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    Early human impact on lake cyanobacteria revealed by a Holocene record of sedimentary ancient DNA

    Taranu, Z. E. et al. Acceleration of cyanobacterial dominance in north temperate-subarctic lakes during the Anthropocene. Ecol. Lett. 18, 375–384 (2015).Article 

    Google Scholar 
    Huisman, J. et al. Cyanobacterial blooms. Nat. Rev. Microbiol. 16, 471–483 (2018).Article 
    CAS 

    Google Scholar 
    Monchamp, M. E. et al. Homogenization of lake cyanobacterial communities over a century of climate change and eutrophication. Nat. Ecol. Evol. 2, 317–324 (2018).Article 

    Google Scholar 
    Chorus, I. & Bartram, J. Toxic Cyanobacteria in Water. A Guide to Their Public Health Consequences, Monitoring, and Management. In: World Health Organization (eds. Chorus I. & Bertram J.) (CRC Press, 1999).Rabalais, N. N. et al. Dynamics and distribution of natural and human-caused hypoxia. Biogeosciences 7, 585–619 (2010).Article 
    CAS 

    Google Scholar 
    Carmichael, W. W. Health effects of toxin-producing cyanobacteria: “The CyanoHABs”. Hum. Ecol. Risk Assess. Int. J. 7, 1393–1407 (2001).Article 

    Google Scholar 
    Whitton, B. A. Ecology of Cyanobacteria II: Their Diversity in Space and Time (Springer, 2012).Smol, J. P., Birks, H. J. B. & Last, W. M. Tracking Environmental Change Using Lake Sediments. Volume 4: Zoological Indicators, Developments in Paleoenvironmental Research. (Springer, 2002).Domaizon, I., Winegardner, A., Capo, E., Gauthier, J. & Gregory-Eaves, I. DNA-based methods in paleolimnology: new opportunities for investigating long-term dynamics of lacustrine biodiversity. J. Paleolimnol. 52, 1–21 (2017).Article 

    Google Scholar 
    Livingstone, D. & Jaworski, G. H. M. The viability of akinetes of blue-green algae recovered from the sediments of rostherne mere. Br. Phycol. J. 15, 357–364 (1980).Article 

    Google Scholar 
    van Geel, B., Mur, L. R., Ralska-Jasiewiczowa, M. & Goslar, T. Fossil akinetes of Aphanizomenon and Anabaena as indicators for medieval phosphate-eutrophication of Lake Gosciaz (Central Poland). Rev. Palaeobot. Palynol. 83, 97–105 (1994).Article 

    Google Scholar 
    Hillbrand, M., van Geel, B., Hasenfratz, A., Hadorn, P. & Haas, J. N. Non-pollen palynomorphs show human- and livestock-induced eutrophication of Lake Nussbaumersee (Thurgau, Switzerland) since Neolithic times (3840 bc). Holocene 24, 559–568 (2014).Article 

    Google Scholar 
    Gosling, W. D. et al. Human occupation and ecosystem change on Upolu (Samoa) during the Holocene. J. Biogeogr. 47, 600–614 (2020).Article 

    Google Scholar 
    Hertzberg, S., Liaaen-Jensen, S. & Siegelman, H. W. The carotenoids of blue-green algae. Phytochemistry 10, 3121–3127 (1971).Article 
    CAS 

    Google Scholar 
    Leavitt, P. R. & Findlay, D. L. Comparison of fossil pigments with 20 years of phytoplankton data from eutrophic Lake 227, Experimental Lakes Area, Ontario. Can. J. Fish. Aquat. Sci. 51, 2286–2299 (1994).Article 
    CAS 

    Google Scholar 
    Kaiser, J., Ön, B., Arz, H. & Akçer-Ön, S. Sedimentary lipid biomarkers in the magnesium-rich and highly alkaline Lake Salda (south-western Anatolia). J. Limnol. 75, 581–596 (2016).
    Google Scholar 
    Bauersachs, T., Talbot, H. M., Sidgwick, F., Sivonen, K. & Schwark, L. Lipid biomarker signatures as tracers for harmful cyanobacterial blooms in the Baltic Sea. PLoS ONE 12, e0186360 (2017).Article 

    Google Scholar 
    Domaizon, I. et al. DNA from lake sediments reveals the long-term dynamics and diversity of Synechococcus assemblages. Biogeosci. Discuss. 10, 2515–2564 (2013).
    Google Scholar 
    Britton, G., Liaaen-Jensen, S. & Pfander, H. in Carotenoids (eds. Britton, G., Liaaen-Jensen, S., Pfander, H.). Vol. 4, 1–6 (Birkhäuser Press, 2008).Capo, E. et al. Lake sedimentary dna research on past terrestrial and aquatic biodiversity: overview and recommendations. Quaternary 4, 6 (2021).Article 

    Google Scholar 
    Monchamp, M. E., Walser, J. C., Pomati, F. & Spaak, P. Sedimentary DNA reveals cyanobacterial community diversity over 200 years in two perialpine lakes. Appl. Environ. Microbiol. 82, 6472–6482 (2016).Article 
    CAS 

    Google Scholar 
    Nwosu, E. C. et al. Evaluating sedimentary DNA for tracing changes in cyanobacteria dynamics from sediments spanning the last 350 years of Lake Tiefer See, NE Germany. J. Paleolimnol. 66, 279–296 (2021).Article 

    Google Scholar 
    Zhang, J. et al. Pre-industrial cyanobacterial dominance in Lake Moon (NE China) revealed by sedimentary ancient DNA. Quat. Sci. Rev. 261, 106966 (2021).Article 

    Google Scholar 
    Brauer, A., Schwab, M. J., Brademann, B., Pinkerneil, S. & Theuerkauf, M. Tiefer See–a key site for lake sediment research in NE Germany. DEUQUA Spec. Publ. 2, 89–93 (2019).Article 

    Google Scholar 
    Dräger, N. et al. Varve microfacies and varve preservation record of climate change and human impact for the last 6000 years at Lake Tiefer See (NE Germany). Holocene 27, 450–464 (2017).Article 

    Google Scholar 
    Dräger, N. et al. Hypolimnetic oxygen conditions influence varve preservation and δ13C of sediment organic matter in Lake Tiefer See, NE Germany. J. Paleolimnol. 62, 181–194 (2019).Article 

    Google Scholar 
    Theuerkauf, M., Dräger, N., Kienel, U., Kuparinen, A. & Brauer, A. Effects of changes in land management practices on pollen productivity of open vegetation during the last century derived from varved lake sediments. Holocene 25, 733–744 (2015).Article 

    Google Scholar 
    Heinrich, I. et al. Interdisciplinary geo-ecological research across time scales in the Northeast German Lowland Observatory (TERENO-NE). Vadose Zone J. 17, 1–25 (2018).Article 

    Google Scholar 
    Roeser, P. et al. Advances in understanding calcite varve formation: new insights from a dual lake monitoring approach in the southern Baltic lowlands. Boreas 50, 419–440 (2021).Article 

    Google Scholar 
    Nwosu, E. C. et al. From water into sediment—tracing freshwater Cyanobacteria via DNA analyses. Microorganisms 9, 1778 (2021).Article 
    CAS 

    Google Scholar 
    Schmidt, J. -P. Ein Fremdling im Nordischen Kreis Jungbronzezeitliche Funde aus dem Flachen See bei Sophienhof, Lkr. Mecklenburgische Seenplatte. In: D. Brandherm/B. Nessel (Hrsg.), Phasenübergänge und Umbrüche im bronzezeitlichen Europa. Beiträge zur Sitzung der Arbeitsgemeinschaft Bronzezeit auf der 80. Jahrestagung des Nordwestdeutschen Verbandes für Altertumskunde. Vol. 297, 271–281. (Universitätsforschungen zur Prähistorischen Archäologie, 2017).Raese, H. & Schmidt, J. -P. Zur Besiedlung Mecklenburg-Vorpommernswährend des Spätneolithikums und der frühenBronzezeit (2500–1500 v. Chr.). In: Siedlungsarchäologie des Endneolithikums und der frühen Bronzezeit. 11. Mitteldeutscher Archäologentag (eds. Meller, H., Friedderich, S., Küßner, M., Stäuble, H. & Risch, R.) 621–634 (2019).Kienel, U., Dulski, P., Ott, F., Lorenz, S. & Brauer, A. Recently induced anoxia leading to the preservation of seasonal laminae in two NE-German lakes. J. Paleolimnol. 50, 535–544 (2013).Article 

    Google Scholar 
    Callieri, C. & Stockner, J. Picocyanobacteria success in oligotrophic lakes: fact or fiction? J. Limnol. 59, 72–76 (2000).Article 

    Google Scholar 
    Sollai, M. et al. The Holocene sedimentary record of cyanobacterial glycolipids in the Baltic Sea: an evaluation of their application as tracers of past nitrogen fixation. Biogeosciences 14, 5789–5804 (2017).Article 

    Google Scholar 
    Mur, L. R., Skulberg, O. M. & Utkilen, H. In: Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring, and Management. (eds. Chorus, I. and Bartram, J.) 15–40 (St Edmundsbury Press, 1999).Schmidt, J.-P. Ein bronzenes Hallstattschwert der Periode VI aus dem Flachen See bei Sophienhof, Lkr. Mecklenburgische Seenplatte. Arch.äologische Ber. aus Mecklenbg.-Vorpommern 26, 26–34 (2019).
    Google Scholar 
    Schmidt, J.-P. “Aller guten Dinge sind drei!”–Ein weiteres bronzezeitliches Schwert aus dem Flachen See bei Lütgendorf, Lkr. Mecklenburgische Seenplatte. Arch.äologische Ber. aus Mecklenbg.-Vorpommern 27, 49–55 (2020).
    Google Scholar 
    Küster, M., Stöckmann, M., Fülling, A. & Weber, R. Kulturlandschaftselemente, Kolluvien und Flugsande als Archive der spätholozänen Landschaftsentwicklung im Bereich des Messtischblattes Thurow (Müritz-Nationalpark, Mecklenburg). In: Neue Beiträge zum Naturraum und zur Landschaftsgeschichte im Teilgebiet. (Geozon Science Media, 2015).Feeser, I., Dörfler, W., Kneisel, J., Hinz, M. & Dreibrodt, S. Human impact and population dynamics in the Neolithic and Bronze Age: Multi-proxy evidence from north-western Central Europe. Holocene 29, 1596–1606 (2019).Article 

    Google Scholar 
    Alsleben, A. In How’s Life? Living Conditions in the 2nd and 1st Millennia BCE. Scales of Transformation in Prehistoric and Archaic Societies (eds. Dal Corso, M. et al.) 85–102 (Sidestone Press, 2019).Kneisel, J., Bork, H.-R. & Czebreszuk, J. In Defensive Structures from Central Europe to the Aegean in the 3rd and 2nd Millennia bc (eds. Czebreszuk, J., Kadrow, S. & Müller, J.) 155–170 (Habelt, 2008).Haas, J. N. & Wahlmüller, N. Floren-, Vegetations- und Milieuveränderungen im Zuge der bronzezeitlichen Besiedlung von Bruszczewo (Polen) und der landwirtschaftlichen Nutzung der umliegenden Gebiete. In: Ausgrabungen und Forschungen in einer prähistorischen Siedlungskammer Großpolens. (eds. Müller, J., Czebreszuk, J. & Kneisel, J.) Studien zur Archäologie in Ostmitteleuropa Vol. 6.1, 50–81 (Bonn, 2010).Theuerkauf, M. et al. Holocene lake-level evolution of Lake Tiefer See, NE Germany, caused by climate and land cover changes. Boreas 51, 299–316 (2021).Article 

    Google Scholar 
    Büntgen, U. et al. 2500 years of European climate variability and human susceptibility. Science 331, 578–582 (2011).Article 

    Google Scholar 
    Büntgen, U. et al. Cooling and societal change during the Late Antique Little Ice Age from 536 to around 660 AD. Nat. Geosci. 9, 231–236 (2016).Article 

    Google Scholar 
    Kienel, U. et al. Effects of spring warming and mixing duration on diatom deposition in deep Tiefer See, NE Germany. J. Paleolimnol. 57, 37–49 (2017).Article 

    Google Scholar 
    Monchamp, M. E., Spaak, P. & Pomati, F. High dispersal levels and lake warming are emergent drivers of cyanobacterial community assembly in peri-Alpine lakes. Sci. Rep. 9, 7366 (2019).Article 

    Google Scholar 
    Erratt, K. et al. Paleolimnological evidence reveals climate-related preeminence of cyanobacteria in a temperate meromictic lake. Can. J. Fish. Aquat. Sci. 79, 558–565 (2021).Article 

    Google Scholar 
    Schmidt, J.-P. ders., Kein Ende in Sicht? Neue Untersuchungen auf dem Feuerstellenplatz von Naschendorf, Lkr. Nordwestmecklenburg. Arch.äologische Ber. aus Mecklenbg.-Vorpommern 19, 26–46 (2012).
    Google Scholar 
    Marcott, S. A., Shakun, J. D., Clark, P. U. & Mix, A. C. A reconstruction of regional and global temperature for the past 11,300 years. Science 339, 1198–1201 (2013).Article 
    CAS 

    Google Scholar 
    Wanner, H. et al. Holocene climate variability and change; a data-based review. J. Geol. Soc. Lond. 172, 254–263 (2015).Article 

    Google Scholar 
    Rigosi, A., Carey, C. C., Ibelings, B. W. & Brookes, J. D. The interaction between climate warming and eutrophication to promote cyanobacteria is dependent on trophic state and varies among taxa. Limnol. Oceanogr. 59, 99–114 (2014).Article 

    Google Scholar 
    Dittmann, E., Fewer, D. P. & Neilan, B. A. Cyanobacterial toxins: Biosynthetic routes and evolutionary roots. FEMS Microbiol. Rev. 37, 23–43 (2013).Article 
    CAS 

    Google Scholar 
    Dolman, A. M. et al. Cyanobacteria and cyanotoxins: the influence of nitrogen versus phosphorus. PLoS ONE 7, e38757 (2012).Article 
    CAS 

    Google Scholar 
    Kurmayer, R., Christiansen, G., Fastner, J. & Börner, T. Abundance of active and inactive microcystin genotypes in populations of the toxic cyanobacterium Planktothrix spp. Environ. Microbiol. 6, 831–841 (2004).Article 
    CAS 

