplankton community throughout the water column over ten years. ISME J. 9, 563–580 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    29.Freeland, H. J. Evidence of change in the winter mixed layer in the Northeast Pacific Ocean: a problem revisited. Atmos. Ocean 51, 126–133 (2013).CAS 
    Article 

    Google Scholar 
    30.Stevens, H. & Ulloa, O. Bacterial diversity in the oxygen minimum zone of the eastern tropical South Pacific. Environ. Microbiol. 10, 1244–1259 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    31.Bryant, J. A., Stewart, F. J., Eppley, J. M. & DeLong, E. F. Microbial community phylogenetic and trait diversity declines with depth in a marine oxygen minimum zone. Ecology 93, 1659–1673 (2012).PubMed 
    Article 

    Google Scholar 
    32.Muck, S. et al. Niche differentiation of aerobic and anaerobic ammonia oxidizers in a high latitude deep oxygen minimum zone. Front. Microbiol. 10, 2141 (2019).33.Medina Faull, L., Mara, P., Taylor, G. T. & Edgcomb, V. P. Imprint of trace dissolved oxygen on prokaryoplankton community structure in an oxygen minimum zone. Front. Mar. Sci. 7, 360 (2020).34.Reji, L., Tolar, B. B., Chavez, F. P. & Francis, C. A. Depth-differentiation and seasonality of planktonic microbial assemblages in the monterey bay upwelling system. Front. Microbiol. 11, 1075 (2020).35.Wright, J. J., Konwar, K. M. & Hallam, S. J. Microbial ecology of expanding oxygen minimum zones. Nat. Rev. Microbiol. 10, 381–394 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    36.Tsementzi, D. et al. SAR11 bacteria linked to ocean anoxia and nitrogen loss. Nature 536, 179–183 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    37.Choi, D. H., Karen, Selph & Noh, J. H. Niche partitioning of picocyanobacterial lineages in the oligotrophic northwestern Pacific Ocean. ALGAE 30, 223–232 (2015).38.Johnson, Z. I. et al. Niche partitioning among prochlorococcus ecotypes along ocean-scale environmental gradients. Science 311, 1737–1740 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    39.Sohm, J. A. et al. Co-occurring Synechococcus ecotypes occupy four major oceanic regimes defined by temperature, macronutrients and iron. ISME J. 10, 333–345 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    40.Not, F. et al. in Advances in Botanical Research (ed. Piganeau, G.) vol. 64, 1–53 (Academic Press, 2012).41.Lutz, M., Dunbar, R. & Caldeira, K. Regional variability in the vertical flux of particulate organic carbon in the ocean interior. Glob. Biogeochemical Cycles 16, 11-1–11–18 (2002).
    Google Scholar 
    42.Richardson, T. L., Jackson, G. A., Ducklow, H. W. & Roman, M. R. Carbon fluxes through food webs of the eastern equatorial Pacific: an inverse approach. Deep Sea Res. Part I: Oceanographic Res. Pap. 51, 1245–1274 (2004).CAS 
    Article 

    Google Scholar 
    43.Michaels, A. F. & Silver, M. W. Primary production, sinking fluxes and the microbial food web. Deep Sea Res. Part A. Oceanographic Res. Pap. 35, 473–490 (1988).Article 

    Google Scholar 
    44.Dufrêne, M. & Legendre, P. Species assemblages and indicator species:the need for a flexible asymmetrical approach. Ecol. Monogr. 67, 345–366 (1997).
    Google Scholar 
    45.Cáceres, M. D., Legendre, P. & Moretti, M. Improving indicator species analysis by combining groups of sites. Oikos 119, 1674–1684 (2010).Article 

    Google Scholar 
    46.Shade, A. et al. Conditionally rare taxa disproportionately contribute to temporal changes in microbial diversity. mBio 5, e01371-14 (2014).47.Thrash, J. C. et al. Metabolic Roles of Uncultivated Bacterioplankton lineages in the Northern Gulf of Mexico “Dead Zone”. mBio 8, e01017-17 (2017).48.Kirchman, D. L. The ecology of Cytophaga–Flavobacteria in aquatic environments. FEMS Microbiol Ecol. 39, 91–100 (2002).CAS 
    PubMed 

    Google Scholar 
    49.Alonso, C., Warnecke, F., Amann, R. & Pernthaler, J. High local and global diversity of Flavobacteria in marine plankton. Environ. Microbiol. 9, 1253–1266 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    50.Teeling, H. et al. Recurring patterns in bacterioplankton dynamics during coastal spring algae blooms. eLife 5, e11888 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    51.Selje, N., Simon, M. & Brinkhoff, T. A newly discovered Roseobacter cluster in temperate and polar oceans. Nature 427, 445 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    52.Buchan, A., González, J. M. & Moran, M. A. Overview of the marine Roseobacter lineage. Appl. Environ. Microbiol. 71, 5665–5677 (2005).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    53.Luo, H. & Moran, M. A. Evolutionary ecology of the marine roseobacter clade. Microbiol. Mol. Biol. Rev. 78, 573–587 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    54.Simon, M. et al. Phylogenomics of Rhodobacteraceae reveals evolutionary adaptation to marine and non-marine habitats. ISME J. 11, 1483–1499 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    55.Sato, S. et al. Genome-enabled phylogenetic and functional reconstruction of an araphid pennate diatom Plagiostriata sp. CCMP470, previously assigned as a radial centric diatom, and its bacterial commensal. Sci. Rep. 10, 9449 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    56.Sañudo-Wilhelmy, S. A., Gómez-Consarnau, L., Suffridge, C. & Webb, E. A. The role of B vitamins in marine biogeochemistry. Annu. Rev. Mar. Sci. 6, 339–367 (2014).Article 

    Google Scholar 
    57.Landa, M. et al. Sulfur metabolites that facilitate oceanic phytoplankton–bacteria carbon flux. ISME J. 13, 2536–2550 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    58.Georges, A. A., El-Swais, H., Craig, S. E., Li, W. K. & Walsh, D. A. Metaproteomic analysis of a winter to spring succession in coastal northwest Atlantic Ocean microbial plankton. ISME J. 8, 1301–1313 (2014).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    59.Baker, B. J., Lazar, C. S., Teske, A. P. & Dick, G. J. Genomic resolution of linkages in carbon, nitrogen, and sulfur cycling among widespread estuary sediment bacteria. Microbiome 3, 14 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    60.Andrei, A.-Ş. et al. Niche-directed evolution modulates genome architecture in freshwater Planctomycetes. ISME J 13, 1056–1071 (2019).61.Fukunaga, Y. et al. Phycisphaera mikurensis gen. nov., sp. nov., isolated from a marine alga, and proposal of Phycisphaeraceae fam. nov., Phycisphaerales ord. nov. and Phycisphaerae classis nov. in the phylum Planctomycetes. J. Gen. Appl. Microbiol. 55, 267–275 (2009).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    62.Gade, D., Stührmann, T., Reinhardt, R. & Rabus, R. Growth phase dependent regulation of protein composition in Rhodopirellula baltica. Environ. Microbiol. 7, 1074–1084 (2005).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    63.Luecker, S., Nowka, B., Rattei, T., Spieck, E. & Daims, H. The genome of nitrospina gracilis illuminates the metabolism and evolution of the major marine nitrite oxidizer. Front. Microbiol. 4, 27 (2013).64.Winder, M. & Schindler, D. E. Climate change uncouples trophic interactions in an aquatic ecosystem. Ecology 85, 2100–2106 (2004).Article 

    Google Scholar 
    65.Brown, M. V. et al. Global biogeography of SAR11 marine bacteria. Mol. Syst. Biol. 8, 595 (2012).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    66.Haro‐Moreno, J. M. et al. Ecogenomics of the SAR11 clade. Environ. Microbiol 22, 1748–1763 (2020).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    67.Grote, J. et al. Streamlining and core genome conservation among highly divergent members of the SAR11 clade. mBio 3, e00252–12 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    68.Giovannoni, S. J. SAR11 Bacteria: The Most Abundant Plankton in the Oceans. Annu. Rev. Mar. Sci. 9, 231–255 (2017).Article 

    Google Scholar 
    69.Getz, E. W., Tithi, S. S., Zhang, L. & Aylward, F. O. Parallel evolution of genome streamlining and cellular bioenergetics across the marine radiation of a bacterial phylum. mBio. 9, e01089-18 (2018).70.Aylward, F. O. & Santoro, A. E. Heterotrophic thaumarchaea with small genomes are widespread in the dark ocean. mSystems 5, e00415-20 (2020).71.Prosser, J. I. & Nicol, G. W. Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environ. Microbiol. 10, 2931–2941 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    72.Santoro, A. E., Casciotti, K. L. & Francis, C. A. Activity, abundance and diversity of nitrifying archaea and bacteria in the central California Current. Environ. Microbiol. 12, 1989–2006 (2010).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    73.Horak, R. E. A. et al. Ammonia oxidation kinetics and temperature sensitivity of a natural marine community dominated by Archaea. ISME J. 7, 2023–2033 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    74.Qin, W. et al. Marine ammonia-oxidizing archaeal isolates display obligate mixotrophy and wide ecotypic variation. PNAS 111, 12504–12509 (2014).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    75.Rinke, C. et al. A phylogenomic and ecological analysis of the globally abundant Marine Group II archaea (Ca. Poseidoniales ord. nov.). ISME J. 13, 663 (2019).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    76.Haro-Moreno, J. M., Rodriguez-Valera, F., López-García, P., Moreira, D. & Martin-Cuadrado, A.-B. New insights into marine group III Euryarchaeota, from dark to light. ISME J. 11, 1102–1117 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    77.Orsi, W. D. et al. Diverse, uncultivated bacteria and archaea underlying the cycling of dissolved protein in the ocean. ISME J. 10, 2158–2173 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    78.Orsi, W. D. et al. Ecophysiology of uncultivated marine euryarchaea is linked to particulate organic matter. ISME J. 9, 1747–1763 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    79.Hugoni, M. et al. Structure of the rare archaeal biosphere and seasonal dynamics of active ecotypes in surface coastal waters. Proc. Natl Acad. Sci. USA 110, 6004–6009 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    80.Matheus Carnevali, P. B. et al. Hydrogen-based metabolism as an ancestral trait in lineages sibling to the Cyanobacteria. Nat. Commun. 10, 463 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    81.Saw, J. H. W. et al. Pangenomics analysis reveals diversification of enzyme families and niche specialization in globally abundant SAR202 bacteria. mBio 11, e02975-19 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    82.Alonso‐Sáez, L., Díaz‐Pérez, L. & Morán, X. A. G. The hidden seasonality of the rare biosphere in coastal marine bacterioplankton. Environ. Microbiol. 17, 3766–3780 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    83.Lambert, S. et al. Rhythmicity of coastal marine picoeukaryotes, bacteria and archaea despite irregular environmental perturbations. ISME J. 13, 388–401 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    84.Mehrshad, M., Rodriguez-Valera, F., Amoozegar, M. A., López-García, P. & Ghai, R. The enigmatic SAR202 cluster up close: shedding light on a globally distributed dark ocean lineage involved in sulfur cycling. ISME J. 12, 655–668 (2018).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    85.Mullins, T. D., Britschgi, T. B., Krest, R. L. & Giovannoni, S. J. Genetic comparisons reveal the same unknown bacterial lineages in Atlantic and Pacific bacterioplankton communities. Limnol. Oceanogr. 40, 148–158 (1995).CAS 
    Article 

    Google Scholar 
    86.Acinas, S. G., Antón, J. & Rodríguez-Valera, F. Diversity of free-living and attached bacteria in offshore western mediterranean waters as depicted by analysis of genes encoding 16S rRNA. Appl. Environ. Microbiol. 65, 514–522 (1999).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    87.Hoarfrost, A. et al. Global ecotypes in the ubiquitous marine clade SAR86. ISME J. 14, 178–188 (2020).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    88.Alonso-Sáez, L., Galand, P. E., Casamayor, E. O., Pedrós-Alió, C. & Bertilsson, S. High bicarbonate assimilation in the dark by Arctic bacteria. ISME J. 4, 1581–1590 (2010).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    89.Swan, B. K. et al. Potential for chemolithoautotrophy among ubiquitous bacteria lineages in the dark ocean. Science 333, 1296–1300 (2011).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    90.Maldonado, M. T., Boyd, P. W., Harrison, P. J. & Price, N. M. Co-limitation of phytoplankton growth by light and Fe during winter in the NE subarctic Pacific Ocean. Deep Sea Res. Part II: Topical Stud. Oceanogr. 46, 2475–2485 (1999).CAS 
    Article 

    Google Scholar 
    91.Peña, M. A. & Varela, D. E. Seasonal and interannual variability in phytoplankton and nutrient dynamics along Line P in the NE subarctic Pacific. Prog. Oceanogr. 75, 200–222 (2007).Article 

    Google Scholar 
    92.Whitney, F. A., Wong, C. S. & Boyd, P. W. Interannual variability in nitrate supply to surface waters of the Northeast Pacific Ocean. Mar. Ecol. Prog. Ser. 170, 15–23 (1998).CAS 
    Article 

    Google Scholar 
    93.Crawford, W., Galbraith, J. & Bolingbroke, N. Line P ocean temperature and salinity, 1956–2005. Prog. Oceanogr. 75, 161–178 (2007).Article 

    Google Scholar 
    94.Whitney, F. A. & Freeland, H. J. Variability in upper-ocean water properties in the NE Pacific Ocean. Deep Sea Res. Part II: Topical Stud. Oceanogr. 46, 2351–2370 (1999).CAS 
    Article 

    Google Scholar 
    95.Whitney, F. A., Freeland, H. J. & Robert, M. Persistently declining oxygen levels in the interior waters of the eastern subarctic Pacific. Prog. Oceanogr. 75, 179–199 (2007).Article 

    Google Scholar 
    96.Siegel, D. A. et al. Prediction of the Export and Fate of Global Ocean Net Primary Production: The EXPORTS Science Plan. Front. Mar. Sci. 3, 030 (2016).97.Buesseler, K. O. et al. High-resolution spatial and temporal measurements of particulate organic carbon flux using thorium-234 in the northeast Pacific Ocean during the EXport Processes in the Ocean from RemoTe Sensing field campaign. Elementa: Sci. Anthrop. 8, (2020).98.Stephens, B. M. et al. Organic matter composition at ocean station papa affects its bioavailability, bacterioplankton growth efficiency and the responding taxa. Front. Mar. Sci. 7, 590273 (2020).99.Mackinson, B. L., Moran, S. B., Lomas, M. W., Stewart, G. M. & Kelly, R. P. Estimates of micro-, nano-, and picoplankton contributions to particle export in the northeast Pacific. Biogeosciences 12, 3429–3446 (2015).Article 

    Google Scholar 
    100.Fisher, J. et al. Copepod responses to, and recovery from, the recent marine heatwave in the Northeast Pacific. PICES Sci. 2019: Notes Sci. Board Chair 28, 65 (2020).
    Google Scholar 
    101.Batten, S. D. et al. Interannual variability in lower trophic levels on the Alaskan Shelf. Deep Sea Res. Part II: Topical Stud. Oceanogr. 147, 58–68 (2018).Article 

    Google Scholar 
    102.Geider, R. & Roche, J. L. Redfield revisited: variability of C:N:P in marine microalgae and its biochemical basis. Eur. J. Phycol. 37, 1–17 (2002).Article 

