More stories

  • in

    Viral metagenomes of Lake Soyang, the largest freshwater lake in South Korea

    1.
    Dion, M. B., Oechslin, F. & Moineau, S. Phage diversity, genomics and phylogeny. Nat. Rev. Microbiol. 18, 125–138 (2020).
    CAS  Article  Google Scholar 
    2.
    Steen, A. D. et al. High proportions of bacteria and archaea across most biomes remain uncultured. ISME J. 13, 3126–3130 (2019).
    Article  Google Scholar 

    3.
    Roux, S. et al. Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature. 537, 689–693 (2016).
    CAS  Article  Google Scholar 

    4.
    Okazaki, Y., Nishimura, Y., Yoshida, T., Ogata, H. & Nakano, S.-i Genome-resolved viral and cellular metagenomes revealed potential key virus-host interactions in a deep freshwater lake. Environ. Microbiol. 21, 4740–4754 (2019).
    CAS  Article  Google Scholar 

    5.
    Williamson, K. E., Fuhrmann, J. J., Wommack, K. E. & Radosevich, M. Viruses in soil ecosystems: an unknown quantity within an unexplored territory. Annu.Rev. Virol. 4, 201–219 (2017).
    CAS  Article  Google Scholar 

    6.
    Yutin, N. et al. Discovery of an expansive bacteriophage family that includes the most abundant viruses from the human gut. Nat. Microbiol. 3, 38–46 (2018).
    CAS  Article  Google Scholar 

    7.
    Davison, M., Treangen, T. J., Koren, S., Pop, M. & Bhaya, D. Diversity in a polymicrobial community revealed by analysis of viromes, endolysins and CRISPR spacers. PLoS One. 11, e0160574 (2016).
    Article  Google Scholar 

    8.
    Paez-Espino, D. et al. Uncovering earth’s virome. Nature. 536, 425–430 (2016).
    ADS  CAS  Article  Google Scholar 

    9.
    Ghai, R., Mehrshad, M., Mizuno, C. M. & Rodriguez-Valera, F. Metagenomic recovery of phage genomes of uncultured freshwater actinobacteria. ISME J. 11, 304–308 (2017).
    CAS  Article  Google Scholar 

    10.
    Kavagutti, V. S., Andrei, A.-Ş., Mehrshad, M., Salcher, M. M. & Ghai, R. Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomics. Microbiome. 7, 135 (2019).
    Article  Google Scholar 

    11.
    Balcazar, J. L. Bacteriophages as vehicles for antibiotic resistance genes in the environment. PLoS Pathog. 10, e1004219 (2014).
    Article  Google Scholar 

    12.
    Moon, K. et al. Freshwater viral metagenome reveals novel and functional phage-borne antibiotic resistance genes. Microbiome. 8, 75 (2020).
    Article  Google Scholar 

    13.
    Weathers, K. C. et al. The global lake ecological observatory network (GLEON): the evolution of grassroots network science. Limnol. Oceanogr. Bull. 22, 71–73 (2013).
    Article  Google Scholar 

    14.
    Kim, B., Choi, K., Kim, C., Lee, U.-H. & Kim, Y.-H. Effects of the summer monsoon on the distribution and loading of organic carbon in a deep reservoir, Lake Soyang, Korea. Water Res. 34, 3495–3504 (2000).
    CAS  Article  Google Scholar 

    15.
    Moon, K., Kang, I., Kim, S., Kim, S.-J. & Cho, J.-C. Genomic and ecological study of two distinctive freshwater bacteriophages infecting a Comamonadaceae bacterium. Sci. Rep. 8, 7989 (2018).
    ADS  Article  Google Scholar 

    16.
    Moon, K., Kang, I., Kim, S., Cho, J.-C. & Kim, S.-J. Complete genome sequence of bacteriophage P26218 infecting Rhodoferax sp. strain IMCC26218. Stand. Genomic. Sci. 10, 111 (2015).
    Article  Google Scholar 

    17.
    Park, M., Song, J., Nam, G. G. & Cho, J.-C. Rhodoferax lacus sp. nov., isolated from a large freshwater lake. Int. J. Syst. Evol. Microbiol. 69, 3135–3140 (2019).
    Article  Google Scholar 

    18.
    Joung, Y. et al. Lacihabitans soyangensis gen. nov., sp. nov., a new member of the family Cytophagaceae, isolated from a freshwater reservoir. Int. J. Syst. Evol. Microbiol. 64, 3188–3194 (2014).
    CAS  Article  Google Scholar 

    19.
    Moon, K., Kang, I., Kim, S., Kim, S.-J. & Cho, J.-C. Genome characteristics and environmental distribution of the first phage that infects the LD28 clade, a freshwater methylotrophic bacterial group. Environ. Microbiol. 19, 4714–4727 (2017).
    CAS  Article  Google Scholar 

    20.
    Kim, S., Kang, I., Seo, J.-H. & Cho, J.-C. Culturing the ubiquitous freshwater actinobacterial acI lineage by supplying a biochemical ‘helper’ catalase. ISME J. 13, 2252–2263 (2019).
    CAS  Article  Google Scholar 

    21.
    Meyer, F. et al. The metagenomic RAST server – a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9, 386 (2008).
    CAS  Article  Google Scholar 

    22.
    Roux, S., Enault, F., Hurwitz, B. L. & Sullivan, M. B. VirSorter: mining viral signal from microbial genomic data. PeerJ. 3, e985 (2015).
    Article  Google Scholar 

    23.
    John, S. G. et al. A simple and efficient method for concentration of ocean viruses by chemical flocculation. Environ. Microbiol. Rep. 3, 195–202 (2011).
    CAS  Article  Google Scholar 

    24.
    Moon, K. Ecological and genomic study on freshwater bacteriophages. (Seoul National University, 2018).

    25.
    Hurwitz, B. L., Deng, L., Poulos, B. T. & Sullivan, M. B. Evaluation of methods to concentrate and purify ocean virus communities through comparative, replicated metagenomics. Environ. Microbiol. 15, 1428–1440 (2013).
    CAS  Article  Google Scholar 

    26.
    Thurber, R. V., Haynes, M., Breitbart, M., Wegley, L. & Rohwer, F. Laboratory procedures to generate viral metagenomes. Nat. Protoc. 4, 470–483 (2009).
    CAS  Article  Google Scholar 

    27.
    Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 30, 2114–2120 (2014).
    CAS  Article  Google Scholar 

    28.
    Zolfo, M. et al. Detecting contamination in viromes using ViromeQC. Nat. Biotechnol. 37, 1408–1412 (2019).
    CAS  Article  Google Scholar 

    29.
    Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477 (2012).
    MathSciNet  CAS  Article  Google Scholar 

    30.
    Moon, K., Kang, I. & Cho, J.-C. Viral metagenome of Lake Soyang. European Nucleotide Archieve https://identifiers.org/ncbi/bioproject:PRJEB15535 (2018).

    31.
    Moon, K., Kang, I. & Cho, J.-C. Viral metagenome of Lake Soyang. MG-RAST http://www.mg-rast.org/linkin.cgi?project=mgp13279 (2020).

    32.
    Moon, K., Kang, I. & Cho, J.-C. Freshwater viral communities from Lake Soyang, Gangwon-do, South Korea. Joint Genome Institute IMG/MER https://gold.jgi.doe.gov/study?id=Gs0118096 (2020).

    33.
    Chen, S., Zhou, Y., Chen, Y. & Gu, J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884–i890 (2018).
    Article  Google Scholar  More

  • in

    Life-history strategies of soil microbial communities in an arid ecosystem

    1.
    Fierer N. Embracing the unknown: disentangling the complexities of the soil microbiome. Nat Rev Microbiol. 2017;15:579–90.
    CAS  PubMed  Article  Google Scholar 
    2.
    Whitman WB, Coleman DC, Wiebe WJ. Prokaryotes: the unseen majority. Proc Natl Acad Sci USA. 1998;95:6578–83.
    CAS  PubMed  Article  Google Scholar 

    3.
    Bardgett RD, van der Putten WH. Belowground biodiversity and ecosystem functioning. Nature. 2014;515:505–11.
    CAS  PubMed  Article  Google Scholar 

    4.
    Green JL, Bohannan BJM, Whitaker RJ. Microbial biogeography: from taxonomy to traits. Science. 2008;320:1039–43.
    CAS  PubMed  Article  Google Scholar 

    5.
    Martiny JBH, Jones SE, Lennon JT, Martiny AC. Microbiomes in light of traits: a phylogenetic perspective. Science. 2015;350:aac9323.
    PubMed  Article  CAS  Google Scholar 

    6.
    Koch AL. Oligotrophs versus copiotrophs. BioEssays. 2001;23:657–61.
    CAS  PubMed  Article  Google Scholar 

    7.
    Fierer N, Bradford MA, Jackson RB. Toward an ecological classification of soil bacteria. Ecology. 2007;88:1354–64.
    PubMed  Article  Google Scholar 

    8.
    Ho A, Di Lonardo DP, Bodelier PLE. Revisiting life strategy concepts in environmental microbial ecology. FEMS Microbiol Ecol. 2017;93:fix006.
    Article  CAS  Google Scholar 

    9.
    Klappenbach JA, Dunbar JM, Schmidt TM. rRNA operon copy number reflects ecological strategies of bacteria. Appl Environ Microbiol. 2000;66:1328–33.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    10.
    Roller BRK, Stoddard SF, Schmidt TM. Exploiting rRNA operon copy number to investigate bacterial reproductive strategies. Nat Microbiol. 2016;1:1–7.
    Article  CAS  Google Scholar 

    11.
    Botzman M, Margalit H. Variation in global codon usage bias among prokaryotic organisms is associated with their lifestyles. Genome Biol. 2011;12:R109.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    12.
    Vieira-Silva S, Rocha EPC. The systemic imprint of growth and its uses in ecological (meta)genomics. PLoS Genet. 2010;6:e1000808.
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    13.
    Pereira-Flores E, Glöckner FO, Fernandez-Guerra A. Fast and accurate average genome size and 16S rRNA gene average copy number computation in metagenomic data. BMC Bioinforma. 2019;20:453.
    Article  CAS  Google Scholar 

    14.
    Lauro FM, McDougald D, Thomas T, Williams TJ, Egan S, Rice S, et al. The genomic basis of trophic strategy in marine bacteria. Proc Natl Acad Sci USA. 2009;106:15527–33.
    CAS  PubMed  Article  Google Scholar 

    15.
    Wyman SK, Avila-Herrera A, Nayfach S, Pollard KS. A most wanted list of conserved microbial protein families with no known domains. PLoS ONE. 2018;13:e0205749.
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    16.
    Galand PE, Pereira O, Hochart C, Auguet JC, Debroas D. A strong link between marine microbial community composition and function challenges the idea of functional redundancy. ISME J. 2018;12:2470–8.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    17.
    Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M. KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res. 2016;44:D457–62.
    CAS  PubMed  Article  Google Scholar 

    18.
    Steen AD, Crits-Christoph A, Carini P, DeAngelis KM, Fierer N, Lloyd KG, et al. High proportions of bacteria and archaea across most biomes remain uncultured. ISME J. 2019;13:3126–30.
    PubMed  PubMed Central  Article  Google Scholar 

    19.
    Delgado-Baquerizo M, Oliverio AM, Brewer TE, Benavent-González A, Eldridge DJ, Bardgett RD, et al. A global atlas of the dominant bacteria found in soil. Science. 2018;359:320–5.
    CAS  PubMed  Article  Google Scholar 

    20.
    Jaroszewski L, Li Z, Krishna SS, Bakolitsa C, Wooley J, Deacon AM, et al. Exploration of uncharted regions of the protein universe. PLoS Biol. 2009;7:e1000205.
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    21.
    Giovannoni S, Stingl U. The importance of culturing bacterioplankton in the ‘omics’ age. Nat Rev Microbiol. 2007;5:820–6.
    CAS  PubMed  Article  Google Scholar 

    22.
    Barberán A, Caceres Velazquez H, Jones S, Fierer N. Hiding in plain sight: Mining bacterial species records for phenotypic trait information. mSphere. 2017;2:e00237–17.
    PubMed  PubMed Central  Article  Google Scholar 

    23.
    Aguiar MR, Sala OE. Patch structure, dynamics and implications for the functioning of arid ecosystems. Trends Ecol Evol. 1999;14:273–7.
    CAS  PubMed  Article  Google Scholar 

    24.
    Schlesinger WH, Raikes JA, Hartley AE, Cross AF. On the spatial pattern of soil nutrients in desert ecosystems. Ecology. 1996;77:364–74.
    Article  Google Scholar 

    25.
    Maestre FT, Bautista S, Cortina J, Bellot J. Potential for using facilitation by grasses to establish shrubs on a semiarid degraded steppe. Ecol Appl. 2001;11:1641–55.
    Article  Google Scholar 

    26.
    Butterfield BJ, Betancourt JL, Turner RM, Briggs JM. Facilitation drives 65 years of vegetation change in the Sonoran Desert. Ecology. 2010;91:1132–9.
    PubMed  Article  Google Scholar 

    27.
    Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    28.
    Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 2011;17:10–2.
    Article  Google Scholar 

    29.
    Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    30.
    Li D, Liu CM, Luo R, Sadakane K, Lam TW. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics. 2015;31:1674–6.
    CAS  PubMed  Article  Google Scholar 

    31.
    Hyatt D, Chen GL, LoCascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinforma. 2010;11:119.
    Article  CAS  Google Scholar 

    32.
    Steinegger M, Söding J. MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets. Nat Biotechnol. 2017;35:1026–8.
    CAS  PubMed  Article  Google Scholar 

    33.
    Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009;25:1754–60.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    34.
    Kanehisa M, Sato Y, Morishima K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol. 2016;428:726–31.
    CAS  PubMed  Article  Google Scholar 

    35.
    Huerta-Cepas J, Forslund K, Coelho LP, Szklarczyk D, Jensen LJ, von Mering C, et al. Fast genome-wide functional annotation through orthology assignment by eggNOG-mapper. Mol Biol Evol. 2017;34:2115–22.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    36.
    Huerta-Cepas J, Szklarczyk D, Heller D, Hernández-Plaza A, Forslund SK, Cook H, et al. eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res. 2019;47:D309–14.
    CAS  PubMed  Article  Google Scholar 

    37.
    Novembre JA. Accounting for background nucleotide composition when measuring codon usage bias. Mol Biol Evol. 2002;19:1390–4.
    CAS  PubMed  Article  Google Scholar 

    38.
    Vieira-Silva S, Falony G, Darzi Y, Lima-Mendez G, Yunta RG, Okuda S, et al. Species–function relationships shape ecological properties of the human gut microbiome. Nat Microbiol. 2016;1:1–8.
    Article  CAS  Google Scholar 

    39.
    Barberán A, Fenández-Guerra A, Bohannan BJ, Casamayor EO. Exploration of community traits as ecological markers in microbial metagenomes. Mol Ecol. 2012;21:1909–17.
    PubMed  Article  CAS  Google Scholar 

    40.
    R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2018. https://www.R-project.org/.

    41.
    Nakagawa S, Schielzeth H. A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol. 2013;4:133–42.
    Article  Google Scholar 