    Google Scholar 
    Liu, A., Zhu, T., Lu, X. & Song, L. Hydrocarbon profiles and phylogenetic analyses of diversified cyanobacterial species. Appl. Energy 11, 383–393 (2013).Article 

    Google Scholar 
    Coates, R. C. et al. Characterization of cyanobacterial hydrocarbon composition and distribution of biosynthetic pathways. PLoS ONE 9, e85140 (2014).Article 

    Google Scholar 
    Marciniak, S. et al. Ancient human genomics: the methodology behind reconstructing evolutionary pathways. J. Hum. Evol. 79, 21–34 (2015).Article 

    Google Scholar 
    Jónsson, H., Ginolhac, A., Schubert, M., Johnson, P. L. F. & Orlando, L. MapDamage2.0: fast approximate Bayesian estimates of ancient DNA damage parameters. in. Bioinformatics 29, 1682–1684 (2013).Article 

    Google Scholar 
    Borry, M., Hübner, A., Rohrlach, A. B. & Warinner, C. PyDamage: automated ancient damage identification and estimation for contigs in ancient DNA de novo assembly. PeerJ 9, e11845 (2021).Article 

    Google Scholar 
    Murchie, T. J. et al. Optimizing extraction and targeted capture of ancient environmental DNA for reconstructing past environments using the PalaeoChip Arctic-1.0 bait-set. Quat. Res. (U. S.) 99, 305–328 (2021).Article 
    CAS 

    Google Scholar 
    Armbrecht, L., Hallegraeff, G., Bolch, C. J. S., Woodward, C. & Cooper, A. Hybridisation capture allows DNA damage analysis of ancient marine eukaryotes. Sci. Rep. 11, 3220 (2021).Article 
    CAS 

    Google Scholar 
    Wulf, S. et al. Holocene tephrostratigraphy of varved sediment records from Lakes Tiefer See (NE Germany) and Czechowskie (N Poland). Quat. Sci. Rev. 132, 1–14 (2016).Article 

    Google Scholar 
    Sugita, S. Theory of quantitative reconstruction of vegetation I: Pollen from large sites REVEALS regional vegetation composition. Holocene 17, 2 (2007).Article 

    Google Scholar 
    Epp, L. S., Zimmermann, H. H. & Stoof-Leichsenring, K. R. In: Ancient DNA. Methods in Molecular Biology (eds. Shapiro B., Barlow A., Heintzman P., Hofreiter M., Paijmans J., Soares A.) Vol. 1963, 31–44 (Humana Press, 2019).Janse, I., Meima, M., Kardinaal, W. E. A. & Zwart, G. High-resolution differentiation of Cyanobacteria by using rRNA-internal transcribed spacer denaturing gradient gel electrophoresis. Appl. Environ. Microbiol. 69, 6634–6643 (2003).Article 
    CAS 

    Google Scholar 
    Nwosu, E. C. et al. Species-level spatio-temporal dynamics of cyanobacteria in a hard-water temperate lake in the Southern Baltics. Front. Microbiol. 12, https://doi.org/10.3389/fmicb.2021.761259 (2021).Savichtcheva, O. et al. Quantitative PCR enumeration of total/toxic Planktothrix rubescens and total cyanobacteria in preserved DNA isolated from lake sediments. Appl. Environ. Microbiol. 77, 8744–8753 (2011).Article 
    CAS 

    Google Scholar 
    Coolen, M. J. L. et al. Ancient DNA derived from alkenone-biosynthesizing haptophytes and other algae in Holocene sediments from the Black Sea. Paleoceanography 21, PA1005 (2006).Article 

    Google Scholar 
    Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina 7 amplicon data. Nat. Methods 13, 581–583 (2016).Article 
    CAS 

    Google Scholar 
    Kieser, S., Brown, J., Zdobnov, E. M., Trajkovski, M. & McCue, L. A. ATLAS: a Snakemake workflow for assembly, annotation, and genomic binning of metagenome sequence data. BMC Bioinformat. 21, 257 (2020).Article 

    Google Scholar 
    Yilmaz, P. et al. The SILVA and ‘all-species Living Tree Project (LTP)’ taxonomic frameworks. Nucleic Acids Res. 42, 643–648 (2014).Article 

    Google Scholar 
    Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).Article 
    CAS 

    Google Scholar 
    Hyatt, D. et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformat. 11, 119–119 (2010).Article 

    Google Scholar 
    Huerta-Cepas, J. et al. EggNOG 5.0: A hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res. 47, D309–D314 (2019).Article 
    CAS 

    Google Scholar 
    Cantalapiedra, C. P., Hernández-Plaza, A., Letunic, I., Bork, P. & Huerta-Cepas, J. eggNOG-mapper v2: Functional Annotation, Orthology Assignments, and Domain Prediction at the Metagenomic Scale. Mol. Biol. Evol. https://doi.org/10.1093/molbev/msab293 (2021).Shen, W. & Ren, H. TaxonKit: a practical and efficient NCBI taxonomy toolkit. J. Genet. Genomics. 48, 844–850 (2021).Article 

    Google Scholar 
    Hammer, Ø., Harper, D. A. T. & Ryan, P. D. PAST: paleontological statistics software package for education and data analysis. Palaeontol. Electron. 29, 471–482 (2001).
    Google Scholar 
    Oksanen, J. et al. vegan: Community Ecology Package. R Package Version 2.5-2. Cran R (2019).Wu, T. et al. clusterProfiler 4.0: a universal enrichment tool for interpreting omics data. Innovation 2, 100141 (2021).CAS 

    Google Scholar 
    Legendre, P. & Gallagher, E. D. Ecologically meaningful transformations for ordination of species data. Oecologia 129, 271–280 (2001).Article 

    Google Scholar  More

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    Artificial intelligence for automated detection of large mammals creates path to upscale drone surveys

    Chapman, A. It’s okay to call them drones. J. Unmanned Veh. Syst. 2, iii–v (2014).Article 

    Google Scholar 
    Chabot, D., Hodgson, A. J., Hodgson, J. C. & Anderson, K. ‘Drone’: Technically correct, popularly accepted, socially acceptable. Drone Syst. Appl. 10, 399–405 (2022).Article 

    Google Scholar 
    Chabot, D. & Bird, D. M. Wildlife research and management methods in the 21st century: Where do unmanned aircraft fit in?. J. Unmanned Veh. Syst. 3, 137–155 (2015).Article 

    Google Scholar 
    Christie, K. S., Gilbert, S. L., Brown, C. L., Hatfield, M. & Hanson, L. Unmanned aircraft systems in wildlife research: Current and future applications of a transformative technology. Front. Ecol. Environ. 14, 241–251 (2016).Article 

    Google Scholar 
    Whitehead, K. & Hugenholtz, C. H. Remote sensing of the environment with small unmanned aircraft systems (UASs), part 1: A review of progress and challenges. J. Unmanned Veh. Syst. 2, 69–85 (2014).Article 

    Google Scholar 
    Barnas, A. et al. Evaluating behavioral responses of nesting lesser snow geese to unmanned aircraft surveys. Ecol. Evol. 8, 1328–1338 (2018).Article 

    Google Scholar 
    Mulero-Pázmány, M. et al. Unmanned aircraft systems as a new source of disturbance for wildlife: A systematic review. PLoS ONE 12, e0178448 (2017).Article 

    Google Scholar 
    Linchant, J., Lisein, J., Semeki, J., Lejeune, P. & Vermeulen, C. Are unmanned aircraft systems (UAS s) the future of wildlife monitoring? A review of accomplishments and challenges. Mammal Rev. 45, 239–252 (2015).Article 

    Google Scholar 
    Whitehead, K. et al. Remote sensing of the environment with small unmanned aircraft systems (UASs), part 2: Scientific and commercial applications. J. Unmanned Veh. Syst. 2, 86–102 (2014).Article 

    Google Scholar 
    Barasona, J. A. et al. Unmanned aircraft systems for studying spatial abundance of ungulates: Relevance to spatial epidemiology. PLoS ONE 9, e115608 (2014).Article 
    ADS 

    Google Scholar 
    Chrétien, L. P., Théau, J. & Ménard, P. Wildlife multispecies remote sensing using visible and thermal infrared imagery acquired from an unmanned aerial vehicle (UAV). Int. Arch. Photogramm. Remote Sens. Spat. Inf. Sci. 40, 241 (2015).Article 

    Google Scholar 
    Guo, X. et al. Application of UAV remote sensing for a population census of large wild herbivores—Taking the headwater region of the yellow river as an example. Remote Sens. 10, 1041 (2018).Article 
    ADS 

    Google Scholar 
    Hu, J., Wu, X. & Dai, M. Estimating the population size of migrating Tibetan antelopes Pantholops hodgsonii with unmanned aerial vehicles. Oryx 54, 101–109 (2020).Article 

    Google Scholar 
    Mulero-Pázmány, M., Stolper, R., Van Essen, L. D., Negro, J. J. & Sassen, T. Remotely piloted aircraft systems as a rhinoceros anti-poaching tool in Africa. PLoS ONE 9, e83873 (2014).Article 
    ADS 

    Google Scholar 
    Rey, N., Volpi, M., Joost, S. & Tuia, D. Detecting animals in African Savanna with UAVs and the crowds. Remote Sens. Environ. 200, 341–351 (2017).Article 
    ADS 

    Google Scholar 
    Schroeder, N. M., Panebianco, A., Gonzalez Musso, R. & Carmanchahi, P. An experimental approach to evaluate the potential of drones in terrestrial mammal research: A gregarious ungulate as a study model. R. Soc. Open Sci. 7, 191482 (2020).Article 
    ADS 

    Google Scholar 
    Su, X. et al. Using an unmanned aerial vehicle (UAV) to study wild yak in the highest desert in the world. Int. J. Remote Sens. 39, 5490–5503 (2018).Article 

    Google Scholar 
    Vermeulen, C., Lejeune, P., Lisein, J., Sawadogo, P. & Bouché, P. Unmanned aerial survey of elephants. PLoS ONE 8, e54700 (2013).Article 
    ADS 
    CAS 

    Google Scholar 
    Mallory, M. L. et al. Financial costs of conducting science in the Arctic: Examples from seabird research. Arct. Sci. 4, 624–633 (2018).Article 

    Google Scholar 
    Sasse, D. B. Job-related mortality of wildlife workers in the United States, 1937–2000. Wildl. Soc. Bull. 31, 1015–1020 (2003).
    Google Scholar 
    Loarie, S. R., Joppa, L. N. & Pimm, S. L. Satellites miss environmental priorities. Trends Ecol. Evol. 22, 630–632 (2007).Article 

    Google Scholar 
    IUCN. The IUCN Red List of Threatened Species. IUCN Red List of Threatened Species https://www.iucnredlist.org/en (2021).Mech, L. D. & Barber, S. M. A critique of wildlife radio-tracking and its use in National Parks: a report to the National Park Service. (2002).Patterson, C., Koski, W., Pace, P., McLuckie, B. & Bird, D. M. Evaluation of an unmanned aircraft system for detecting surrogate caribou targets in Labrador. J. Unmanned Veh. Syst. 4, 53–69 (2015).Article 

    Google Scholar 
    Hodgson, J. C. et al. Drones count wildlife more accurately and precisely than humans. Methods Ecol. Evol. 9, 1160–1167 (2018).Article 

    Google Scholar 
    Seymour, A. C., Dale, J., Hammill, M., Halpin, P. N. & Johnston, D. W. Automated detection and enumeration of marine wildlife using unmanned aircraft systems (UAS) and thermal imagery. Sci. Rep. 7, 1–10 (2017).Article 

    Google Scholar 
    COSEWIC. COSEWIC assessment and status report on the caribou (Rangifer tarandus) eastern migratory population, Torngat mountain population in Canada. (COSEWIC, Committee on the Status of Endangered Wildlife in Canada, 2017).Albawi, S., Mohammed, T. A. & Al-Zawi, S. Understanding of a convolutional neural network. in 2017 international conference on engineering and technology (ICET) 1–6 (IEEE, 2017).Gu, J. et al. Recent advances in convolutional neural networks. Pattern Recognit. 77, 354–377 (2018).Article 
    ADS 

    Google Scholar 
    Teuwen, J. & Moriakov, N. Convolutional neural networks. in Handbook of medical image computing and computer assisted intervention 481–501 (Elsevier, 2020).Corcoran, E., Winsen, M., Sudholz, A. & Hamilton, G. Automated detection of wildlife using drones: Synthesis, opportunities and constraints. Methods Ecol. Evol. 12, 1103–1114 (2021).Article 

    Google Scholar 
    Corcoran, E., Denman, S., Hanger, J., Wilson, B. & Hamilton, G. Automated detection of koalas using low-level aerial surveillance and machine learning. Sci. Rep. 9, 3208 (2019).Article 
    ADS 

    Google Scholar 
    Gray, P. C. et al. Drones and convolutional neural networks facilitate automated and accurate cetacean species identification and photogrammetry. Methods Ecol. Evol. 10, 1490–1500 (2019).Article 

    Google Scholar 
    Gray, P. C. et al. A convolutional neural network for detecting sea turtles in drone imagery. Methods Ecol. Evol. 10, 345–355 (2019).Article 

    Google Scholar 
    Peng, J. et al. Wild animal survey using UAS imagery and deep learning: modified Faster R-CNN for kiang detection in Tibetan Plateau. ISPRS J. Photogramm. Remote Sens. 169, 364–376 (2020).Article 
    ADS 

    Google Scholar 
    Borowicz, A. et al. Multi-modal survey of Adélie penguin mega-colonies reveals the Danger Islands as a seabird hotspot. Sci. Rep. 8, 3926 (2018).Article 
    ADS 

    Google Scholar 
    Francis, R. J., Lyons, M. B., Kingsford, R. T. & Brandis, K. J. Counting mixed breeding aggregations of animal species using drones: Lessons from waterbirds on semi-automation. Remote Sens. 12, 1185 (2020).Article 
    ADS 

    Google Scholar 
    Santangeli, A. et al. Integrating drone-borne thermal imaging with artificial intelligence to locate bird nests on agricultural land. Sci. Rep. 10, 1–8 (2020).Article 

    Google Scholar 
    Bowley, C., Mattingly, M., Barnas, A., Ellis-Felege, S. & Desell, T. An analysis of altitude, citizen science and a convolutional neural network feedback loop on object detection in unmanned aerial systems. J. Comput. Sci. 34, 102–116 (2019).Article 