    Google Scholar 
    103.Wohlers, J. et al. Changes in biogenic carbon flow in response to sea surface warming. Proc.Natl. Acad. Sci. USA 106, 7067–7072 (2009).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    104.Bif, M. B. & Hansell, D. A. Seasonality of dissolved organic carbon in the upper Northeast Pacific Ocean. Glob. Biogeochem. Cycles 33, 526–539 (2019).CAS 
    Article 

    Google Scholar 
    105.Ferrer-González, F. X. et al. Resource partitioning of phytoplankton metabolites that support bacterial heterotrophy. ISME J. https://doi.org/10.1038/s41396-020-00811-y. (2020).106.Gies, E. A., Konwar, K. M., Beatty, J. T. & Hallam, S. J. Illuminating microbial dark matter in meromictic Sakinaw Lake. Appl. Environ. Microbiol. 80, 6807–6818 (2014).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    107.Pachiadaki, M. G. et al. Charting the complexity of the marine microbiome through single-cell genomics. Cell 179, 1623–1635.e11 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    108.Fuhrman, J. A. et al. Annually reoccurring bacterial communities are predictable from ocean conditions. Proc. Natl Acad. Sci. USA 103, 13104–13109 (2006).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    109.Ono, T., Shiomoto, A. & Saino, T. Recent decrease of summer nutrients concentrations and future possible shrinkage of the subarctic North Pacific high-nutrient low-chlorophyll region. Global Biogeochemical Cycles 22, GB3027 (2008).110.Walsh, D. A., Zaikova, E. & Hallam, S. J. Small Volume (1-3L) Filtration of Coastal Seawater Samples. JoVE https://doi.org/10.3791/1163 (2009).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    111.Barwell-Clarke, J. & Whitney, F. Institute of Ocean Sciences nutrient Methods and Analysis. (1996).112.Zapata, M., Rodríguez, F. & Garrido, J. L. Separation of chlorophylls and carotenoids from marine phytoplankton: a new HPLC method using a reversed phase C8 column and pyridine-containing mobile phases. Mar. Ecol. Prog. Ser. 195, 29–45 (2000).CAS 
    Article 

    Google Scholar 
    113.Nemcek, N. & Peña, M. A. Institute of Ocean Sciences Protocols for Phytoplankton Pigment Analysis by HPLC. (2014).114.Wright, J. J., Lee, S., Zaikova, E., Walsh, D. A. & Hallam, S. J. DNA Extraction from 0.22 μM Sterivex Filters and Cesium Chloride Density Gradient Centrifugation. J. Vis. Exp. e1352, https://doi.org/10.3791/1352 (2009).115.Parada, A. E., Needham, D. M. & Fuhrman, J. A. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ. Microbiol. 18, 1403–1414 (2016).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    116.Rivers, A. R. iTag amplicon sequencing for taxonomix identification at JGI. http://1ofdmq2n8tc36m6i46scovo2e.wpengine.netdna-cdn.com/wp-content/uploads/2013/05/iTagger-methods-1.pdf (2016).117.Magoč, T. & Salzberg, S. L. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957–2963 (2011).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    118.Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    119.Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    120.Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C. & Knight, R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    121.Yilmaz, P. et al. The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks. Nucleic Acids Res. 42, D643–D648 (2014).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    122.Bolyen, E. et al. QIIME 2: Reproducible, interactive, scalable, and extensible microbiome data science. Nat. Biotechnol. 37, 852–857 (2019).123.R Core Team. R: A language and environment for statistical computing. (R Foundation for Statistical Computing, 2018).124.Rstudio Team. Rstudio: Integrated Development Environment for R (Rstudio Inc, 2016).125.Faust, K. & Raes, J. CoNet app: inference of biological association networks using Cytoscape. F1000Res 5, 1519 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    126.Shannon, P. et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13, 2498–2504 (2003).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar  More

  • in

    Identification of ecological networks and nodes in Fujian province based on green and blue corridors

    1.Garcia-Garcia, M. J., Christien, L., García-Escalona, E. & González-García, C. Sensitivity of green spaces to the process of urban planning: Three case studies of Madrid (Spain). Cities 100, 102655. https://doi.org/10.1016/j.cities.2020.102655 (2020).Article 

    Google Scholar 
    2.Kondo, M. C., Fluehr, J. M., McKeon, T. & Branas, C. C. Urban green space and its impact on human health. Environ. Res. Public Health 15(3), 445. https://doi.org/10.3390/ijerph15030445 (2018).Article 

    Google Scholar 
    3.Nesbitt, L. et al. The social and economic value of cultural ecosystem services provided by urban forests in North America: A review and suggestions for future research. Urban For. Urban Green. 25, 103–111. https://doi.org/10.1016/j.ufug.2017.05.005 (2017).Article 

    Google Scholar 
    4.Hasan, S. S., Zhen, L., Miah, G., Ahamed, T. & Samie, A. Impact of land use change on ecosystem services: A review. Environ. Dev. 34, 100527. https://doi.org/10.1016/j.envdev.2020.100527 (2020).Article 

    Google Scholar 
    5.Kolodziejczyk, B. et al. Frontiers 2018/19: Emerging issues of environmental concern. United Nations Environment Programme, Nairobi, 24–37 (2019).6.Steffen, W., Crutzen, P. J. & McNeill, J. R. The anthropocene: Are humans now overwhelming the great forces of nature. Hum. Environ. 36(8), 614–621. https://doi.org/10.1579/0044-7447(2007)36[614:TAAHNO]2.0.CO;2 (2007).CAS 
    Article 

    Google Scholar 
    7.CC & SC. Views on Accelerating the Ecological Civilization Construction (2015).8.Ministry of Housing and Urban-Rural Development (MHURD). City Green Space Planning Standards, GB/T51346-2019 (2019).9.Raei, E. et al. Multi-objective decision-making for green infrastructure planning (LID-BMPs) in urban storm water management under uncertainty. J. Hydrol. 579, 124091. https://doi.org/10.1016/j.jhydrol.2019.124091 (2019).CAS 
    Article 

    Google Scholar 
    10.Tzoulas, K. et al. Promoting ecosystem and human health in urban areas using Green Infrastructure: A literature review. Landsc. Urban Plan. 81(3), 167–178. https://doi.org/10.1016/j.landurbplan.2007.02.001 (2007).Article 

    Google Scholar 
    11.Xiao, F., Shu, J. & Zhang, L. Research on applying minimal cumulative resistance model in urban land ecological suitability assessment: As an example of Xiamen City. Acta Ecol. Sin. 30(2), 421–428 (2010).
    Google Scholar 
    12.Zhao, S., Ma, Y., Wang, J. & You, X. Landscape pattern analysis and ecological network planning of Tianjin City. Urban For. Urban Green. 46, 126479. https://doi.org/10.1016/j.ufug.2019.126479 (2019).Article 

    Google Scholar 
    13.Davies, C. & Lafortezza, R. Urban green infrastructure in Europe: Is greenspace planning and policy compliant? Land Use Policy 69, 93–101. https://doi.org/10.1016/j.landusepol.2017.08.018 (2017).Article 

    Google Scholar 
    14.Central Committee & State Council (CC & SC). Views on establishment and monitoring of Territorial Space Planning system (2019).15.Zhou, Q. et al. China’s Green space system planning: Development, experiences, and characteristics. Urban For. Urban Green. 60, 127017. https://doi.org/10.1016/j.ufug.2021.127017 (2021).Article 

    Google Scholar 
    16.Zhou, X., Zhang, S. & Zhu, D. Impact of urban water networks on microclimate and PM25 distribution in downtown areas: A case study of wuhan. Build. Environ. 203, 108073. https://doi.org/10.1016/j.buildenv.2021.108073 (2021).Article 

    Google Scholar 
    17.Ministry of Natural Resources (MNR). Guidelines for Formulation of Provincial Territorial Space Planning (Trial) (2020).18.Rushdi, A. M. A. & Hassan, A. K. Reliability of migration between habitat patches with heterogeneous ecological corridors. Ecol. Model. 304, 1–10. https://doi.org/10.1016/j.ecolmodel.2015.02.014 (2015).Article 

    Google Scholar 
    19.Wang, T., Li, H. & Huang, Y. The complex ecological network’s resilience of the Wuhan metropolitan area. Ecol. Ind. 130, 108101. https://doi.org/10.1016/j.ecolind.2021.108101 (2021).Article 

    Google Scholar 
    20.Wu, H. et al. A novel remote sensing ecological vulnerability index on large scale: A case study of the China-Pakistan Economic Corridor region. Ecol. Ind. 129, 107955. https://doi.org/10.1016/j.ecolind.2021.107955 (2021).Article 

    Google Scholar 
    21.Janauer, G. A. Ecohydrology: Fusing concepts and scales. Ecol. Eng. 16(1), 9–16. https://doi.org/10.1016/S0925-8574(00)00072-0 (2000).Article 

    Google Scholar 
    22.Rinaldo, A., Gatto, M. & Rodriguez-Iturbe, I. River networks as ecological corridors: A coherent ecohydrological perspective. Adv. Water Resour. 112, 27–58. https://doi.org/10.1016/j.advwatres.2017.10.005 (2018).ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    23.Fletcher, T. D. et al. SUDS, LID, BMPs, WSUD and more: The evolution and application of terminology surrounding urban drainage. Urban Water J. 12(7), 525–542. https://doi.org/10.1080/1573062X.2014.916314 (2015).Article 

    Google Scholar 
    24.Nieuwenhuis, E., Cuppen, E., Langeveld, J. & Bruijn, H. Towards the integrated management of urban water systems: Conceptualizing integration and its uncertainties. J. Clean. Prod. 280(2), 124977. https://doi.org/10.1016/j.jclepro.2020.124977 (2021).Article 

    Google Scholar 
    25.Knaapen, J. P., Scheffer, M. & Harms, B. Estimating habitat isolation in landscape planning. Landscape Urban Plann. 23(1), 1–16. https://doi.org/10.1016/0169-2046(92)90060-D (1992).Article 

    Google Scholar 
    26.Yu, K. Security patterns and surface model in landscape ecological planning. Landscape Urban Plann. 36(1), 1–17. https://doi.org/10.1016/S0169-2046(96)00331-3 (1996).Article 

    Google Scholar 
    27.Yu, K. Landscape ecological security pattern of biological protection. Acta Ecologica Sinica 1, 3–5 (1999).
    Google Scholar 
    28.Zhang, Z., Meerow, S., Newell, J. P. & Lindquist, M. Enhancing landscape connectivity through multifunctional green infrastructure corridor modeling and design. Urban For. Urban Green. 38, 305–317. https://doi.org/10.1016/j.ufug.2018.10.014 (2019).Article 

    Google Scholar 
    29.Fu, Y., Shi, X., He, J., Yuan, Y. & Qu, L. Identification and optimization strategy of county ecological security pattern: A case study in the Loess Plateau, China. Ecol. Ind. 112, 106030. https://doi.org/10.1016/j.ecolind.2019.106030 (2020).Article 

    Google Scholar 
    30.Kong, F., Yin, H., Nakagoshi, N. & Zong, Y. Urban green space network development for biodiversity conservation: Identification based on graph theory and gravity modeling. Landsc. Urban Plan. 95, 16–27. https://doi.org/10.1016/j.landurbplan.2009.11.001 (2010).Article 

    Google Scholar 
    31.Kong, F. & Yin, H. Construction of Jinan urban green space ecological network. Acta Ecol. Sin. 4, 1711–1719 (2008).
    Google Scholar 
    32.Linehan, J., Gross, M. & Finn, J. Greenway planning: Developing a landscape ecological network approach. Landsc. Urban Plan. 33(1–3), 179–193. https://doi.org/10.1016/0169-2046(94)02017-A (1995).Article 

    Google Scholar 
    33.Yang, H., Chen, W. & Chen, X. Regional ecological network planning for biodiversity conservation: A case study of China’s Poyang lake eco-economic region. Pol. J. Environ. Stud. 26(4), 1825–1833. https://doi.org/10.15244/pjoes/68877 (2017).Article 

    Google Scholar 
    34.Fahrig, L. Rethinking patch size and isolation effects: The habitat amount hypothesis. J. Biogeogr. 40(9), 1649–1663. https://doi.org/10.1111/jbi.12130 (2013).Article 

    Google Scholar 
    35.Gilbert-Norton, L., Wilson, R., Stevens, J. R. & Beard, K. H. A meta-analytic review of corridor effectiveness. Conserv. Biol. 24(3), 660–668. https://doi.org/10.1111/j.1523-1739.2010.01450.x (2010).Article 
    PubMed 

    Google Scholar 
    36.Saura, S. & Torné, J. Conefor Sensinode 2.2: A software package for quantifying the importance of habitat patches for landscape connectivity. Environ. Model. Softw. 24(1), 135–139. https://doi.org/10.1016/j.envsoft.2008.05.005 (2009).Article 

    Google Scholar 
    37.Saura, S., Vogt, P., Velázquez, J., Hernando, A. & Tejera, R. Key structural forest connectors can be identified by combining landscape spatial pattern and network analyses. For. Ecol. Manag. 262(2), 150–160. https://doi.org/10.1016/j.foreco.2011.03.017 (2011).Article 

    Google Scholar 
    38.Bueno, J. A., Tsihrintzis, V. A. & Alvarez, L. South Florida greenways: a conceptual framework for the ecological reconnectivity of the region. Landsc. Urban Plan. 33(1–3), 247–266. https://doi.org/10.1016/0169-2046(94)02021-7 (1995).Article 

    Google Scholar 
    39.Cook, E. A. Landscape structure indices for assessing urban ecological networks. Landsc. Urban Plan. 58(2–4), 269–280. https://doi.org/10.1016/S0169-2046(01)00226-2 (2002).Article 

    Google Scholar 
    40.Dalton, R., Garlick, J., Minshull, R. & Robinson, A. Networks in Geography (Phillip, 1973).
    Google Scholar 
    41.Forman, R. T. T. & Godron, M. Landscape Ecology (Wiley, 1986).
    Google Scholar 
    42.Haggett, P. & Chorley, R. J. Network Analysis in Geography (Edward Arnold, 1972).
    Google Scholar 
    43.Yu, K. The identification method of landscape ecological strategic points and the surface model of theoretical geography. J. Geog. Sci. S1, 3–5 (1998).
    Google Scholar 
    44.Yu, Q. et al. Optimization of ecological node layout and stability analysis of ecological network in desert oasis: A typical case study of ecological fragile zone located at Deng Kou County (Inner Mongolia). Ecol. Indic. 84, 304–318. https://doi.org/10.1016/j.ecolind.2017.09.002 (2018).Article 

    Google Scholar 
    45.Zhang, Y. & Yu, B. Evaluation of urban ecological network space and its structure optimization. Acta Ecol. Sin. 36(21), 6969–6984 (2016).
    Google Scholar 
    46.Hong, W. et al. Sensitivity evaluation and land-use control of urban ecological corridors: A case study of Shenzhen, China. Land Use Policy 62, 316–325. https://doi.org/10.1016/j.landusepol.2017.01.010 (2017).Article 

    Google Scholar 
    47.Monaco, R., Negrini, G., Salizzoni, E., Soares, A. J. & Voghera, A. Inside-outside park planning: A mathematical approach to assess and support the design of ecological connectivity between Protected Areas and the surrounding landscape. Ecol. Eng. 149, 105748. https://doi.org/10.1016/j.ecoleng.2020.105748 (2020).Article 