    42.
    Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550.
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    43.
    Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B. 1995;57:289–300.
    Google Scholar 

    44.
    Goberna M, Navarro‐Cano JA, Valiente‐Banuet A, García C, Verdú M. Abiotic stress tolerance and competition‐related traits underlie phylogenetic clustering in soil bacterial communities. Ecol Lett. 2014;17:1191–201.
    PubMed  Article  Google Scholar 

    45.
    Rodríguez-Echeverría S, Lozano YM, Bardgett RD. Influence of soil microbiota in nurse plant systems. Funct Ecol. 2016;30:30–40.
    Article  Google Scholar 

    46.
    Yahdjian L, Gherardi L, Sala OE. Nitrogen limitation in arid-subhumid ecosystems: a meta-analysis of fertilization studies. J Arid Environ. 2011;75:675–80.
    Article  Google Scholar 

    47.
    Giovannoni SJ, Thrash JC, Temperton B. Implications of streamlining theory for microbial ecology. ISME J. 2014;8:1553–65.
    PubMed  PubMed Central  Article  Google Scholar 

    48.
    Leff JW, Jones SE, Prober SM, Barberán A, Borer ET, Firn JL, et al. Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proc Natl Acad Sci USA. 2015;112:10967–72.
    CAS  PubMed  Article  Google Scholar 

    49.
    Musto H, Naya H, Zavala A, Romero H, Alvarez-Valı́n F, Bernardi G. Correlations between genomic GC levels and optimal growth temperatures in prokaryotes. FEBS Lett. 2004;573:73–7.
    CAS  PubMed  Article  Google Scholar 

    50.
    Yakovchuk P, Protozanova E, Frank-Kamenetskii MD. Base-stacking and base-pairing contributions into thermal stability of the DNA double helix. Nucleic Acids Res. 2006;34:564–74.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    51.
    Neilson JW, Quade J, Ortiz M, Nelson WM, Legatzki A, Tian F, et al. Life at the hyperarid margin: novel bacterial diversity in arid soils of the Atacama Desert, Chile. Extremophiles. 2012;16:553–66.
    PubMed  Article  Google Scholar 

    52.
    Lajoie G, Kembel SW. Making the most of trait-based approaches for microbial ecology. Trends Microbiol. 2019;27:814–23.
    CAS  PubMed  Article  Google Scholar 

    53.
    Reich PB. The world-wide ‘fast-slow’ plant economics spectrum: a traits manifesto. J Ecol. 2014;102:275–301.
    Article  Google Scholar 

    54.
    Nemergut DR, Knelman JE, Ferrenberg S, Bilinski T, Melbourne B, Jiang L, et al. Decreases in average bacterial community rRNA operon copy number during succession. ISME J. 2016;10:1147–56.
    CAS  PubMed  Article  Google Scholar 

    55.
    Ortiz-Álvarez R, Fierer N, de Los Ríos A, Casamayor EO, Barberán A. Consistent changes in the taxonomic structure and functional attributes of bacterial communities during primary succession. ISME J. 2018;12:1658–67.
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    56.
    Song H-K, Song W, Kim M, Tripathi BM, Kim H, Jablonski P, et al. Bacterial strategies along nutrient and time gradients, revealed by metagenomic analysis of laboratory microcosms. FEMS Microbiol Ecol. 2017;93:fix114.
    Article  CAS  Google Scholar 

    57.
    Ferenci T. Trade-off mechanisms shaping the diversity of bacteria. Trends Microbiol. 2016;24:209–23.
    CAS  PubMed  Article  Google Scholar 

    58.
    Gray DA, Dugar G, Gamba P, Strahl H, Jonker MJ, Hamoen LW. Extreme slow growth as alternative strategy to survive deep starvation in bacteria. Nat Commun. 2019;10:890.
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    59.
    Trivedi P, Anderson IC, Singh BK. Microbial modulators of soil carbon storage: integrating genomic and metabolic knowledge for global prediction. Trends Microbiol. 2013;21:641–51.
    CAS  PubMed  Article  Google Scholar 

    60.
    Müller DB, Vogel C, Bai Y, Vorholt JA. The plant microbiota: systems-level insights and perspectives. Annu Rev Genet. 2016;50:211–34.
    PubMed  Article  CAS  Google Scholar 

    61.
    Brewer TE, Aronson EL, Arogyaswamy K, Billings SA, Botthoff JK, Campbell AN, et al. Ecological and genomic attributes of novel bacterial taxa that thrive in subsurface soil horizons. MBio. 2019;10:e01318–19.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    62.
    Price MN, Wetmore KM, Waters RJ, Callaghan M, Ray J, Liu H, et al. Mutant phenotypes for thousands of bacterial genes of unknown function. Nature. 2018;557:503–9.
    CAS  PubMed  Article  Google Scholar 

    63.
    Stewart EJ. Growing unculturable bacteria. J Bacteriol. 2012;194:4151–60.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    64.
    Pascual-García A, Bell T. Community-level signatures of ecological succession in natural bacterial communities. Nat Commun. 2020;11:1–1.
    Article  CAS  Google Scholar  More

  • in

    Study on the spatial-temporal variation in evapotranspiration in China from 1948 to 2018

    Trend analysis of the ET from 1948 to 2018
    To reveal the ET trend in the 71 years from 1948 to 2018 in the study area, we extracted the ET in the study area throughout this period from the GLDAS data, calculated the Z value of each pixel throughout this period with the TFPW-MK test method, and generated an ET change trend distribution map with the Z value of each pixel.
    First, we adopt the annual ET of each pixel as the statistical value to establish the 71-year time series. The trend of each pixel from 1948 to 2018 is analysed to examine the general trend of the ET in China and its spatial distribution characteristics. Then, we select the ET of each pixel in each month from January to December as the statistical value, establish 12-month time series over the 71-year study period, and analyse the trend in each month over the 71 years from January to December to examine the influence of the month on the ET change trend in China.
    Trend analysis of the ET over the years
    First, we analyse the annual ET trend of each pixel throughout this period, and Fig. 1 shows the distribution of the Z value reflecting this trend.
    According to the obtained statistics, there are approximately 15258 pixels in the study area, of which 13662 pixels exhibit Z values larger than 0, accounting for approximately 89.5% of all pixels. The other pixels with Z values smaller than 0 account for approximately 10.5% of all pixels. This shows that the overall trend in most regions of China since 1948 is an increasing trend, and only a small part exhibits a decreasing trend. Figure 1 shows that the regions where ET has significantly decreased are distributed across parts of Western China and the two islands in southern China, while the ET in most other regions exhibits a relatively significant growth trend.
    Figure 1 shows that the ET change trend in Western China is quite different. The change trends in most areas are consistent with the overall ET change trend in China, showing a significant upward trend. The ET in a small part of the area (the red area in the figure), namely, the western Qiangtang Plateau and its surrounding areas, exhibits a significant downward trend. The Qiangtang Plateau is the main body of the Qinghai-Tibet Plateau in southwestern China. Most of the plateau is above 4600 metres above sea level. It is a typical area with very harsh climate conditions and an extremely fragile ecological environment in China. The environmental characteristics are mainly exemplified by a dry and cold climate, windy conditions, and abundant surface sand areas, sparse vegetation and a low ecological capacity49. Since the 1950s, the western Qiangtang Plateau has increasingly become arid with global changes50, and the precipitation in the southern surrounding area has decreased significantly51.These factors together led to the most obvious ET decreasing trend on the western Qiangtang Plateau and its surrounding areas in Southwest China. The reason for the significant increase in ET in Western China is basically the same as the reason for the increase in ET in the other parts of China, namely, climate change and human activities. Climate change is mainly due to the increase in precipitation17 and the increase in warming and aridification in most parts of China, which has greatly increased the temperature and relative humidity52. However, the increase in human activities is primarily caused by the fact that since 2000, the state has heavily invested in ecological restoration and has successively implemented a number of major ecological environmental protection and construction projects, such as returning farmland to forestland and grassland, returning grazing land to grassland, natural forest protection, and forest system protection projects. With the implementation of the above ecological projects, the vegetation conditions in certain areas have been improved53, and the areas where the ET has notably increased are mainly located in areas with a high vegetation cover54.
    Figure 1

    Spatial-temporal trend of the ET in China from 1948 to 2018.

    Full size image

    When the absolute Z value is greater than or equal to 2.32, the confidence level is 99%, and when it is greater than 1.64 but less than 2.32, the confidence level is 95%. When the absolute Z value is greater than 1.28 but less than 1.64, the confidence level is 90%. Table 1 lists the proportion of the number of pixels in each distribution interval of the Z value. The Z value in 63% of all pixels is greater than 2.32, and the areas covered by these pixels have a 99% chance of exhibiting an increasing trend. Analogously, the areas with Z values greater than 1.28, accounting for 89.7% of all pixels, have a 90% chance of exhibiting an increasing trend. All of these statistics indicate that in China, the ET in most regions exhibits a very obvious increasing trend.
    Table 1 Confidence level of the Z value and pixel proportion.
    Full size table

    Variation trend of ET with the different months
    From January to December, solar radiation changes with the time, temperature, precipitation and other meteorological elements, and ET also changes over time55. To reveal the ET trend with the month, we calculated the ET trend of each pixel throughout the 71-year period from January to December. Figure 2 shows a distribution map of the Z value reflecting this trend.
    Figure 2 reveals that the ET trend in China varies greatly with the change in months, and many regions show the most or least obvious increasing trend (or decreasing trend) at different times. The details are as follows:
    (1)
    In Northeast China, especially the Middle-Lower Yangtze Plain and the eastern Tibetan Plateau, the ET increasing trend is the most obvious in April and the least obvious in January and December.

    (2)
    On the North China Plain, the ET increasing trend is the most obvious in March, and the ET decreasing trend is the most obvious in November and December.

    (3)
    On the Yunnan-Guizhou Plateau and Chiang-nan Hilly Region, ET increased the most from June to August and decreased the most in January.

    (4)
    The increasing trend on the Inner Mongolia Plateau is the most obvious in February and March and the least obvious in August.

    (5)
    Compared to the other months, the increasing trend on the western Tibetan Plateau from May to September is more obvious. However, the annual ET increasing trend is not obvious, but the decreasing trend is very obvious.

    (6)
    The decreasing trend in January and December in Northwest China is obvious, and the increasing trend in the other months is obvious.

    (7)
    The annual ET trend in the Tarim Basin and its surrounding areas is an obvious increasing trend. However, the ET trends in the east and west of the Tarim Basin are obviously different. In August and September, the west of the Tarim Basin reaches the maximum value of the ET trend, while the east of the Tarim Basin exhibits the most obvious decreasing trend.

    In general, the ET trend in Northeast China varies greatly from month to month. The ET in most areas of Northeast China mainly increases from March to October, while the ET mainly decreases from December to February. This is related to the concentrated distribution of the forest areas in the Greater Khingan Mountains and Changbai Mountains in Northeast China. The ET in forest ecosystems is the highest. From March to October every year, plants are subject to the growing season, the vegetation is lush, transpiration and evaporation occur vigorously, and ET is on the rise. From December to February of the following year, plants are in the declining or non-growing season. Moreover, due to the low temperature, energy and stomatal conductance levels, the ET values reveal a downward trend54.
    The variation trend of the ET in southern China, northwestern China, and northern China is also relatively obvious. The ET from June to August mainly reveals an upward trend, and the ET mainly shows a downward trend from September to May of the following year. This is mainly related to the temperature and precipitation. Between June and August, the temperature and precipitation increase, and the ET is also very notable; from September to May of the following year, the temperature drops, and the precipitation and ET also decrease56.
    However, the ET in most parts of Southwest China exhibits a downward trend in almost all months, but it is also observed that the area with a decreasing trend in winter is relatively large, while that in summer is relatively small. The main reason why the ET in each month decreases is that this region is located on the Qiangtang Plateau, an alpine and cold region with an altitude higher than 4600 metres, which has a unique natural environment and climatic conditions51. Drought and precipitation reduction are the leading factors of the ET decrease50,51, , and the ET throughout the whole year mostly presents a downward trend. Moreover, the monthly changes in the climate of the Qiangtang Plateau are very obvious, with distinct cold and wet seasons. Generally, the period from May to September is the warm, rainy and less windy season, but the period from October to April of the following year is the cold, dry, and windy season50, and the area with an ET decreasing trend from May to September shrinks, while the area with an ET decreasing trend from October to April expands.
    Figure 2

    Spatial-temporal trend of the monthly ET in China from 1948 to 2018.

    Full size image

    According to the monthly change trend, we calculated the proportion of the number of pixels with an increasing trend, i.e., those pixels with Z values greater than 0. Figure 3 shows the calculation results. The figure shows the ET trend in China with the change in months.
    Figure 3 shows that in January, only 57.95% of the study area exhibited an increasing trend, which quickly increased to over 76.0% in February, reaching a maximum value in May, after which it began to decrease. However, the area increased in September, rising to 81.81%, and then continued to decrease, until it reached a minimum value in December, similar to January. On the whole, the proportion of (Z >0) from January to December was ( >50%), and all months of the year were dominated by a growth trend, and from January to May, the pixels with (Z >0) increased, with a total increase of 29.65%. The growth rate was the highest from January to February, with a total increase of 18.05%, accounting for 60.88% of the increase, indicating that the area where the ET was on the rise from January to February exhibited the fastest growth, and the number of pixels with (Z >0) reached a maximum value of 87.60% in May, after which it decreased. There was a small fluctuation in the middle of September, but an overall decrease was still observed, and the rate of decrease increased, with a total decrease of 30%, reaching a minimum value of 57.60% in December, which was still higher than 50%. From Fig. 3,we can deduce that the number of pixels with an increasing trend in the study area was the largest in May and the smallest in December and January. In particular, the region in the study area with an increasing trend was the largest in May and the smallest in December. In all months of the year, more than half of the pixels exhibited an increasing trend, which also indicates that in regard to the study area, the annual ET trend was still dominated by an increasing trend, which is consistent with the finding from Fig. 1.
    Figure 3

    Proportion of pixels with an increasing trend over the 12 months.

    Full size image

    Figure 2 does not directly show the monthly fluctuation in the ET trend of each pixel from January to December. Standard deviation analysis of the 12 subgraphs of Fig. 2 is conducted, and Fig. 4 is obtained. The standard deviation can be adopted to analyse the dispersion of the Z value of each pixel from January to December, and based on Fig. 4 we can determine the monthly fluctuation in the ET trend.
    Figure 4

    Standard deviation distribution of the monthly ET trend in China.

    Full size image

    Figure 4 shows that in the dark blue parts, i.e., in Northeast China, West China, Northwest China and South China , a large variation occurs, especially in the border area of Northeast China and a small number of pixels in Northwest China, where the standard deviation exceeds 4.5, indicating that the ET trend in these regions is greatly affected by the months. In regard to the light blue parts of the map, such as the northwest Tarim Basin, Tianshan Mountains and its surrounding areas, east Tibet Plateau and middle Inner Mongolia Plateau, the impact of the month is relatively small.
    Coefficient of variation analysis
    Through statistical analysis of the ET CV in time and space, the dispersion of ET in time and space can be analysed, and the stability of the ET fluctuation in time and space can then be determined.
    Spatial distribution of the time series CV of ET
    The time series CV of ET from 1948 to 2018 is calculated for each pixel, and Fig. 5 is obtained.
    Figure 5

    Spatial distribution of the time series CV of ET.