    Google Scholar 
    Bowley, C., Mattingly, M., Barnas, A., Ellis-Felege, S. & Desell, T. Detecting wildlife in unmanned aerial systems imagery using convolutional neural networks trained with an automated feedback loop. in International Conference on Computational Science 69–82 (Springer, 2018).Delplanque, A., Foucher, S., Lejeune, P., Linchant, J. & Théau, J. Multispecies detection and identification of African mammals in aerial imagery using convolutional neural networks. Remote Sens. Ecol. Conserv. 8, 166–179 (2021).Article 

    Google Scholar 
    Eikelboom, J. A. J. et al. Improving the precision and accuracy of animal population estimates with aerial image object detection. Methods Ecol. Evol. 10, 1875–1887 (2019).Article 

    Google Scholar 
    Kellenberger, B., Marcos, D. & Tuia, D. Detecting mammals in UAV images: Best practices to address a substantially imbalanced dataset with deep learning. Remote Sens. Environ. 216, 139–153 (2018).Article 
    ADS 

    Google Scholar 
    Hooge, I. T. C., Niehorster, D. C., Nyström, M., Andersson, R. & Hessels, R. S. Is human classification by experienced untrained observers a gold standard in fixation detection?. Behav. Res. Methods 50, 1864–1881 (2018).Article 

    Google Scholar 
    Barnas, A. F., Darby, B. J., Vandeberg, G. S., Rockwell, R. F. & Ellis-Felege, S. N. A comparison of drone imagery and ground-based methods for estimating the extent of habitat destruction by lesser snow geese (Anser caerulescens caerulescens) in La Pérouse Bay. PLoS ONE 14, e0217049 (2019).Article 
    CAS 

    Google Scholar 
    Brook, R. K. & Kenkel, N. C. A multivariate approach to vegetation mapping of Manitoba’s Hudson Bay Lowlands. Int. J. Remote Sens. 23, 4761–4776 (2002).Article 

    Google Scholar 
    Shilts, W. W., Aylsworth, J. M., Kaszycki, C. A., Klassen, R. A. & Graf, W. L. Canadian shield. in Geomorphic Systems of North America vol. 2 119–161 (Geological Society of America Boulder, Colorado, 1987).Barnas, A. F., Felege, C. J., Rockwell, R. F. & Ellis-Felege, S. N. A pilot (less) study on the use of an unmanned aircraft system for studying polar bears (Ursus maritimus). Polar Biol. 41, 1055–1062 (2018).Article 

    Google Scholar 
    Ellis-Felege, S. N. et al. Nesting common eiders (Somateria mollissima) show little behavioral response to fixed-wing drone surveys. J. Unmanned Veh. Syst. 10, 1–4 (2021).
    Google Scholar 
    Barnas, A. F. et al. A standardized protocol for reporting methods when using drones for wildlife research. J. Unmanned Veh. Syst. 8, 89–98 (2020).Article 

    Google Scholar 
    Ren, S., He, K., Girshick, R. & Sun, J. Faster R-CNN: Towards real-time object detection with region proposal networks. Adv. Neural Inf. Process. Syst. 28, 91–99 (2016).
    Google Scholar 
    Chen, T., Xu, B., Zhang, C. & Guestrin, C. Training Deep Nets with Sublinear Memory Cost. ArXiv160406174 Cs (2016).Pinckaers, H. & Litjens, G. Training convolutional neural networks with megapixel images. ArXiv180405712 Cs (2018).Abadi, M. et al. TensorFlow: Large-scale machine learning on heterogeneous systems. (2015).Janocha, K. & Czarnecki, W. M. On loss functions for deep neural networks in classification. ArXiv Prepr. ArXiv170205659. (2017).Murata, N., Yoshizawa, S. & Amari, S. Learning curves, model selection and complexity of neural networks. Adv. Neural Inf. Process. Syst. 5, 607–614 (1992).
    Google Scholar 
    Hänsch, R. & Hellwich, O. The truth about ground truth: Label noise in human-generated reference data. in IGARSS 2019–2019 IEEE International Geoscience and Remote Sensing Symposium 5594–5597 (IEEE, 2019).Bowler, E., Fretwell, P. T., French, G. & Mackiewicz, M. Using deep learning to count albatrosses from space: Assessing results in light of ground truth uncertainty. Remote Sens. 12, 2026 (2020).Article 
    ADS 

    Google Scholar 
    Brack, I. V., Kindel, A. & Oliveira, L. F. B. Detection errors in wildlife abundance estimates from Unmanned Aerial Systems (UAS) surveys: Synthesis, solutions, and challenges. Methods Ecol. Evol. 9, 1864–1873 (2018).Article 

    Google Scholar 
    Jagielski, P. M. et al. The utility of drones for studying polar bear behaviour in the Canadian Arctic: Opportunities and recommendations. Drone Syst. Appl. 10, 97–110 (2022).Article 

    Google Scholar 
    Williams, P. J., Hooten, M. B., Womble, J. N. & Bower, M. R. Estimating occupancy and abundance using aerial images with imperfect detection. Methods Ecol. Evol. 8, 1679–1689 (2017).Article 

    Google Scholar 
    Link, W. A., Schofield, M. R., Barker, R. J. & Sauer, J. R. On the robustness of N-mixture models. Ecology 99, 1547–1551 (2018).Article 

    Google Scholar 
    Horvitz, D. G. & Thompson, D. J. A generalization of sampling without replacement from a finite universe. J. Am. Stat. Assoc. 47, 663–685 (1952).Article 
    MATH 

    Google Scholar 
    Corcoran, E., Denman, S. & Hamilton, G. New technologies in the mix: Assessing N-mixture models for abundance estimation using automated detection data from drone surveys. Ecol. Evol. 10, 8176–8185 (2020).Article 

    Google Scholar 
    Lunga, D., Arndt, J., Gerrand, J. & Stewart, R. ReSFlow: A remote sensing imagery data-flow for improved model generalization. IEEE J. Sel. Top. Appl. Earth Obs. Remote Sens. 14, 10468–10483 (2021).Article 
    ADS 

    Google Scholar 
    Fromm, M., Schubert, M., Castilla, G., Linke, J. & McDermid, G. Automated detection of conifer seedlings in drone imagery using convolutional neural networks. Remote Sens. 11, 2585 (2019).Article 
    ADS 

    Google Scholar 
    Velumani, K. et al. Estimates of maize plant density from UAV RGB images using Faster-RCNN detection model: Impact of the spatial resolution. Plant Phenomics 2021, 9824843 (2021).Article 
    CAS 

    Google Scholar 
    Hodgson, A., Peel, D. & Kelly, N. Unmanned aerial vehicles for surveying marine fauna: Assessing detection probability. Ecol. Appl. 27, 1253–1267 (2017).Article 

    Google Scholar 
    Ferguson, M. C. et al. Performance of manned and unmanned aerial surveys to collect visual data and imagery for estimating arctic cetacean density and associated uncertainty. J. Unmanned Veh. Syst. 6, 128–154 (2018).Article 

    Google Scholar 
    Zmarz, A. et al. Application of UAV BVLOS remote sensing data for multi-faceted analysis of Antarctic ecosystem. Remote Sens. Environ. 217, 375–388 (2018).Article 
    ADS 

    Google Scholar 
    Lyons, M. B. et al. Monitoring large and complex wildlife aggregations with drones. Methods Ecol. Evol. 10, 1024–1035 (2019).Article 

    Google Scholar  More

  • in

    Future temperature extremes threaten land vertebrates

    Fischer, E. M. & Knutti, R. Anthropogenic contribution to global occurrence of heavy-precipitation and high-temperature extremes. Nat. Clim. Change 5, 560–564 (2015).Article 
    ADS 

    Google Scholar 
    Meehl, G. A. & Tebaldi, C. More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305, 994–997 (2004).Article 
    ADS 
    CAS 

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

    Google Scholar 
    Till, A., Rypel, A. L., Bray, A. & Fey, S. B. Fish die-offs are concurrent with thermal extremes in north temperate lakes. Nat. Clim. Change 9, 637–641 (2019).Article 
    ADS 

    Google Scholar 
    Smale, D. A. et al. Marine heatwaves threaten global biodiversity and the provision of ecosystem services. Nat. Clim. Change 9, 306–312 (2019).Article 
    ADS 

    Google Scholar 
    Vasseur, D. A. et al. Increased temperature variation poses a greater risk to species than climate warming. Proc. R. Soc. B 281, 20132612 (2014).Article 

    Google Scholar 
    Ma, G., Rudolf, V. H. & Ma, C. Extreme temperature events alter demographic rates, relative fitness, and community structure. Glob. Change Biol. 21, 1794–1808 (2015).Article 
    ADS 

    Google Scholar 
    Vázquez, D. P., Gianoli, E., Morris, W. F. & Bozinovic, F. Ecological and evolutionary impacts of changing climatic variability. Biol. Rev. 92, 22–42 (2017).Article 

    Google Scholar 
    Tewksbury, J. J., Huey, R. B. & Deutsch, C. A. Putting the heat on tropical animals. Science 320, 1296–1297 (2008).Article 
    CAS 

    Google Scholar 
    Dillon, M. E., Wang, G. & Huey, R. B. Global metabolic impacts of recent climate warming. Nature 467, 704–706 (2010).Article 
    ADS 
    CAS 

    Google Scholar 
    Power, S. B. & Delage, F. P. Setting and smashing extreme temperature records over the coming century. Nat. Clim. Change 9, 529–534 (2019).Article 
    ADS 

    Google Scholar 
    Fischer, E. M., Sippel, S. & Knutti, R. Increasing probability of record-shattering climate extremes. Nat. Clim. Change 11, 689–695 (2021).Article 
    ADS 

    Google Scholar 
    Román-Palacios, C. & Wiens, J. J. Recent responses to climate change reveal the drivers of species extinction and survival. Proc. Natl Acad. Sci. USA 117, 4211–4217 (2020).Article 
    ADS 

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

    Google Scholar 
    McKechnie, A. E. & Wolf, B. O. Climate change increases the likelihood of catastrophic avian mortality events during extreme heat waves. Biol. Lett. 6, 253–256 (2010).Article 

    Google Scholar 
    Maxwell, S. L. et al. Conservation implications of ecological responses to extreme weather and climate events. Divers. Distrib. 25, 613–625 (2019).Article 

    Google Scholar 
    Seneviratne, S. I. et al. in Climate Change 2021: The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change (eds Masson-Delmotte, V. et al.) Ch. 11, 1571–1759 (Cambridge Univ. Press, 2021).Mora, C. et al. Global risk of deadly heat. Nat. Clim. Change 7, 501–506 (2017).Article 
    ADS 

    Google Scholar 
    Battisti, D. S. & Naylor, R. L. Historical warnings of future food insecurity with unprecedented seasonal heat. Science 323, 240–244 (2009).Article 
    CAS 

    Google Scholar 
    Warren, R., Price, J., Graham, E., Forstenhaeusler, N. & VanDerWal, J. The projected effect on insects, vertebrates, and plants of limiting global warming to 1.5°C rather than 2°C. Science 360, 791–795 (2018).Article 
    CAS 

    Google Scholar 
    Trisos, C. H., Merow, C. & Pigot, A. L. The projected timing of abrupt ecological disruption from climate change. Nature 580, 496–501 (2020).Article 
    ADS 
    CAS 

    Google Scholar 
    Deutsch, C. A. et al. Impacts of climate warming on terrestrial ectotherms across latitude. Proc. Natl Acad. Sci. USA 105, 6668–6672 (2008).Article 
    ADS 
    CAS 

    Google Scholar 
    Ma, G., Hoffmann, A. A. & Ma, C.-S. Daily temperature extremes play an important role in predicting thermal effects. J. Exp. Biol. 218, 2289–2296 (2015).
    Google Scholar 
    Paaijmans, K. P. et al. Temperature variation makes ectotherms more sensitive to climate change. Glob. Change Biol. 19, 2373–2380 (2013).Article 
    ADS 

    Google Scholar 
    Bütikofer, L. et al. The problem of scale in predicting biological responses to climate. Glob. Change Biol. 26, 6657–6666 (2020).Article 
    ADS 

    Google Scholar 
    Seneviratne, S. I., Donat, M. G., Pitman, A. J., Knutti, R. & Wilby, R. L. Allowable CO2 emissions based on regional and impact-related climate targets. Nature 529, 477–483 (2016).Article 
    ADS 
    CAS 

    Google Scholar 
    Buckley, L. B. & Huey, R. B. Temperature extremes: geographic patterns, recent changes, and implications for organismal vulnerabilities. Glob. Change Biol. 22, 3829–3842 (2016).Article 
    ADS 

    Google Scholar 
    Garcia, R. A., Cabeza, M., Rahbek, C. & Araújo, M. B. Multiple dimensions of climate change and their implications for biodiversity. Science 344, 1247579 (2014).Article 

    Google Scholar 
    Vogel, M. M. et al. Regional amplification of projected changes in extreme temperatures strongly controlled by soil moisture-temperature feedbacks. Geophys. Res. Lett. 44, 1511–1519 (2017).Article 
    ADS 

    Google Scholar 
    Tamarin-Brodsky, T., Hodges, K., Hoskins, B. J. & Shepherd, T. G. Changes in Northern Hemisphere temperature variability shaped by regional warming patterns. Nat. Geosci. 13, 414–421 (2020).Article 
    ADS 
    CAS 

    Google Scholar 
    Schär, C. et al. The role of increasing temperature variability in European summer heatwaves. Nature 427, 332–336 (2004).Article 
    ADS 

    Google Scholar 
    Pinsky, M. L., Eikeset, A. M., McCauley, D. J., Payne, J. L. & Sunday, J. M. Greater vulnerability to warming of marine versus terrestrial ectotherms. Nature 569, 108–111 (2019).Article 
    ADS 
    CAS 

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

    Google Scholar 
    Perkins, S. E. & Alexander, L. V. On the measurement of heat waves. J. Clim. 26, 4500–4517 (2013).Article 
    ADS 

    Google Scholar 
    Sunday, J. et al. Thermal tolerance patterns across latitude and elevation. Philos. Trans. R. Soc. B 374, 20190036 (2019).Article 