    Google Scholar 
    48.Morandi, D. T. et al. Delimitation of ecological corridors between conservation units in the Brazilian Cerrado using a GIS and AHP approach. Ecol. Ind. 115, 106440. https://doi.org/10.1016/j.ecolind.2020.106440 (2020).Article 

    Google Scholar 
    49.Santos, J. S. et al. Delimitation of ecological corridors in the Brazilian Atlantic Forest. Ecol. Ind. 88, 414–424. https://doi.org/10.1016/j.ecolind.2018.01.011 (2018).Article 

    Google Scholar 
    50.Dai, L., Liu, Y., Luo, X. I. & the MCR and, ,. DOI models to construct an ecological security network for the urban agglomeration around Poyang Lake, China. Sci. Total Environ. https://doi.org/10.1016/j.scitotenv.2020.141868 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    51.Ferreira, C. S. S. et al. Spatiotemporal variability of hydrologic soil properties and the implications for overland flow and land management in a peri-urban Mediterranean catchment. J. Hydrol. 525, 249–263. https://doi.org/10.1016/j.jhydrol.2015.03.039 (2015).ADS 
    Article 

    Google Scholar 
    52.Kalantari, Z. et al. Assessing flood probability for transportation infrastructure based on catchment characteristics, sediment connectivity and remotely sensed soil moisture. Sci. Total Environ. 661, 393–406. https://doi.org/10.1016/j.scitotenv.2019.01.009 (2019).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    53.Kalantari, Z., Ferreira, C. S. S., Walsh, R. P. D., Ferreira, A. J. D. & Destouni, G. Urbanization development under climate change: Hydrological responses in a peri-urban Mediterranean catchment. Land Degrad. Dev. 28, 2207–2221. https://doi.org/10.1002/ldr.2747 (2017).Article 

    Google Scholar 
    54.Grillakis, M. G. et al. Initial soil moisture effects on flash flood generation: A comparison between basins of contrasting hydro-climatic conditions. J. Hydrol. 541(A), 206–217. https://doi.org/10.1016/j.jhydrol.2016.03.007 (2016).ADS 
    Article 

    Google Scholar 
    55.Zhang, K., Fong, T. & Chui, M. A comprehensive review of spatial allocation of LID-BMP-GI practices: Strategies and optimization tools. Sci. Total Environ. 621, 915–929. https://doi.org/10.1016/j.scitotenv.2017.11.281 (2018).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    56.Liu, Z., Lin, Y., De Meulder, B. & Wang, S. Heterogeneous landscapes of urban greenways in Shenzhen: Traffic impact, corridor width and land use. Urban For. Urban Green. 126, 785. https://doi.org/10.1016/j.ufug.2020.126785 (2020).Article 

    Google Scholar 
    57.Wakefield, S. Great expectations: Waterfront redevelopment and the Hamilton Harbour Waterfront Trail. Cities 24(4), 298–310. https://doi.org/10.1016/j.cities.2006.11.001 (2007).Article 

    Google Scholar 
    58.Rimaze, D., Machumu, A., Mremi, R. & Eustace, A. Diversity and abundance of wild mammals between different accommodation facilities in the Kwakuchinja Wildlife Corridor, Tanzania. Sci. Afr. 9, e00480. https://doi.org/10.1016/j.sciaf.2020.e00480 (2020).Article 

    Google Scholar 
    59.Franco, D., Mannino, I. & Zanetto, G. The impact of agroforestry networks on scenic beauty estimation: The role of a landscape ecological network on a socio-cultural process. Landsc. Urban Plan. 62(3), 119–138. https://doi.org/10.1016/S0169-2046(02)00127-5 (2003).Article 

    Google Scholar 
    60.Wu, X. et al. Increasing green infrastructure-based ecological resilience in urban systems: A perspective from locating ecological and disturbance sources in a resource-based city. Sustain. Cities Soc. 61, 102354. https://doi.org/10.1016/j.scs.2020.102354 (2020).Article 

    Google Scholar 
    61.Yang, C., Zeng, W. & Yang, X. Coupling coordination evaluation and sustainable development pattern of geo-ecological environment and urbanization in Chongqing municipality, China. Sustain. Cities Soc. 61, 102271. https://doi.org/10.1016/j.scs.2020.102271 (2020).Article 

    Google Scholar 
    62.Yang, J., Zeng, C. & Cheng, Y. Spatial influence of ecological networks on land use intensity. Sci. Total Environ. https://doi.org/10.1016/j.scitotenv.2020.137151 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    63.Théau, J., Bernier, A. & Fournier, R. A. An evaluation framework based on sustainability-related indicators for the comparison of conceptual approaches for ecological networks. Ecol. Indic. 52, 444–457. https://doi.org/10.1016/j.ecolind.2014.12.029 (2015).Article 

    Google Scholar 
    64.Neri, M., Jameli, D., Bernard, E. & Melo, F. P. L. Green versus green? Adverting potential conflicts between wind power generation and biodiversity conservation in Brazil. Perspect. Ecol. Conserv. 17(3), 131–135. https://doi.org/10.1016/j.pecon.2019.08.004 (2019).Article 

    Google Scholar 
    65.Zeng, Y. & Zhong, L. Identifying conflicts tendency between nature-based tourism development and ecological protection in China. Ecol. Indic. 109, 105791. https://doi.org/10.1016/j.ecolind.2019.105791 (2020).Article 

    Google Scholar 
    66.Cunha, N. S. & Magalhães, M. R. Methodology for mapping the national ecological network to mainland Portugal: A planning tool towards a green infrastructure. Ecol. Ind. 104, 802–818. https://doi.org/10.1016/j.ecolind.2019.04.050 (2019).Article 

    Google Scholar 
    67.Dong, J., Peng, J., Liu, Y., Qiu, S. & Han, Y. Integrating spatial continuous wavelet transform and kernel density estimation to identify ecological corridors in megacities. Landsc. Urban Plan. 199, 103815. https://doi.org/10.1016/j.landurbplan.2020.103815 (2020).Article 

    Google Scholar 
    68.Gasanov, G. et al. Data on the productivity of plant cover of the main types of soils of the North-Western precaspian in connection with the dynamics of ecological factors. Data Brief 24, 103713. https://doi.org/10.1016/j.dib.2019.103713 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    69.Montis, A. D. et al. Resilient ecological networks: A comparative approach. Land Use Policy 89, 104207. https://doi.org/10.1016/j.landusepol.2019.104207 (2019).Article 

    Google Scholar 
    70.Du, H. et al. Urban blue-green space planning based on thermal environment simulation: A case study of Shanghai, China. Ecol. Indic. 106, 105501. https://doi.org/10.1016/j.ecolind.2019.105501 (2020).Article 

    Google Scholar 
    71.Guo, X. et al. The impact of onshore wind power projects on ecological corridors and landscape connectivity in Shanxi, China. J. Clean. Prod. 254, 120075. https://doi.org/10.1016/j.jclepro.2020.120075 (2020).Article 

    Google Scholar 
    72.Li, J., Wang, Y., Ni, Z., Chen, S. & Xia, B. An integrated strategy to improve the microclimate regulation of green-blue-grey infrastructures in specific urban forms. J. Clean. Prod. 271, 122555. https://doi.org/10.1016/j.jclepro.2020.122555 (2020).Article 

    Google Scholar 
    73.Afriyanie, D. et al. Re-framing urban green spaces planning for flood protection through socio-ecological resilience in Bandung City, Indonesia. Cities 101, 102710. https://doi.org/10.1016/j.cities.2020.102710 (2020).Article 

    Google Scholar 
    74.Ioan-Cristian, I. et al. Integrating urban blue and green areas based on historical evidence. Urban For. Urban Green. 34, 217–225. https://doi.org/10.1016/j.ufug.2018.07.001 (2019).Article 

    Google Scholar 
    75.Jaung, W. L., Carrasco, R., Ahmad, S., Tan, P. Y. & Richards, D. R. Temperature and air pollution reductions by urban green spaces are highly valued in a tropical city-state. Urban For. Urban Green. https://doi.org/10.1016/j.ufug.2020.126827 (2020).Article 

    Google Scholar 
    76.La Sorte, F. A., Aronson, M. F. J., Lepczyk, C. A. & Horton, K. G. Area is the primary correlate of annual and seasonal patterns of avian species richness in urban green spaces. Landsc. Urban Plan. 203, 103892. https://doi.org/10.1016/j.landurbplan.2020.103892 (2020).Article 

    Google Scholar 
    77.Moradpour, M. & Hosseini, V. An investigation into the effects of green space on air quality of an urban area using CFD modeling. Urban Clim. 34, 100686. https://doi.org/10.1016/j.uclim.2020.100686 (2020).Article 

    Google Scholar 
    78.Nouri, H., Borujeni, S. C. & Hoekstra, A. Y. The blue water footprint of urban green spaces: An example for Adelaide, Australia. Landsc. Urban Plan. 190, 103613. https://doi.org/10.1016/j.landurbplan.2019.103613 (2019).Article 

    Google Scholar 
    79.Sikuzani, Y. U. et al. Tree diversity and structure on green space of urban and peri-urban zones: The case of Lubumbashi City in the Democratic Republic of Congo. Urban For. Urban Green. 41, 67–74. https://doi.org/10.1016/j.ufug.2019.03.008 (2019).Article 

    Google Scholar  More

  • in

    Enhancement of extreme events through the Allee effect and its mitigation through noise in a three species system

    One of the most interesting observations from the time series presented in the section above is the following: when the magnitude of the Allee parameter (theta) is low, vegetation and prey densities are confined to low values. However, the predator densities deviate very significantly away from their mean. Now for very small (theta) the system is attracted to a periodic orbit, and so the large deviations are completely correlated with time and occur periodically. So they cannot be considered to be extreme events, as they are neither aperiodic, nor rare. But for larger (theta), both predator and prey densities can sometime shoot up over 7 standard deviations away from the mean value. This is evident clearly in Fig. 2c,e where one can see that both predator and prey populations exceed the (7sigma) threshold from time to time. The instants at which prey and predator populations exceed the (7sigma) threshold are now completely uncorrelated with time. This is consistent with the underlying chaotic dynamics that emerges under increasing Allee parameter (theta).In order to illustrate this, we mark the time instances at which a population exceeds the (7sigma) threshold, for different values of Allee parameter (theta). Figure 4 shows this for the vegetation, prey and predator populations. The density of points signifying the occurrence of extreme events is clearly the highest for the predator population. This indicates that the predator population has the greatest propensity for large deviations. It is also clear that vegetation has the least number of extreme events in the same time window. The uncorrelated nature of the extreme events is also evident in the scatter of these points, except in the small periodic windows that occur for certain special ranges of (theta). The increasing density of these points also illustrate the increasing probability of extreme events in the populations with increasing Allee parameter (theta).Figure 4Figure marking the time instances at which a population exceeds the (7sigma) threshold, for different values of Allee parameter (theta), for the case of (top to bottom) vegetation, prey and predator populations.Full size imageIn order to understand the phenomena quantitatively, we first estimate the maximum densities of vegetation, prey and predator populations (denoted by (u_{max}), (v_{max}) and (w_{max}) respectively) for varying the Allee parameter (theta). To estimate this, we find the global maximum of the populations sampled over a time interval (T=1000), averaged over a large set of random initial conditions.Figure 5 shows (u_{max}), (v_{max}) and (w_{max}), for Allee parameter (theta in [0,theta _{c})), scaled by their values at (theta = 0). These scaled maxima help us gauge the relative change in the maximum population densities arising due to the Allee effect. It is evident from our simulation results that the magnitude of the global maximum of vegetation does not change very significantly for increasing Allee parameter (theta), with its magnitude around (theta _c) being approximately 4 fold the value at (theta =0). However, the magnitude of maximum prey and predator populations change very significantly with respect to Allee parameter (theta) and exceeds over 10 fold the value obtained for (theta =0).Figure 5Global maximum of vegetation (u_{max}) (blue), prey (v_{max}) (red) and predator (black) populations, with respect to the Allee parameter (theta), scaled by their values obtained for (theta =0). Clearly, when Allee parameter (theta) is sufficiently large, the maximum prey and predator populations are an order of magnitude larger than that obtained in systems with no Allee effect.Full size imageWe then go on to numerically calculate the probability density of the vegetation, prey, and predator population densities, for increasing Allee effect parameter (theta). The tail of this probability density function reflects the influence of the Allee effect on the probability of obtaining extreme events. To illustrate this, we show the probability density function for the prey population in Fig. 6, for three different values of (theta). Extreme events are confined to the tail of the distribution that lie beyond the vertical red line, marking the (mu + 7 sigma) value in the figure. So it is clear from these probability distributions that the Allee effect in prey population promotes the occurrence of extreme events as the tail of the distribution is flatter and extends further with increasing Allee parameter (theta).Figure 6Probability Density Function (PDF) of the prey population v, for the system given by Eq. (1), with increasing magnitude of (theta) with (a) (theta =0), (b) (theta =0.015) and (c) (theta =0.02). The threshold for extreme event (mu + 7sigma) is denoted by vertical red dashed line.Full size imageIn order to ascertain that the extreme values are uncorrelated and aperiodic we examine the time intervals between successive extreme events in the population. Figure 7 (left panel) shows representative results for the return map of the intervals between extreme events in the prey population and it is clearly shows no regularity. The probability distribution of the intervals is also Poisson distributed and so the extreme population buildups are uncorrelated aperiodic events, as clearly evident from the right panel of the figure.Figure 7(Left) Return Map of (Delta t_{i+1}) versus (Delta t_i), and (right) Probability distribution of (Delta t_i) fitted with exponentially decaying function, where (Delta t_i) is the ith interval between successive extreme events, where an extreme event is defined at the instant when the prey population crosses the (mu +7sigma) line (cf. Fig. 2). Here (theta =0.024).Full size imageIn order to further quantify how Allee effect influences extreme events, we estimate the probability of obtaining large deviations, in a large sample of initial states tracked over a long period of time. We denote this probability by (P_{ext}), and we calculate it by following a large set of random initial conditions and recording the number of occurrences of the population crossing the threshold value in a prescribed period of time, with this time window being several orders of magnitude larger than the mean oscillation period. This time-averaged and ensemble-averaged quantity yields a good estimate of (P_{ext}). With no loss of generality, we choose the threshold for determining extreme events to be (mu + 7 sigma), i.e. when the variable crosses the (7 sigma) level, it is labelled as extreme.This probability, estimated for all three populations is shown in Fig. 8. First, it is clear from Fig. 8, that the probability of the occurrence of extreme events is the lowest for vegetation, and the highest for predator populations, for any value of the Allee parameter (theta in [0,theta _{c})). We also observe that, for values of the Allee parameter (theta) lower than a critical value denoted by (theta ^{u}_{c}) the probability of obtaining extreme events in the vegetation population tends to zero. Beyond the critical value (theta ^u_c), the vegetation population starts to exhibit extreme events. A similar trend emerges for the prey population. However, the critical value of the Allee parameter (theta) necessary for the emergence of a finite probability of extreme events, denoted by (theta ^{v}_{c}), is much smaller than (theta ^u_c). So for the prey population, a weaker Allee effect can induce extreme events.Figure 8Probability of obtaining extreme event in unit time ((P_{ext})), with respect to Allee parameter (theta), estimated by sampling a time series of length (T=5000), and averaging over 500 random initial states. Here we consider that an extreme event occurs when a population level crosses the threshold (mu + 7sigma). (P_{ext}) for vegetation, prey and predator are displayed in blue, red and black colors respectively. Note that there exists a narrow periodic window around (theta sim 0.02) (cf. Fig. 9), and so the large deviations in this window of Allee parameter are not associated with true extreme events, as they occur periodically.Full size imageNote that some mechanisms have been proposed for the generation of extreme events in deterministic dynamical systems, which typically have been excitable systems. These include interior crisis, Pomeau-Manneville intermittency, and the breakdown of quasiperiodic motion. However the extreme events generated by these mechanisms occur typically at very specific critical points in parameter space, or narrow windows around it. The first important difference in our system here is that the extreme events do not emerge only at some special values alone. Rather, there is a broad range in Allee parameter space where extreme events have a very significant presence. This makes our extreme event phenomenon more robust, and thus increases its potential observability. This also rules out the intermittency-induced mechanisms that have been proposed, as is evident through the lack of sudden expansion in attractor size in our bifurcation diagram (Fig. 3) in general.However, interestingly, the system does have one parameter window where there is attractor widening and this gives rise to a markedly enhanced extreme event count. The peak observed in Fig. 8 can be directly correlated with a sudden attractor widening leading to a marked increase of extreme event in a narrow window of parameter space located near the crisis (see Fig. 9). Additionally, for a narrow window around (theta sim 0.02), the emergent dynamics is periodic. So the large deviations are no longer uncorrelated, and so they are not extreme events in the true sense.Figure 9Bifurcation diagram of prey populations with respect to Allee parameter, in the range (theta in [0.0189 : 0.0191]). Here we display the local maxima of the prey population. The parameter values in Eq. (1) are as mentioned in the text.Full size imageLastly we notice that the predator population shows extreme events for all values of (theta in [0,theta _{c})). So the predator population is most prone to experiencing unusually large deviations from the mean. We also observe that the probability of occurrence of extreme events in the predator population is not affected significantly by the Allee effect. This is in marked contrast to the case of vegetation and prey, where the Allee effect crucially influences the advent of extreme events. Also, for the predator population there is no marked transition from zero to finite (P_{ext}) under increasing Allee parameter (theta), as evident for vegetation and prey populations. More