    Full size image

    Figure 5 shows that the ET CV of each pixel in China from 1948 to 2018 shows a trend of gradually decreasing from northwest to southeast. The ET in northern China is more discrete than that in the south, and the ET in the west is more discrete than that in the east. The higher the dispersion degree is, the more unstable the ET in these regions is over the 71-year period. The lower the dispersion degree is, the more stable the change in ET is.
    In summary, from 1948 to 2018, the variation in ET in northern China was more severe than that in southern China, and the variation in ET in Western China was more severe than that in eastern China. The ET in the surrounding areas of the Tarim Basin in northwestern China revealed the most dramatic changes, and the ET changes in most parts of East China remained the most stable.
    Time fluctuation in the spatial distribution CV of ET
    From 1948 to 2018, the CV of the yearly ET spatial distribution in the study area was calculated to analyse the fluctuation in the ET spatial variation over time. Figure 6 shows a linear graph based on the 71 CV yearly values, from which we can observe the changes in the spatial variation from 1948 to 2018. Moreover, we also calculated the SD and mean from 1948 to 2018. To facilitate a comparison of the change trends of the SD and mean with the change trend of the CV, we mapped the SD and mean to the range of the CV, [0.55, 0.67], and accordingly plotted a line graph of the SD and mean.
    Figure 6

    Time fluctuation in the spatial distribution CV of ET.

    Full size image

    In Fig. 6, the yellow solid line is the change curve of the SD over time, and the blue solid line is the variation line of the CV over time. The blue solid line reveals that the change in the spatial distribution CV over time from 1948 to 2018 can be roughly divided into two stages: 1948–2001 and 2002–2018. The red dotted line is the mean value of the CV in each year in the two stages. The following is a description of these two stages:
    The first stage: 1948–2001. During this period, the CV value of ET fluctuated within a high range, ranging from 0.61 to 0.67, and the average value was approximately 0.63, but the fluctuation range in most years was approximately 0.62 to 0.65, and the change was relatively small. Among them, the CV of ET in 1959 and 2000 was relatively small, indicating that the ET in the study area in these two years remained relatively uniform, while the CV in the other years (such as 1951, 1965, and 1986) were relatively large, indicating that the ET in the study area varied greatly in these years. However, on the whole, the CV in each year in this stage was larger than that in the second stage, indicating that the spatial difference in ET in the study area in this stage was large, and the overall ET was uneven.
    The second stage: 2002–2018. Figure 6 shows that the CV began to decrease in 2002, and it decreased to a minimum value of 0.55 in 2003. Thereafter, up to 2018, the value of the CV fluctuated within a low range, ranging from 0.55 to 0.62, with an average value of 0.58, which is a decrease of 0.05 over the first stage value. Although it reached a maximum value of 0.62 in the second stage in 2018, the value was smaller than the average value in the first stage , indicating that the CV in this stage was generally smaller than that in the first stage. Notably, the difference in ET between the various regions in the study area decreased in 2002, and the ET in China became more even. According to the change curve of the average ET, the average ET in China began to increase in 2002. Although fluctuations occurred, the average ET also fluctuated within a relatively high range. This is consistent with the research results of Bing Longfei7, namely, after 2000, the annual ET greatly exceeded the previous ET level. Combined with the decrease in the CV value, this shows that after 2002, the ET in the various regions of China started to increase. The main reason for this result is that the state invested heavily in ecological restoration in 2000 and successively implemented a number of major ecological environmental protection and construction projects, such as returning farmland to forestland and grassland, returning grazing land to grassland, natural forest protection and shelterbelt system projects53. After 2002, good results were achieved, and vegetation conditions were improved, while the regions with a notably increased ET primarily occurred in those regions with an improved vegetation cover54. Therefore, after 2002, the ET in all regions in China began to increase, and the CV began to decrease.
    By comparing the SD line chart and the CV line chart, it is observed that the trend of these two lines in the first stage and the second stage is basically the same, but after the first stage, the CV exhibits a decrease, the SD does not change, and there is an increasing trend after 2002. However, the SD is an absolute indicator. When the sample mean level is different, an absolute difference index cannot be considered in a comparative analysis57, while the CV measures the degree of variation between samples with different units or with a large difference in the mean. Here, the annual average ET value constantly changes, and it is more accurate to adopt the CV to compare the dispersion degree between the different regions within the study area.
    In other words, the annual ET spatial difference within the study area was relatively large from 1948 to 2001, and the annual ET in the study area was very uneven. After 2002, the annual spatial difference decreased, and in 2003, the spatial distribution of the ET in the study area was the most uniform.
    Future trend analysis of ET
    The variation in ET in the study area from 1948 to 2018 has been previously analysed. This section assesses the future ET variation in China, i.e., whether the future ET variation in the study area will follow the trend from 1948 to 2018. This is evaluated with the Hurst index. The value range of the Hurst index is between 0 and 1. If the Hurst index is larger than 0.5, this indicates that the future trend will follow the original trend. The closer the Hurst index is to 1, the stronger the continuity is. If the Hurst index is smaller than 0.5, this indicates that the future trend will contradict the original trend. If the Hurst index is equal to 0.5, this indicates that the future trend is uncertain and not related to the original trend. Figure 7 shows a map of the distribution based on the calculated Hurst index of each pixel.
    Figure 7

    Spatial distribution of the Hurst index from 1948 to 2018.

    Full size image

    According to the calculated Hurst index of each pixel, only 26 pixels in Fig. 7 have a Hurst index smaller than 0.5, no pixels exhibit a Hurst index equal to 0.5, and most of the pixels in the study area reveal a Hurst index larger than 0.5. This implies that in the future, the vast majority of the study area will continue the trend from 1948 to 2018, as shown in Fig. 1. In terms of the possibility of this continuity, the number of pixels with a Hurst index larger than 0.9 accounts for approximately 23.2% of all pixels, and the number of pixels with a Hurst index between 0.8 and 0.9 accounts for approximately 36.8% of all pixels, while the number of pixels with a Hurst larger than 0.8 accounts for approximately 60% of all pixels. These results indicate that it is very possible for these pixels to continue the current trend in the future. Especially in Northeast China, South-Central China and West China, the Hurst index values are all close to 1, and the ET trend in these regions exhibits a notable continuity. For example, according to Fig. 1, it is found that the ET in Northeast China has a strong increasing trend from 1948 to 2018. Combined with the Hurst index analysis results in Northeast China, as shown in Fig. 7, it is concluded that in the future, the ET in Northeast China will increase more than that in the other regions. More

  • in

    Scale-dependent effects of habitat fragmentation on the genetic diversity of Actinidia chinensis populations in China

    1.
    Wu, J. Key concepts and research topics in landscape ecology revisited: 30 years after the Allerton Park workshop. Landsc. Ecol. 28, 1–11 (2013).
    CAS  Article  Google Scholar 
    2.
    Wilson, M. C. et al. Habitat fragmentation and biodiversity conservation: key findings and future challenges. Landsc. Ecol. 31, 219–227 (2016).
    Article  Google Scholar 

    3.
    Leimu, R., Vergeer, P., Angeloni, F. & Ouborg, N. J. Habitat fragmentation, climate change, and inbreeding in plants. Ann. NY Acad. Sci. 1195, 84–98 (2010).
    PubMed  Article  Google Scholar 

    4.
    Young, A., Boyle, T. & Brown, T. The population genetic consequences of habitat fragmentation for plants. Trends Ecol. Evolution 11, 413–418 (1996).
    CAS  Article  Google Scholar 

    5.
    Yuan, N., Comes, H. P., Mao, Y., Qi, X. & Qiu, Y. Genetic effects of recent habitat fragmentation in the Thousand-Island Lake region of southeast China on the distylous herb Hedyotis chrysotricha (Rubiaceae). Am. J. Bot. 99, 1715–1725 (2012).
    PubMed  Article  Google Scholar 

    6.
    MacArthur, R. H. & Wilson, E. O. An equilibrium theory of insular zoogeography. Evolution 17, 373–387 (1963).
    Article  Google Scholar 

    7.
    MacArthur, R. H. & Wilson, E. O. The Theory of Island Biogeography (Princeton University Press, Princeton, NJ, 1967).

    8.
    Guo, Q. Island biogeography theory: emerging patterns and human effects. Earth Syst. Environ. Sci. 32, 1–5 (2015).
    Google Scholar 

    9.
    Wroblewska, A. High genetic diversity within island-like peripheral populations of Pedicularis sceptrum-carolinum, a species with a northern geographic distribution. Ann. Bot. Fenn. 50, 289–299 (2013).
    Article  Google Scholar 

    10.
    Csergo, A.-M. et al. Genetic structure of peripheral, island-like populations: a case study of Saponaria bellidifolia Sm. (Caryophyllaceae) from the Southeastern Carpathians. Plant Syst. Evol. 278, 33–41 (2009).
    Article  Google Scholar 

    11.
    Doyle, J. M., Hacking, C. C., Willoughby, J. R., Sundaram, M. & DeWoody, J. A. Mammalian genetic diversity as a function of habitat, body size, trophic class, and conservation status. J. Mammal. 96, 564–572 (2015).
    Article  Google Scholar 

    12.
    Reynolds, R. G. et al. Archipelagic genetics in a widespread Caribbean anole. J. Biogeogr. 44, 2631–2647 (2017).
    Article  Google Scholar 

    13.
    Costanzi, J.-M. & Steifetten, Ø. Island biogeography theory explains the genetic diversity of a fragmented rock ptarmigan (Lagopus muta) population. Ecol. Evol. 9, 3837–3849 (2019).
    PubMed  PubMed Central  Article  Google Scholar 

    14.
    Hermansen, T., Minchinton, T. & Ayre, D. Habitat fragmentation leads to reduced pollinator visitation, fruit production and recruitment in urban mangrove forests. Oecologia 185, 221–231 (2017).
    PubMed  Article  Google Scholar 

    15.
    Broeck, A. et al. Dispersal constraints for the conservation of the grassland herb Thymus pulegioides L. in a highly fragmented agricultural landscape. Conserv Genet. 16, 765–776 (2015).
    Article  Google Scholar 

    16.
    Browne, L. & Karubian, J. Habitat loss and fragmentation reduce effective gene flow by disrupting seed dispersal in a neotropical palm. Mol. Ecol. 27, 3055–3069 (2018).
    PubMed  Article  Google Scholar 

    17.
    Bijlsma, R. & Loeschcke, V. Genetic erosion impedes adaptive responses to stressful environments. Evol. Appl. 5, 117–129 (2012).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    18.
    Lienert, J. Habitat fragmentation effects on fitness of plant populations-a review. J. Nat. Conserv. 12, 53–72 (2004).
    Article  Google Scholar 

    19.
    Luquet, E. et al. Genetic erosion in wild populations makes resistance to a pathogen more costly. Evolution 66, 1942–1952 (2012).
    PubMed  Article  Google Scholar 

    20.
    Toczydlowski, R. H. & Waller, D. M. Drift happens: molecular genetic diversity and differentiation among populations of jewelweed (Impatiens capensis Meerb.) reflect fragmentation of floodplain forests. Mol. Ecol. 28, 2459–2475 (2019).
    PubMed  Article  PubMed Central  Google Scholar 

    21.
    Jimenez, J. F., Sanchez-Gomez, P., Canovas, J. L., Hensen, I. & Aouissat, M. Influence of natural habitat fragmentation on the genetic structure of Canarian populations of Juniperus turbinata. Silva Fenn. 51, 1–14 (2017).
    Article  Google Scholar 

    22.
    Garciaverdugo, C. et al. Do island plant populations really have lower genetic variation than mainland populations? Effects of selection and distribution range on genetic diversity estimates. Mol. Ecol. 24, 726–741 (2015).
    CAS  Article  Google Scholar 

    23.
    Vandepitte, K., Jacquemyn, H., Roldan-Ruiz, I. & Honnay, O. Landscape genetics of the self-compatible forest herb Geum urbanum: effects of habitat age, fragmentation and local environment. Mol. Ecol. 16, 4171–4179 (2007).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    24.
    Krauss, J. et al. Habitat fragmentation causes immediate and time-delayed biodiversity loss at different trophic levels. Ecol. Lett. 13, 597–605 (2010).
    PubMed  PubMed Central  Article  Google Scholar 

    25.
    Heinken, T. & Weber, E. Consequences of habitat fragmentation for plant species: do we know enough? Perspect. Plant Ecol. Syst. 15, 205–216 (2013).
    Article  Google Scholar 

    26.
    Duminil, J. et al. Large-scale pattern of genetic differentiation within African rainforest trees: insights on the roles of ecological gradients and past climate changes on the evolution of Erythrophleum spp (Fabaceae). BMC Evol. Biol. 13, 195- (2013).
    PubMed  PubMed Central  Article  Google Scholar 

    27.
    Yuan, N. et al. A comparative study on genetic effects of artificial and natural habitat fragmentation on Loropetalum chinense (Hamamelidaceae) in Southeast China. Heredity 114, 544 (2014).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    28.
    Muyle, A. et al. Dioecy in plants: an evolutionary dead end? Insights from a population genomics study in the Silene genus. Preprint at https://www.biorxiv.org/content/10.1101/414771v1.full (2018).