    Google Scholar 
    Hoffmann, A. A. Physiological climatic limits in Drosophila: patterns and implications. J. Exp. Biol. 213, 870–880 (2010).Article 
    CAS 

    Google Scholar 
    Buckley, L. B. & Huey, R. B. How extreme temperatures impact organisms and the evolution of their thermal tolerance. Integr. Comp. Biol. 56, 98–109 (2016).Article 

    Google Scholar 
    Cohen, J. M., Fink, D. & Zuckerberg, B. Avian responses to extreme weather across functional traits and temporal scales. Glob. Change Biol. 26, 4240–4250 (2020).Article 
    ADS 

    Google Scholar 
    Schwalm, C. R., Glendon, S. & Duffy, P. B. RCP8.5 tracks cumulative CO2 emissions. Proc. Natl Acad. Sci. USA 117, 19656–19657 (2020).Article 
    ADS 
    CAS 

    Google Scholar 
    Urban, M. C. Accelerating extinction risk from climate change. Science 348, 571–573 (2015).Article 
    ADS 
    CAS 

    Google Scholar 
    Jentsch, A., Kreyling, J. & Beierkuhnlein, C. A new generation of climate-change experiments: events, not trends. Front. Ecol. Environ. 5, 365–374 (2007).Article 

    Google Scholar 
    Riddell, E. A. et al. Exposure to climate change drives stability or collapse of desert mammal and bird communities. Science 371, 633–636 (2021).Article 
    ADS 
    CAS 

    Google Scholar 
    Welbergen, J. A., Klose, S. M., Markus, N. & Eby, P. Climate change and the effects of temperature extremes on Australian flying-foxes. Proc. R. Soc. B 275, 419–425 (2008).Article 

    Google Scholar 
    McKechnie, A. E., Rushworth, I. A., Myburgh, F. & Cunningham, S. J. Mortality among birds and bats during an extreme heat event in eastern South Africa. Austral Ecol. 46, 687–691 (2021).Article 

    Google Scholar 
    Thompson, R. M., Beardall, J., Beringer, J., Grace, M. & Sardina, P. Means and extremes: building variability into community-level climate change experiments. Ecol. Lett. 16, 799–806 (2013).Article 

    Google Scholar 
    Perez, T. M., Stroud, J. T. & Feeley, K. J. Thermal trouble in the tropics. Science 351, 1392–1393 (2016).Article 
    ADS 
    CAS 

    Google Scholar 
    Huey, R. B. et al. Why tropical forest lizards are vulnerable to climate warming. Proc. R. Soc. B 276, 1939–1948 (2009).Article 

    Google Scholar 
    Kingsolver, J. G., Diamond, S. E. & Buckley, L. B. Heat stress and the fitness consequences of climate change for terrestrial ectotherms. Funct. Ecol. 27, 1415–1423 (2013).Article 

    Google Scholar 
    R. Kearney, M. Activity restriction and the mechanistic basis for extinctions under climate warming. Ecol. Lett. 16, 1470–1479 (2013).Article 

    Google Scholar 
    Rezende, E. L., Bozinovic, F., Szilágyi, A. & Santos, M. Predicting temperature mortality and selection in natural Drosophila populations. Science 369, 1242–1245 (2020).Article 
    ADS 
    CAS 
    MATH 

    Google Scholar 
    Chen, I.-C., Hill, J. K., Ohlemüller, R., Roy, D. B. & Thomas, C. D. Rapid range shifts of species associated with high levels of climate warming. Science 333, 1024–1026 (2011).Article 
    ADS 
    CAS 

    Google Scholar 
    Cohen, J. M., Lajeunesse, M. J. & Rohr, J. R. A global synthesis of animal phenological responses to climate change. Nat. Clim. Change 8, 224–228 (2018).Article 
    ADS 

    Google Scholar 
    Levy, O., Dayan, T., Porter, W. P. & Kronfeld-Schor, N. Time and ecological resilience: can diurnal animals compensate for climate change by shifting to nocturnal activity? Ecol. Monogr. 89, e01334 (2019).Article 

    Google Scholar 
    Faurby, S. & Araújo, M. B. Anthropogenic range contractions bias species climate change forecasts. Nat. Clim. Change 8, 252–256 (2018).Article 
    ADS 

    Google Scholar 
    Sunday, J. M. et al. Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation. Proc. Natl Acad. Sci. USA 111, 5610–5615 (2014).Article 
    ADS 
    CAS 

    Google Scholar 
    Scheffers, B. R., Edwards, D. P., Diesmos, A., Williams, S. E. & Evans, T. A. Microhabitats reduce animal’s exposure to climate extremes. Glob. Change Biol. 20, 495–503 (2014).Article 
    ADS 

    Google Scholar 
    Huey, R. B. et al. Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation. Philos. Trans. R. Soc. B 367, 1665–1679 (2012).Article 

    Google Scholar 
    Kearney, M., Shine, R. & Porter, W. P. The potential for behavioral thermoregulation to buffer “cold-blooded” animals against climate warming. Proc. Natl Acad. Sci. USA 106, 3835–3840 (2009).Article 
    ADS 
    CAS 

    Google Scholar 
    Morley, S. A., Peck, L. S., Sunday, J. M., Heiser, S. & Bates, A. E. Physiological acclimation and persistence of ectothermic species under extreme heat events. Glob. Ecol. Biogeogr. 28, 1018–1037 (2019).Article 

    Google Scholar 
    Cahill, A. E. et al. How does climate change cause extinction? Proc. R. Soc. B 280, 20121890 (2013).Article 

    Google Scholar 
    Lewis, F. et al. in Climate Change 2021: The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change (eds Masson-Delmotte, V. et al.) 147–1926 (Cambridge Univ. Press, 2021).Thakur, M. P., Bakker, E. S., Veen, G. C. & Harvey, J. A. Climate extremes, rewilding, and the role of microhabitats. One Earth 2, 506–509 (2020).Article 
    ADS 

    Google Scholar 
    Albright, T. P. et al. Mapping evaporative water loss in desert passerines reveals an expanding threat of lethal dehydration. Proc. Natl Acad. Sci. USA 114, 2283–2288 (2017).Article 
    ADS 
    CAS 

    Google Scholar 
    Thrasher, B. et al. NASA Global daily downscaled projections, CMIP6. Sci. Data 9, 262 (2022).Article 

    Google Scholar 
    Thrasher, B., Maurer, E. P., McKellar, C. & Duffy, P. B. Bias correcting climate model simulated daily temperature extremes with quantile mapping. Hydrol. Earth Syst. Sci. 16, 3309–3314 (2012).Article 
    ADS 

    Google Scholar 
    Jin, Z. et al. Do maize models capture the impacts of heat and drought stresses on yield? Using algorithm ensembles to identify successful approaches. Glob. Change Biol. 22, 3112–3126 (2016).Article 
    ADS 

    Google Scholar 
    Zhang, L., Yang, B., Li, S., Hou, Y. & Huang, D. Potential rice exposure to heat stress along the Yangtze River in China under RCP8.5 scenario. Agric. Forest Meteorol. 248, 185–196 (2018).Article 
    ADS 

    Google Scholar 
    Al-Bakri, J. et al. Assessment of climate changes and their impact on barley yield in Mediterranean environment using NEX-GDDP downscaled GCMs and DSSAT. Earth Syst. Environ. 5, 751–766 (2021).Semakula, H. M. et al. Prediction of future malaria hotspots under climate change in sub-Saharan Africa. Clim. Change 143, 415–428 (2017).Article 
    ADS 
    CAS 

    Google Scholar 
    Iwamura, T., Guzman-Holst, A. & Murray, K. A. Accelerating invasion potential of disease vector Aedes aegypti under climate change. Nat. Commun. 11, 2130 (2020).Article 
    ADS 
    CAS 

    Google Scholar 
    Jones, A. E. et al. Bluetongue risk under future climates. Nat. Clim. Change 9, 153–157 (2019).Article 
    ADS 

    Google Scholar 
    Obradovich, N. & Fowler, J. H. Climate change may alter human physical activity patterns. Nat. Hum. Behav. 1, 0097 (2017).Article 

    Google Scholar 
    Obradovich, N., Migliorini, R., Mednick, S. C. & Fowler, J. H. Nighttime temperature and human sleep loss in a changing climate. Sci. Adv. 3, e1601555 (2017).Article 
    ADS 

    Google Scholar 
    Meehl, G. A. et al. Context for interpreting equilibrium climate sensitivity and transient climate response from the CMIP6 Earth system models. Sci. Adv. 6, eaba1981 (2020).Article 
    ADS 

    Google Scholar 
    Hausfather, Z., Marvel, K., Schmidt, G. A., Nielsen-Gammon, J. W. & Zelinka, M. Climate simulations: recognize the ‘hot model’ problem. Nature 605, 26–29 (2022).O’Neill, B. C. et al. The scenario model intercomparison project (ScenarioMIP) for CMIP6. Geosci. Model Dev. 9, 3461–3482 (2016).Article 
    ADS 

    Google Scholar 
    IPCC Special Report on Global Warming of 1.5 °C (eds Masson-Delmotte, V. et al.) (WMO, 2018).IUCN Red List of Threatened Species Version 2017, 3 (IUCN, 2017).Roll, U. et al. The global distribution of tetrapods reveals a need for targeted reptile conservation. Nat. Ecol. Evol. 1, 1677 (2017).Article 

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

    Google Scholar 
    Maclean, I. M. Predicting future climate at high spatial and temporal resolution. Glob. Change Biol. 26, 1003–1011 (2020).Article 
    ADS 

    Google Scholar 
    Warren, R. et al. Quantifying the benefit of early climate change mitigation in avoiding biodiversity loss. Nat. Clim. Change 3, 678–682 (2013).Article 
    ADS 

    Google Scholar 
    Jiguet, F. et al. Thermal range predicts bird population resilience to extreme high temperatures. Ecol. Lett. 9, 1321–1330 (2006).Article 

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

    Google Scholar 
    Laufkötter, C., Zscheischler, J. & Frölicher, T. L. High-impact marine heatwaves attributable to human-induced global warming. Science 369, 1621–1625 (2020).Article 
    ADS 

    Google Scholar 
    Coumou, D. & Rahmstorf, S. A decade of weather extremes. Nat. Clim. Change 2, 491–496 (2012).Article 
    ADS 

    Google Scholar 
    Oliver, E. C. et al. Longer and more frequent marine heatwaves over the past century. Nat. Commun. 9, 1324 (2018).Article 
    ADS 

    Google Scholar 
    Field, C. B., Barros, V., Stocker, T. F. & Dahe, Q. Managing the Risks of Extreme Events and Disasters to Advance Climate Change Adaptation: Special Report of the Intergovernmental Panel on Climate Change (Cambridge Univ. Press, 2012).Woolway, R. I. et al. Lake heatwaves under climate change. Nature 589, 402–407 (2021).Article 
    ADS 
    CAS 

    Google Scholar 
    Gruber, N., Boyd, P. W., Frölicher, T. L. & Vogt, M. Biogeochemical extremes and compound events in the ocean. Nature 600, 395–407 (2021).Article 
    ADS 
    CAS 

    Google Scholar 
    Cahill, A. E. et al. Causes of warm-edge range limits: systematic review, proximate factors and implications for climate change. J. Biogeogr. 41, 429–442 (2014).Article 

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

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

    Google Scholar 
    Bennett, J. M. et al. The evolution of critical thermal limits of life on Earth. Nat. Commun. 12, 1198 (2021).Article 
    ADS 
    CAS 

    Google Scholar 
    Sunday, J. M., Bates, A. E. & Dulvy, N. K. Thermal tolerance and the global redistribution of animals. Nat. Clim. Change 2, 686–690 (2012).Article 
    ADS 

    Google Scholar 
    Pearson, R. G. & Dawson, T. P. Predicting the impacts of climate change on the distribution of species: are bioclimate envelope models useful? Glob. Ecol. Biogeogr. 12, 361–371 (2003).Article 

    Google Scholar 
    Louthan, A. M., Doak, D. F. & Angert, A. L. Where and when do species interactions set range limits? Trends Ecol. Evol. 30, 780–792 (2015).Article 

    Google Scholar 
    Barbarossa, V. et al. Threats of global warming to the world’s freshwater fishes. Nat. Commun. 12, 1701 (2021).Article 
    ADS 
    CAS 

    Google Scholar 
    Clusella-Trullas, S., Blackburn, T. M. & Chown, S. L. Climatic predictors of temperature performance curve parameters in ectotherms imply complex responses to climate change. Am. Nat. 177, 738–751 (2011).Article 

    Google Scholar 
    Qu, Y.-F. & Wiens, J. J. Higher temperatures lower rates of physiological and niche evolution. Proc. R. Soc. B 287, 20200823 (2020).Article 

    Google Scholar 
    Pither, J. Climate tolerance and interspecific variation in geographic range size. Proc. R. Soc. Lond. B 270, 475–481 (2003).Article 

    Google Scholar 
    Bennett, J. M. et al. GlobTherm, a global database on thermal tolerances for aquatic and terrestrial organisms. Sci. Data 5, 180022 (2018).Article 

    Google Scholar 
    R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2019); http://www.R-project.org/Chen, H., Sun, J., Lin, W. & Xu, H. Comparison of CMIP6 and CMIP5 models in simulating climate extremes. Sci. Bull. 65, 1415–1418 (2020).Article 

    Google Scholar  More

  • in

    The performance of protected-area expansions in representing tropical Andean species: past trends and climate change prospects

    Possingham, H. P., Wilson, K. A., Andelman, S. J. & Vynne, C. H. Protected areas. Goals, limitations, and design. In Principles of Conservation Biology (eds Groom, M. J. et al.) 507–549 (Sinauer Associates Inc, 2006).
    Google Scholar 
    Marquet, P. A., Lessmann, J. & Shaw, M. R. Protected-area management and climate change. In Biodiversity and Climate Change: Transforming the Biosphere (eds Lovejoy, T. E. & Hannah, L.) 283–293 (Yale University Press, 2019).Chapter 

    Google Scholar 
    Geldmann, J., Manica, A., Burgess, N. D., Coad, L. & Balmford, A. A global-level assessment of the effectiveness of protected areas at resisting anthropogenic pressures. PNAS https://doi.org/10.1073/pnas.1908221116 (2019).Article 

    Google Scholar 
    Potapov, P. et al. The last frontiers of wilderness: Tracking loss of intact forest landscapes from 2000 to 2013. Sci. Adv. 3, e1600821 (2017).Article 
    ADS 