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    Field evidence for microplastic interactions in marine benthic invertebrates

    1.Geyer, R., Jambeck, J. R. & Law, K. L. Production, use and fate of all plastics ever made. Sci. Adv. 3, e1700782 (2017).2.Napper, I. E. & Thompson, R. C. Marine plastic pollution: other than microplastic in Waste: A Handbook for Management, Second Edition (ed. Letcher, T. & Vallero, D.) chapter 22, 425–442 (Academic Press, 2019).3.Eriksen, M. et al. Plastic pollution in the world’s oceans: more than 5 trillion plastic pieces weighing over 250,000 tons afloat at sea. PLoS ONE 9, e111913 (2014).4.Sharma, S. & Chatterjee, S. Microplastic pollution, a threat to marine ecosystem and human health: a short review. Environ. Sci. Pollut. Res. 24, 21530–21547 (2017).Article 

    Google Scholar 
    5.Rocha-Santos, T. & Duarte, A. C. A critical overview of the analytical approaches to the occurrence, the fate and the behavior or microplastics in the environment. TrAC Trends Anal. Chem. 65, 47–53 (2015).CAS 
    Article 

    Google Scholar 
    6.Cózar, A. et al. Plastic accumulation in the mediterranean sea. PLoS ONE 10, e0121762 (2015).7.Suaria, G. & Aliani, S. Floating debris in the Mediterranean Sea. Mar. Pollut. Bull. 86, 494–504 (2014).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    8.Auta, H. S., Emenike, C. U. & Fauziah, S. H. Distribution and importance of microplastics in the marine environment: A review of the sources, fate, effects, and potential solutions. Environ. Int. 102, 165–176 (2017).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    9.Woodall, L. C. et al. The deep sea is a major sink for microplastic debris. R. Soc. Open Sci. 1, 140317 (2014).10.Kershaw, P., Turra, A. & Galgani, F. Guidelines for the monitoring and assessment of plastic litter in the ocean. GESAMP Reports and Studies No. 99 (2019).11.Desforges, J. P. W., Galbraith, M. & Ross, P. S. Ingestion of microplastics by zooplankton in the Northeast Pacific Ocean. Arch. Environ. Contam. Toxicol. 69, 320–330 (2015).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    12.Van Cauwenberghe, L., Claessens, M., Vandegehuchte, M. B. & Janssen, C. R. Microplastics are taken up by mussels (Mytilus edulis) and lugworms (Arenicola marina) living in natural habitats. Environ. Pollut. 199, 10–17 (2015).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    13.Setälä, O., Norkko, J. & Lehtiniemi, M. Feeding type affects microplastic ingestion in a coastal invertebrate community. Mar. Pollut. Bull. 102, 95–101 (2016).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    14.Amelineau, F. et al. Microplastic pollution in the Greenland Sea: Background levels and selective contamination of planktivorous diving seabirds. Environ. Pollut. 219, 1131–1139 (2016).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    15.Zhu, J. et al. Cetaceans and microplastics: First report of microplastic ingestion by a coastal delphinid Sousa chinensis. Sci. Total Environ. 659, 649–654 (2019).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    16.Sbrana, A. et al. Spatial variability and influence of biological parameters on microplastic ingestion by Boops boops (L.) along the Italian coasts (Western Mediterranean Sea). Environ. Pollut. 263, 114429 (2020).17.De Sa, L. C., Luís, L. G. & Guilhermino, L. Effects of microplastics on juveniles of the common goby (Pomatoschistus microps): confusion with prey, reduction of the predatory performance and efficiency, and possible influence of developmental conditions. Environ. Pollut. 196, 359–362 (2015).Article 
    CAS 

    Google Scholar 
    18.Gallitelli, L., Cera, A., Cesarini, G., Pietrelli, L. & Scalici, M. Preliminary indoor evidences of microplastic effects on freshwater benthic macroinvertebrates. Sci. Rep. 11, 720 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    19.Karlsson, T. M. et al. Screening for microplastics in sediment, water, marine invertebrates and fish: Method development and microplastic accumulation. Mar. Pollut. Bull. 122, 403–408 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    20.Bour, A., Avio, C. G., Gorbi, S., Regoli, F. & Hylland, K. Presence of microplastics in benthic and epibenthic organisms: Influence of habitat, feeding mode and trophic level. Environ. Pollut. 243, 1217–1225 (2018).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    21.Díaz-Castañeda, V., & Reish, D. Polychaetes in environmental studies in Annelids as Model Systems in the Biological Sciences (ed. Shain, D. H.) chapter 11, 205–227 (Wiley, 2009).22.Gusmão, F. et al. In situ ingestion of microfibres by meiofauna from sandy beaches. Environ. Pollut. 216, 584–590 (2016).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    23.Missawi, O. et al. Abundance and distribution of small microplastics (≤ 3 μm) in sediments and seaworms from the Southern Mediterranean coasts and characterisation of their potential harmful effects. Environ. Pollut. 263, 114634 (2020).24.Piarulli, S. et al. Do different habits affect microplastics contents in organisms? A trait-based analysis on salt marsh species. Mar. Pollut. Bull. 153, 110983 (2020).25.Knutsen, et al. Microplastic accumulation by tube-dwelling, suspension feeding polychaetes from the sediment surface: A case study from the Norwegian Continental Shelf. Mar. Environ. Res. 161, 105073 (2020).26.Lusher, A. L., Welden, N. A., Sobral, P. & Cole, M. Sampling, isolating and identifying microplastics ingested by fish and invertebrates. Anal. Methods 9, 1346–1360 (2017).Article 

    Google Scholar 
    27.Foekema, E. M. et al. Plastics in North Sea fish. Environ. Sci. Technol. 47, 8818–8824 (2013).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    28.Rochman, C. M. et al. Anthropogenic debris in seafood: Plastic debris and fibers from textiles in fish and bivalves sold for human consumption. Sci. Rep. 5, 1–10 (2015).Article 
    CAS 

    Google Scholar 
    29.Avio, C. G., Gorbi, S. & Regoli, F. Experimental development of a new protocol for extraction and characterization of microplastics in fish tissues: First observations in commercial species from Adriatic Sea. Mar. Environ. Res. 111, 18–26 (2015).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    30.Li, J., Yang, D., Li, L., Jabeen, K. & Shi, H. Microplastics in commercial bivalves from China. Environ. Pollut. 207, 190–195 (2015).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    31.Claessens, M., Van Cauwenberghe, L., Vandegehuchte, M. B. & Janssen, C. R. New techniques for the detection of microplastics in sediments and field collected organisms. Mar. Pollut. Bull. 70, 227–233 (2013).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    32.Bianchi, J. et al. Food preference determines the best suitable digestion protocol for analysing microplastic ingestion by fish. Mar. Pollut. Bull. 154, 1–9 (2020).Article 
    CAS 

    Google Scholar 
    33.Cole, M. et al. Isolation of microplastics in biota-rich seawater samples and marine organisms. Sci. Rep. 4, 4528 (2014).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    34.Dehaut, A. et al. Microplastics in seafood: Benchmark protocol for their extraction and characterization. Environ. Pollut. 215, 223–233 (2016).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    35.Phuong, N. N., Poirier, L., Pham, Q. T., Lagarde, F. & Zalouk-Vergnoux, A. Factors influencing the microplastic contamination of bivalves from the French Atlantic coast: Location, season and/or mode of life?. Mar. Pollut. Bull. 129, 664–674 (2018).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    36.Valente, T. et al. Exploring microplastic ingestion by three deepwater elasmobranch species: a case study from the Tyrrhenian Sea. Environ. Pollut. 253, 342–350 (2019).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    37.Thompson, R. C. et al. Lost at sea: Where is all the plastic?. Science 304, 838 (2004).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    38.Mathalon, A. & Hill, P. Microplastic fibers in the intertidal ecosystem surrounding Halifax Harbor Nova Scotia. Mar. Pollut. Bull. 81, 69–79 (2014).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    39.Setälä, O., Fleming-Lehtinen, V. & Lehtiniemi, M. Ingestion and transfer of microplastics in the planktonic food web. Environ. Pollut. 185, 77–83 (2014).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    40.Jang, M., Shim, W. J., Han, G. M., Song, Y. K. & Hong, S. H. Formation of microplastics by polychaetes (Marphysa sanguinea) inhabiting expanded polystyrene marine debris. Mar. Pollut. Bull. 131, 365–369 (2018).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    41.Naidu, S. A., Rao, V. R. & Ramu, K. Microplastics in the benthic invertebrates from the coastal waters of Kochi Southeastern Arabian Sea. Environ. Geochem. Health 40, 1377–1383 (2018).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    42.Revel, M. et al. (2018). Accumulation and immunotoxicity of microplastics in the estuarine worm Hediste diversicolor in environmentally relevant conditions of exposure. Environ. Sci. Pollut. Res. 27, 3574–3583 (2018).43.Näkki, P., Setälä, O. & Lehtiniemi, M. Seafloor sediments as microplastic sinks in the northern Baltic Sea-Negligible upward transport of buried microplastics by bioturbation. Environ. Pollut. 249, 74–81 (2019).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    44.Amin, R. M., Sohaimi, E. S., Anuar, S. T. & Bachok, Z. Microplastic ingestion by zooplankton in Terengganu coastal waters, southern South China Sea. Mar. Pollut. Bull. 150, 110616 (2020).45.Jang, M. et al. A close relationship between microplastic contamination and coastal area use pattern. Water Res. 171, 115400 (2020).46.Torre, M., Digka, N., Anastasopoulou, A., Tsangaris, C. & Mytilineou, C. Anthropogenic microfibres pollution in marine biota. A new and simple methodology to minimize airborne contamination. Mar. Pollut. Bull. 113, 55–61 (2016).47.Courtene-Jones, W., Quinn, B., Murphy, F., Gary, S. F. & Narayanaswamy, B. E. Optimisation of enzymatic digestion and validation of specimen preservation methods for the analysis of ingested microplastics. Anal. Methods 9, 1437–1445 (2017).CAS 
    Article 

    Google Scholar 
    48.Digka, N., Tsangaris, C., Torre, M., Anastasopoulou, A. & Zeri, C. Microplastics in mussels and fish from the Northern Ionian Sea. Mar. Pollut. Bull. 135, 30–40 (2018).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    49.Ding, J. et al. Detection of microplastics in local marine organisms using a multi-technology system. Anal. Methods 11, 78–87 (2019).CAS 
    Article 

    Google Scholar 
    50.Botterell, Z. L. et al. Bioavailability and effects of microplastics on marine zooplankton: A review. Environ. Pollut. 245, 98–110 (2019).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    51.Huerta Lwanga, E. et al. Microplastics in the Terrestrial Ecosystem: Implications for Lumbricus terrestris (Oligochaeta, Lumbricidae). Environ. Sci. Technol. 50, 2685–2691 (2016).52.Hurley, R. R., Woodward, J. C. & Rothwell, J. J. Ingestion of microplastics by freshwater Tubifex worms. Environ. Sci. Technol. 51, 12844–12851 (2017).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    53.Kowalski, N., Reichardt, A. M. & Waniek, J. J. Sinking rates of microplastics and potential implications of their alteration by physical, biological, and chemical factors. Mar. Pollut. Bull. 109, 310–319 (2016).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    54.PlasticsEurope. Plastics – the Facts 2019. An analysis of European plastics production, demand and waste data, p. 42 (2019). FINAL web version Plastics the facts2019 14102019.pdf.55.Horton, T. et al. World Register of Marine Species (2021). https://doi.org/10.14284/170.56.Currie, D. R., McArthur, M. A. & Cohen, B. F. Reproduction and distribution of the invasive European fanworm Sabella spallanzanii (Polychaeta: Sabellidae) in Port Phillip Bay, Victoria Australia. Mar. Biol. 136, 645–656 (2000).Article 

    Google Scholar 
    57.Giangrande, A. et al. Utilization of the filter feeder polychaete Sabella. Aquac. Int. 13, 129–136 (2005).Article 

    Google Scholar 
    58.Stabili, L., Licciano, M., Giangrande, A., Fanelli, G. & Cavallo, R. A. Sabella spallanzanii filter-feeding on bacterial community: ecological implications and applications. Mar. Environ. Res. 61, 74–92 (2006).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    59.Schulze, A., Grimes, C. J. & Rudek, T. E. Tough, armed and omnivorous: Hermodice carunculata (Annelida: Amphinomidae) is prepared for ecological challenges. J. Mar. Biolog. Assoc. U. K. 97, 1075–1080 (2017).CAS 
    Article 

    Google Scholar 
    60.Jumars, P. A., Dorgan, K. M. & Lindsay, S. M. Diet of worms emended: an update of polychaete feeding guilds. Annu. Rev. Mar. Sci. 7, 497–520 (2015).ADS 
    Article 