    29.
    Fuller, M. R. & Doyle, M. W. Gene flow simulations demonstrate resistance of long-lived species to genetic erosion from habitat fragmentation. Conserv Genet. 19, 1439–1448 (2018).
    Article  Google Scholar 

    30.
    Hu, Y. et al. Genetic structuring and recent demographic history of red pandas (Ailurus fulgens) inferred from microsatellite and mitochondrial DNA. Mol. Ecol. 20, 2662–2675 (2011).
    PubMed  Article  Google Scholar 

    31.
    Moore, J. A., Miller, H. C., Daugherty, C. H. & Nelson, N. J. Fine-scale genetic structure of a long-lived reptile reflects recent habitat modification. Mol. Ecol. 17, 4630–4641 (2008).
    CAS  PubMed  Article  Google Scholar 

    32.
    Martínez-López, V., García, C., Zapata, V., Robledano, F. & De la Rúa, P. Intercontinental long-distance seed dispersal across the Mediterranean Basin explains population genetic structure of a bird-dispersed shrub. Mol. Ecol. 29, 1408–1420 (2020).
    PubMed  Article  Google Scholar 

    33.
    Grover, A. & Sharma, P. C. Development and use of molecular markers: past and present. Crit. Rev. Biotechnol. 36, 290–302 (2016).
    CAS  PubMed  Article  Google Scholar 

    34.
    Vieira, M. L. C., Santini, L., Diniz, A. L. & Munhoz, C. D. F. Microsatellite markers: what they mean and why they are so useful. Genet Mol. Biol. 39, 312–328 (2016).
    PubMed  PubMed Central  Article  Google Scholar 

    35.
    Selkoe, K. A. & Toonen, R. J. Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol. Lett. 9, 615–629 (2006).
    PubMed  Article  Google Scholar 

    36.
    Huang, H. et al. Genetic diversity in the genus Actinidia (in Chinese). Chin. Biodivers. 8, 1–12 (2000).
    CAS  Google Scholar 

    37.
    Logan, D. P. & Xu, X. Germination of kiwifruit, Actinidia chinensis, after passage through Silvereyes, Zosterops lateralis. New Zeal. J. Ecol. 30, 407–411 (2006).
    Google Scholar 

    38.
    Costa, G., Testolin, R. & Vizzotto, G. Kiwifruit pollination: an unbiased estimate of wind and bee contribution. N. Zeal J. Crop Hort. 21, 189–195 (1993).
    Article  Google Scholar 

    39.
    Huang, H. The Genus Actinidia, A World Monograph (Science Press, Beijing, 2014).

    40.
    Lv, K. et al. Habitat fragmentation influences gene structure and gene differentiation among the Loxoblemmus aomoriensis populations in the Thousand Island Lake. Mitochondrial DNA A 29, 222–227 (2017).
    Article  CAS  Google Scholar 

    41.
    Liu, Y. F. et al. Rapid radiations of both kiwifruit hybrid lineages and their parents shed light on a two-layer mode of species diversification. N. Phytol. 215, 877–890 (2017).
    CAS  Article  Google Scholar 

    42.
    Huang, W. G., Cipriani, G., Morgante, M. & Testolin, R. Microsatellite DNA in Actinidia chinensis: isolation, characterisation, and homology in related species. Theor. Appl. Genet. 97, 1269–1278 (1998).
    CAS  Article  Google Scholar 

    43.
    Van Oosterhout, C., Hutchinson, W. F., Wills, D. P. M. & Shipley, P. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4, 535–538 (2004).
    Article  CAS  Google Scholar 

    44.
    Excoffier, L. & Lischer, H. E. L. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10, 564–567 (2010).
    PubMed  Article  PubMed Central  Google Scholar 

    45.
    Peakall, R. & Smouse, P. E. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes 6, 288–295 (2006).
    Article  Google Scholar 

    46.
    Pallant, J. SPSS survival manual: a step by step guide to data analysis using SPSS. Aust. N.Z. J. Public Health 37, 597–598 (2013).
    Google Scholar 

    47.
    Excoffier, L., Smouse, P. E. & Quattro, J. M. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479–491 (1992).
    CAS  PubMed  PubMed Central  Google Scholar 

    48.
    Smouse, P. E., Long, J. C. & Sokal, R. R. Multiple regression and correlation extensions of the mantel test of matrix correspondence. Syst. Biol. 35, 627–632 (1986).
    Google Scholar 

    49.
    Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945 (2000).
    CAS  PubMed  PubMed Central  Google Scholar 

    50.
    Evanno, G., Regnaut, S. & Goudet, J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14, 2611–2620 (2005).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    51.
    Earl, D. & Vonholdt, B. M. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4, 359–361 (2012).
    Article  Google Scholar 

    52.
    Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725–2729 (2013).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    53.
    Pickrell, J. K. & Pritchard, J. K. Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genet. 8, e1002967 (2012).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    54.
    Cornuet, J. M. & Luikart, G. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144, 2001–2014 (1996).
    CAS  PubMed  PubMed Central  Google Scholar 

    55.
    Di Rienzo, A. et al. Mutational processes of simple-sequence repeat loci in human populations. Proc. Natl Acad. Sci. USA 91, 3166–3170 (1994).
    PubMed  Article  PubMed Central  Google Scholar 

    56.
    Wang, S. et al. Population size and time since island isolation determine genetic diversity loss in insular frog populations. Mol. Ecol. 23, 637–648 (2014).
    PubMed  Article  PubMed Central  Google Scholar 

    57.
    Luikart, G., Allendorf, F., Cornuet, J. & Sherwin, W. Distortion of allele frequency distributions provides a test for recent population bottlenecks. J. Hered. 89, 238–247 (1998).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    58.
    Cornuet, J.-M. et al. DIYABC v2.0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics 30, 1187–1189 (2014).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    59.
    Ewers, R. M. & Didham, R. K. The effect of fragment shape and species’ sensitivity to habitat edges on animal population size. Conserv Biol. 21, 926–936 (2007).
    PubMed  Article  Google Scholar 

    60.
    Ortego, J., Bonal, R. & Munoz, A. Genetic consequences of habitat fragmentation in long-lived tree species: the case of the Mediterranean holm oak (Quercus ilex, L.). J. Hered. 101, 717–726 (2010).
    CAS  PubMed  Article  Google Scholar 

    61.
    Fletcher, J. R. J. et al. Is habitat fragmentation good for biodiversity? Biol. Conserv 226, 9–15 (2018).
    Article  Google Scholar 

    62.
    Fattorini, S., Borges, P. A. V., Dapporto, L. & Strona, G. What can the parameters of the species-area relationship (SAR) tell us? Insights from Mediterranean islands. J. Biogeogr. 44, 1018–1028 (2017).
    Article  Google Scholar 

    63.
    Matthews, T. J. et al. Island species-area relationships and species accumulation curves are not equivalent: an analysis of habitat island datasets. Global Ecol. Biogeogr. 25, 607–618 (2016).
    Article  Google Scholar 

    64.
    Matthews, T., Cottee-Jones, H., Whittaker, R. & Brotons, L. Habitat fragmentation and the species-area relationship: a focus on total species richness obscures the impact of habitat loss on habitat specialists. Divers Distrib. 20, 1136–1146 (2014).
    Article  Google Scholar 

    65.
    McGlaughlin, M. E. et al. Do the island biogeography predictions of MacArthur and Wilson hold when examining genetic diversity on the near mainland California Channel Islands? Examples from endemic Acmispon (Fabaceae). Bot. J. Linn. Soc. 174, 289–304 (2014).
    Article  Google Scholar 

    66.
    Jangjoo, M., Matter, S. F., Roland, J. & Keyghobadi, N. Connectivity rescues genetic diversity after a demographic bottleneck in a butterfly population network. Proc. Natl Acad. Sci. USA 113, 10914–10919 (2016).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    67.
    Reisch, C. et al. Genetic diversity of calcareous grassland plant species depends on historical landscape configuration. BMC Ecol. 17, 1–13 (2017).
    Article  Google Scholar 

    68.
    Bottin, L. et al. Genetic diversity and population structure of an insular tree, Santalum austrocaledonicum in New Caledonian archipelago. Mol. Ecol. 14, 1979–1989 (2005).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    69.
    Breed, M. F. et al. Mating patterns and pollinator mobility are critical traits in forest fragmentation genetics. Heredity 115, 108–114 (2015).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    70.
    Llorens, T. M., Byrne, M., Yates, C. J., Nistelberger, H. M. & Coates, D. J. Evaluating the influence of different aspects of habitat fragmentation on mating patterns and pollen dispersal in the bird-pollinated Banksia sphaerocarpa var.caesia. Mol. Ecol. 21, 314–328 (2012).
    CAS  PubMed  Article  Google Scholar 

    71.
    Rosche, C. et al. Sex ratio rather than population size affects genetic diversity in Antennaria dioica. Plant Biol. 20, 789–796 (2018).
    CAS  PubMed  Article  Google Scholar 

    72.
    Liu, Y., Li, D., Yan, L. & Huang, H. The microgeographical patterns of morphological and molecular variation of a mixed ploidy population in the species complex Actinidia chinensis. PLoS ONE 10, e0117596 (2015).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    73.
    Guijun, Y., Ferguson, A. R. & McNeilage, M. A. Ploidy races in Actinidia chinensis. Euphytica 78, 175–183 (1994).
    Article  Google Scholar 

    74.
    Chat, J., Jáuregui, B., Petit, R. J. & Nadot, S. Reticulate evolution in kiwifruit (Actinidia, Actinidiaceae) identified by comparing their maternal and paternal phylogenies. Am. J. Bot. 91, 736–747 (2004).
    CAS  PubMed  Article  Google Scholar 

    75.
    Crowhurst, R. N. et al. Analysis of expressed sequence tags from Actinidia: applications of a cross species EST database for gene discovery in the areas of flavor, health, color and ripening. BMC Genomics 9, 351 (2008).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    76.
    Zheng, Y. Q., Li, Z. Z. & Huang, H. W. Preliminary study on SSR analysis in kiwifruit cultivars. J. WH Bot. Res. 21, 444–448 (2003).
    Google Scholar 

    77.
    Llorens, T. M., Ayre, D. J. & Whelan, R. J. Anthropogenic fragmentation may not alter pre-existing patterns of genetic diversity and differentiation in perennial shrubs. Mol. Ecol. 27, 1541–1555 (2018).
    PubMed  Article  Google Scholar 

    78.
    Van de Peer, Y., Mizrachi, E. & Marchal, K. The evolutionary significance of polyploidy. Nat. Rev. Genet. 18, 411–424 (2017).
    PubMed  Article  CAS  Google Scholar 

    79.
    Bommarco, R., Lindborg, R., Marini, L. & Ockinger, E. Extinction debt for plants and flower-visiting insects in landscapes with contrasting land use history. Divers. Distrib. 20, 591–599 (2014).
    Article  Google Scholar  More

  • in

    Increasing decision relevance of ecosystem service science

    1.
    IPBES Summary for Policymakers. In Global Assessment Report on Biodiversity and Ecosystem Services (eds Díaz, S. et al.) (IPBES Secretariat, 2019).
    2.
    Schaefer, M., Goldman, E., Bartuska, A. M., Sutton-Grier, A. & Lubchenco, J. Nature as capital: advancing and incorporating ecosystem services in United States federal policies and programs. Proc. Natl Acad. Sci. USA 112, 7383–7389 (2015).
    CAS  Article  Google Scholar 

    3.
    Mastrángelo, M. E. et al. Key knowledge gaps to achieve global sustainability goals. Nat. Sustain. https://doi.org/10.1038/s41893-019-0412-1 (2019).

    4.
    Olander, L. et al. So you want your research to be relevant? Building the bridge between ecosystem services research and practice. Ecosyst. Serv. 26, 170–182 (2017).
    Article  Google Scholar 

    5.
    Polasky, S., Tallis, H. & Reyers, B. Setting the bar: standards for ecosystem services. Proc. Natl Acad. Sci. USA https://doi.org/10.1073/pnas.1406490112 (2015).

    6.
    Rieb, J. et al. When, where and how nature matters for ecosystem services: challenges for the next generation of ecosystem service models. BioScience 67, 820–833 (2017).
    Article  Google Scholar 

    7.
    Natural Capital Protocol (Natural Capital Coalition, 2016).

    8.
    Mandle, L., Ouyang, Z., Salzman, J. & Daily, G. C. Green Growth that Works: Natural Capital Policy and Finance Mechanisms from the World (Island Press, 2019).

    9.
    Transforming our World: The 2030 Agenda for Sustainable Development (UN, 2015).

    10.
    Díaz, S. et al. Assessing nature’s contributions to people: recognizing culture, and diverse sources of knowledge, can improve assessments. Science 359, 270–272 (2018).
    Article  Google Scholar 

    11.
    Arkema, K. K. et al. Embedding ecosystem services in coastal planning leads to better outcomes for people and nature. Proc. Natl Acad. Sci. USA 112, 7390–7395 (2015).
    CAS  Article  Google Scholar 

    12.
    Van Wensem, J. et al. Identifying and assessing the application of ecosystem services approaches in environmental policies and decision making. Integr. Environ. Assess. Manag. 13, 41–51 (2017).
    Article  Google Scholar 

    13.
    Ricketts, T. H. & Lonsdorf, E. Mapping the margin: comparing marginal values of tropical forest remnants for pollination services. Ecol. Appl. 23, 1113–1123 (2013).
    Article  Google Scholar 

    14.
    Mandle, L., Tallis, H., Sotomayor, L. & Vogl, A. L. Who loses? Tracking ecosystem service redistribution from road development and mitigation in the Peruvian Amazon. Front. Ecol. Environ. 13, 309–315 (2015).
    Article  Google Scholar 

    15.
    Wieland, R., Ravensbergen, S., Gregr, E. J., Satterfield, T. & Chan, K. M. A. Debunking trickle-down ecosystem services: the fallacy of omnipotent, homogeneous beneficiaries. Ecol. Econ. 121, 175–180 (2016).
    Article  Google Scholar 

    16.
    Polasky, S. & Segerson, K. Integrating ecology and economics in the study of ecosystem services: some lessons learned. Annu. Rev. Resour. Econ. 1, 409–434 (2009).
    Article  Google Scholar 

    17.
    Keeler, B. L. et al. Linking water quality and well-being for improved assessment and valuation of ecosystem services. Proc. Natl Acad. Sci. USA 109, 18619–18624 (2012).
    CAS  Article  Google Scholar 

    18.
    Vogl, A. L. et al. Valuing investments in sustainable land management in the Upper Tana River basin, Kenya. J. Environ. Manag. 195, 78–91 (2017).
    Article  Google Scholar 

    19.
    Arkema, K., Guannel, G. & Verutes, G. Coastal habitats shield people and property from sea-level rise and storms. Nat. Clim. Change 3, 913–918 (2013).
    Article  Google Scholar 

    20.
    Plummer, M. L. Assessing benefit transfer for the valuation of ecosystem services. Front. Ecol. Environ. 7, 38–45 (2009).
    Article  Google Scholar 

    21.
    Tallis, H., Polasky, S., Lozano, J. S. & Wolny, S. in Inclusive Wealth Report 2012: Measuring Progress Toward Sustainability 195–214 (Cambridge Univ. Press, 2012).

    22.
    Costanza, R. et al. Changes in the global value of ecosystem services. Glob. Environ. Change https://doi.org/10.1016/j.gloenvcha.2014.04.002 (2014).

    23.
    Granek, E. F. et al. Ecosystem services as a common language for coastal ecosystem-based management. Conserv. Biol. 24, 207–216 (2010).
    Article  Google Scholar 

    24.
    Ruckelshaus, M. et al. Notes from the field: lessons learned from using ecosystem service approaches to inform real-world decisions. Ecol. Econ. https://doi.org/10.1016/j.ecolecon.2013.07.009 (2013).

    25.
    Ellis, A. M., Myers, S. S. & Ricketts, T. H. Do pollinators contribute to nutritional health? PLoS ONE 10, e114805 (2015).
    Article  Google Scholar 

    26.
    Olsson, P., Folke, C. & Hughes, T. P. Navigating the Transition to Ecosystem-Based Management of the Great Barrier Reef, Australia. Proc. Natl Acad. Sci. USA 105, 9489–9494 (2008).
    CAS  Article  Google Scholar 

    27.
    Costanza, R. et al. The value of the world’s ecosystem services and natural capital. Nature 387, 253–260 (1997).
    CAS  Article  Google Scholar 

    28.
    SEEA Experimental Ecosystem Accounting Revision (System of Environmental Economic Accounting, 2020); https://go.nature.com/2sqGqFn

    29.
    Aburto-Oropeza, O. et al. Mangroves in the Gulf of California increase fishery yields. Proc. Natl Acad. Sci. USA https://doi.org/10.1073/pnas.0804601105 (2008).