    Google Scholar 
    Cazalis, V. et al. Effectiveness of protected areas in conserving tropical forest birds. Nat. Commun. 11, 4461 (2020).Article 
    ADS 
    CAS 

    Google Scholar 
    Dudley, N., Mansourian, S., Stolton, S. & Suksuwan, S. Do protected areas contribute to poverty reduction?. Biodiversity 11, 5–7 (2010).Article 

    Google Scholar 
    Dudley, N. & Stolton, S. Arguments for Protected Areas (Earthscan, 2010).Book 

    Google Scholar 
    CBD. Strategic Plan for Biodiversity 2011–2020, Including Aichi Biodiversity Targets. http://www.cbd.int/sp/ and http://www.cbd.int/decision/cop/?id=12268 (2010).UNEP-WCMC & IUCN. Protected Planet: The World Database on Protected Areas (WDPA). www.protectedplanet.net. Accessed October 2022 (2022).Watson, J. E. M. et al. Persistent disparities between recent rates of habitat conversion and protection and implications for future global conservation targets. Conserv. Lett. 9, 413–421 (2016).Article 

    Google Scholar 
    Díaz, S. et al. Summary for Policymakers of the IPBES Global Assessment Report on Biodiversity and Ecosystem Services. (2019).Barnes, M. D., Glew, L., Wyborn, C. & Craigie, I. D. Prevent perverse outcomes from global protected area policy. Nat. Ecol. Evol. 2, 759–762 (2018).Article 

    Google Scholar 
    Visconti, P. et al. Protected area targets post-2020. Science 364, 239–241 (2019).Article 
    ADS 
    CAS 

    Google Scholar 
    Kukkala, A. S. & Moilanen, A. Core concepts of spatial prioritisation in systematic conservation planning. Biol. Rev. 88, 443–464 (2013).Article 

    Google Scholar 
    Joppa, L. N. & Pfaff, A. High and Far: Biases in the location of protected areas. PLoS ONE 4, e8273 (2009).Article 
    ADS 

    Google Scholar 
    Maxwell, S. L. et al. Area-based conservation in the twenty-first century. Nature 586, 217–227 (2020).Article 
    ADS 
    CAS 

    Google Scholar 
    CBD. CoP 7 Decision VII/30. Strategic Plan: Future Evaluation of progress. 12 https://www.cbd.int/doc/decisions/cop-07/cop-07-dec-30-en.pdf (2004).Venter, O. et al. Bias in protected-area location and its effects on long-term aspirations of biodiversity conventions. Conserv. Biol. 32, 127–134 (2017).Article 

    Google Scholar 
    Kuempel, C. D., Chauvenet, A. L. M. & Possingham, H. P. Equitable representation of ecoregions is slowly improving despite strategic planning shortfalls. Conserv. Lett. 9, 422–428 (2016).Article 

    Google Scholar 
    Barr, L. M., Watson, J. E. M., Possingham, H. P., Iwamura, T. & Fuller, R. A. Progress in improving the protection of species and habitats in Australia. Biol. Conserv. 200, 184–191 (2016).Article 

    Google Scholar 
    Hoffmann, S., Irl, S. D. H. & Beierkuhnlein, C. Predicted climate shifts within terrestrial protected areas worldwide. Nat. Commun. 10, 1–10 (2019).Article 

    Google Scholar 
    Hannah, L. Protected areas and climate change. Ann. N. Y. Acad. Sci. 1134, 201–212 (2008).Article 
    ADS 

    Google Scholar 
    Thomas, C. D. & Gillingham, P. K. The performance of protected areas for biodiversity under climate change. Biol. J. Lin. Soc. 115, 718–730 (2015).Article 

    Google Scholar 
    Ramirez-Villegas, J. et al. Using species distributions models for designing conservation strategies of Tropical Andean biodiversity under climate change. J. Nat. Conserv. 22, 391–404 (2014).Article 

    Google Scholar 
    Bax, V. & Francesconi, W. Conservation gaps and priorities in the Tropical Andes biodiversity hotspot: Implications for the expansion of protected areas. J. Environ. Manage. 232, 387–396 (2019).Article 

    Google Scholar 
    Jenkins, C. N., Pimm, S. L. & Joppa, L. N. Global patterns of terrestrial vertebrate diversity and conservation. PNAS 110, E2602–E2610 (2013).Article 
    ADS 
    CAS 

    Google Scholar 
    Rodrigues, A. S. L. et al. Global gap analysis: Priority regions for expanding the global protected-area network. Bioscience 54, 1092–1100 (2004).Article 

    Google Scholar 
    Thuiller, W., Georges, D., Engler, R. & Breiner, F. biomod2: Ensemble Platform for Species Distribution Modeling. (2015).Breiman, L. Random forests. Mach. Learn. 45, 5–32 (2001).Article 
    MATH 

    Google Scholar 
    Friedman, J. H. Greedy function approximation: A gradient boosting machine. Ann. Stat. 29, 1189–1232 (2001).Article 
    MATH 

    Google Scholar 
    Phillips, S. J., Anderson, R. P., Dudík, M., Schapire, R. E. & Blair, M. E. Opening the black box: An open-source release of Maxent. Ecography 40, 887–893 (2017).Article 

    Google Scholar 
    IUCN. The IUCN Red List of Threatened Species. (2017).Gotelli, N. J. & Graves, G. R. Null Models in Ecology. (1996).Araújo, M. B. & Pearson, R. G. Equilibrium of species’ distributions with climate. Ecography 28, 693–695 (2005).Article 

    Google Scholar 
    Watson, J. E. M., Grantham, H. S., Wilson, K. A. & Possingham, H. P. Systematic conservation planning: Past, present and future. In Conservation Biogeography (eds Ladle, R. J. & Whittaker, R. J.) (Wiley, 2011).
    Google Scholar 
    Bevilacqua, M. Áreas protegidas y conservación de la diversidad biológica. Biodivers. Venezuela 2, 922–943 (2003).
    Google Scholar 
    Franco, P., Saavedra-Rodríguez, C. A. & Kattan, G. H. Bird species diversity captured by protected areas in the Andes of Colombia: A gap analysis. Oryx 41, 57–63 (2007).Article 

    Google Scholar 
    Barzetti, V. Parks and Progress: Protected Areas and Economic Development in Latin America and the Caribbean. (1993).Schulman, L. et al. Amazonian biodiversity and protected areas: Do they meet?. Biodivers. Conserv. 16, 3011–3051 (2007).Article 

    Google Scholar 
    Dourojeanni, M. J. Áreas naturales protegidas e investigación científica en el Perú. Rev. For. Perú 33, 91–101 (2018).
    Google Scholar 
    Rodriguez, L. & Young, K. Biological diversity of peru: Determining priority areas for conservation. Ambio 29, 329–337 (2000).Article 

    Google Scholar 
    Ministerio del Ambiente & SERNANP. Plan Director de las Áreas Naturales Protegidas (Estrategia Nacional) (2009).Cuesta-Camacho, F. et al. Identificación de Vacíos y Prioridades de Conservación Para la Biodiversidad Terrestre en el Ecuador Continental. http://protectedareas.info/upload/document/ecuador_terrestrial_gap_analysis.pdf (2006).Naveda, J. A. Evaluación del grado de representatividad ecológica y geográfica del sistema de parques nacionales de Venezuela al norte del Orinoco: Anteproyecto. Rev. Geog. Venez. 38, 193–208 (1997).
    Google Scholar 
    Araujo, N., Müller, R., Nowicki, C. & Ibisch, P. L. Prioridades de conservación de la biodiversidad de Bolivia (editorial FAN, 2010)Arango, N. et al. Vacíos de Conservación del Sistema de Parques Nacionales Naturales de Colombia desde una Perspectiva Ecorregional. https://wwflac.awsassets.panda.org/downloads/vacios_de_conservacion.pdf (2003).Margules, C. R. & Pressey, R. L. Systematic conservation planning. Nature 405, 243–253 (2000).Article 
    CAS 

    Google Scholar 
    Sarkar, S., Sánchez-Cordero, V., Londoño, M. C. & Fuller, T. Systematic conservation assessment for the Mesoamerica, Chocó, and Tropical Andes biodiversity hotspots: A preliminary analysis. Biodivers. Conserv. 18, 1793–1828 (2009).Article 

    Google Scholar 
    Lessmann, J., Muñoz, J. & Bonaccorso, E. Maximizing species conservation in continental Ecuador: A case of systematic conservation planning for biodiverse regions. Ecol. Evol. 4, 2410–2422 (2014).Article 

    Google Scholar 
    Young, B. E. et al. Using spatial models to predict areas of endemism and gaps in the protection of Andean slope birds. Auk 126, 554–565 (2009).Article 

    Google Scholar 
    Fajardo, J., Lessmann, J., Bonaccorso, E., Devenish, C. & Muñoz, J. Combined use of systematic conservation planning, species distribution modelling, and connectivity analysis reveals severe conservation gaps in a megadiverse country (Peru). PLoS ONE 9, 1–23 (2014).Article 

    Google Scholar 
    Butchart, S. H. M. et al. Shortfalls and solutions for meeting national and global conservation area targets. Conserv. Lett. 8, 329–337 (2015).Article 

    Google Scholar 
    Pimm, S. L. et al. The biodiversity of species and their rates of extinction, distribution, and protection. Science 344, 6187 (2014).Article 

    Google Scholar 
    Swenson, J. J. et al. Plant and animal endemism in the eastern Andean slope: Challenges to conservation. BMC Ecol. 12, 1 (2012).Article 

    Google Scholar 
    Lessmann, J., Fajardo, J., Bonaccorso, E. & Bruner, A. Cost-effective protection of biodiversity in the western Amazon. Biol. Conserv. 235, 250–259 (2019).Article 

    Google Scholar 
    Rodrigues, A. S. L. & Gaston, K. J. How large do reserve networks need to be?. Ecol. Lett. 4, 602–609 (2001).Article 

    Google Scholar 
    Reyes-Puig, C. Diversity, threat, and conservation of reptiles from continental Ecuador. Amphib. Reptile Conserv. 11, 8 (2017).
    Google Scholar 
    Shanee, S. et al. Protected area coverage of threatened vertebrates and ecoregions in Peru: Comparison of communal, private and state reserves. J. Environ. Manage. 202, 12–20 (2017).Article 

    Google Scholar 
    Kujala, H., Moilanen, A., Araújo, M. B. & Cabeza, M. Conservation planning with uncertain climate change projections. PLoS ONE 8, e53315 (2013).Article 
    ADS 
    CAS 

    Google Scholar 
    Hannah, L. et al. 30% land conservation and climate action reduces tropical extinction risk by more than 50%. Ecography 43, 1–11 (2020).Article 

    Google Scholar 
    Velásquez-Tibatá, J., Salaman, P. & Graham, C. H. Effects of climate change on species distribution, community structure, and conservation of birds in protected areas in Colombia. Reg. Environ. Change 13, 235–248 (2013).Article 

    Google Scholar 
    del Avalos, V. R. & Hernández, J. Projected distribution shifts and protected area coverage of range-restricted Andean birds under climate change. Glob. Ecol. Conserv. 4, 459–469 (2015).Article 

    Google Scholar 
    Warren, R. et al. Quantifying the benefit of early climate change mitigation in avoiding biodiversity loss. Nat. Clim. Change 3, 678–682 (2013).Article 
    ADS 

    Google Scholar 
    Golden Kroner, R. et al. COVID-era policies and economic recovery plans: Are governments building back better for protected and conserved areas?. PARKS 27, 135–148 (2021).Article 

    Google Scholar 
    IPCC Summary for Policymakers. In Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (eds Stocker, T. F. et al.) (Cambridge University Press, 2013).
    Google Scholar 
    Chevalier, M., Zarzo-Arias, A., Guélat, J., Mateo, R. G. & Guisan, A. Accounting for niche truncation to improve spatial and temporal predictions of species distributions. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2022.944116 (2022).Article 

    Google Scholar 
    Watson, J. E. M. et al. Bolder science needed now for protected areas. Conserv. Biol. 30, 243–248 (2016).Article 

    Google Scholar 
    CBD. Kunming-Montreal Global Biodiversity Framework, Draft Decision Submitted by the PRESIDENT. (2022). CBD/COP/15/L.25. https://www.cbd.int/doc/c/e6d3/cd1d/daf663719a03902a9b116c34/cop-15-l-25-en.pdfCBD. Report of the Expert Workshop on the Monitoring Framework for the Post-2020 Global Biodiversity Framework (CBD, 2022).
    Google Scholar 
    Chaplin-Kramer, R. et al. Mapping the planet’s critical natural assets. Nat. Ecol. Evol. https://doi.org/10.1038/s41559-022-01934-5 (2022).Article 

    Google Scholar 
    Watson, J. E. M. et al. The exceptional value of intact forest ecosystems. Nat. Ecol. Evol. 2, 599–610 (2018).Article 

    Google Scholar 
    Elbers, J. Las Áreas Protegidas de América Latina: Situación Actual y Perspectivas PARA el Futuro (2011).Miller, D. C. & Nakamura, K. S. Protected areas and the sustainable governance of forest resources. Curr. Opin. Environ. Sustain. 32, 96–103 (2018).Article 

    Google Scholar 
    Guisan, A. & Zimmermann, N. E. Predictive habitat distribution models in ecology. Ecol. Model. 135, 147–186 (2000).Article 

    Google Scholar 
    Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005).Article 

    Google Scholar 
    van Proosdij, A. S. J., Sosef, M. S. M., Wieringa, J. J. & Raes, N. Minimum required number of specimen records to develop accurate species distribution models. Ecography 39, 542–552 (2016).Article 

    Google Scholar 
    Breiner, F. T., Guisan, A., Bergamini, A. & Nobis, M. P. Overcoming limitations of modelling rare species by using ensembles of small models. Methods Ecol. Evol. 6, 1210–1218 (2015).Article 

    Google Scholar 
    Phillips, S. J. et al. Sample selection bias and presence-only distribution models: Implications for background and pseudo-absence data. Ecol. Appl. 19, 181–197 (2009).Article 

    Google Scholar 
    Thornhill, A. H. et al. Spatial phylogenetics of the native California flora. BMC Biol 15, 96 (2017).Article 