    Google Scholar 
    61.Nel, H. A., Hean, J. W., Noundou, X. S. & Froneman, P. W. Do microplastic loads reflect the population demographics along the southern African coastline?. Mar. Pollut. Bull. 115, 115–119 (2016).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    62.Stolte, A., Forster, S., Gerdts, G. & Schubert, H. Microplastic concentrations in beach sediments along the German Baltic coast. Mar. Pollut. Bull. 99, 216–229 (2015).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    63.Karami, A. et al. A high-performance protocol for extraction of microplastics in fish. Sci. Total Environ. 578, 485–494 (2017).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    64.Hermsen, E., Mintenig, S. M., Besseling, E. & Koelmans, A. A. Quality criteria for the analysis of microplastic in biota samples: A critical review. Environ. Sci. Technol. 52, 10230–10240 (2018).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    65.Developer Core Team, R. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing (2019).66.Hui, W., Gel, Y. R. & Gastwirth, J. L. Lawstat: An R package for law, public policy and biostatistics. J. Stat. Softw. 28, 1–26 (2008).Article 

    Google Scholar 
    67.Ripley, B. et al. Support Functions and Datasets for Venables and Ripley’s MASS (4th edition) (Springer, 2002).68.Breheny, P. & Burchett, W. Visualization of regression models using visreg. R. J. 9, 56–71 (2017).Article 

    Google Scholar  More

  • in

    High canopy cover of invasive Acer negundo L. affects ground vegetation taxonomic richness

    1.Vinogradova, Y. K., Mayorov, S. R. & Khorun, L. V. Chernaya kniga flory Sredney Rossii (Chuzherodnye vidy rasteniy v ekosistemakh Sredney Rossii) (The Black-book of the flora of the Middle Russia (Alien species in the plant communities of the Middle Russia). (GEOS, 2010).2.Straigytė, L., Cekstere, G., Laivins, M. & Marozas, V. The spread, intensity and invasiveness of the Acer negundo in Riga and Kaunas. Dendrobiology 74, 157–168 (2015).Article 

    Google Scholar 
    3.Merceron, N. R., Lamarque, L. J., Delzon, S. & Porté, A. J. Killing it softly: girdling as an efficient eco-friendly method to locally remove invasive Acer negundo. Ecol. Restor. 34, 297–305 (2016).Article 

    Google Scholar 
    4.Gusev, A. P., Shpilevskaya, N. S. & Veselkin, D. V. The influence of Acer negundo L. on progressive successions in Belarusian landscapes. Vestnik Vitebskogo Gosudarstvennogo Universiteta. 94, 47–53 (2017).
    Google Scholar 
    5.Veselkin, D. V. & Korzhinevskaya, A. A. Spatial factors of understory adventization in park forests of a large city. Izvestiya Akademii Nauk, Seriya Geograficheskaya. 4, 54–64 (2018).
    Google Scholar 
    6.Veselkin, D. V., Korzhinevskaya, A. A. & Podgayevskaya, E. N. The species composition and abundance of alien and invasive understory shrubs and trees in urban forests of Yekaterinburg. Vestnik Tomskogo gosudarstvennogo universiteta. Biologiya. 42, 102–118 (2018).
    Google Scholar 
    7.Emelyanov, A. V. & Frolova, S. V. Ash-leaf maple (Acer negundo L.) in coastal phytocenoses of the Vorona River. Russ. J. Biol. Invasions 2, 161–163 (2011).Article 

    Google Scholar 
    8.Saccone, P., Pagès, J.-P., Girel, J., Brun, J.-J. & Michalet, R. Acer negundo invasion along a successional gradient: Early direct facilitation by native pioneers and late indirect facilitation by conspecifics. New Phytol. 187, 831–842. https://doi.org/10.1111/j.1469-8137.2010.03289.x (2010).Article 
    PubMed 

    Google Scholar 
    9.Kostina, M. V., Yasinskaya, O. I., Barabanshchikova, N. S. & Orlyuk, F. A. Toward a issue of box elder invasion into the forests around Moscow. Russ. J. Biol. Invasions 7, 47–51 (2016).Article 

    Google Scholar 
    10.Veselkin, D. V. & Dubrovin, D. I. Diversity of the grass layer of urbanized communities dominated by invasive Acer negundo. Russ. J. Ecol. 50, 413–421 (2019).Article 

    Google Scholar 
    11.Reinhart, K. O., Greene, E. & Callaway, R. M. Effects of Acer platanoides invasion on understory plant communities and tree regeneration in the Rocky Mountains. Ecography 28, 573–582 (2005).Article 

    Google Scholar 
    12.Schuster, M. J. & Reich, P. B. Amur maple (Acer ginnala): an emerging invasive plant in North America. Biol. Invasions 20, 2997–3007 (2018).Article 

    Google Scholar 
    13.Richardson, D. M. et al. Naturalization and invasion of alien plants: Concepts and definitions. Divers. Distrib. 6, 93–107 (2000).Article 

    Google Scholar 
    14.Gorchov, D. L. & Trisel, D. E. Competitive effects of the invasive shrub, Lonicera maackii (Rupr.) Herder (Caprifoliaceae), on the growth and survival of native tree seedlings. Plant Ecol. 166, 13–24 (2003).Article 

    Google Scholar 
    15.Knight, K. S., Oleksyn, J., Jagodzinski, A. M., Reich, P. B. & Kasprowicz, M. Overstorey tree species regulate colonization by native and exotic plants: A source of positive relationships between understorey diversity and invasibility. Divers. Distrib. 14, 666–675 (2008).Article 

    Google Scholar 
    16.Niinemets, Ü. A review of light interception in plant stands from leaf to canopy in different plant functional types and in species with varying shade tolerance. Ecol. Res. 25, 693–714 (2010).Article 

    Google Scholar 
    17.Allison, S. D. & Vitousek, P. M. Rapid nutrient cycling in leaf litter from invasive plants in Hawaii. Oecologia 141, 612–619 (2004).ADS 
    PubMed 
    Article 

    Google Scholar 
    18.Gioria, M. & Osborne, B. A. Resource competition in plant invasions: Emerging patterns and research needs. Front. Plant Sci. https://doi.org/10.3389/fpls.2014.00501 (2014).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    19.Bonifacio, E. et al. Alien red oak affects soil organic matter cycling and nutrient availability in low-fertility well-developed soils. Plant Soil 395, 215–229 (2015).CAS 
    Article 

    Google Scholar 
    20.Horodecki, P. & Jagodzínski, A. M. Tree species effects on litter decomposition in pure stands on afforested post-mining sites. For. Ecol. Manag. 406, 1–11 (2017).Article 

    Google Scholar 
    21.Zhang, P., Li, B., Wu, J. & Hu, S. Invasive plants differentially affect soil biota through litter and rhizosphere pathways: a meta-analysis. Ecol. Lett. 22, 200–210 (2019).ADS 
    PubMed 
    Article 

    Google Scholar 
    22.Callaway, R. M., Thelen, G. C., Rodriguez, A. & Holben, W. E. Soil biota and exotic plant invasion. Nature 427, 731–733 (2004).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    23.Stinson, K. A. et al. Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol. https://doi.org/10.1371/journal.pbio.0040140 (2006).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    24.Suding, K. N. et al. Consequences of plant-soil feedbacks in invasion. J. Ecol. 101, 298–308 (2013).Article 

    Google Scholar 
    25.Mueller, K. E. et al. Light, earthworms, and soil resources as predictors of diversity of 10 soil invertebrate groups across monocultures of 14 tree species. Soil Biol. Biochem. 92, 184–198 (2016).CAS 
    Article 

    Google Scholar 
    26.Kamczyc, J., Dyderski, M. K., Horodecki, P. & Jagodzinski, A. M. Mite communities (Acari, Mesostigmata) in the initially decomposed ‘litter islands’ of 11 tree species in scots pine (Pinus sylvestris L.) forest. Forests https://doi.org/10.3390/f10050403 (2019).Article 

    Google Scholar 
    27.Veselkin, D. V., Rafikova, O. S. & Ekshibarov, E. D. The soil of invasive Acer negundo thickets is unfavorable for mycorrhizal formation in native herbs. Zh. Obshch. Biol. 80, 214–225 (2019).
    Google Scholar 
    28.Gilliam, F. S. & Roberts, M. R. Interactions between the herbaceous layer and overstory canopy of eastern forests in The herbaceous layer in forests of Eastern North America (ed. Gilliam, F. S.) 233–254 (Oxford, 2014).29.Landuyt, D. et al. The functional role of temperate forest understorey vegetation in a changing world. Glob. Change Biol. 25, 3625–3641 (2019).ADS 
    Article 

    Google Scholar 
    30.Czapiewska, N., Dyderski, M. K. & Jagodzinski, A. M. Seasonal dynamics of floodplain forest understory—Impacts of degradation, light availability and temperature on biomass and species composition. Forests https://doi.org/10.3390/f10010022 (2019).Article 

    Google Scholar 
    31.Canham, C. D., Finzi, A. C., Pacala, S. W. & Burbank, D. H. Causes and consequences of resource heterogeneity in forests: Interspecific variation in light transmission by canopy trees. Can. J. For. Res. 24, 337–349 (1994).Article 

    Google Scholar 
    32.Barbier, S., Gosselin, F. & Balandier, P. Influence of tree species on understory vegetation diversity and mechanisms involved—A critical review for temperate and boreal forests. For. Ecol. Manag. 254, 1–15 (2008).Article 

    Google Scholar 
    33.Reinhart, K. O., Gurnee, J., Tirado, R. & Callaway, R. M. Invasion through quantitative effects: Intense shade drives native decline and invasive success. Ecol. Appl. 16, 1821–1831 (2006).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    34.Nilsson, C., Engelmark, O., Cory, J., Forsslund, A. & Carlborg, E. Differences in litter cover and understory flora between stands of introduced lodgepole pine and native Scots pine in Sweden. For. Ecol. Manag. 255, 1900–1905 (2008).Article 

    Google Scholar 
    35.Bravo-Monasterio, P., Pauchard, A. & Fajardo, A. Pinus contorta invasion into treeless steppe reduces species richness and alters species traits of the local community. Biol. Invasions 18, 1883–1894 (2016).Article 

    Google Scholar 
    36.Lanta, V., Hyvönen, T. & Norrdahl, K. Non-native and native shrubs have differing impacts on species diversity and composition of associated plant communities. Plant Ecol. 214, 1517–1528 (2013).Article 

    Google Scholar 
    37.Dyderski, M. K. & Jagodzinski, A. M. Similar impacts of alien and native tree species on understory light availability in a temperate forest. Forests https://doi.org/10.3390/f10110951 (2019).Article 

    Google Scholar 
    38.Bottollier-Curtet, M. et al. Light interception principally drives the understory response to boxelder invasion in riparian forests. Biol. Invasions 14, 1445–1458 (2012).Article 

    Google Scholar 
    39.Cusack, D. F. & McCleery, T. L. Patterns in understory woody diversity and soil nitrogen across native- and non-native-urban tropical forests. For. Ecol. Manag. 318, 34–43 (2014).Article 

    Google Scholar 
    40.Berg, C., Drescherl, A. & Essl, F. Using relevé-based metrics to explain invasion patterns of alien trees in temperate forests. Tuexenia. 37, 127–142 (2017).
    Google Scholar 
    41.Hladyz, S., Abjornsson, K., Giller, P. S. & Woodward, G. Impacts of an aggressive riparian invader on community structure and ecosystem functioning in stream food webs. J. Appl. Ecol. 48, 443–452 (2011).Article 

    Google Scholar 
    42.Call, L. J. & Nilsen, E. T. Analysis of interactions between the invasive tree-of-heaven (Ailanthus altissima) and the native black locust (Robinia pseudoacacia). Plant Ecol. 176, 275–285 (2005).Article 

    Google Scholar 
    43.Dorning, M. & Cipollini, D. Leaf and root extracts of the invasive shrub, Lonicera maackii, inhibit seed germination of three herbs with no autotoxic effects. Plant Ecol. 184, 287–296 (2006).Article 

    Google Scholar 
    44.Kumar, A. S. & Bais, H. P. Allelopathy and exotic plant invasion in Plant communication from an ecological perspective. Signaling and communication in plants (ed. Baluška, F. & Ninkovic, V.) 61–74 (Berlin, 2010).45.Cipollini, D., Rigsby, C. M. & Barto, E. K. Microbes as targets and mediators of allelopathy in plants. J. Chem. Ecol. 38, 714–727 (2012).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    46.Nielsen, J. A., Frew, R. D., Whigam, P. A., Callaway, R. M. & Dickinson, K. J. M. Germination and growth responses of co-occurring grass species to soil from under invasive Thymus vulgaris. Allelopath. J. 35, 139–152 (2015).
    Google Scholar 
    47.Gruntman, M., Segev, U., Glauser, G. & Tielbörger, K. Evolution of plant defences along an invasion chronosequence: Defence is lost due to enemy release—but not forever. J. Ecol. 105, 255–264 (2017).CAS 
    Article 

    Google Scholar 
    48.Maron, J. L. & Marler, M. Effects of native species diversity and resource additions on invader impact. Am. Nat. 172, 18–33 (2008).Article 

    Google Scholar 
    49.Hejda, M., Pyšek, P. & Jarošík, V. Impact of invasive plants on the species richness, diversity and composition of invaded communities. J. Ecol. 97, 393–403 (2009).Article 

    Google Scholar 
    50.Adams, J. M. et al. A cross-continental test of the enemy release hypothesis: leaf herbivory on Acer platanoides (L.) is three times lower in North America than in its native Europe. Biol. Invasions 11, 1005–1016 (2009).Article 

    Google Scholar 
    51.Cincotta, C. L., Adams, J. M. & Holzapfel, C. Testing the enemy release hypothesis: A comparison of foliar insect herbivory of the exotic Norway maple (Acer platanoides L.) and the native sugar maple (A. saccharum L.). Biol. Invasions 11, 379–388 (2009).Article 

    Google Scholar 
    52.Veselkin, D. V. et al. Levels of leaf damage by phyllophages in invasive Acer negundo and Native Betula pendula and Salix caprea. Russ. J. Ecol. 50, 511–516 (2019).Article 

    Google Scholar 
    53.Gioria, M., Pyšek, P. & Moravcová, L. Soil seed banks in plant invasions: promoting species invasiveness and long-term impact on plant community dynamics. Preslia 84, 327–350 (2012).
    Google Scholar 
    54.Csiszár, A. Allelopathic effect of invasive woody plant species in Hungary. Acta Silvatica et Lignaria Hungarica. 5, 9–17 (2009).
    Google Scholar 
    55.Csiszár, Á. et al. Allelopathic potential of some invasive plant species occurring in Hungary. Allelopath. J. 31, 309–318 (2013).
    Google Scholar 
    56.Yeryomenko, Y. A. Allelopathic activity of invasive arboreal species. Russ. J. Biol. Invasions 5, 146–150 (2014).Article 

    Google Scholar 
    57.Veselkin, D. V., Kiseleva, O. A., Ekshibarov, E. D., Rafikova, O. S. & Korzhinevskaya, A. A. Abundance and diversity of seedlings of the soil seed bank in the monospecific stands of the invasive species Acer negundo L.. Russ. J. Biol. Invasions. 9, 108–113 (2018).Article 

    Google Scholar 
    58.Davies, C. E., Moss, D. & Hill, M. O. EUNIS Habitat Classification Revised 2004 (European Topic Centre on Nature Protection and Biodiversity, (2004).59.Dopico, E., Ardura, A. & Garcia-Valguez, E. Exploring changes in biodiversity through pictures: A citizen science experience. Soc. Nat. Resour. 30, 1049–1063. https://doi.org/10.1080/08941920.2017.1284292 (2017).Article 