    30.
    Keeler, B. L. et al. The social costs of nitrogen. Sci. Adv. 2, e1600219 (2016).
    Article  Google Scholar 

    31.
    Kenter, J. O. et al. What are shared and social values of ecosystems? Ecol. Econ. 111, 86–99 (2015).
    Article  Google Scholar 

    32.
    Pascual, U. et al. Valuing nature’s contributions to people: the IPBES approach. Curr. Opin. Environ. Sustain. 26–27, 7–16 (2017).
    Article  Google Scholar 

    33.
    Samberg, L. H., Gerber, J. S., Ramankutty, N., Herrero, M. & West, P. C. Subnational distribution of average farm size and smallholder contributions to global food production. Environ. Res. Lett. 11, 124010 (2016).
    Article  Google Scholar 

    34.
    Jean, N. et al. Combining satellite imagery and machine learning to predict poverty. Science 353, 790–794 (2016).
    CAS  Article  Google Scholar 

    35.
    Wolff, S., Schulp, C. J. E. & Verburg, P. H. Mapping ecosystem services demand: a review of current research and future perspectives. Ecol. Indic. 55, 159–171 (2015).
    Article  Google Scholar 

    36.
    Dawson, N. & Martin, A. Assessing the contribution of ecosystem services to human wellbeing: a disaggregated study in western Rwanda. Ecol. Econ. 117, 62–72 (2015).
    Article  Google Scholar 

    37.
    Daw, T., Brown, K., Rosendo, S. & Pomeroy, R. Applying the ecosystem services concept to poverty alleviation: the need to disaggregate human well-being. Environ. Conserv. 38, 370–379 (2011).
    Article  Google Scholar 

    38.
    Ruhl, J. B. & Salzman, J. The effects of wetland mitigation banking on people. Natl Wetl. Newsl. 28, 7–13 (2006).
    Google Scholar 

    39.
    Kabisch, N. & Haase, D. Green justice or just green? Provision of urban green spaces in Berlin, Germany. Landsc. Urban Plan. 122, 129–139 (2014).
    Article  Google Scholar 

    40.
    Farley, K. A. & Bremer, L. L. ‘Water Is Life’: local perceptions of páramo grasslands and land management strategies associated with payment for ecosystem services. Ann. Am. Assoc. Geogr. 107, 371–381 (2017).
    Google Scholar 

    41.
    Pascual, U. et al. Social equity matters in payments for ecosystem services. BioScience 64, 1027–1036 (2014).
    Article  Google Scholar 

    42.
    Mastrangelo, M. E. & Laterra, P. From biophysical to social-ecological trade-offs: integrating biodiversity conservation and agricultural production in the Argentine Dry Chaco. Ecol. Soc. 20, 20 (2015).
    Article  Google Scholar 

    43.
    Guerry, A. D. et al. Natural capital and ecosystem services informing decisions: from promise to practice. Proc. Natl Acad. Sci. USA 112, 7348–7355 (2015).
    CAS  Article  Google Scholar 

    44.
    Rieb, J. T. et al. When, where, and how nature matters for ecosystem services: challenges for the next generation of ecosystem service models. BioScience 67, 820–833 (2017).
    Article  Google Scholar 

    45.
    Villa, F., Bagstad, K. J., Voigt, B., Johnson, G. W. & Portela, R. A methodology for adaptable and robust ecosystem services assessment. PLoS ONE 9, e91001 (2014).
    Article  Google Scholar 

    46.
    Díaz, S. et al. Assessing nature’s contributions to people. Science 359, 270–272 (2018).
    Article  Google Scholar 

    47.
    Millennium Ecosystem Assessment Ecosystems and Human Well-being: A Framework for Assessment (Island Press, 2003).

    48.
    Fleiss, J. L. Measuring nominal scale agreement among many raters. Psychol. Bull. 76, 378–382 (1971).
    Article  Google Scholar 

    49.
    Gamer, M., Lemon, J., Fellows, I. & Singh, P. irr: Various Coefficients of Interrater Reliability and Agreement (2012).

    50.
    Landis, J. R. & Koch, G. G. The measurement of observer agreement for categorical data. Biometrics 33, 159–174 (1977).
    CAS  Article  Google Scholar 

    51.
    Tallis, H. et al. A global system for monitoring ecosystem service change. BioScience 62, 977–986 (2012).
    Article  Google Scholar 

    52.
    Daily, G. C. et al. Ecosystem services in decision making: time to deliver. Front. Ecol. Environ. 7, 21–28 (2009).
    Article  Google Scholar  More

  • in

    Size-specific recolonization success by coral-dwelling damselfishes moderates resilience to habitat loss

    1.
    Fahrig, L. Effects of habitat fragmentation on biodiversity. Ann. Rev. Ecol. Evol. Syst. 34, 487–515 (2003).
    Article  Google Scholar 
    2.
    Foley, J. A. et al. Global consequences of land use. Science 309, 570–574 (2005).
    ADS  CAS  PubMed  Article  Google Scholar 

    3.
    Nee, S. & May, R. M. Dynamics of metapopulations: Habitat destruction and competitive coexistence. J. Anim. Ecol. 1, 37–40 (1992).
    Article  Google Scholar 

    4.
    Petit, S., Moilanen, A., Hanski, I. & Baguette, M. Metapopulation dynamics of the bog fritillary butterfly: Movements between habitat patches. Oikos 292, 491–500 (2001).
    Article  Google Scholar 

    5.
    Munday, P. L. Does habitat availability determine geographical-scale abundances of coral-dwelling fishes?. Coral Reefs 21, 105–116 (2002).
    ADS  Article  Google Scholar 

    6.
    Wong, M. Y., Fauvelot, C., Planes, S. & Buston, P. M. Discrete and continuous reproductive tactics in a hermaphroditic society. Anim. Behav. 84, 897–906 (2012).
    Article  Google Scholar 

    7.
    Chase, T. J., Pratchett, M. S., Walker, S. P. & Hoogenboom, M. O. Small-scale environmental variation influences whether coral-dwelling fish promote or impede coral growth. Oecologia 176, 1009–1022 (2014).
    ADS  CAS  PubMed  Article  Google Scholar 

    8.
    Kuwamura, T., Yogo, Y. & Nakashima, Y. Population dynamics of goby Paragobiodon echinocephalus and host coral Stylophora pistillata. Mar. Ecol. Prog. Ser. 6, 17–23 (1994).
    ADS  Article  Google Scholar 

    9.
    Holbrook, S. J., Forrester, G. E. & Schmitt, R. J. Spatial patterns in abundance of a damselfish reflect availability of suitable habitat. Oecologia 122, 109–120 (2000).
    ADS  CAS  PubMed  Article  Google Scholar 

    10.
    Boström-Einarsson, L., Bonin, M. C., Munday, P. L. & Jones, G. P. Strong intraspecific competition and habitat selectivity influence abundance of a coral-dwelling damselfish. J. Exp. Mar. Biol. Ecol. 448, 85–92 (2013).
    Article  Google Scholar 

    11.
    Munday, P. L. Habitat loss, resource specialization, and extinction on coral reefs. Glob. Change Biol. 10, 1642–1647 (2004).
    ADS  Article  Google Scholar 

    12.
    Wilson, S. K. et al. Habitat utilization by coral reef fish: Implications for specialists vs. generalists in a changing environment. J. Anim. Ecol. 77, 220–228 (2008).
    PubMed  Article  Google Scholar 

    13.
    Emslie, M. J., Cheal, A. J. & Johns, K. A. Retention of habitat complexity minimizes disassembly of reef fish communities following disturbance: A large-scale natural experiment. PLoS ONE 9, e105384. https://doi.org/10.1371/journal.pone.0105384 (2014).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    14.
    Bellwood, D. R. et al. Coral recovery may not herald the return of fishes on damaged coral reefs. Oecologia 170, 567–573 (2012).
    ADS  PubMed  Article  Google Scholar 

    15.
    Pratchett, M. S., Coker, D. J., Jones, G. P. & Munday, P. L. Specialization in habitat use by coral reef damselfishes and their susceptibility to habitat loss. Ecol. Evol. 2, 2168–2180 (2012).
    PubMed  PubMed Central  Article  Google Scholar 

    16.
    Ortiz, J. C. et al. Impaired recovery of the Great Barrier Reef under cumulative stress. Sci. Adv. 4, eaar6127. https://doi.org/10.1126/sciadv.aar6127 (2018).
    ADS  Article  PubMed  PubMed Central  Google Scholar 

    17.
    Bellwood, D. R. et al. Coral reef conservation in the Anthropocene: Confronting spatial mismatches and prioritizing functions. Biol. Conserv. 236, 604–615 (2019).
    Article  Google Scholar 

    18.
    Gilmour, J. P. et al. The state of Western Australia’s coral reefs. Coral Reefs 38, 651–667 (2019).
    ADS  Article  Google Scholar 

    19.
    Pisapia, C., Burn, D. & Pratchett, M. S. Changes in the population and community structure of corals during recent disturbances (February 2016–October 2017) on Maldivian coral reefs. Sci. Rep. 9, 8402. https://doi.org/10.1038/s41598-019-44809-9 (2019).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    20.
    Hoegh-Guldberg, O. et al. Coral reefs under rapid climate change and ocean acidification. Science 318, 1737–1742 (2007).
    ADS  CAS  PubMed  Article  Google Scholar 

    21.
    Bruno, J. F. & Valdivia, A. Coral reef degradation is not correlated with local human population density. Sci. Rep. 6, 29778. https://doi.org/10.1038/srep29778 (2016).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    22.
    Hughes, T. P. et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359, 80–83 (2018).
    ADS  CAS  PubMed  Article  Google Scholar 

    23.
    Bruno, J. F. & Selig, E. R. Regional decline of coral cover in the Indo-Pacific: Timing, extent, and subregional comparisons. PLoS ONE 2, e711. https://doi.org/10.1371/journal.pone.0000711 (2017).
    ADS  Article  Google Scholar 

    24.
    Kayal, M. et al. Predator crown-of-thorns starfish (Acanthaster planci) outbreak, mass mortality of corals, and cascading effects on reef fish and benthic communities. PLoS ONE 7, e47363. https://doi.org/10.1371/journal.pone.0047363 (2012).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    25.
    Mellin, C. et al. Spatial resilience of the Great Barrier Reef under cumulative disturbance impacts. Glob. Change Biol. 25, 2431–2445 (2019).
    Google Scholar 

    26.
    Chesher, R. H. Destruction of Pacific corals by sea star Acanthaster planci. Science 165, 280–283 (1969).
    ADS  CAS  PubMed  Article  Google Scholar 

    27.
    Pratchett, M. S., Schenk, T. J., Baine, M., Syms, C. & Baird, A. H. Selective coral mortality associated with outbreaks of Acanthaster planci L. in Bootless Bay, Papua New Guinea. Mar. Environ. Res. 67, 230–236 (2009).
    CAS  PubMed  Article  Google Scholar 

    28.
    Kayal, M., Lenihan, H. S., Pau, C., Penin, L. & Adjeroud, M. Associational refuges among corals mediate impacts of a crown-of-thorns starfish Acanthaster planci outbreak. Coral Reefs 30, 827–837 (2011).
    ADS  Article  Google Scholar 

    29.
    Pratchett, M. S., Caballes, C. F., Rivera-Posada, J. A. & Sweatman, H. P. A. Limits to understanding and managing outbreaks of crown-of-thorns stafish (Acanthaster spp.). Oceanogr. Mar. Biol. Ann. Rev. 52, 133–199 (2014).
    Google Scholar 

    30.
    Glynn, P. W. Some ecological consequences of coral-crustacean guard mutualisms in the Indian and Pacific Oceans. Symbiosis 4, 301–323 (1987).
    Google Scholar 

    31.
    Pratchett, M. S. Influence of coral symbionts on feeding preferences of crown-of-thorns starfish Acanthaster planci in the western Pacific. Mar. Ecol. Prog. Ser. 214, 111–119 (2001).
    ADS  Article  Google Scholar 

    32.
    McKeon, C. S., Stier, A. C., McIlroy, S. E. & Bolker, B. M. Multiple defender effects: Synergistic coral defense by mutualist crustaceans. Oecologia 169, 1095–1103 (2012).
    ADS  PubMed  Article  Google Scholar 

    33.
    Weber, J. N. & Woodhead, P. M. Ecological studies of coral predator Acanthaster planci in South Pacific. Mar. Biol. 6, 12–17 (1970).
    Article  Google Scholar 

    34.
    Birkeland, C. & Lucas, J. S. Acanthaster planci: Major Management Problem of Coral Reefs (CRC Press, Boca Raton, 1990).
    Google Scholar 

    35.
    Lassig, B. R. Communication and coexistence in a coral community. Mar. Biol. 42, 85–92 (1977).
    Article  Google Scholar 

    36.
    Cowan, Z. L., Dworjanyn, S. A., Caballes, C. F. & Pratchett, M. S. Predation on crown-of-thorns starfish larvae by damselfishes. Coral Reefs 35, 1253–1262 (2016).
    ADS  Article  Google Scholar 

    37.
    Cowan, Z. L., Ling, S. D., Caballes, C. F., Dworjanyn, S. A. & Pratchett, M. S. Crown-of-thorns starfish larvae are vulnerable to predation even in the presence of alternative prey. Coral Reefs 39, 293–303 (2020).
    Article  Google Scholar 

    38.
    Bonin, M. C. Specializing on vulnerable habitat: Acropora selectivity among damselfish recruits and the risk of bleaching-induced habitat loss. Coral Reefs 31, 287–297 (2012).
    ADS  Article  Google Scholar 

    39.
    Wilson, S. K., Graham, N. A. J., Pratchett, M. S., Jones, G. P. & Polunin, N. V. C. Multiple disturbances and the global degradation of coral reefs: Are reef fishes at risk or resilient?. Global Change Biol. 12, 2220–2234 (2006).
    ADS  Article  Google Scholar 

    40.
    Pratchett, M. S. et al. Effects of climate-induced coral bleaching on coral-reef fishes—Ecological and economic consequences. Oceanogr. Mar. Biol. Ann. Rev. 46, 257–302 (2008).
    Google Scholar 

    41.
    Pratchett, M. S., Thompson, C. A., Hoey, A. S., Cowman, P. F. & Wilson, S. K. Effects of coral bleaching and coral loss on the structure and function of reef fish assemblages. In Coral Bleaching (eds. van Oppen, M. J. & Lough, J. M.) 265–293 (Springer, Berlin, 2018).