    Google Scholar 
    Radosavljevic, A. & Anderson, R. P. Making better Maxent models of species distributions: Complexity, overfitting and evaluation. J. Biogeogr. 41, 629–643 (2014).Article 

    Google Scholar 
    Kershaw, F. et al. Informing conservation units: Barriers to dispersal for the yellow anaconda. Divers. Distrib. 19, 1164–1174 (2013).Article 

    Google Scholar 
    Venter, O. et al. Targeting global protected area expansion for imperiled biodiversity. PLoS Biol. 12, e1001891 (2014).Article 

    Google Scholar 
    Gaston, K. J. The Structure and Dynamics of Geographic Ranges (Oxford University Press, 2003).
    Google Scholar 
    Yin, L., Fu, R., Shevliakova, E. & Dickinson, R. E. How well can CMIP5 simulate precipitation and its controlling processes over tropical South America?. Clim. Dyn. 41, 3127–3143 (2013).Article 

    Google Scholar  More

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    Plant nitrogen retention in alpine grasslands of the Tibetan Plateau under multi-level nitrogen addition

    Study siteThe field experiment was conducted at Namco Station (30°47’N, 90°58’E, altitude 4730 m) of the Institute of Tibetan Plateau Research, Chinese Academy of Sciences (ITPCAS), which is located in the alpine steppes of TP in China. The experiment was permitted by ITPCAS, complied with local and national guidelines and regulations. From 2006 to 2017, the mean annual temperature (MAT) and mean annual precipitation (MAP) was about − 0.6 °C and 406 mm, respectively. Monthly mean temperature varied from − 10.8 °C in January to 9.1 °C in July and most of the precipitation occurred from May to October37,38. During our six-year observations (2010, 2011, 2012, 2013, 2015 and 2017), climate change during the growing season from May to September varied differently, with the annual precipitation ranged from 255.9 mm to 493.8 mm and the MAT from 6.7 to 7.4 °C. Androsace tapete, Kobresia pygmaea, Stipa purpurea and Leontopodium pusillum were the dominant plant species at the alpine steppe.Experimental design and treatmentsThe long-term experiment began in May, 2010. Three homogenous plots were randomly arranged as replicates at the alpine steppe and six subplots (~ 13 m2) were distributed in each plot by a cycle, with a 2 m buffer zone between each adjacent subplot (Appendix S1: Fig. S1). In this experiment, six treatments of N fertilization rate (0, 1, 2, 4, 8, and 16 g N m−2 yr−1) were clockwise applied in each subplot. The subplots of 0 g N m−2 yr−1 were control group. We sprayed NH4NO3 solution on the first day of each month in the growing season (from May to September) each year. After fertilizing, we rinsed plant residual fertilizer with a little deionized water (no more than 2 mm rainfall). For the control groups, we added equivalent amount of water. The experiment was conducted from 2010 to 2017 (it should be pointed out that there was no fertilization in 2014 and 2016).Sampling and measurementsThe samples were collected with the training and permission of ITPCAS and involved plants that are common species and not endangered or protected. The identification of the plants was done by referring to a book of Chen and Yang39. Pictures of the corresponding specimens can be seen on the website of ITPCAS (http://itpcas.cas.cn/kxcb/kxtp/nmc_normal_plant/).Vegetation samples were collected in August in 2011 and repeated at the same time in 2012, 2013, 2015 and 2017. We established one 50 × 50 cm quadrat in each subplot, clipped aboveground biomass (AGB) and sorted species by families. The biomass was used to measure ANPP (g m−2 yr−1). Following aboveground portion collected, we used three soil cores (5 cm diameter) to collect the belowground roots at 0–30 cm depth and mixed into one sample, which were used to assess belowground net primary productivity (BNPP, g m−2 yr−1). The roots were cleaned with running water to remove sand and stones.Both plant and root samples were dried at 75 °C for 48 h and then ground into powder (particle size ~ 5 μm) by a laboratory mixer mill (MM400, Retsch). To determine N and C content of plants, we weighed the samples into tin capsules and measured with the elemental analyzer (MAT253, Finnigan MAT GmbH, Germany).Estimation of the critical N rate (Ncr), N retention fraction (NRF), N retention capacity and N-induced C gainAccording to the N saturation hypothesis, plant productivity increases gradually during N addition, reaches a maximum at the Ncr, and eventually declines16,17. We considered the Ncr to be the rate where ANPP no longer remarkably changed with N addition (Fig. 1).We defined plant N retention fraction (NRF, %; Eq. 1) as the aboveground N storage caused by unit N addition rate, and N retention capacity (g N m−2 yr−1; Eq. 2) was the increment of N storage due to exogenous N addition compared to the control40. The equations are as following:$$N;retention;fraction = frac{{ANPP_{tr} times N;content_{tr} – ANPP_{ck} times N;content_{ck} }}{N;rate}$$
    (1)
    $$N;retention;capacity = ANPP_{tr} times N;content_{tr} – ANPP_{ck} times N;content_{ck}$$
    (2)
    where ANPPtr and N contenttr (%) refer to those in the treatment (tr) groups, and ANPPck and N contentck refer to those in the control (ck) groups. These expressions are also used in the following equations (Eqs. 3–5).The N-induced C gain (g C m−2 yr−1; Eq. 3) was estimated by the increment of C storage owing to exogenous N addition compared to the control40. Maximum N retention capacity (MNRC, Eq. 4) and maximum N-induced C gain (Eq. 5) mean the maximum N and C storage increment in plant caused by exogenous N input at Ncr, respectively. The formulas are as following:$$N{text{-}}induced;C;gain = ANPP_{tr} times C;content_{tr} – ANPP_{ck} times C;content_{ck}$$
    (3)
    $$MNRC = ANPP_{max } times N;content_{max } – ANPP_{ck} times N;content_{ck}$$
    (4)
    $$Maximum;N{text{-}}induced;C;gain = ANPP_{max } times C;content_{max } – ANPP_{ck} times C;content_{ck}$$
    (5)
    where ANPPmax, N contentmax and C contentmax refer to the value of ANPP, N content and C content at Ncr, respectively.Data synthesisTo evaluate N limitation and saturation on the TP more accurately, we searched papers from the Web of Science (https://www.webofscience.com) and the China National Knowledge Infrastructure (https://www.cnki.net). The keywords used by article searching were: (a) N addition, N deposition or N fertilization, (b) grassland, steppe or meadow. Article selection was based on the following conditions. First, the experimental site must be conducted in a grassland ecosystem. Second, the experiment had at least three N addition levels and a control group. Third, if the experiment lasted for many years, we analyzed data with multi-year average. Based on the above, we collected 89 independent experimental cases. Among these, 27 cases were located on the TP alpine grasslands, 25 in the Inner Mongolia (IM) grasslands and 37 in other terrestrial grasslands (detailed information sees Appendix S2: Table S1).We extracted ANPP data and N addition rate of these cases and estimated Ncr and ANPPmax (Appendix S2: Fig. S2). We then calculated NRF, N retention and C gain of each group of data for further analysis (Appendix S2: Table S2). Most of the 89 cases did not have data on N and C content. To facilitate the calculation, we summarized N and C content from 40 articles in the neighboring areas of the cases and divided the N and C content into seven intervals according to the N addition rate (Appendix S2: Table S3 and Fig. S3). The unit of N addition rate was unified to “g N m−2 yr−1”. All the original data were obtained directly from texts and tables of published papers. If the data were displayed only in graphs, Getdata 2.20 was used to digitize the numerical data. For the estimation of N retention and C gain of the TP at current N deposition rates and future at Ncr, we fitted the exponential relationship to the data from 27 cases on the TP, and then substituted N rates into the fitted equations (Eq. 6):$$y = a times left[ {1 – exp left( { – bx} right)} right].$$
    (6)
    We also included MAT, MAP, soil C:N ratio, fencing management (fencing or grazing) and grassland type (meadow, steppe and desert steppe) of the experiment sites for exploring the drivers affecting N limitation (Appendix S2: Table S1). When climatic data were missing from the article, MAT and MAP were obtained from the WorldClim (http://www.worldclim.org).Species were usually divided into four functional groups (grasses, sedges, legumes and forbs) to study the response of species composition to N addition in previous study41. We synthesized 13 TP experimental cases (including our field experiment) from the data synthesis and each case included at least three functional groups (detailed references see Appendix S2).Statistical analysisThere were 42 species in our field experiment. We divided them by family into eleven groups: Asteraceae (forbs), Poaceae (grasses), Leguminosae (legumes), Rosaceae (forbs), Boraginaceae (forbs), Caryophyllaceae (forbs), Cyperaceae (sedges), Labiatae (forbs), Primulaceae (forbs), Scrophulariaceae (forbs) and Others. Due to species in the group of Others contributed only 1.22% of AGB, we analyzed AGB and foliar stoichiometry among other ten families (Appendix S1: Table S1). In Namco steppe, forbs, grasses, sedges and legumes accounted for 78.0%, 7.4%, 8.2% and 5.2% of the AGB respectively (Appendix S1: Table S1 and Fig. S2). Such a large number of forbs suggested that our experiment was conducted on a severely degraded grassland.For our field data, two-way ANOVAs were used to analyze the effects of year, N fertilization rate and their interactions on species AGB. One-way ANOVAs were used to test the response of ANPP, BNPP, root:shoot ratio, species foliar C content, N content and C:N ratio to N addition rate. Duncan’s new multiple range test was used to compare the fertilization influences at each rate in these ANOVAs. Prior to the above ANOVAs, we performed homogeneity of variance test and transformed the data logarithmically when necessary. Simple regression was used to estimate the relevance among ANPP, NRF, N retention capacity and C gain with N addition rates.Structural equation modeling (SEM) was used to explore complex relationships among multiple variables. To quantify the contribution of drivers such as climate and soil to Ncr, ANPP, NRF and MNRC, we constructed SEM based on existing ecological knowledge and the possible relationships between variables. We considered environmental factors (MAT, MAP and soil C:N) and ANPPck as explanatory variables, and Ncr, NRF and MNRC as response variables. We included the ANPPck in the SEM rather than the ANPPmax because we wonder whether there was a relationship between ANPP in the absence of exogenous N input and the ecosystem N retention in the presence of N saturation. This has important implications for assessing N input. Before constructing the SEM, we excluded collinearity between the factors. In addition, Student’s t-test and one-way ANOVAs were performed to explain the effect of fencing management and grassland type on above response variables, respectively. The SEM was constructed using the R package “piecewiseSEM”42. Fisher’s C was used to assess the goodness-of-model fit, and AIC was for model comparison.Given the influence of extreme values in the data synthesis, we calculated the geometric mean of Ncr, NRF, N retention and N-induced C gain. All statistical analyses were performed with SPSS 26.0 and RStudio (Version 1.2.1335) based on R version 3.6.2 (R Core Team, 2019). More

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    Smart forest management boosts both carbon storage and bioenergy

    Timothy Searchinger and his colleagues raise concerns that the European Union’s plan to produce energy from biomass could compromise forest carbon stocks and biodiversity (Nature 612, 27–30; 2022). However, it is possible for improved forest management to reconcile increased bioenergy production by maintaining and restoring forest ecosystems.
    Competing Interests
    The authors declare no competing interests. More

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    Organic amendment treatments for antimicrobial resistance and mobile element genes risk reduction in soil-crop systems

    D’Costa, V. M. et al. Antibiotic resistance is ancient. Nature 477, 457–461. https://doi.org/10.1038/nature10388 (2011).Article 
    ADS 

    Google Scholar 
    Cytryn, E. The soil resistome: The anthropogenic, the native, and the unknown. Soil Biol. Biochem. 63, 18–23. https://doi.org/10.1016/j.soilbio.2013.03.017 (2013).Article 

    Google Scholar 
    Holmes, A. H. et al. Understanding the mechanisms and drivers of antimicrobial resistance. Lancet 387, 176–187. https://doi.org/10.1016/S0140-6736(15)00473-0 (2016).Article 

    Google Scholar 
    Regulation (EC) No 1831/2003 of the European parliament and of the council of 22 September 2003 on additives for use in animal nutrition.European Commission. Communication from the commission to the European parliament, the council, the European economic and social committee and the committee of the regions: A farm to fork strategy for a fair, healthy and environmentally-friendly food system COM/2020/381 Final, (2020).Kumar, K. C., Gupta, S. C., Chander, Y. & Singh, A. K. Antibiotic use in agriculture and its impact on the terrestrial environment. Adv. Agron. 87, 1–54. https://doi.org/10.1016/S0065-2113(05)87001-4 (2005).Article 

    Google Scholar 
    Chee-Sanford, J. C. et al. Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. J. Environ. Qual. 38, 1086–1108. https://doi.org/10.2134/jeq2008.0128 (2009).Article 

    Google Scholar 
    Heuer, H., Schmitt, H. & Smalla, K. Antibiotic resistance gene spread due to manure application on agricultural fields. Curr. Opin. Microbiol. 14, 236–243. https://doi.org/10.1016/j.mib.2011.04.009 (2011).Article 

    Google Scholar 
    Epelde, L. et al. Characterization of composted organic amendments for agricultural use. Front. Sustain. Food Syst. 2, 44. https://doi.org/10.3389/fsufs.2018.00044 (2018).Article 

    Google Scholar 
    Youngquist, C. P., Mitchell, S. M. & Cogger, C. G. Fate of antibiotics and antibiotic resistance during digestion and composting: A review. J. Environ. Qual. 45, 537–545. https://doi.org/10.2134/jeq2015.05.0256 (2016).Article 

    Google Scholar 
    Ma, X., Xue, X., González-Mejía, A., Garland, J. & Cashdollar, J. Sustainable water systems for the city of tomorrow: A conceptual framework. Sustainability 7, 12071–12105. https://doi.org/10.3390/su70912071 (2015).Article 

    Google Scholar 
    Wang, Y. et al. Degradation of antibiotic resistance genes and mobile gene elements in dairy manure anerobic digestion. PLoS ONE 16, e0254836. https://doi.org/10.1371/journal.pone.0254836 (2021).Article 

    Google Scholar 
    Thanomsub, B. et al. Effects of ozone treatment on cell growth and ultrastructural changes in bacteria. J. Gen. Appl. Microbiol. 48, 193–199. https://doi.org/10.2323/jgam.48.193 (2002).Article 