    Google Scholar 
    60.Fitzgerald, N. B., Kirkpatrick, J. B. & Scott, J. J. Rephotography, permanent plots and remote sensing data provide varying insights on vegetation change on subantarctic Macquarie Island, 1980–2015. Austral Ecol. https://doi.org/10.1111/aec.13015 (2021).Article 

    Google Scholar 
    61.Rosenberg, M. S. & Anderson, C. D. PASSAGE: Pattern analysis, spatial statistics, and geographic exegesis version 2. Methods Ecol. Evol. 2, 229–232. https://doi.org/10.1111/j.2041-210X.2010.00081.x (2011).Article 

    Google Scholar  More

  • in

    Microsatellites reveal that genetic mixing commonly occurs between invasive fall armyworm populations in Africa

    1.CABI. Fall Armyworm (FAW) Portal. www.cabi.org/isc/fallarmyworm (2020).2.Westbrook, J., Nagoshi, R., Meagher, R., Fleischer, S. & Jairam, S. Modeling seasonal migration of fall armyworm moths. Int. J. Biometeorol. 60, 255–267. https://doi.org/10.1007/s00484-015-1022-x (2016).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    3.Nagoshi, R. & Meagher, R. Review of fall armyworm (Lepidoptera: noctuidae) genetic complexity and migration. Fla. Entomol. 91, 546–554. https://doi.org/10.1653/0015-4040-91.4.546 (2008).Article 

    Google Scholar 
    4.Nagoshi, R. N., Meagher, R. L. & Jenkins, D. A. Puerto Rico fall armyworm has only limited interactions with those from Brazil or Texas but could have substantial exchanges with Florida populations. J. Econ. Entomol. 103, 360–367. https://doi.org/10.1603/EC09253 (2010).Article 
    PubMed 

    Google Scholar 
    5.Johnson, S. J. Migration and the life history strategy of the fall armyworm, Spodoptera frugiperda in the western hemisphere. Int. J. Trop. Insect Sci. 8, 543–549. https://doi.org/10.1017/S1742758400022591 (1987).Article 

    Google Scholar 
    6.Abrahams, P. et al. Fall Armyworm: Impacts and Implications for Africa. Evidence Note 2 (CABI, 2017).
    Google Scholar 
    7.Nagoshi, R. N. et al. Fall armyworm migration across the Lesser Antilles and the potential for genetic exchanges between North and South American populations. PLoS ONE 12, e0171743. https://doi.org/10.1371/journal.pone.0171743 (2017).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    8.Arias, O. et al. Population genetic structure and demographic history of Spodoptera frugiperda (Lepidoptera: Noctuidae): Implications for insect resistance management programs. Pest Manag. Sci. 75, 2948–2957. https://doi.org/10.1002/ps.5407 (2019).CAS 
    Article 
    PubMed 

    Google Scholar 
    9.Nagoshi, R. et al. Analysis of strain distribution, migratory potential, and invasion history of fall armyworm populations in northern Sub-Saharan Africa. Sci. Rep. 8, 3710–3710. https://doi.org/10.1038/s41598-018-21954-1 (2018).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    10.Nagoshi, R. N., Adamczyk, J. J., Meagher, R. L., Gore, J. & Jackson, R. Using stable isotope analysis to examine fall armyworm (Lepidoptera: Noctuidae) host strains in a cotton habitat. J. Econ. Entomol. 100, 1569. https://doi.org/10.1603/0022-0493(2007)100[1569:USIATE]2.0.CO2 (2007).Article 
    PubMed 

    Google Scholar 
    11.Nagoshi, R. N. et al. Southeastern Asia fall armyworms are closely related to populations in Africa and India, consistent with common origin and recent migration. Sci. Rep. 10, 1421. https://doi.org/10.1038/s41598-020-58249-3 (2020).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    12.Nagoshi, R. N. et al. Genetic characterization of fall armyworm infesting South Africa and India indicate recent introduction from a common source population. PLoS ONE 14, e0217755. https://doi.org/10.1371/journal.pone.0217755 (2019).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    13.Nayyar, N. et al. Population structure and genetic diversity of invasive Fall Armyworm after 2 years of introduction in India. Sci. Rep. 11, 7760. https://doi.org/10.1038/s41598-021-87414-5 (2021).ADS 
    MathSciNet 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    14.Zhang, L. et al. Genetic structure and insecticide resistance characteristics of fall armyworm populations invading China. Mol. Ecol. Resour. 20, 1682–1696. https://doi.org/10.1111/1755-0998.13219 (2020).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    15.Raymond, L., Plantegenest, M. & Vialatte, A. Migration and dispersal may drive to high genetic variation and significant genetic mixing: The case of two agriculturally important, continental hoverflies (E. pisyrphus balteatus and S. phaerophoria scripta). Mol. Ecol. 22, 5329–5339. https://doi.org/10.1111/mec.12483 (2013).Article 
    PubMed 

    Google Scholar 
    16.Stevens, L. et al. Migration and gene flow among domestic populations of the Chagas insect vector Triatoma dimidiata (Hemiptera: Reduviidae) detected by microsatellite loci. J. Med. Entomol. 52, 419–428. https://doi.org/10.1093/jme/tjv002 (2015).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    17.Arias, R. S., Blanco, C. A., Portilla, M., Snodgrass, G. L. & Scheffler, B. E. First microsatellites from Spodoptera frugiperda (Lepidoptera: Noctuidae) and their potential use for population genetics. Ann. Entomol. Soc. Am. 104, 576–587. https://doi.org/10.1603/an10135 (2011).CAS 
    Article 

    Google Scholar 
    18.Pavinato, V. A., Martinelli, S., de Lima, P. F., Zucchi, M. I. & Omoto, C. Microsatellite markers for genetic studies of the fall armyworm, Spodoptera frugiperda. Genet. Mol. Res.: GMR https://doi.org/10.4238/2013.February.8.1 (2013).Article 
    PubMed 

    Google Scholar 
    19.Nagoshi, R., Silvie, P. & Meagher, R. Comparison of haplotype frequencies differentiate fall armyworm (Lepidoptera: Noctuidae) corn-strain populations from Florida and Brazil. J. Econ. Entomol. 100, 954–961 (2007).Article 

    Google Scholar 
    20.Agapow, P.-M. & Burt, A. Indices of multilocus linkage disequilibrium. Mol. Ecol. Notes 1, 101–102. https://doi.org/10.1046/j.1471-8278.2000.00014.x (2001).CAS 
    Article 

    Google Scholar 
    21.Weir, B. S. Genetic Data Analysis II: Methods for Discrete Population Genetic Data (Sinauer, 1996).
    Google Scholar 
    22.Nei, M. Analysis of gene diversity in subdivided populations. Proc. Natl. Acad. Sci. 70, 3321. https://doi.org/10.1073/pnas.70.12.3321 (1973).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar 
    23.Hedrick, P. W. A standardized genetic differentiation measure. Evolution 59, 1633–1638. https://doi.org/10.1111/j.0014-3820.2005.tb01814.x (2005).CAS 
    Article 
    PubMed 

    Google Scholar 
    24.Jost, L. O. U. GST and its relatives do not measure differentiation. Mol. Ecol. 17, 4015–4026. https://doi.org/10.1111/j.1365-294X.2008.03887.x (2008).Article 
    PubMed 

    Google Scholar 
    25.Evanno, G., Regnaut, S. & Goudet, J. Detecting the number of clusters of individuals using the software structure: A simulation study. Mol. Ecol. 14, 2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x (2005).CAS 
    Article 
    PubMed 

    Google Scholar 
    26.Jombart, T. adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403–1405. https://doi.org/10.1093/bioinformatics/btn129 (2008).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    27.Nagoshi, R. N. et al. Comparative molecular analyses of invasive fall armyworm in Togo reveal strong similarities to populations from the eastern United States and the Greater Antilles. PLoS ONE 12, e0181982. https://doi.org/10.1371/journal.pone.0181982 (2017).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    28.Nagoshi, R. N., Goergen, G., Plessis, H. D., van den Berg, J. & Meagher, R. Genetic comparisons of fall armyworm populations from 11 countries spanning sub-Saharan Africa provide insights into strain composition and migratory behaviors. Sci. Rep. 9, 8311. https://doi.org/10.1038/s41598-019-44744-9 (2019).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    29.Buès, R., Bouvier, J. C. & Boudinhon, L. Insecticide resistance and mechanisms of resistance to selected strains of Helicoverpa armigera (Lepidoptera: Noctuidae) in the south of France. Crop Prot. 24, 814–820. https://doi.org/10.1016/j.cropro.2005.01.006 (2005).CAS 
    Article 

    Google Scholar 
    30.Armes, N. J., Jadhav, D. R. & DeSouza, K. R. A survey of insecticide resistance in Helicoverpa armigera in the Indian subcontinent. Bull. Entomol. Res. 86, 499–514. https://doi.org/10.1017/S0007485300039298 (1996).CAS 
    Article 

    Google Scholar 
    31.Parry, H. R. et al. Estimating the landscape distribution of eggs by Helicoverpa spp., with implications for Bt resistance management. Ecol. Model. 365, 129–140. https://doi.org/10.1016/j.ecolmodel.2017.10.004 (2017).Article 

    Google Scholar 
    32.Jones, C. M., Parry, H., Tay, W. T., Reynolds, D. R. & Chapman, J. W. Movement ecology of pest Helicoverpa: Implications for ongoing spread. Annu. Rev. Entomol. 64, 277–295. https://doi.org/10.1146/annurev-ento-011118-111959 (2019).CAS 
    Article 
    PubMed 

    Google Scholar 
    33.Tucker, M. R., Mwandoto, S. & Pedgley, D. E. Further evidence for windborne movement of armyworm moths, Spodoptera exempta, in East Africa. Ecol. Entomol. 7, 463–473. https://doi.org/10.1111/j.1365-2311.1982.tb00689.x (1982).Article 

    Google Scholar 
    34.Rose, D. J. W. et al. Downwind migration of the African army worm moth, Spodoptera exempta, studied by mark-and-capture and by radar. Ecol. Entomol. 10, 299–313. https://doi.org/10.1111/j.1365-2311.1985.tb00727.x (1985).Article 

    Google Scholar 
    35.Rose, D. J. W., Dewhurst, C. F. & Page, W. W. The African Armyworm Handbook: The Status, Biology, Ecology, Epidemiology and Management of Spodoptera exempta (Lepidoptera: Noctuidae) (Natural Resources Institute, 2000).
    Google Scholar 
    36.Chapman, J. W., Reynolds, D. R. & Wilson, K. Long-range seasonal migration in insects: Mechanisms, evolutionary drivers and ecological consequences. Ecol. Lett. 18, 287–302. https://doi.org/10.1111/ele.12407 (2015).Article 
    PubMed 

    Google Scholar 
    37.Nagoshi, R. N. & Meagher, R. L. Using intron sequence comparisons in the triose-phosphate isomerase gene to study the divergence of the fall armyworm host strains. Insect Mol. Biol. 25, 324–337. https://doi.org/10.1111/imb.12223 (2016).CAS 
    Article 
    PubMed 

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

    Google Scholar 
    39.Thompson, J. D., Higgins, D. G. & Gibson, T. J. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22, 4673–4680. https://doi.org/10.1093/nar/22.22.4673 (1994).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    40.R Core Team. R Foundation for Statistical Computing (R Core Team, 2020).
    Google Scholar 
    41.Paradis, E. pegas: An R package for population genetics with an integrated–modular approach. Bioinformatics 26, 419–420. https://doi.org/10.1093/bioinformatics/btp696 (2010).CAS 
    Article 
    PubMed 

    Google Scholar 
    42.Adamack, A. & Gruber, B. PopGenReport: Simplifying basic population genetic analyses in R. Methods Ecol. Evol. https://doi.org/10.1111/2041-210X.12158 (2014).Article 

    Google Scholar 
    43.Goudet, J. Hierfstat, a package for r to compute and test hierarchical F-statistics. Mol. Ecol. Notes 5, 184–186. https://doi.org/10.1111/j.1471-8286.2004.00828.x (2005).Article 

    Google Scholar 
    44.Winter, D. MMOD: An R library for the calculation of population differentiation statistics. Mol. Ecol. Resour. https://doi.org/10.1111/j.1755-0998.2012.03174.x (2012).Article 
    PubMed 

    Google Scholar 
    45.Kamvar, Z. N., Tabima, J. F. & Grünwald, N. J. Poppr: An R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2, e281. https://doi.org/10.7717/peerj.281 (2014).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    46.Raymond, M. & Rousset, F. GENEPOP (version 1.2): Population genetics software for exact tests and ecumenicism. J. Hered. 86, 248–249. https://doi.org/10.1093/oxfordjournals.jhered.a111573 (1995).Article 

    Google Scholar 
    47.Oksanen, J. et al. Vegan: Community Ecology Package. R package version 2.0-2. (2012).48.Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000).CAS 
    Article 

    Google Scholar 
    49.Earl, D. A. & von Holdt, B. M. STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4, 359–361. https://doi.org/10.1007/s12686-011-9548-7 (2012).Article 

    Google Scholar 
    50.Jakobsson, M. & Rosenberg, N. A. CLUMPP: A cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23, 1801–1806. https://doi.org/10.1093/bioinformatics/btm233 (2007).CAS 
    Article 
    PubMed 

    Google Scholar 
    51.Rosenberg, N. A. DISTRUCT: A program for the graphical display of population structure. Mol. Ecol. Notes 4, 137–138. https://doi.org/10.1046/j.1471-8286.2003.00566.x (2004).Article 

    Google Scholar  More

  • in

    The invasive cactus Opuntia stricta creates fertility islands in African savannas and benefits from those created by native trees

    1.Pyšek, P. et al. Naturalized alien flora of the world. Preslia 89, 203–274 (2017).Article 

    Google Scholar 
    2.Pyšek, P. et al. Scientists’ warning on invasive alien species. Biol. Rev. (2020).3.Vilà, M. et al. Ecological impacts of invasive alien plants: A meta-analysis of their effects on species, communities and ecosystems. Ecol. Lett. 14, 702–708 (2011).PubMed 
    Article 

    Google Scholar 
    4.Pyšek, P. et al. A global assessment of invasive plant impacts on resident species, communities and ecosystems: The interaction of impact measures, invading species’ traits and environment. Glob. Chang. Biol. 18, 1725–1737 (2012).ADS 
    PubMed Central 
    Article 
    PubMed 

    Google Scholar 
    5.Le Roux, J. J. et al. Recent anthropogenic plant extinctions differ in biodiversity hotspots and coldspots. Curr. Biol. 29, 2912-2918.e2 (2019).PubMed 
    Article 
    CAS 

    Google Scholar 
    6.Hulme, P. E. et al. Greater focus needed on alien plant impacts in protected areas. Conserv. Lett. 7, 459–466 (2014).Article 

    Google Scholar 
    7.Foxcroft, L. C., Pyšek, P., Richardson, D. M., Genovesi, P. & MacFadyen, S. Plant invasion science in protected areas: progress and priorities. Biol. Invasions 19, 1353–1378 (2017).Article 

    Google Scholar 
    8.Novoa, A. et al. Invasion syndromes: A systematic approach for predicting biological invasions and facilitating effective management. Biol. Invasions 22, 1801–1820 (2020).Article 

    Google Scholar 
    9.Foxcroft, L. C., Pickett, S. T. A. & Cadenasso, M. L. Expanding the conceptual frameworks of plant invasion ecology. Perspect. Plant Ecol. Evol. Syst. 13, 89–100 (2011).Article 