    42.
    Bernal, M. A. et al. Species-specific molecular responses of wild coral reef fishes during a marine heatwave. Sci. Adv. 6, eaay3423. https://doi.org/10.1126/sciadv.aay3423 (2020).
    ADS  Article  PubMed  PubMed Central  Google Scholar 

    43.
    Magel, J. M., Dimoff, S. A. & Baum, J. K. Direct and indirect effects of climate change-amplified pulse heat stress events on coral reef fish communities. Ecol. Appl. https://doi.org/10.1002/eap.2124 (2020).
    Article  PubMed  Google Scholar 

    44.
    Booth, D. J. Opposing climate-change impacts on poleward-shifting coral-reef fishes. Coral Reefs 39, 577–581 (2020).
    Article  Google Scholar 

    45.
    Coker, D. J., Walker, S. P., Munday, P. L. & Pratchett, M. S. Social group entry rules may limit population resilience to patchy habitat disturbance. Mar. Ecol. Prog. Ser. 493, 237–242 (2013).
    ADS  Article  Google Scholar 

    46.
    Thompson, C. A., Matthews, S., Hoey, A. S. & Pratchett, M. S. Changes in sociality of butterflyfishes linked to population declines and coral loss. Coral Reefs 38, 527–537 (2019).
    ADS  Article  Google Scholar 

    47.
    Sano, M., Shimizu, M. & Nose, Y. Long-term effects of destruction of hermatypic corals by Acanthaster planci infestation on reef fish communities at Iriomote Island, Japan. Mar. Ecol. Prog. Ser. 37, 191–199 (1987).
    ADS  Article  Google Scholar 

    48.
    Jones, G. P., McCormick, M. I., Srinivasan, M. & Eagle, J. V. Coral decline threatens fish biodiversity in marine reserves. Proc. Nat. Acad. Sci. USA 101, 8251–8253 (2004).
    ADS  CAS  PubMed  Article  Google Scholar 

    49.
    Feary, D. A., Almany, G. R., McCormick, M. I. & Jones, G. P. Habitat choice, recruitment and the response of coral reef fishes to coral degradation. Oecologia 153, 727–737 (2007).
    ADS  PubMed  Article  Google Scholar 

    50.
    McCormick, M. I. Lethal effects of habitat degradation on fishes through changing competitive advantage. Proc. R. Soc. B. 279, 3899–3904 (2012).
    PubMed  Article  Google Scholar 

    51.
    Coker, D. J., Pratchett, M. S. & Munday, P. L. Coral bleaching and habitat degradation increase susceptibility to predation for coral-dwelling fishes. Behav. Ecol. 20, 1204–1210 (2009).
    Article  Google Scholar 

    52.
    Coker, D. J., Wilson, S. K. & Pratchett, M. S. of live coral habitat for reef fishes. Rev. Fish Biol. Fish. 24, 89–126 (2014).
    Article  Google Scholar 

    53.
    Pratchett, M. S., Hoey, A. S., Wilson, S. K., Hobbs, J. P. & Allen, G. R. Habitat-use and specialisation among coral reef damselfishes. In Biology of Damselfishes (ed. Frederich, B. & Parmentier, E.) 84–121 (Taylor & Francis, London, 2016).

    54.
    Sale, P. F. Extremely limited home range in a coral reef fish, Dascyllus aruanus (Pisces, Pomacentridae). Copeia 1971, 324–327 (1971).
    Article  Google Scholar 

    55.
    Robertson, D. R. & Lassig, B. Spatial distribution patterns and coexistence of a group of territorial damselfishes from the Great Barrier Reef. Bull. Mar. Sci. 30, 187–203 (1980).
    Google Scholar 

    56.
    D’Agostino, D. et al. The influence of thermal extremes on coral reef fish behaviour in the Arabian/Persian Gulf. Coral Reefs 39, 733–744 (2019).
    Article  Google Scholar 

    57.
    Adam, T. C. et al. How will coral reef fish communities respond to climate-driven disturbances? Insight from landscape-scale perturbations. Oecologia 176, 285–296 (2014).
    ADS  PubMed  Article  Google Scholar 

    58.
    Coker, D. J., Pratchett, M. S. & Munday, P. L. Influence of coral bleaching, coral mortality and conspecific aggression on movement and distribution of coral-dwelling fish. J. Exp. Mar. Biol. Ecol. 414, 62–68 (2012).
    Article  Google Scholar 

    59.
    Chase, T. J., Pratchett, M. S., Frank, G. E. & Hoogenboom, M. O. Coral-dwelling fish moderate bleaching susceptibility of coral hosts. PLoS ONE 13, e0208545. https://doi.org/10.1371/journal.pone.0208545 (2018).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    60.
    Wismer, S., Tebbett, S. B., Streit, R. P. & Bellwood, D. R. Spatial mismatch in fish and coral loss following 2016 mass coral bleaching. Sci. Total Environ. 50, 1487–1498 (2019).
    ADS  Article  CAS  Google Scholar 

    61.
    Wilson, S. K. et al. Maintenance of fish diversity on disturbed coral reefs. Coral Reefs 28, 3–14 (2009).
    ADS  Article  Google Scholar 

    62.
    Wilson, S. K., Robinson, J. P., Chong-Seng, K., Robinson, J. & Graham, N. A. Boom and bust of keystone structure on coral reefs. Coral Reefs 38, 625–635 (2019).
    ADS  Article  Google Scholar 

    63.
    Schmidt-Roach, S. et al. Assessing hidden species diversity in the coral Pocillopora damicornis from Eastern Australia. Coral Reefs 32, 161–172 (2013).
    ADS  Article  Google Scholar 

    64.
    Booth, D. J. & Beretta, G. A. Changes in a fish assemblage after a coral bleaching event. Mar. Ecol. Prog. Ser. 245, 205–212 (2002).
    ADS  Article  Google Scholar 

    65.
    Sano, M., Shimizu, M. & Nose, Y. Changes in structure of coral reef fish communities by destruction of hermatypic corals: Observational and experimental views. Pac. Sci. 38, 51–79 (1984).
    Google Scholar 

    66.
    Bonin, M. C., Munday, P. L., McCormick, M. I., Srinivasan, M. & Jones, G. P. Coral-dwelling fishes resistant to bleaching but not to mortality of host corals. Mar. Ecol. Prog. Ser. 394, 215–222 (2009).
    ADS  Article  Google Scholar 

    67.
    Paddack, M. J. et al. Recent region-wide declines in Caribbean reef fish abundance. Curr. Biol. 19, 590–595 (2009).
    CAS  PubMed  Article  Google Scholar 

    68.
    Booth, D. J. Larval settlement patterns and preferences by domino damselfish Dascyllus albisella Gill. J. Exp. Mar. Biol. Ecol. 155, 85–104 (1992).
    Article  Google Scholar 

    69.
    Sweatman, H. P. A. The influence of adults of some coral reef fishes on larval recruitment. Ecol. Monogr. 55, 469–485 (1985).
    Article  Google Scholar 

    70.
    Karplus, I., Katzenstein, R. & Goren, M. Predator recognition and social facilitation of predator avoidance in coral reef fish Dascyllus marginatus juveniles. Mar. Ecol. Prog. Ser. 319, 215–223 (2006).
    ADS  Article  Google Scholar 

    71.
    Forrester, G. E. Social rank, individual size and group composition as determinants of food consumption by humbug damselfish, Dascyllus aruanus. Anim. Behav. 42, 701–711 (1991).
    Article  Google Scholar 

    72.
    Holbrook, S. J., Brooks, A. J., Schmitt, R. J. & Stewart, H. L. Effects of sheltering fish on growth of their host corals. Mar. Biol. 155, 521–530 (2008).
    Article  Google Scholar 

    73.
    Noonan, S. H., Jones, G. P. & Pratchett, M. S. Coral size, health and structural complexity: Effects on the ecology of a coral reef damselfish. Mar. Ecol. Prog. Ser. 456, 127–137 (2012).
    ADS  Article  Google Scholar 

    74.
    Holbrook, S. J. & Schmitt, R. J. Competition for shelter space causes density-dependent predation mortality in damselfishes. Ecology 83, 2855–2868 (2002).
    Article  Google Scholar 

    75.
    Turgeon, K. & Kramer, D. L. Immigration rates during population density reduction in a coral reef fish. PLoS ONE 11, e0156417. https://doi.org/10.1371/journal.pone.0156417 (2016).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    76.
    Shpigel, M. & Fishelson, L. Behavior and physiology of coexistence in 2 species of Dascyllus (Pomacentridae, Teleostei). Environ. Biol. Fish. 17, 253–265 (1986).
    Article  Google Scholar 

    77.
    Wong, M. Y., Buston, P. M., Munday, P. L. & Jones, G. P. The threat of punishment enforces peaceful cooperation and stabilizes queues in a coral-reef fish. Proc. R. Soc. B. 274, 1093–1099 (2007).
    PubMed  Article  Google Scholar 

    78.
    Hixon, M. A. & Carr, M. H. Synergistic predation, density dependence, and population regulation in marine fish. Science 277, 946–949 (1997).
    CAS  Article  Google Scholar 

    79.
    Almany, G. R. Differential effects of habitat complexity, predators and competitors on abundance of juvenile and adult coral reef fishes. Oecologia 141, 105–113 (2004).
    ADS  PubMed  Article  Google Scholar 

    80.
    Wilson, S. K. et al. Influence of nursery microhabitats on the future abundance of a coral reef fish. Proc. R. Soc. B. 283, 20160903. https://doi.org/10.1098/rspb.2016.0903 (2016).
    Article  PubMed  Google Scholar 

    81.
    Graham, N. A. J., McClanahan, T. R., MacNeil, M. A., Wilson, S. K. & Polunin, N. V. C. Climate warming, marine protected areas and the ocean-scale integrity of coral reef ecosystems. PLoS ONE 3, e3039. https://doi.org/10.1371/journal.pone.0003039 (2008).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    82.
    Hing, M. L., Klanten, O. S., Dowton, M., Brown, K. R. & Wong, M. Y. Repeated cyclone events reveal potential causes of sociality in coral-dwelling Gobiodon fishes. PLoS ONE 13, e0202407. https://doi.org/10.1371/journal.pone.0202407 (2018).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    83.
    Hughes, et al. Global warming transforms coral reef assemblages. Nature 556, 492–496 (2018).
    ADS  CAS  PubMed  Article  Google Scholar 

    84.
    Emslie, M. J., Pratchett, M. S. & Cheal, A. J. Effects of different disturbance types on butterflyfish communities of Australia’s Great Barrier Reef. Coral Reefs 30, 461–471 (2011).
    ADS  Article  Google Scholar 

    85.
    Buchanan, J. R. et al. Living on the edge: Vulnerability of coral-dependent fishes in the Gulf. Mar. Poll. Bull. 105, 480–488 (2016).
    CAS  Article  Google Scholar 

    86.
    Pratchett, M. S. Dynamics of an outbreak population of Acanthaster planci at Lizard Island, northern Great Barrier Reef (1995–1999). Coral Reefs 24, 453–462 (2005).
    ADS  Article  Google Scholar 

    87.
    Pratchett, M. S. et al. Spatial, temporal and taxonomic variation in coral growth—Implications for the structure and function of coral reef ecosystems. Oceanogr. Mar. Biol. Ann. Rev. 53, 215–295 (2015).
    Google Scholar 

    88.
    Manly, B. F., McDonald, L., Thomas, D. L., McDonald, T. L. & Erickson, W. P. Resource selection by animals (Kluwer Academic Publishers, Dordrecht, 2010).
    Google Scholar 

    89.
    Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & R Core Team. nlme: Linear and nonlinear mixed effects models. https://CRAN.R-project.org/package=nlme (2020).

    90.
    R Core Team. R: A language and environment for statistical computing. https://www.R-project.org (2016). More

  • in

    Using machine learning to understand the implications of meteorological conditions for fish kills

    1.
    Burkholder, J. M., Mallin, M. A. & Glasgow, J. H. B. Fish kills, bottom-water hypoxia, and the toxic Pfiesteria complex in the Neuse River and Estuary. Mar. Ecol. Prog. Ser. 179, 301–310. https://doi.org/10.3354/meps179301 (1999).
    ADS  Article  Google Scholar 
    2.
    Ochumba, P. B. O. Massive fish kills within the Nyanza Gulf of Lake Victoria, Kenya. Hydrobiologia 208, 93–99. https://doi.org/10.1007/BF00008448 (1990).
    Article  Google Scholar 

    3.
    Thronson, A. & Quigg, A. Fifty-five years of fish kills in Coastal Texas. Estuaries Coasts 31, 802–813. https://doi.org/10.1007/s12237-008-9056-5 (2008).
    CAS  Article  Google Scholar 

    4.
    Wang, C. H., Hsu, C. C., Tzeng, W. N., You, C. F. & Chang, C. W. Origin of the mass mortality of the flathead grey mullet (Mugil cephalus) in the Tanshui River, northern Taiwan, as indicated by otolith elemental signatures. Mar. Pollut. Bull. 62, 1809–1813. https://doi.org/10.1016/j.marpolbul.2011.05.011 (2011).
    CAS  Article  PubMed  Google Scholar 

    5.
    Yñiguez, A. T. & Ottong, Z. J. Predicting fish kills and toxic blooms in an intensive mariculture site in the Philippines using a machine learning model. Sci. Total Environ. 707, 136173. https://doi.org/10.1016/j.scitotenv.2019.136173 (2020).
    ADS  CAS  Article  Google Scholar 

    6.
    La, V. T. & Cooke, S. J. Advancing the Science and Practice of Fish Kill Investigations. Rev. Fish. Sci. 19, 21–33. https://doi.org/10.1080/10641262.2010.531793 (2011).
    Article  Google Scholar 

    7.
    Epaphras, A. M., Gereta, E., Lejora, I. A. & Mtahiko, M. G. G. The importance of shading by riparian vegetation and wetlands in fish survival in stagnant water holes, Great Ruaha River, Tanzania. Wetl. Ecol. Manag. 15, 329–333. https://doi.org/10.1007/s11273-007-9033-y (2007).
    Article  Google Scholar 

    8.
    Peña, M. A., Katsev, S., Oguz, T. & Gilbert, D. Modeling dissolved oxygen dynamics and hypoxia. Biogeosciences 7, 933–957. https://doi.org/10.5194/bg-7-933-2010 (2010).
    ADS  Article  Google Scholar 

    9.
    Ekau, W., Auel, H., Pörtner, H. O. & Gilbert, D. Impacts of hypoxia on the structure and processes in pelagic communities (zooplankton, macro-invertebrates and fish). Biogeosciences 7, 1669–1699. https://doi.org/10.5194/bg-7-1669-2010 (2010).
    ADS  CAS  Article  Google Scholar 

    10.
    Levin, L. A. et al. Effects of natural and human-induced hypoxia on coastal benthos. Biogeosciences 6, 2063–2098. https://doi.org/10.5194/bg-6-2063-2009 (2009).
    ADS  CAS  Article  Google Scholar 

    11.
    Tyler, R. M., Brady, D. C. & Targett, T. E. Temporal and spatial dynamics of diel-cycling hypoxia in estuarine tributaries. Estuaries Coasts 32, 123–145. https://doi.org/10.1007/s12237-008-9108-x (2009).
    CAS  Article  Google Scholar 

    12.
    Townsend, S. A. & Edwards, C. A. A fish kill event, hypoxia and other limnological impacts associated with early wet season flow into a lake on the Mary River floodplain, tropical northern Australia. Lakes Reserv. Res. Manag. 8, 169–176. https://doi.org/10.1111/j.1440-1770.2003.00222.x (2003).
    Article  Google Scholar 