    Google Scholar 
    Sousa, J. M. et al. Ozonation and UV254nm radiation for the removal of microorganisms and antibiotic resistance genes from urban wastewater. J. Hazard. Mater. 323, 434–441. https://doi.org/10.1016/j.jhazmat.2016.03.096 (2017).Article 

    Google Scholar 
    Park, J. H., Choppala, G. K., Bolan, N. S., Chung, J. W. & Chuasavathi, T. Biochar reduces the bioavailability and phytotoxicity of heavy metals. Plant Soil 348, 439–451. https://doi.org/10.1007/s11104-011-0948-y (2011).Article 

    Google Scholar 
    Jeffery, S. et al. The way forward in biochar research: targeting trade-offs between the potential wins. GCB Bioenergy 7, 1–13. https://doi.org/10.1111/gcbb.12132 (2015).Article 

    Google Scholar 
    Krasucka, P. et al. Engineered biochar: A sustainable solution for the removal of antibiotics from water. Chem. Eng. J. 405, 126926. https://doi.org/10.1016/j.cej.2020.126926 (2021).Article 

    Google Scholar 
    Ken, D. S. & Sinha, A. Recent developments in surface modification of Nano zero-valent iron (nZVI): remediation, toxicity and environmental impacts. Environ. Nanotechnol. Monit. Manag. 14, 100344. https://doi.org/10.1016/j.enmm.2020.100344 (2020).Article 

    Google Scholar 
    Zhao, X. et al. An overview of preparation and applications of stabilized zero-valent iron nanoparticles for soil and groundwater remediation. Water Res. 100, 245–266. https://doi.org/10.1016/j.watres.2016.05.019 (2016).Article 

    Google Scholar 
    Diao, M. & Yao, M. Use of zero-valent iron nanoparticles in inactivating microbes. Water Res. 43, 5243–5251. https://doi.org/10.1016/j.watres.2009.08.051 (2009).Article 

    Google Scholar 
    Shi, C. J., Wei, J., Jin, Y., Kniel, K. E. & Chiu, P. C. Removal of viruses and bacteriophages from drinking water using zero-valent iron. Sep. Purif. Technol. 84, 72–78. https://doi.org/10.1016/j.seppur.2011.06.036 (2012).Article 

    Google Scholar 
    Anza, M., Salazar, O., Epelde, L., Alkorta, I. & Garbisu, C. The application of nanoscale zero-valent iron promotes soil remediation while negatively affecting soil microbial biomass and activity. Front. Environ. Sci. 7, 19. https://doi.org/10.3389/fenvs.2019.00019 (2019).Article 

    Google Scholar 
    FAOSTAT. Mushrooms and truffles, production quantity (tons). https://www.tilasto.com/en/topic/geography-and-agriculture/crop/mushrooms-and-truffles/mushrooms-and-truffles-production-quantity/spain, (2020).Polat, E., Uzun, H., Topçuo, B., Önal, K. & Onus, A. N. Effects of spent mushroom compost on quality and productivity of cucumber (Cucumis sativus L.) grown in greenhouses. Afr. J. Biotechnol. 8, 176–180 (2009).
    Google Scholar 
    Fazaeli, H. & Masoodi, A. R. T. Spent wheat straw compost of Agaricus bisporus mushroom as ruminant feed. Asian-Australas. J. Anim. Sci. 19, 845–851. https://doi.org/10.5713/ajas.2006.845 (2006).Article 

    Google Scholar 
    Phan, C. W. & Sabaratnam, V. Potential uses of spent mushroom substrate and its associated lignocellulosic enzymes. Appl. Microbiol. Biotechnol. 96, 863–873. https://doi.org/10.1007/s00253-012-4446-9 (2012).Article 

    Google Scholar 
    Lau, K. L., Tsang, Y. Y. & Chiu, S. W. Use of spent mushroom compost to bioremediate PAH-contaminated samples. Chemosphere 52, 1539–1546. https://doi.org/10.1016/S0045-6535(03)00493-4 (2003).Article 
    ADS 

    Google Scholar 
    Mayans, B. et al. An assessment of Pleurotus ostreatus to remove sulfonamides, and its role as a biofilter based on its own spent mushroom substrate. Environ. Sci. Pollut. Res. Int. 28, 7032–7042. https://doi.org/10.1007/s11356-020-11078-3 (2021).Article 

    Google Scholar 
    Congilosi, J. L. & Aga, D. S. Review on the fate of antimicrobials, antimicrobial resistance genes, and other micropollutants in manure during enhanced anaerobic digestion and composting. J. Hazard. Mater. 405, 123634. https://doi.org/10.1016/j.jhazmat.2020.123634 (2021).Article 

    Google Scholar 
    Oliver, J. P. et al. Invited review: fate of antibiotic residues, antibiotic-resistant bacteria, and antibiotic resistance genes in US dairy manure management systems. J. Dairy Sci. 103, 1051–1071. https://doi.org/10.3168/jds.2019-16778 (2020).Article 

    Google Scholar 
    Beneragama, N. et al. Survival of multidrug-resistant bacteria in thermophilic and mesophilic anaerobic co-digestion of dairy manure and waste milk. Anim. Sci. J. 84, 426–433. https://doi.org/10.1111/asj.12017 (2013).Article 

    Google Scholar 
    Sun, W., Qian, X., Gu, J., Wang, X. J. & Duan, M. L. Mechanism and effect of temperature on variations in antibiotic resistance genes during anaerobic digestion of dairy manure. Sci. Rep. 6, 30237. https://doi.org/10.1038/srep30237 (2016).Article 
    ADS 

    Google Scholar 
    Sun, W., Gu, J., Wang, X., Qian, X. & Peng, H. Solid-state anaerobic digestion facilitates the removal of antibiotic resistance genes and mobile genetic elements from cattle manure. Bioresour. Technol. 274, 287–295. https://doi.org/10.1016/j.biortech.2018.09.013 (2019).Article 

    Google Scholar 
    Zou, Y., Xiao, Y., Wang, H., Fang, T. & Dong, P. New insight into fates of sulfonamide and tetracycline resistance genes and resistant bacteria during anaerobic digestion of manure at thermophilic and mesophilic temperatures. J. Hazard. Mater. 384, 121433. https://doi.org/10.1016/j.jhazmat.2019.121433 (2020).Article 

    Google Scholar 
    Agga, G. E., Kasumba, J., Loughrin, J. H. & Conte, E. D. Anaerobic digestion of tetracycline spiked livestock manure and poultry litter increased the abundances of antibiotic and heavy metal resistance genes. Front Microbiol. 11, 614424. https://doi.org/10.3389/fmicb.2020.614424 (2020).Article 

    Google Scholar 
    Jauregi, L., Epelde, L., González, A., Lavín, J. L. & Garbisu, C. Reduction of the resistome risk from cow slurry and manure microbiomes to soil and vegetable microbiomes. Environ. Microbiol. 23, 7643–7660. https://doi.org/10.1111/1462-2920.15842 (2021).Article 

    Google Scholar 
    Zhang, Z. et al. Assessment of global health risk of antibiotic resistance genes. Nat Commun 13, 1553. https://doi.org/10.1038/s41467-022-29283-8 (2022).Article 
    ADS 

    Google Scholar 
    He, Y. et al. Antibiotic resistance genes from livestock waste: occurrence, dissemination, and treatment. npj Clean Water 3, 4. https://doi.org/10.1038/s41545-020-0051-0 (2020).Article 

    Google Scholar 
    Cui, E., Wu, Y., Zuo, Y. & Chen, H. Effect of different biochars on antibiotic resistance genes and bacterial community during chicken manure composting. Bioresour. Technol. 203, 11–17. https://doi.org/10.1016/j.biortech.2015.12.030 (2016).Article 

    Google Scholar 
    Fu, Y., Zhang, A., Guo, T., Zhu, Y. & Shao, Y. Biochar and hyperthermophiles as additives accelerate the removal of antibiotic resistance genes and mobile genetic elements during composting. Materials (Basel) 14, 5428. https://doi.org/10.3390/ma14185428 (2021).Article 
    ADS 

    Google Scholar 
    Forsberg, K. J. et al. Bacterial phylogeny structures soil resistomes across habitats. Nature 509, 612–616. https://doi.org/10.1038/nature13377 (2014).Article 
    ADS 

    Google Scholar 
    Li, H. et al. Effects of bamboo charcoal on antibiotic resistance genes during chicken manure composting. Ecotoxicol. Environ. Saf. 140, 1–6. https://doi.org/10.1016/j.ecoenv.2017.01.007 (2017).Article 
    ADS 

    Google Scholar 
    Bondarenko, O., Ivask, A., Käkinen, A. & Kahru, A. Sub-toxic effects of CuO nanoparticles on bacteria: Kinetics, role of Cu ions and possible mechanisms of action. Environ. Pollut. 169, 81–89. https://doi.org/10.1016/j.envpol.2012.05.009 (2012).Article 

    Google Scholar 
    Wang, X. et al. Bacterial exposure to ZnO nanoparticles facilitates horizontal transfer of antibiotic resistance genes. NanoImpact 10, 61–67. https://doi.org/10.1016/j.impact.2017.11.006 (2018).Article 
    ADS 

    Google Scholar 
    Qiu, X., Zhou, G. & Wang, H. Nanoscale zero-valent iron inhibits the horizontal gene transfer of antibiotic resistance genes in chicken manure compost. J. Hazard. Mater. 422, 126883. https://doi.org/10.1016/j.jhazmat.2021.126883 (2022).Article 

    Google Scholar 
    Zeng, T., Wilson, C. J. & Mitch, W. A. Effect of chemical oxidation on the sorption tendency of dissolved organic matter to a model hydrophobic surface. Environ. Sci. Technol. 48, 5118–5126. https://doi.org/10.1021/es405257b (2014).Article 
    ADS 

    Google Scholar 
    Pak, G. et al. Comparison of antibiotic resistance removal efficiencies using ozone disinfection under different pH and suspended solids and humic substance concentrations. Environ. Sci. Technol. 50, 7590–7600. https://doi.org/10.1021/acs.est.6b01340 (2016).Article 
    ADS 

    Google Scholar 
    Zhuang, Y. et al. Inactivation of antibiotic resistance genes in municipal wastewater by chlorination, ultraviolet, and ozonation disinfection. Environ. Sci. Pollut. Res. Int. 22, 7037–7044. https://doi.org/10.1007/s11356-014-3919-z (2015).Article 

    Google Scholar 
    Park, S., Rana, A., Sung, W. & Munir, M. Competitiveness of quantitative polymerase chain reaction (qPCR) and droplet digital polymerase chain reaction (ddPCR) technologies, with a particular focus on detection of antibiotic resistance genes (ARGs). Appl. Microbiol. 1, 426–444. https://doi.org/10.3390/applmicrobiol1030028 (2021).Article 

    Google Scholar 
    European Medicines Agency. European surveillance of veterinary antimicrobial consumption, (2020). Sales of Veterinary Antimicrobial Agents in 31 European Countries in 2018 (EMA/24309/2020).Heuer, H. et al. The complete sequences of plasmids pB2 and pB3 provide evidence for a recent ancestor of the IncP-1β group without any accessory genes. Microbiology (Reading) 150, 3591–3599. https://doi.org/10.1099/mic.0.27304-0 (2004).Article 

    Google Scholar 
    World Health Organization. Critically Important Antimicrobials for Human Medicine, 6th Revision (WHO, Geneva, Switzerland, 2019).Zhu, Y. G. et al. Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc. Natl Acad. Sci. U. S. A. 110, 3435–3440. https://doi.org/10.1073/pnas.1222743110 (2013).Article 
    ADS 

    Google Scholar 
    Guo, T. et al. Increased occurrence of heavy metals, antibiotics and resistance genes in surface soil after long-term application of manure. Sci. Total Environ. 635, 995–1003. https://doi.org/10.1016/j.scitotenv.2018.04.194 (2018).Article 
    ADS 

    Google Scholar 
    Nõlvak, H. et al. Inorganic and organic fertilizers impact the abundance and proportion of antibiotic resistance and integron-integrase genes in agricultural grassland soil. Sci. Total Environ. 562, 678–689. https://doi.org/10.1016/j.scitotenv.2016.04.035 (2016).Article 
    ADS 

    Google Scholar 
    Chen, Q. L. et al. Effect of biochar amendment on the alleviation of antibiotic resistance in soil and phyllosphere of Brassica chinensis L.. Soil Biol. Biochem. 119, 74–82. https://doi.org/10.1016/j.soilbio.2018.01.015 (2018).Article 

    Google Scholar 
    Zhu, B., Chen, Q., Chen, S. & Zhu, Y. G. Does organically produced lettuce harbor higher abundance of antibiotic resistance genes than conventionally produced?. Environ. Int. 98, 152–159. https://doi.org/10.1016/j.envint.2016.11.001 (2017) .Article 

    Google Scholar 
    Métodos, M. A. P. A. Oficiales de análisis de suelos y Aguas Para riego. Minist. Agric. Pesca Aliment. Métodos Oficiales Anal. III (1994).Muziasari, W. I. et al. Aquaculture changes the profile of antibiotic resistance and mobile genetic element associated genes in Baltic Sea sediments. FEMS Microbiol. Ecol. 92, fiw052. https://doi.org/10.1093/femsec/fiw052 (2016).Article 

    Google Scholar 
    Muurinen, J. et al. Influence of manure application on the environmental resistome under Finnish agricultural practice with restricted antibiotic use. Environ. Sci. Technol. 51, 5989–5999. https://doi.org/10.1021/acs.est.7b00551 (2017).Article 
    ADS 

    Google Scholar 
    Muziasari, W. I. et al. The resistome of farmed fish feces contributes to the enrichment of antibiotic resistance genes in sediments below Baltic Sea fish farms. Front. Microbiol. 7, 2137. https://doi.org/10.3389/fmicb.2016.02137 (2017).Article 

    Google Scholar 
    Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408. https://doi.org/10.1006/meth.2001.1262 (2001).Article 

    Google Scholar 
    Ovreås, L., Forney, L., Daae, F. L. & Torsvik, V. Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl. Environ. Microbiol. 63, 3367–3373. https://doi.org/10.1128/aem.63.9.3367-3373.1997 (1997) .Article 
    ADS 

    Google Scholar 
    Caporaso, J. G. et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 6, 1621–1624. https://doi.org/10.1038/ismej.2012.8 (2012).Article 