    Google Scholar 
    10.Scholes, R. J. & Archer, S. R. Tree-grass interactions in savannas. Annu. Rev. Ecol. Syst. 28, 517–544 (1997).Article 

    Google Scholar 
    11.Millennium Ecosystem Assessment. Ecosystems and Human Well-Being: Biodiversity Synthesis (Island Press, 2005).
    Google Scholar 
    12.Foxcroft, L. C., Richardson, D. M., Rejmánek, M. & Pyšek, P. Alien plant invasions in tropical and sub-tropical savannas: Patterns, processes and prospects. Biol. Invasions 12, 3913–3933 (2010).Article 

    Google Scholar 
    13.Rejmánek, M., Huntley, B. J., Le Roux, J. J. & Richardson, D. M. A rapid survey of the invasive plant species in western Angola. Afr. J. Ecol. 55, 56–69 (2017).Article 

    Google Scholar 
    14.Shackleton, R. T., Foxcroft, L. C., Pyšek, P., Wood, L. E. & Richardson, D. M. Assessing biological invasions in protected areas after 30 years: Revisiting nature reserves targeted by the 1980s SCOPE programme. Biol. Conserv. 243, 108424 (2020).Article 

    Google Scholar 
    15.Skarpe, C. Dynamics of savanna ecosystems. J. Veg. Sci. 3, 293–300 (1992).Article 

    Google Scholar 
    16.Okin, G. S. et al. Spatial patterns of soil nutrients in two southern African savannas. J. Geophys. Res. Biogeosci. 113, G2 (2008).Article 

    Google Scholar 
    17.Ridolfi, L., Laio, F. & D’Odorico, P. Fertility island formation and evolution in dryland ecosystems. Ecol. Soc. 13, 5 (2008).Article 

    Google Scholar 
    18.Perroni-Ventura, Y., Montaña, C. & Garcí-a-Oliva, F. Carbon-nitrogen interactions in fertility island soil from a tropical semi-arid ecosystem. Funct. Ecol. 24, 233–242 (2010).Article 

    Google Scholar 
    19.Belnap, J. & Susan, L. P. Soil biota in an ungrazed grassland: response to annual grass (Bromus tectorum) invasion. Ecol. Appl. 51, 1261–1275. (2001).Article 

    Google Scholar 
    20.Ludwig, F., Kroon, H., Prins, H. H. T. & Berendse, F. Effects of nutrients and shade on tree-grass interactions in an East African savanna. J. Veg. Sci. 12, 579–588 (2001).Article 

    Google Scholar 
    21.Reinhart, K. O. & Callaway, R. M. Soil biota and invasive plants. New Phytol. 170, 445–457 (2006).PubMed 
    Article 

    Google Scholar 
    22.Weidenhamer, J. D. & Callaway, R. M. Direct and indirect effects of invasive plants on soil chemistry and ecosystem function. J. Chem. Ecol. 36, 59–69 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    23.Levine, J. M., Pachepsky, E., Kendall, B. E., Yelenik, S. G. & Lambers, J. H. R. Plant-soil feedbacks and invasive spread. Ecol. Lett. 9, 1005–1014 (2006).PubMed 
    Article 

    Google Scholar 
    24.du Toit, J. T., Rogers, K. H. & Biggs, H. C. The Kruger Experience: Ecology and Management of Savanna Heterogeneity. (Island Press, 2003).25.Foxcroft, L. C., Van Wilgen, N. J., Baard, J. A. & Cole, N. S. Biological invasions in South African National Parks. Bothalia 47, 11 (2017).Article 

    Google Scholar 
    26.Pyšek, P. et al. Into the great wide open: do alien plants spread from rivers to dry savanna in the Kruger National Park?. NeoBiota 60, 61–77 (2020).Article 

    Google Scholar 
    27.Kueffer, C., Pyšek, P. & Richardson, D. M. Integrative invasion science: Model systems, multi-site studies, focused meta-analysis and invasion syndromes. New Phytol. 200, 615–633 (2013).PubMed 
    Article 

    Google Scholar 
    28.Lotter, W. D. & Hoffmann, J. H. An integrated management plan for the control of Opuntia stricta (Cactaceae) in the Kruger National Park, South Africa. Koedoe 41, 63–68 (1998).Article 

    Google Scholar 
    29.Hoffmann, J. H., Moran, V. C., Zimmermann, H. G. & Impson, F. A. C. Biocontrol of a prickly pear cactus in South Africa: Reinterpreting the analogous, renowned case in Australia. J. Appl. Ecol. 13737, 1365–2664. (2020).
    Google Scholar 
    30.Foxcroft, L. C., Rouget, M., Richardson, D. M. & MacFadyen, S. Reconstructing 50 years of Opuntia stricta invasion in the Kruger National Park, South Africa: Environmental determinants and propagule pressure. Divers. Distrib. 10, 427–437 (2004).Article 

    Google Scholar 
    31.Novoa, A., Le Roux, J. J., Robertson, M. P., Wilson, J. R. U. & Richardson, D. M. Introduced and invasive cactus species: A global review. AoB Plants 7, 1 (2015).Article 

    Google Scholar 
    32.Foxcroft, L. C., Hoffmann, J. H., Viljoen, J. J. & Kotze, J. J. Environmental factors influencing the distribution of Opuntia stricta, an invasive alien plant in the Kruger National Park, South Africa. S. Afr. J. Bot. 73, 109–112 (2007).Article 

    Google Scholar 
    33.Foxcroft, L. C. & Rejmánek, M. What helps Opuntia stricta invade Kruger National Park, South Africa: Baboons or elephants?. Appl. Veg. Sci. 10, 265–270 (2007).Article 

    Google Scholar 
    34.Anderson, E. F. The Cactus Family. (Timber Press, 2001).35.Reyes-Agüero, J. A., Aguirre, R. J. R. & Valiente-Banuet, A. Reproductive biology of Opuntia: A review. J. Arid Environ. 64, 549–585 (2006).ADS 
    Article 

    Google Scholar 
    36.Robertson, M. P. et al. Assessing local scale impacts of Opuntia stricta (Cactaceae) invasion on beetle and spider diversity in Kruger National Park, South Africa. Afr. Zool. 46, 205–223 (2011).Article 

    Google Scholar 
    37.Butterfield, B. J. & Briggs, J. M. Patch dynamics of soil biotic feedbacks in the Sonoran Desert. J. Arid Environ. 73, 96–102 (2009).ADS 
    Article 

    Google Scholar 
    38.Neffar, S., Chenchouni, H., Beddiar, A. & Redjel, N. Rehabilitation of degraded rangeland in drylands by Prickly Pear (Opuntia ficus-indica L.) plantations: Effect on soil and spontaneous vegetation. Ecol. Balk. 5, 63–76 (2013).39.Garner, W. & Steinberger, Y. A proposed mechanism for the formation of ‘Fertile Islands’ in the desert ecosystem. J. Arid Environ. 16, 257–262 (1989).ADS 
    Article 

    Google Scholar 
    40.Marchante, H., Elizabete M, & Helena, F. Invasion of the Portuguese dune ecosystems by the exotic species Acacia longifolia (Andrews) Willd.: effects at the community level. Plant invasions: ecological threats and management solutions. pp. 75–85 (2003).41.Marchante, E. et al. Short-and long-term impacts of Acacia longifolia invasion on the belowground processes of a Mediterranean coastal dune ecosystem. Appl. Soil Ecol. 40(2), 210–217 (2008).Article 

    Google Scholar 
    42.Yelenik, S. G., Stock, W. D. & Richardson, D. M. Ecosystem level impacts of invasive Acacia saligna in the South African fynbos. Restor. Ecol. 12(1), 44–51 (2004).Article 

    Google Scholar 
    43.Werner, C. et al. High competitiveness of a resource demanding invasive acacia under low resource supply. Plant Ecol. 206(1), 83–96 (2010).Article 

    Google Scholar 
    44.Le Maitre, D. C. et al. Impacts of invasive Australian acacias: implications for management and restoration. Divers. Distrib. 17(5), 1015–1029 (2011).Article 

    Google Scholar 
    45.Bargali, K. & Bargali, S. S. Acacia nilotica: a multipurpose leguminous plant. Nat. Sci. 7, 11–19 (2009).
    Google Scholar 
    46.Rughöft, S. et al. Community composition and abundance of bacterial, archaeal and nitrifying populations in savanna soils on contrasting bedrock material in Kruger National Park, South Africa. Front. Microbiol. 7, 1638 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    47.Neilson, J. W. et al. Life at the hyperarid margin: Novel bacterial diversity in arid soils of the Atacama Desert, Chile. Extremophiles 16, 553–566 (2012).PubMed 
    Article 

    Google Scholar 
    48.de Vos, P. et al. The Firmicutes. Bergey’s Manual of Systematic Bacteriology. (Springer, 2009).49.Brockett, B. F. T., Prescott, C. E. & Grayston, S. J. Soil moisture is the major factor influencing microbial community structure and enzyme activities across seven biogeoclimatic zones in western Canada. Soil Biol. Biochem. 44, 9–20 (2012).CAS 
    Article 

    Google Scholar 
    50.Yang, Y., Dou, Y. & An, S. Testing association between soil bacterial diversity and soil carbon storage on the Loess Plateau. Sci. Total Environ. 626, 48–58 (2018).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    51.Rajaniemi, T. K. & Allison, V. J. Abiotic conditions and plant cover differentially affect microbial biomass and community composition on dune gradients. Soil Biol. Biochem. 41, 102–109 (2009).CAS 
    Article 

    Google Scholar 
    52.Novoa, A., Rodríguez, R., Richardson, D. & González, L. Soil quality: A key factor in understanding plant invasion? The case of Carpobrotus edulis (L.) N.E.Br. Biol. Invasions 16, 429–443 (2014).53.Penfield, S. Seed dormancy and germination. Curr. Biol. 27, R874–R878 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    54.Tielbörger, K. & Prasse, R. Do seeds sense each other? Testing for density-dependent germination in desert perennial plants. Oikos 118, 792–800 (2009).Article 

    Google Scholar 
    55.Renne, I. J. et al. Eavesdropping in plants: delayed germination via biochemical recognition. J. Ecol. 102, 86–94 (2014).Article 

    Google Scholar 
    56.Yannelli, F. A., Novoa, A., Lorenzo, P., Rodríguez, J. & Le Roux, J. J. No evidence for novel weapons: biochemical recognition modulates early ontogenetic processes in native species and invasive acacias. Biol. Invasions 22, 549–562 (2020).Article 

    Google Scholar 
    57.Al-Wakeel, S. A. M., Gabr, M. A., Hamid, A. A. & Abu-El-Soud, W. M. Allelopathic effects of Acacia nilotica leaf residue on Pisum sativum L. Allelopath. J. 19, 411 (2007).
    Google Scholar 
    58.Scholes, M. C., Scholes, R. J., Otter, L. B. & Woghiren, A. J. Biogeochemistry: The cycling of elements. in The Kruger Experience: Ecology and Management of Savanna Heterogeneity (eds. du Toit, J. T., Rogers, K. H. & Biggs, H. C.) 130–148 (Island Press, 2003).59.Kyalangalilwa, B., Boatwright, J. S., Daru, B. H., Maurin, O. & van der Bank, M. Phylogenetic position and revised classification of Acacia s.l. (Fabaceae: Mimosoideae) in Africa, including new combinations in Vachellia and Senegalia. Bot. J. Linn. Soc. 172, 500–523 (2013).Article 

    Google Scholar 
    60.van Wyk, B. & van Wyk, P. Field Guide to Trees of Southern Africa. (Struik Nature, 2013).61.Coates Palgrave, K. & Coates Palgrave, M. Palgrave’s Trees of Southern Africa. (Struik Publishers, 2002).62.Novoa, A., Kumschick, S., Richardson, D. M., Rouget, M. & Wilson, J. R. U. Native range size and growth form in Cactaceae predict invasiveness and impact. NeoBiota 30, 75–90 (2016).Article 

    Google Scholar 
    63.Allen, S. E. Chemical Analysis of Ecological Materials. (Blackwell Scientific Publications, 1989).64.Tabatabai, M. A. & Bremner, J. M. Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol. Biochem. 1, 301–307 (1969).CAS 
    Article 

    Google Scholar 
    65.Kandeler, E. & Gerber, H. Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol. Fertil. Soils 6, 68–72 (1988).CAS 
    Article 

    Google Scholar 
    66.Allison, S. D. & Vitousek, P. M. Extracellular enzyme activities and carbon chemistry as drivers of tropical plant litter decomposition. Biotropica 36, 285–296 (2004).
    Google Scholar 
    67.German, D. P., Chacon, S. S. & Allison, S. D. Substrate concentration and enzyme allocation can affect rates of microbial decomposition. Ecology 92, 1471–1480 (2011).PubMed 
    Article 

    Google Scholar 
    68.Lane, D. J. et al. Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc. Natl. Acad. Sci. 82, 6955–6959 (1985).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    69.Tringe, S. G. & Hugenholtz, P. A renaissance for the pioneering 16S rRNA gene. Curr. Opin. Microbiol. 11, 442–446 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    70.Bukin, Y. S. et al. The effect of 16s rRNA region choice on bacterial community metabarcoding results. Sci. Data 6, 1–14 (2019).Article 
    CAS 

    Google Scholar 
    71.Chakravorty, S., Helb, D., Burday, M., Connell, N. & Alland, D. A detailed analysis of 16S ribosomal RNA gene segments for the diagnosis of pathogenic bacteria. J. Microbiol. Methods 69, 330–339 (2007).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    72.Beckers, B. et al. Performance of 16s rDNA primer pairs in the study of rhizosphere and endosphere bacterial microbiomes in metabarcoding studies. Front. Microbiol. 7, 1–15 (2016).Article 

    Google Scholar 
    73.Thijs, S. et al. Comparative evaluation of four bacteria-specific primer pairs for 16S rRNA gene surveys. Front. Microbiol. 8, 1–15 (2017).Article 

    Google Scholar 
    74.Schloss, P. D., & Westcott, S. L. Assessing and improving methods used in operational taxonomic unit-based approaches for 16S rRNA gene sequence analysis. Appl. Environ. Microbiol. 77(10), 3219–3226 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    75.Schloss, P. D. et al. Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537–7541 (2009).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    76.Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C. & Knight, R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    77.Wang, Q., Garrity, G. M., Tiedje, J. M. & Cole, J. R. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261–5267 (2007).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    78.McMurdie, P. J. & Holmes, S. Waste not, want not: Why rarefying microbiome data is inadmissible. PLoS Comput. Biol. 10, e1003531 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    79.Weiss, S. et al. Normalization and microbial differential abundance strategies depend upon data characteristics. Microbiome 5, 1–18 (2017).Article 

    Google Scholar 
    80.de Cárcer, D. A., Denman, S. E., McSweeney, C. & Morrison, M. Evaluation of subsampling-based normalization strategies for tagged high-throughput sequencing data sets from gut microbiomes. Appl. Environ. Microbiol. 77, 8795–8798 (2011).ADS 
    PubMed 
    Article 
    CAS 

    Google Scholar 
    81.Chiapusio, G., Sánchez, A. M., Reigosa, M. J., González, L. & Pellissier, F. Do germination indices adequately reflect allelochemical effects on the germination process?. J. Chem. Ecol. 23, 2445–2453 (1997).CAS 
    Article 