    13.
    Evans, M. A. & Scavia, D. Forecasting hypoxia in the Chesapeake Bay and Gulf of Mexico: model accuracy, precision, and sensitivity to ecosystem change. Environ. Res. Lett. 6, 015001. https://doi.org/10.1088/1748-9326/6/1/015001 (2011).
    ADS  CAS  Article  Google Scholar 

    14.
    Yang, C. P., Lung, W. S., Liu, J. H. & Hsiao, W. P. Establishment and application of water quality model of hypoxic stream. J. Taiwan Agric. Eng. 55, 27–39. https://doi.org/10.29974/JTAE.200903.0004 (2009).
    Article  Google Scholar 

    15.
    Nelson, N. G., Muñoz-Carpena, R., Neale, P. J., Tzortziou, M. & Megonigal, J. P. Temporal variability in the importance of hydrologic, biotic, and climatic descriptors of dissolved oxygen dynamics in a shallow tidal-marsh creek. Water Resour. Res. 53, 7103–7120. https://doi.org/10.1002/2016wr020196 (2017).
    ADS  CAS  Article  Google Scholar 

    16.
    Ouellet, V., Mingelbier, M., Saint-Hilaire, A. & Morin, J. Frequency analysis as a tool for assessing adverse conditions during a massive fish kill in the St. Lawrence River, Canada. Water Qual. Res. J. 45, 47–57. https://doi.org/10.2166/wqrj.2010.006 (2010).
    CAS  Article  Google Scholar 

    17.
    Chin, D. A. Water-Quality Engineering in Natural Systems: Fate and Transport Processes in the Water Environment (Wiley, New York, 2013).
    Google Scholar 

    18.
    Carpenter, J. H. New measurements of oxygen solubility in pure and natural water. Limnol. Oceanogr. 11, 264–277. https://doi.org/10.4319/lo.1966.11.2.0264 (1966).
    ADS  CAS  Article  Google Scholar 

    19.
    Gameson, A. L. H. & Robertsonn, K. G. The solubility of oxygen in pure water and sea-water. J. Appl. Chem. 5, 502. https://doi.org/10.1002/jctb.5010050909 (1955).
    CAS  Article  Google Scholar 

    20.
    Liss, P. S. Processes of gas exchange across an air-water interface. Deep-Sea Res. Oceanogr. Abstr. 20, 221–238. https://doi.org/10.1016/0011-7471(73)90013-2 (1973).
    ADS  CAS  Article  Google Scholar 

    21.
    Marino, R. & Howarth, R. W. Atmospheric oxygen exchange in the Hudson River. Estuaries 16, 433–445. https://doi.org/10.2307/1352591 (1993).
    CAS  Article  Google Scholar 

    22.
    Loucks, D. P. & van Beek, E. Water Resources Systems Planning and Management: An Introduction to Methods, Models and Applications (UNESCO, Paris, 2005).
    Google Scholar 

    23.
    Lucas, M. C. & Baras, E. Methods for studying spatial behaviour of freshwater fishes in the natural environment. Fish Fish. 1, 283–316. https://doi.org/10.1046/j.1467-2979.2000.00028.x (2000).
    Article  Google Scholar 

    24.
    Roscoe, R. W. & Hinch, S. G. Effectiveness monitoring of fish passage facilities: historical trends, geographic patterns and future directions. Fish Fish. 11, 12–33. https://doi.org/10.1111/j.1467-2979.2009.00333.x (2010).
    Article  Google Scholar 

    25.
    Townsend, S. A., Boland, K. T. & Wrigley, T. J. Factors contributing to a fish kill in the Australian wet/dry tropics. Water Res. 26, 1039–1044. https://doi.org/10.1016/0043-1354(92)90139-U (1992).
    CAS  Article  Google Scholar 

    26.
    Cheng, S. T., Hwang, G. W., Chen, C. P., Hou, W. S. & Hsieh, H. L. An integrated modeling approach to evaluate the performance of an oxygen enhancement device in the Hwajiang wetland, Taiwan. Ecol. Eng. 42, 244–248. https://doi.org/10.1016/j.ecoleng.2012.02.011 (2012).
    Article  Google Scholar 

    27.
    Nakamura, Y. & Stefan, H. G. Effect of flow velocity on sediment oxygen demand: theory. J. Environ. Eng. 120, 996–1016. https://doi.org/10.1061/(ASCE)0733-9372(1994)120:5(996) (1994).
    CAS  Article  Google Scholar 

    28.
    Welcomme, R. L. Fisheries Ecology of Floodplain Rivers (Longman, Harlow, 1979).
    Google Scholar 

    29.
    Hsu, H. H. & Chen, C. T. Observed and projected climate change in Taiwan. Meteorol. Atmos. Phys. 79, 87–104. https://doi.org/10.1007/s703-002-8230-x (2002).
    ADS  Article  Google Scholar 

    30.
    Yu, P. S., Yang, T. C. & Wu, C. K. Impact of climate change on water resources in southern Taiwan. J. Hydrol. 260, 161–175. https://doi.org/10.1016/S0022-1694(01)00614-X (2002).
    ADS  Article  Google Scholar 

    31.
    Huang, W. C., Chiang, Y., Wu, R. Y., Lee, J. L. & Lin, S. H. The impact of climate change on rainfall frequency in Taiwan. Terr. Atmos. Ocean. Sci. https://doi.org/10.3319/TAO.2012.05.03.04(WMH) (2012).
    Article  Google Scholar 

    32.
    IPCC, Working Groups I, II and III to the Fifth Assessment Report.Climate Change 2014: Synthesis Report (2014).

    33.
    Seneviratne, S. I. et al. Changes in climate extremes and their impacts on the natural physical environment. In Managing the Risks of Extreme Events and Disasters to Advance Climate Change Adaptation (eds Field C.B. et al.) 109–230 (A Special Report of Working Groups I and II of the Intergovernmental Panel on Climate Change (IPCC), 2012).

    34.
    Altieri, A. H. & Gedan, K. B. Climate change and dead zones. Glob. Change Biol. 21, 1395–1406. https://doi.org/10.1111/gcb.12754 (2015).
    ADS  Article  Google Scholar 

    35.
    Kuo, C. W. & Lee, C. T. Trend analysis of water quality in the upper watershed of the Feitsui reservoir. J. Geogr. Sci. 38, 111–128 (2004).
    Google Scholar 

    36.
    Turner, R. E., Rabalais, N. N., Swenson, E. M., Kasprzak, M. & Romaire, T. Summer hypoxia in the northern Gulf of Mexico and its prediction from 1978 to 1995. Mar. Environ. Res. 59, 65–77. https://doi.org/10.1016/j.marenvres.2003.09.002 (2005).
    CAS  Article  PubMed  Google Scholar 

    37.
    Urbina, W. A. & Glover, C. N. Relationship between fish size and metabolic rate in the oxyconforming inanga Galaxias maculatus reveals size-dependent strategies to withstand hypoxia. Physiol. Biochem. Zool. 86, 740–749. https://doi.org/10.1086/673727 (2013).
    Article  PubMed  Google Scholar 

    38.
    Brett, J. R. & Groves, T. D. D. Physiological energetics. In Fish Physiology (eds Hoar, W. S. et al.) 279–352 (Academic Press, Cambridge, 1979).
    Google Scholar 

    39.
    Chang, C. W., Tzeng, W. N. & Lee, Y. C. Recruitment and hatching dates of grey-mullet (Mugil cephalus L.) juveniles in the Tanshui estuary of northwest Taiwan. Zool. Stud. 39, 99–106 (2000).
    Google Scholar 

    40.
    Young, J. L. et al. Integrating physiology and life history to improve fisheries management and conservation. Fish Fish. 7, 262–283. https://doi.org/10.1111/j.1467-2979.2006.00225.x (2006).
    Article  Google Scholar 

    41.
    Hamilton, P. B. et al. Population-level consequences for wild fish exposed to sublethal concentrations of chemicals—a critical review. Fish Fish. 17, 545–566. https://doi.org/10.1111/faf.12125 (2016).
    Article  Google Scholar 

    42.
    Cheng, S. T., Herricks, E. E., Tsai, W. P. & Chang, F. J. Assessing the natural and anthropogenic influences on basin-wide fish species richness. Sci. Total Environ. 572, 825–836. https://doi.org/10.1016/j.scitotenv.2016.07.120 (2016).
    ADS  CAS  Article  PubMed  Google Scholar 

    43.
    Radinger, J. et al. Effective monitoring of freshwater fish. Fish Fish. 20, 729–747. https://doi.org/10.1111/faf.12373 (2019).
    Article  Google Scholar 

    44.
    Junninen, H., Niska, H., Tuppurainen, K., Ruuskanen, J. & Kolehmainen, M. Methods for imputation of missing values in air quality data sets. Atmos. Environ. 38, 2895–2907. https://doi.org/10.1016/j.atmosenv.2004.02.026 (2004).
    ADS  CAS  Article  Google Scholar 

    45.
    Cheng, S. T., Tsai, W. P., Yu, T. C., Herricks, E. E. & Chang, F. J. Signals of stream fish homogenization revealed by AI-based clusters. Sci. Rep. 8, 15960. https://doi.org/10.1038/s41598-018-34313-x (2018).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    46.
    Kohonen, T. Essentials of the self-organizing map. Neural Netw. 37, 52–65. https://doi.org/10.1016/j.neunet.2012.09.018 (2013).
    Article  PubMed  Google Scholar 

    47.
    Kohonen, T. The self-organizing map. Proc. IEEE 78, 1464–1480. https://doi.org/10.1109/5.58325 (1990).
    Article  Google Scholar 

    48.
    Kohonen, T. et al. Self organization of a massive document collection. IEEE Trans. Neural Netw. 11, 574–585. https://doi.org/10.1109/72.846729 (2000).
    CAS  Article  PubMed  Google Scholar 

    49.
    Tsai, W. P., Huang, S. P., Cheng, S. T., Shao, K. T. & Chang, F. J. A data-mining framework for exploring the multi-relation between fish species and water quality through self-organizing map. Sci. Total Environ. 579, 474–483. https://doi.org/10.1016/j.scitotenv.2016.11.071 (2017).
    ADS  CAS  Article  PubMed  Google Scholar 

    50.
    Wehrens, R. & Buydens, L. M. C. Self- and super-organizing maps in R: the kohonen package. J. Stat. Softw. 21, 1–19. https://doi.org/10.18637/jss.v021.i05 (2007).
    Article  Google Scholar 

    51.
    Kirt, T., Vainik, E. & Võhandu, L. A method for comparing self-organizing maps: case studies of banking and linguistic data. In Proceedings of Eleventh East-European Conference on Advances in Databases and Information Systems (eds Ioannidis, Y., Novikov, B. & Rachev, B.) 107–115 (Technical University of Varna, Levski, 2007).
    Google Scholar 

    52.
    Kohonen, T. Self-Organizing Maps 3rd edn. (Springer, New York, 2001).
    Google Scholar 

    53.
    Kalteh, A. M., Hjorth, P. & Berndtsson, R. Review of the self-organizing map (SOM) approach in water resources: Analysis, modelling and application. Environ. Model. Softw. 23, 835–845. https://doi.org/10.1016/j.envsoft.2007.10.001 (2008).
    Article  Google Scholar  More

  • in

    StableClim, continuous projections of climate stability from 21000 BP to 2100 CE at multiple spatial scales

    1.
    Fordham, D. A., Brook, B. W., Moritz, C. & Nogues-Bravo, D. Better forecasts of range dynamics using genetic data. Trends Ecol. Evol. 29, 436–443, https://doi.org/10.1016/j.tree.2014.05.007 (2014).
    Article  PubMed  Google Scholar 
    2.
    Fordham, D. A. et al. Using paleo-archives to safeguard biodiversity under climate change. Science, https://doi.org/10.1126/science.abc5654 (2020).

    3.
    Nogués-Bravo, D. et al. Cracking the code of biodiversity responses to past climate change. Trends Ecol. Evol. 33, 765–776, https://doi.org/10.1016/j.tree.2018.07.005 (2018).
    Article  PubMed  Google Scholar 

    4.
    Fordham, D. A. & Nogues-Bravo, D. Open-access data is uncovering past responses of biodiversity to global environmental change. PAGES 26, 77–77, https://doi.org/10.22498/pages.26.2.77 (2018).
    Article  Google Scholar 

    5.
    Fine, P. V. A. Ecological and evolutionary drivers of geographic variation in species diversity. Annu. Rev. Ecol. Evol. Syst. 46, 369–392, https://doi.org/10.1146/annurev-ecolsys-112414-054102 (2015).
    Article  Google Scholar 

    6.
    Rangel, T. F. et al. Modeling the ecology and evolution of biodiversity: biogeographical cradles, museums, and graves. Science 361, eaar5452, https://doi.org/10.1126/science.aar5452 (2018).
    CAS  Article  PubMed  Google Scholar 

    7.
    Lister, A. M. & Stuart, A. J. The impact of climate change on large mammal distribution and extinction: Evidence from the last glacial/interglacial transition. C. R. Geosci. 340, 615–620, https://doi.org/10.1016/j.crte.2008.04.001 (2008).
    Article  Google Scholar 

    8.
    Brown, S. C., Wigley, T. M. L., Otto-Bliesner, B. L., Rahbek, C. & Fordham, D. A. Persistent quaternary climate refugia are hospices for biodiversity in the anthropocene. Nat. Clim. Change., https://doi.org/10.1038/s41558-019-0682-7 (2020).

    9.
    Fjeldså, J. & Lovett, J. C. Geographical patterns of old and young species in African forest biota: The significance of specific montane areas as evolutionary centres. Biodivers. Conserv. 6, 325–346, https://doi.org/10.1023/A:1018356506390 (1997).
    Article  Google Scholar 

    10.
    Haffer, J. Speciation in Amazonian forest birds. Science 165, 131–137, https://doi.org/10.1126/science.165.3889.131 (1969).
    ADS  CAS  Article  PubMed  Google Scholar 

    11.
    Harrison, S. & Noss, R. Endemism hotspots are linked to stable climatic refugia. Ann. Bot. 119, 207–214, https://doi.org/10.1093/aob/mcw248 (2017).
    Article  PubMed  PubMed Central  Google Scholar 

    12.
    Armstrong, E., Hopcroft, P. O. & Valdes, P. J. A simulated northern hemisphere terrestrial climate dataset for the past 60,000 years. Sci. Data 6, 265, https://doi.org/10.1038/s41597-019-0277-1 (2019).
    Article  PubMed  PubMed Central  Google Scholar 

    13.
    Brown, J. L., Hill, D. J., Dolan, A. M., Carnaval, A. C. & Haywood, A. M. Paleoclim, high spatial resolution paleoclimate surfaces for global land areas. Sci. Data 5, 180254, https://doi.org/10.1038/sdata.2018.254 (2018).
    Article  PubMed  PubMed Central  Google Scholar 

    14.
    Lorenz, D. J., Nieto-Lugilde, D., Blois, J. L., Fitzpatrick, M. C. & Williams, J. W. Downscaled and debiased climate simulations for north america from 21,000 years ago to 2100 AD. Sci. Data 3, 160048, https://doi.org/10.1038/sdata.2016.48 (2016).
    Article  PubMed  PubMed Central  Google Scholar 

    15.
    Barnosky, A. D. et al. Merging paleobiology with conservation biology to guide the future of terrestrial ecosystems. Science 355, https://doi.org/10.1126/science.aah4787 (2017).