    Google Scholar 
    Lanzén, A. et al. Multi-targeted metagenetic analysis of the influence of climate and environmental parameters on soil microbial communities along an elevational gradient. Sci. Rep. 6, 28257. https://doi.org/10.1038/srep28257 (2016).Article 
    ADS 

    Google Scholar 
    Pinna, N. K., Dutta, A., Monzoorul, H. M. & Mande, S. S. Can targeting non-contiguous V-regions with paired-end sequencing improve 16S rRNA-based taxonomic resolution of microbiomes?: An in silico evaluation. Front. Genet. 10, 653. https://doi.org/10.3389/fgene.2019.00653 (2019).Article 

    Google Scholar 
    Andrews, S. FastQC: A quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ (2010).Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17, 10–12. https://doi.org/10.14806/ej.17.1.200 (2011).Article 

    Google Scholar 
    Bolyen, E. et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 37, 852–857. https://doi.org/10.1038/s41587-019-0209-9 (2019).Article 

    Google Scholar 
    Amir, A. et al. Deblur rapidly resolves single-nucleotide community sequence patterns. mSystems 2, e00191-e216. https://doi.org/10.1128/mSystems.00191-16 (2017).Article 

    Google Scholar 
    Yang, Y., Li, B., Zou, S., Fang, H. H. P. & Zhang, T. Fate of antibiotic resistance genes in sewage treatment plant revealed by metagenomic approach. Water Res. 62, 97–106. https://doi.org/10.1016/j.watres.2014.05.019 (2014).Article 

    Google Scholar 
    Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer-Verlag, 2016).Book 
    MATH 

    Google Scholar 
    de Mendiburu, F. Agricolae: Statistical procedures for agricultural research. R package version 1.3-3. https://CRAN.R-project.org/package=agricolae (2020).Paradis, E. & Schliep, K. ape 5.0: An environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526–528. https://doi.org/10.1093/bioinformatics/bty633 (2019).Article 

    Google Scholar 
    Oksanen, J. et al. Vegan: Community ecology package. R Package Version 2.3-1. (2015). More

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    Human activities favour prolific life histories in both traded and introduced vertebrates

    Data collectionWe obtained trade data from two different sources: the United States Fish and Wildlife Service (USFWS) Law Enforcement Management Information System (LEMIS)31 and the International Union for Conservation of Nature (IUCN) Red List32. We used the former to obtain data on the live wildlife trade in general and the latter for data on the pet trade specifically. We then matched trade data with our previously compiled global scale datasets of life history traits and introductions in mammals, reptiles and amphibians25,26.We obtained data on the US live wildlife trade from LEMIS by a Freedom of Information Act Request on 12/08/2019. We requested summary data on all US imports and exports of wildlife across all available years (1999-2019) and all trade purposes, including information on species identities and shipment contents (e.g. live individuals, meat, skins, etc.). For each species, we summed the total number of recorded shipments of live individuals (including individuals that died in transit, and live eggs) as a measure of trade frequency. We classified species as in trade if there was at least one shipment of live individuals recorded in the LEMIS database, and as not traded otherwise. The LEMIS dataset is geographically limited to trade by the US, and therefore may not capture the full diversity of species involved in the wildlife trade. For example, the LEMIS database may be missing some species involved in the substantial trade in live wildlife between South–East Asian countries50. However, the US represents one of the most dominant players in the global market for live wildlife16, and by summing both imports and exports we capture demand for species in countries beyond the US to some extent. Supplementary Fig. 2 illustrates the frequency of trade between the US and countries represented in the US LEMIS dataset. LEMIS data should be considered a minimum estimate of the diversity of species involved in the wildlife trade since they mostly record only legal trade (although confiscated shipments are recorded), and shipments are sometimes not identified to the species level16,51,53,53. The LEMIS database also contains some mis-spelled and incorrectly identified species due to human input errors52. To minimise the effect of misidentified shipments on our species level classifications of US trade status, we discarded all LEMIS records that were not identified to the species level (i.e. those identified using genus, common or generic names only), and manually checked the LEMIS data for synonyms and alternate spellings when we could not automatically match any records in LEMIS with species in our life history datasets. Species classified as traded on the basis of a single recorded live shipment in LEMIS are most vulnerable to species level misclassification due to misidentified shipments. The vast majority of traded species have multiple shipments recorded in LEMIS (259/312 [83%] of traded mammals, 265/285 [93%] of traded reptiles and 72/75 [96%] of traded amphibians), reducing the potential impact of shipment level misidentification over the reliability of species level trade classifications. However, to investigate the robustness of our findings to possible errors in species identification in LEMIS, we re-ran our key analyses excluding species classified as traded on the basis of a single live shipment. We found qualitatively the same effects of life history traits on the probability of trade when removing these species as in our full sample (Supplementary Tables 25–27). Despite its limitations, LEMIS is an invaluable resource for identifying broad scale trends in the wildlife trade since few other countries maintain such detailed records, and it is the only large-scale international trade dataset that includes both CITES- and non-CITES-listed species16,41. Including non-CITES listed species in our analyses is important because CITES-listed species represent only a small minority of those in trade14 and are likely to be a biased sample in terms of life history traits, since species vulnerable to extinction typically have slower life histories40.We obtained separate data on the pet trade from the IUCN Red List. The IUCN has assessed the vast majority of mammal, reptile and amphibian species (91%, 79% and 86% respectively54). Here, we classified a species as involved in the pet trade if the IUCN species account included at least one clear description of involvement in the pet trade. Otherwise, we considered a species as not involved in the pet trade. Although LEMIS records the purpose of trade, it uses broad categories (e.g. ‘Commercial’, ‘Personal’, ‘Breeding in captivity’), none of which refers specifically to nor necessarily equates to trade for pets. Therefore, we sought this additional data on the pet trade from the IUCN Red List instead of following the approach of some previous studies which have used LEMIS data as a proxy for the pet trade (e.g. Refs. 15,19). In contrast, the IUCN Red List contains clear textual descriptions of use and trade for many species, allowing us to identify which species are traded specifically for pets32. The IUCN data has further complementary strengths compared with LEMIS in that it is global in scope and includes both legal and illegal trade. We obtained data from the IUCN Red List by manually searching the binomial name of each species in our samples and consulting the ‘Threats’ and ‘Use and Trade’ sections of the species accounts. We classified species as in the pet trade if the information clearly stated this was the case (e.g. “It has been recorded in the pet trade”, “This species appears in the international pet trade”). We discounted descriptions where the information was uncertain (e.g. the species is described as “probably” or “possibly” traded for pets). We did not count as pets those species that the IUCN categorises as used for “Pets/display animals, horticulture” but which are used only for zoos or captive display, such as beluga whales (Delphinapterus leucas). All species described as pets by the IUCN are ‘exotic’, i.e. those without a long history of domestication14, since the IUCN does not list domesticated species.We matched trade data with our previously published global scale datasets on life history traits and introductions25,26. Internationally traded species may or not be released in the wild outside their native range: some may remain in the confines of captivity (e.g. in zoos or kept by private owners). We defined a species as introduced if there was at least one reliable record of its release, by humans, into the wild outside of its native range, either accidentally or intentionally25,26. We included only species with complete data for the same life history traits as used in our prior analyses (mammals: body mass, gestation period, weaning age, neonatal body mass, litter size, litters per year, age at first reproduction and reproductive lifespan; reptiles: body mass, hatchling mass, clutch size, clutches per year, age of sexual maturity, reproductive lifespan and parity; amphibians: snout-vent length, egg size, clutch size, age of sexual maturity and reproductive lifespan) to facilitate direct comparisons with previous results and to allow us to account for covariation between life history traits55. Species with complete life history data represent 7.8%, 3.5% and 1.6% of the total estimated number of species of mammals, reptiles and amphibians respectively56,57,58. These samples are not random as they over-represent orders containing many species of interest and utility to humans (e.g. ungulates, primates, crocodilians) (Supplementary Tables 28–30). However, these biases are unlikely to undermine our results since we examine life history effects on trade and introduction within these samples. Trade and introduction data do not necessarily cover the same time periods: the US dataset covers only the years 1999-present and the IUCN descriptions also typically refer to recent trade. In contrast, our introduction dataset includes both historical and recent introductions25,26. Therefore, the goal of our analyses is not to test causal hypotheses on the direct relationship between trade and introduction but rather to investigate whether the same life history traits predispose species towards both trade and introduction across diverse taxa, locations and circumstances. When combining the datasets and phylogenies59,60,61,62,63, we resolved species name mis-matches by referring to taxonomic information from the IUCN Red List32, the Global Biodiversity Information Facility (GBIF33) and the Integrated Taxonomic Information System (ITIS64). Table 1 summarises final sample sizes and Supplementary Table 1 the degree of overlap between the trade datasets. Most species in the pet trade are also in the general live wildlife trade, but many more species are traded by the US for general purposes than are involved in the pet trade specifically.Finally, we obtained data for a proxy measure of species detectability in order to control for a potential confounding effect on relationships between life history traits and introduction: larger bodied and longer-lived species may be more likely to be recorded by human observers when introduced compared with smaller and shorter-lived species. We obtained data on species occurrence records, geographic range size and population density, assuming that highly detectable species will have a disproportionately large number of recorded observations than expected based on the size of their geographic ranges and average population densities, following similar approaches by e.g. Refs. 65,66. We obtained occurrence records from the Global Biodiversity Information Facility (GBIF33) via the R package rgbif67 selecting only records resulting from human observation. We obtained range sizes (in decimal degrees squared) from the IUCN Red List32 and processed them for analysis using functions from the rgdal package68, excluding areas of uncertain presence (i.e. limiting range to presence code 1, ‘extant’). We obtained population density estimates from the TetraDENSITY database (version 134), a global database of population density estimates for terrestrial vertebrates. Most species in the TetraDENSITY dataset are represented by estimates from multiple different studies (median = 3, range 1–408). We collapsed density estimates to the species level by taking the median value across studies, including all estimates regardless of sampling method to maximise sample size, and converting all units to individuals/km2 to ensure comparability.Statistical analysesTo investigate relationships between life history traits and trade, we run models treating US or pet trade as the outcome variable and life history traits as the predictors. For all analyses, all life history variables were included in the same models to account for covariation among life history traits55. For US trade, where data on trade frequency are available, we run models both in which trade is treated as a binary variable (traded vs. not traded) and as a count variable (frequency of live shipments, including zero values), while for the pet trade, we have no data on trade frequency and so we treat pet trade as a binary variable only. To investigate the effects of life history traits on introduction, we run models in which introduction is the outcome variable and life history traits are the predictors. In introduction models, we only include traded species (running separate models for the set of species in US trade and the set of species in the pet trade). This approach allows us to disentangle effects associated with trade and introduction and thus identify at which stage(s) life history biases emerge. We also run introduction models in which frequency of US trade is included as an additional predictor alongside life history traits, anticipating that highly traded species are more likely to be introduced. Finally, to investigate possible confounding effects of species detectability on relationships between life history traits and introduction, we investigate effects of number of observations, geographic range size and, where sample sizes allowed, population density on the probability of introduction. If highly detectable species are more likely to be recorded as introduced, we expect to find a positive effect of the number of observations (while accounting for geographic range size and population density) on the probability of introduction. If this effect confounds relationships between body mass/lifespan and introduction, the effect of these life history traits on the probability of introduction should disappear when detectability measures are included in the models alongside life history traits. All analyses were conducted using the R statistical programming environment (Version 4.2.069). Plots were coloured using palettes from the viridis package70.To estimate effects of predictor variables, we fit generalized linear mixed models (GLMMs) using Markov chain Monte-Carlo (MCMC) estimation, implemented in the MCMCglmm package35,36. For analyses with binary outcome variables (traded vs. not traded, introduced vs. not introduced) we fit probit models, while for analyses with US trade frequency as the outcome variable we fit hurdle models. Hurdle models estimate two latent variables: the probability that the outcome is zero (on the logit scale), and the probability of the outcome modelled as a Poisson distribution for non-zero values71. This method therefore allows us to estimate effects of life history traits on the probability and frequency of trade in the same model. While the binary component of a hurdle model estimates the probability that outcomes are zero, when reporting results we reverse the sign of coefficients from the binary model for ease of interpretation, so that effects can be interpreted as the probability that the outcome is not zero. Therefore, here predictors with consistent effects on the probability and frequency of trade in hurdle models will have the same sign (so that if, for example, litter size has a positive effect on both the probability and frequency of trade, both coefficients for litter size from the hurdle model will be positive).Datasets comprising biological measures from multiple related species violate the fundamental statistical assumption that observations are independent of one another, since closely related species are more phenotypically similar than expected by chance due to their shared evolutionary history72. To account for the non-independence of species due to shared ancestry, we included a phylogenetic random effect in all models, represented by a variance-covariance (VCV) matrix derived from the phylogeny. The off-diagonal elements of the VCV matrix contain the amount of shared evolutionary history for each pair of species35,37,38 based on the branch lengths of the phylogeny (here proportional to time)59,61,62,63,63. This approach allows us to estimate phylogenetic signal using the heritability (H2) parameter, which measures the proportion of total variance in the latent variable attributable to the phylogeny35,37,38. Heritability is interpreted in the same way as Pagel’s λ in phylogenetic generalized least squares regression35,37,38,72. Specifically, phylogenetic signal is constrained between 0, indicating no phylogenetic effect so that species can be treated as independent, and 1, indicating that similarity between species is directly proportional to their amount of shared evolutionary history35,38,72. As hurdle models estimate two latent variables, for each hurdle model we report two heritability estimates, one for the binary and one for the Poisson component. All continuous independent variables were log-10 transformed due to positively skewed distributions. Although GLMMs do not require normally distributed predictor variables, log-transforming positively skewed life history predictors in phylogenetic comparative analyses allows us to model life history evolution on proportional rather than absolute scales. This is important as it facilitates biologically meaningful comparisons between species across large scales of life history variation73. Further, log-transforming positively skewed predictors helps to meet assumptions of the underlying Brownian motion model of evolutionary change, which assumes that phenotypic change along branches of the phylogeny is normally distributed74.We calculated variance inflation factors (VIFs) using functions from the car R package75 to check for multicollinearity between predictor variables. Where any model reported a variance inflation factor of 5 or above, indicating potentially problematic levels of collinearity76, we re-ran the model removing the variable with the highest VIF iteratively until all the remaining variables had VIFs of More