    Google Scholar 
    82.Oksanen, J. F. et al. vegan: Community Ecology Package. R package version 2.3-3. (2016).83.Jost, L. Entropy and diversity. Oikos 113, 363–375 (2006).Article 

    Google Scholar 
    84.Jost, L. The relation between evenness and diversity. Diversity 2, 207–232 (2010).Article 

    Google Scholar 
    85.Jost, L. Partitioning diversity into independent alpha and beta components. Ecology 88, 2427–2439 (2007).PubMed 
    Article 

    Google Scholar 
    86.Charney, N. & Record, S. vegetarian: Jost Diversity Measures for Community Data. R package version 1.2. (2012).87.Anderson, M. J. A new method for non-parametric multivariate analysis of variance. Austral. Ecol. 26, 32–46 (2001).
    Google Scholar 
    88.Segata, N. et al. Metagenomic biomarker discovery and explanation. Genome Biol. 12, 1–18 (2011).Article 

    Google Scholar 
    89.Clarke, K. R. Non-parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 18, 117–143 (1993).Article 

    Google Scholar  More

  • in

    Interspecific variation in evaporative water loss and temperature response, but not metabolic rate, among hibernating bats

    1.Lyman, C. P. & Chatfield, P. O. Physiology of hibernation in mammals. Physiol. Rev. 35, 403–425 (1955).CAS 
    PubMed 
    Article 

    Google Scholar 
    2.Geiser, F. Hibernation. Curr. Biol. 23, R188–R193 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    3.Humphries, M. M., Thomas, D. W. & Speakman, J. R. Climate-mediated energetic constraints on the distribution of hibernating mammals. Nature 418, 313–316 (2002).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    4.Wilkinson, G. S. & Adams, D. M. Recurrent evolution of extreme longevity in bats. Biol. Lett. 15, 20180860 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    5.Frick, W. F., Reynolds, D. S. & Kunz, T. H. Influence of climate and reproductive timing on demography of little brown myotis Myotis lucifugus. J. Anim. Ecol. 79, 128–136 (2010).PubMed 
    Article 

    Google Scholar 
    6.Willis, C. K. Trade-offs influencing the physiological ecology of hibernation in temperate-zone bats. Integr. Comp. Biol. 57, 1214–1224 (2017).PubMed 
    Article 

    Google Scholar 
    7.Lane, J. E. In Living in a Seasonal World 51–61 (Springer, 2012).8.Inouye, D. W., Barr, B., Armitage, K. B. & Inouye, B. D. Climate change is affecting altitudinal migrants and hibernating species. Proc. Natl. Acad. Sci. 97, 1630–1633 (2000).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    9.Lane, J. E., Kruuk, L. E., Charmantier, A., Murie, J. O. & Dobson, F. S. Delayed phenology and reduced fitness associated with climate change in a wild hibernator. Nature 489, 554–557 (2012).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    10.Feder, M. E. In New Directions in Ecological Physiology (eds M. E. Feder, A. F. Bennett, W. W. Burggren, & R. B Huey) 38–75 (Cambridge University Press, 1987).11.Geiser, F. Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu. Rev. Physiol. 66, 239–274. https://doi.org/10.1146/annurev.physiol.66.032102.115105 (2004).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    12.Boyles, J. G. et al. A global heterothermic continuum in mammals. Glob. Ecol. Biogeogr. 22, 1029–1039 (2013).Article 

    Google Scholar 
    13.Ruf, T. & Arnold, W. Effects of polyunsaturated fatty acids on hibernation and torpor: A review and hypothesis. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294, R1044-1052. https://doi.org/10.1152/ajpregu.00688.2007 (2008).CAS 
    Article 
    PubMed 

    Google Scholar 
    14.Ruf, T. & Geiser, F. Daily torpor and hibernation in birds and mammals. Biol. Rev. Camb. Philos. Soc. https://doi.org/10.1111/brv.12137 (2014).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    15.Heldmaier, G., Ortmann, S. & Elvert, R. Natural hypometabolism during hibernation and daily torpor in mammals. Respir. Physiol. Neurobiol. 141, 317–329 (2004).PubMed 
    Article 

    Google Scholar 
    16.van Breukelen, F. & Martin, S. L. The hibernation continuum: Physiological and molecular aspects of metabolic plasticity in mammals. Physiology 30, 273–281 (2015).PubMed 
    Article 
    CAS 

    Google Scholar 
    17.Nowack, J., Levesque, D. L., Reher, S. & Dausmann, K. H. Variable climates lead to varying phenotypes: ‘Weird’mammalian torpor and lessons from non-Holarctic species. Front. Ecol. Evol. 8, 60 (2020).Article 

    Google Scholar 
    18.Stawski, C., Willis, C. & Geiser, F. The importance of temporal heterothermy in bats. J. Zool. 292, 86–100 (2014).Article 

    Google Scholar 
    19.Thomas, D. W., Dorais, M. & Bergeron, J.-M. Winter energy budgets and cost of arousals for hibernating little brown bats, Myotis lucifugus. J. Mammal. 71, 475–479 (1990).Article 

    Google Scholar 
    20.Kunz, T. H., Wrazen, J. A. & Burnett, C. D. Changes in body mass and fat reserves in pre-hibernating little brown bats (Myotis lucifugus). Ecoscience 5, 8–17 (1998).Article 

    Google Scholar 
    21.Thomas, D. W. & Cloutier, D. Evaporative water loss by hibernating little brown bats, Myotis lucifugus. Physiol. Zool. 65, 443–456 (1992).Article 

    Google Scholar 
    22.Kornfeld, S. F., Biggar, K. K. & Storey, K. B. Differential expression of mature microRNAs involved in muscle maintenance of hibernating little brown bats, Myotis lucifugus: A model of muscle atrophy resistance. Genom. Proteom. Bioinform. 10, 295–301 (2012).CAS 
    Article 

    Google Scholar 
    23.Eddy, S. F., Morin, P. Jr. & Storey, K. B. Differential expression of selected mitochondrial genes in hibernating little brown bats, Myotis lucifugus. J. Exp. Zool. A Comp. Exp. Biol. 305, 620–630 (2006).PubMed 
    Article 
    CAS 

    Google Scholar 
    24.Brigham, R., Ianuzzo, C., Hamilton, N. & Fenton, M. Histochemical and biochemical plasticity of muscle fibers in the little brown bat (Myotis lucifugus). J. Comp. Physiol. B. 160, 183–186 (1990).CAS 
    PubMed 
    Article 

    Google Scholar 
    25.McGuire, L. P., Mayberry, H. W. & Willis, C. K. R. White-nose syndrome increases torpid metabolic rate and evaporative water loss in hibernating bats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 313, R680–R686 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    26.Jonasson, K. A. & Willis, C. K. Hibernation energetics of free-ranging little brown bats. J. Exp. Biol. 215, 2141–2149 (2012).PubMed 
    Article 

    Google Scholar 
    27.Klüg-Baerwald, B. J. & Brigham, R. M. Hung out to dry? Intraspecific variation in water loss in a hibernating bat. Oecologia 183, 977–985 (2017).ADS 
    PubMed 
    Article 

    Google Scholar 
    28.Dunbar, M. B. & Brigham, R. M. Thermoregulatory variation among populations of bats along a latitudinal gradient. J. Comp. Physiol. B 180, 885–893 (2010).PubMed 
    Article 

    Google Scholar 
    29.Yacoe, M. E. Protein metabolism in the pectoralis muscle and liver of hibernating bats, Eptesicus fuscus. J. Comp. Physiol. 152, 137–144 (1983).ADS 
    CAS 
    Article 

    Google Scholar 
    30.Yacoe, M. E. Maintenance of the pectoralis muscle during hibernation in the big brown bat, Eptesicus fuscus. J. Comp. Physiol. 152, 97–104 (1983).Article 

    Google Scholar 
    31.Twente, J. W. & Twente, J. Biological alarm clock arouses hibernating big brown bats, Eptesicus fuscus. Can. J. Zool. 65, 1668–1674 (1987).Article 

    Google Scholar 
    32.Boratyński, J. S., Willis, C. K., Jefimow, M. & Wojciechowski, M. S. Huddling reduces evaporative water loss in torpid Natterer’s bats, Myotis nattereri. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 179, 125–132 (2015).PubMed 
    Article 
    CAS 

    Google Scholar 
    33.Hope, P. R. & Jones, G. Warming up for dinner: Torpor and arousal in hibernating Natterer’s bats (Myotis nattereri) studied by radio telemetry. J. Comp. Physiol. B. 182, 569–578 (2012).PubMed 
    Article 

    Google Scholar 
    34.Park, K. J., Jones, G. & Ransome, R. D. Torpor, arousal and activity of hibernating greater horseshoe bats (Rhinolophus ferrumequinum). Funct. Ecol. 14, 580–588 (2000).Article 

    Google Scholar 
    35.Ben-Hamo, M., Muñoz-Garcia, A., Williams, J. B., Korine, C. & Pinshow, B. Waking to drink: Rates of evaporative water loss determine arousal frequency in hibernating bats. J. Exp. Biol. 216, 573–577 (2013).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    36.Lausen, C. & Barclay, R. Winter bat activity in the Canadian prairies. Can. J. Zool. 84, 1079–1086 (2006).Article 

    Google Scholar 
    37.McGuire, L. P. et al. Similar physiology in hibernating bats across broad geographic ranges. J. Comp. Physiol. B. https://doi.org/10.1007/s00360-021-01400-x (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    38.Zuur, A., Ieno, E. N., Walker, N., Saveliev, A. A. & Smith, G. M. Mixed Effects Models and Extensions in Ecology with R (Springer, New York, 2009).MATH 
    Book 

    Google Scholar 
    39.Hothorn, T. & Everitt, B. S. A handbook of statistical analyses using R (CRC Press, London, 2014).MATH 
    Book 

    Google Scholar 
    40.United States Fish and Wildlife Service. National white-nose syndrome decontamination protocol-Version 09-13-2018. http://www.whitenosesyndrome.org (2018).41.Canadian Cooperative Wildlife Health Centre. Guidelines for decontamination of equipment and clothing to prevent the spread of white-nose syndrome (the causal fungus: Pseudogymnoascus destructans) in Canada, http://www2.cwhc-rcsf.ca/wns_decontamination.php (2020).42.R: A language and environment for statistical computing (R Foundation for Statistical Computing, Vienna, Austria, 2020).43.McGuire, L. P., Guglielmo, C. G., Mackenzie, S. A. & Taylor, P. D. Migratory stopover in the long-distance migrant silver-haired bat, Lasionycteris noctivagans. J. Anim. Ecol. 81, 377–385 (2012).PubMed 
    Article 

    Google Scholar 
    44.Nagorsen, D. W. & Brigham, R. M. Bats of British Columbia. Vol. 1 (UBC Press, 1993).45.Villa, B. R. & Cockrum, E. L. Migration in the guano bat Tadarida brasiliensis mexicana (Saussure). J. Mammal. 43, 43–64 (1962).Article 

    Google Scholar 
    46.Kunkel, E. L. Ecology and energetics of partial migration and facultative hibernation of Mexican free-tailed bats MS thesis, Texas Tech University (2020).47.Sandel, J. K. et al. Use and selection of winter hibernacula by the eastern pipistrelle (Pipistrellus subflavus) in Texas. J. Mammal. 82, 173–178 (2001).Article 

    Google Scholar 
    48.Jones, C. & Pagels, J. Notes on a population of Pipistrellus subflavus in southern Louisiana. J. Mammal. 49, 134–139 (1968).Article 

    Google Scholar 
    49.McClure, M. M. et al. A hybrid corelative-mechanistic approach for modeling and mapping winter distributions of North American bat species. J. Biogeogr. 48, 2429–2444 (2021).Article 

    Google Scholar 
    50.McClure, M. M. et al. Linking surface and subterranean climate: Implications for the study of hibernating bats and other cave dwellers. Ecosphere 11, E03274 (2020).Article 

    Google Scholar 
    51.Perry, R. W. A review of factors affecting cave climates for hibernating bats in temperate North America. Environ. Rev. 21, 28–39. https://doi.org/10.1139/er-2012-0042 (2013).Article 

    Google Scholar 
    52.Hranac, C. R. et al. What is winter? Modelling spatial variation in bat host traits and hibernation and their implications for overwintering energetics. Ecol. Evol. 11, 11604–11614 (2021).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    53.McGuire, L., Muise, K. A., Shrivastav, A. & Willis, C. K. R. No evidence of hyperphagia during prehibernation in a northern population of little brown bats (Myotis lucifugus). Can. J. Zool. 94, 821–827 (2016).CAS 
    Article 

    Google Scholar 
    54.Czenze, Z. J., Jonasson, K. A. & Willis, C. K. Thrifty females, frisky males: Winter energetics of hibernating bats from a cold climate. Physiol. Biochem. Zool. 90, 502–511 (2017).PubMed 
    Article 

    Google Scholar 
    55.Kurta, A. The misuse of relative humidity in ecological studies of hibernating bats. Acta Chiropt. 16, 249–254 (2014).Article 

    Google Scholar 
    56.Weller, T. J. et al. A review of bat hibernacula across the western United States: Implications for white-nose syndrome surveillance and management. PLoS One 13, e0205647 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    57.Gearhart, C., Adams, A. M., Pinshow, B. & Korine, C. Evaporative water loss in Kuhl’s pipistrelles declines along an environmental gradient, from mesic to hyperarid. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 240, 110587 (2020).CAS 
    Article 

    Google Scholar 
    58.Thomas, D. W. & Geiser, F. Periodic arousals in hibernating mammals: Is evaporative water loss involved?. Funct. Ecol. 11, 585–591 (1997).Article 

    Google Scholar 
    59.Haase, C. G. et al. Incorporating evaporative water loss into bioenergetic models of hibernation to test for relative influence of host and pathogen traits on white-nose syndrome. PLoS One 14, e0222311 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    60.Willis, C. K. Conservation physiology and conservation pathogens: White-nose syndrome and integrative biology for host–pathogen systems. Integr. Comp. Biol. 55, 631–641 (2015).PubMed 
    Article 

    Google Scholar 
    61.Frick, W. F. et al. Disease alters macroecological patterns of North American bats. Glob. Ecol. Biogeogr. 24, 741–749 (2015).Article 

    Google Scholar 
    62.Willis, C. K., Menzies, A. K., Boyles, J. G. & Wojciechowski, M. S. Evaporative water loss is a plausible explanation for mortality of bats from white-nose syndrome. Integr. Comp. Biol. 51, 364–373. https://doi.org/10.1093/icb/icr076 (2011).Article 
    PubMed 

    Google Scholar 
    63.Wilder, A. P., Frick, W. F., Langwig, K. E. & Kunz, T. H. Risk factors associated with mortality from white-nose syndrome among hibernating bat colonies. Biol. Lett. 7, 950–953 (2011).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    64.Langwig, K. E. et al. Sociality, density-dependence and microclimates determine the persistence of populations suffering from a novel fungal disease, white-nose syndrome. Ecol. Lett. 15, 1050–1057. https://doi.org/10.1111/j.1461-0248.2012.01829.x (2012).Article 
    PubMed 

    Google Scholar 
    65.Voigt, C. C. & Kingston, T. Bats in the Anthropocene: Conservation of Bats in a Changing World (Springer, New York, 2016).Book 

    Google Scholar 
    66.Kahle, D. & Wickham, H. ggmap: Spatial visualization with ggplot2. R J. 5, 144–161 (2013).Article 

    Google Scholar  More