    16.
    Nogués-Bravo, D. et al. Amplified plant turnover in response to climate change forecast by late quaternary records. Nat. Clim. Change. 6, 1115–1119, https://doi.org/10.1038/nclimate3146 (2016).
    ADS  Article  Google Scholar 

    17.
    Maiorano, L. et al. Building the niche through time: Using 13,000 years of data to predict the effects of climate change on three tree species in Europe. Global Ecol. Biogeogr. 22, 302–317, https://doi.org/10.1111/j.1466-8238.2012.00767.x (2013).
    Article  Google Scholar 

    18.
    Blois, J. L., Zarnetske, P. L., Fitzpatrick, M. C. & Finnegan, S. Climate change and the past, present, and future of biotic interactions. Science 341, 499, https://doi.org/10.1126/science.1237184 (2013).
    ADS  CAS  Article  PubMed  Google Scholar 

    19.
    Lima-Ribeiro, M. S. et al. Ecoclimate: A database of climate data from multiple models for past, present, and future for macroecologists and biogeographers. Biodiversity Informatics 10, 1–21, https://doi.org/10.17161/bi.v10i0.4955 (2015).
    Article  Google Scholar 

    20.
    Liu, Z. et al. Transient simulation of last deglaciation with a new mechanism for Bølling–Allerød warming. Science 325, 310–314, https://doi.org/10.1126/science.1171041 (2009).
    ADS  CAS  Article  PubMed  Google Scholar 

    21.
    Otto-Bliesner, B. L. et al. Coherent changes of southeastern equatorial and northern African rainfall during the last deglaciation. Science 346, 1223, https://doi.org/10.1126/science.1259531 (2014).
    ADS  CAS  Article  PubMed  Google Scholar 

    22.
    Meinshausen, M. et al. The RCP greenhouse gas concentrations and their extensions from 1765 to 2300. Clim. Change 109, 213–241, https://doi.org/10.1007/s10584-011-0156-z (2011).
    ADS  CAS  Article  Google Scholar 

    23.
    van Vuuren, D. P. et al. The representative concentration pathways: An overview. Clim. Change 109, 5–31, https://doi.org/10.1007/s10584-011-0148-z (2011).
    ADS  Article  Google Scholar 

    24.
    van Oldenborgh, G. J. et al. 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.) 1311–1393 (Cambridge University Press, Cambridge, United Kingdom, 2013).

    25.
    Holt, B. G. et al. An update of Wallace’s zoogeographic regions of the world. Science 339, 74, https://doi.org/10.1126/science.1228282 (2013).
    ADS  CAS  Article  PubMed  Google Scholar 

    26.
    Botta, F., Dahl-Jensen, D., Rahbek, C., Svensson, A. & Nogues-Bravo, D. Abrupt change in climate and biotic systems. Curr. Biol. 29, R1045–R1054, https://doi.org/10.1016/j.cub.2019.08.066 (2019).
    CAS  Article  PubMed  Google Scholar 

    27.
    Fordham, D. A. et al. Predicting and mitigating future biodiversity loss using long-term ecological proxies. Nat. Clim. Change. 6, 909–916, https://doi.org/10.1038/nclimate3086 (2016).
    ADS  Article  Google Scholar 

    28.
    Fordham, D. A. et al. Paleoview: A tool for generating continuous climate projections spanning the last 21 000 years at regional and global scales. Ecography 40, 1348–1358, https://doi.org/10.1111/ecog.03031 (2017).
    Article  Google Scholar 

    29.
    Fordham, D. A., Saltré, F., Brown, S. C., Mellin, C. & Wigley, T. M. L. Why decadal to century timescale palaeoclimate data are needed to explain present-day patterns of biological diversity and change. Global Change Biol. 24, 1371–1381, https://doi.org/10.1111/gcb.13932 (2018).
    ADS  Article  Google Scholar 

    30.
    Taylor, K. E., Stouffer, R. J. & Meehl, G. A. An overview of CMIP5 and the experiment design. Bull. Amer. Meteor. 93, 485–498, https://doi.org/10.1175/Bams-D-11-00094.1 (2012).
    ADS  Article  Google Scholar 

    31.
    Otto-Bliesner, B. L. et al. Climate sensitivity of moderate- and low-resolution versions of CCSM3 to preindustrial forcings. J. Clim. 19, 2567–2583, https://doi.org/10.1175/Jcli3754.1 (2006).
    ADS  Article  Google Scholar 

    32.
    Collins, W. D. et al. The community climate system model version 3 (CCSM3). J. Clim. 19, 2122–2143, https://doi.org/10.1175/jcli3761.1 (2006).
    ADS  Article  Google Scholar 

    33.
    Gent, P. R. et al. The community climate system model version 4. J. Clim. 24, 4973–4991, https://doi.org/10.1175/2011jcli4083.1 (2011).
    ADS  Article  Google Scholar 

    34.
    Barker, S. et al. Interhemispheric Atlantic seesaw response during the last deglaciation. Nature 457, 1097–1102, https://doi.org/10.1038/nature07770 (2009).
    ADS  CAS  Article  PubMed  Google Scholar 

    35.
    Carlson, A. E. In The encyclopedia of quaternary science Vol. 3 (ed Elias, S. A.) 126–134 (Elsevier, Amsterdam, 2013).

    36.
    Marsicek, J., Shuman, B. N., Bartlein, P. J., Shafer, S. L. & Brewer, S. Reconciling divergent trends and millennial variations in holocene temperatures. Nature 554, 92, https://doi.org/10.1038/nature25464 (2018).
    ADS  CAS  Article  PubMed  Google Scholar 

    37.
    Deser, C., Knutti, R., Solomon, S. & Phillips, A. S. Communication of the role of natural variability in future north American climate. Nat. Clim. Change. 2, 775, https://doi.org/10.1038/nclimate1562 (2012).
    ADS  Article  Google Scholar 

    38.
    Lutz, A. F. et al. Selecting representative climate models for climate change impact studies: An advanced envelope-based selection approach. Int. J. Climatol. 36, 3988–4005, https://doi.org/10.1002/joc.4608 (2016).
    Article  Google Scholar 

    39.
    Tebaldi, C. & Knutti, R. The use of the multi-model ensemble in probabilistic climate projections. Philos. T. R. Soc. A. 365, 2053–2075, https://doi.org/10.1098/rsta.2007.2076 (2007).
    ADS  MathSciNet  Article  Google Scholar 

    40.
    Schulzweida, U. CDO user guide (version 1.9.3). https://doi.org/10.5281/zenodo.3539275, (2019).

    41.
    Kaplan, J. O. et al. Holocene carbon emissions as a result of anthropogenic land cover change. Holocene 21, 775–791, https://doi.org/10.1177/0959683610386983 (2011).
    ADS  Article  Google Scholar 

    42.
    Santer, B. D. et al. Identifying human influences on atmospheric temperature. Proc. Natl. Acad. Sci. USA 110, 26–33, https://doi.org/10.1073/pnas.1210514109 (2013).
    ADS  Article  PubMed  Google Scholar 

    43.
    Fordham, D. A., Wigley, T. M. L., Watts, M. J. & Brook, B. W. Strengthening forecasts of climate change impacts with multi-model ensemble averaged projections using MAGICC/SCENGEN 5.3. Ecography 35, 4–8, https://doi.org/10.1111/j.1600-0587.2011.07398.x (2012).
    Article  Google Scholar 

    44.
    Fordham, D. A., Brown, S. C., Wigley, T. M. L. & Rahbek, C. Cradles of diversity are unlikely relics of regional climate stability. Curr. Biol. 29, R356–R357, https://doi.org/10.1016/j.cub.2019.04.001 (2019).
    CAS  Article  PubMed  Google Scholar 

    45.
    Sen Gupta, A., Jourdain, N. C., Brown, J. N. & Monselesan, D. Climate drift in the CMIP5 models. J. Clim. 26, 8597–8615, https://doi.org/10.1175/Jcli-D-12-00521.1 (2013).
    ADS  Article  Google Scholar 

    46.
    Pinheiro, J., Bates, D., DebRoy, S., Sarkar D. & R Core Team nlme: linear and nonliner mixed effects models, https://CRAN.R-project.org/package=nlme (2017).

    47.
    R Core Team R: A language and environment for statistical computing https://www.R-project.org/ (R Foundation for Statistical Computing, Vienna, Austria, 2018).

    48.
    Pierce, D. W., Barnett, T. P., Santer, B. D. & Gleckler, P. J. Selecting global climate models for regional climate change studies. Proc. Natl. Acad. Sci. USA 106, 8441, https://doi.org/10.1073/pnas.0900094106 (2009).
    ADS  Article  PubMed  Google Scholar 

    49.
    Hawkins, E. & Sutton, R. Time of emergence of climate signals. Geophys. Res. Lett. 39, https://doi.org/10.1029/2011gl050087 (2012).

    50.
    IPCC 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.) 1535 (Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA, 2013).

    51.
    Theodoridis, S. et al. Evolutionary history and past climate change shape the distribution of genetic diversity in terrestrial mammals. Nat. Commun., https://doi.org/10.1038/s41467-020-16449-5 (2020).

    52.
    Nadeau, C. P., Urban, M. C. & Bridle, J. R. Coarse climate change projections for species living in a fine-scaled world. Globl Chang Biol 23, 12–24, https://doi.org/10.1111/gcb.13475 (2017).
    ADS  Article  Google Scholar 

    53.
    Frame, D., Joshi, M., Hawkins, E., Harrington, L. J. & de Roiste, M. Population-based emergence of unfamiliar climates. Nat. Clim. Change. 7, 407, https://doi.org/10.1038/Nclimate3297 (2017).
    ADS  Article  Google Scholar 

    54.
    Brown, S. C., Wigley, T. M. L., Otto-Bliesner, B. L. & Fordham, D. A., StableClim. The University of Adelaide https://doi.org/10.25909/5ea59831121bc (2020).

    55.
    Dowle, M. & Srinivasan, A. data.table: extension of ‘data.frame’, https://CRAN.R-project.org/package=data.table (2019).

    56.
    Petit, J. R. et al. Climate and atmospheric history of the past 420,000 years from the Vostok ice core, Antarctica. Nature 399, 429–436, https://doi.org/10.1038/20859 (1999).
    ADS  CAS  Article  Google Scholar 

    57.
    Andersen, K. K. et al. The Greenland ice core chronology 2005, 15–42ka. Part 1: Constructing the time scale. Quat. Sci. Rev. 25, 3246–3257, https://doi.org/10.1016/j.quascirev.2006.08.002 (2006).
    ADS  Article  Google Scholar 

    58.
    Rasmussen, S. O. et al. Synchronization of the NGRIP, GRIP, and GISP2 ice cores across MIS 2 and palaeoclimatic implications. Quat. Sci. Rev. 27, 18–28, https://doi.org/10.1016/j.quascirev.2007.01.016 (2008).
    ADS  Article  Google Scholar 

    59.
    Anderson, M. J. Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62, 245–253, https://doi.org/10.1111/j.1541-0420.2005.00440.x (2006).
    MathSciNet  Article  PubMed  PubMed Central  MATH  Google Scholar 

    60.
    Anderson, M. J. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26, 32–46, https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x (2001).
    Article  Google Scholar 

    61.
    Clarke, K. R. & Gorley, R. N. PRIMER v6: User manual/tutorial. (PRIMER-E, Plymouth, 2006).

    62.
    Anderson, M. J., Gorley, R. N. & Clarke, K. R. Permanova+ for PRIMER: Guide to software and statistical methods. (PRIMER-E, Plymouth, 2008).

    63.
    Clark, P. U. et al. Global climate evolution during the last deglaciation. Proc. Natl. Acad. Sci. USA 109, E1134, https://doi.org/10.1073/pnas.1116619109 (2012).
    Article  PubMed  Google Scholar 

    64.
    Liu, Z. et al. Younger Dryas cooling and the Greenland climate response to CO2. Proc. Natl. Acad. Sci. USA, https://doi.org/10.1073/pnas.1202183109 (2012).

    65.
    McManus, J. F., Francois, R., Gherardi, J. M., Keigwin, L. D. & Brown-Leger, S. Collapse and rapid resumption of atlantic meridional circulation linked to deglacial climate changes. Nature 428, 834–837, https://doi.org/10.1038/nature02494 (2004).
    ADS  CAS  Article  PubMed  Google Scholar 

    66.
    Peck, V. L. et al. The relationship of Heinrich events and their European precursors over the past 60ka BP: A multi-proxy ice-rafted debris provenance study in the north east atlantic. Quat. Sci. Rev. 26, 862–875, https://doi.org/10.1016/j.quascirev.2006.12.002 (2007).
    ADS  Article  Google Scholar 

    67.
    Shakun, J. D. et al. Global warming preceded by increasing carbon dioxide concentrations during the last deglaciation. Nature 484, 49, https://doi.org/10.1038/nature10915 (2012).
    ADS  CAS  Article  PubMed  Google Scholar 

    68.
    Carlson, A. E. & Winsor, K. Northern hemisphere ice-sheet responses to past climate warming. Nat. Geosci. 5, 607–613, https://doi.org/10.1038/ngeo1528 (2012).
    ADS  CAS  Article  Google Scholar 

    69.
    Renssen, H. & Isarin, R. F. B. The two major warming phases of the last deglaciation at ∼14.7 and ∼11.5 ka cal BP in Europe: Climate reconstructions and AGCM experiments. Global Planet. Change 30, 117–153, https://doi.org/10.1016/S0921-8181(01)00082-0 (2001).
    ADS  Article  Google Scholar 

    70.
    Alley, R. B. & Ágústsdóttir, A. M. The 8k event: Cause and consequences of a major holocene abrupt climate change. Quat. Sci. Rev. 24, 1123–1149, https://doi.org/10.1016/j.quascirev.2004.12.004 (2005).
    ADS  Article  Google Scholar 

    71.
    Benjamini, Y. & Yekutieli, D. The control of the false discovery rate in multiple testing under dependency. Ann. Stat. 29, 1165–1188, https://doi.org/10.1214/aos/1013699998 (2001).
    MathSciNet  Article  MATH  Google Scholar 

    72.
    Harris, I., Jones, P. D., Osborn, T. J. & Lister, D. H. Updated high-resolution grids of monthly climatic observations – the CRU TS3.10 dataset. Int. J. Climatol. 34, 623–642, https://doi.org/10.1002/joc.3711 (2014).

    73.
    Taylor, K. E. Summarizing multiple aspects of model performance in a single diagram. J. Geophys. Res. Atmos. 106, 7183–7192, https://doi.org/10.1029/2000jd900719 (2001).
    ADS  Article  Google Scholar 

    74.
    Wigley, T. M. MAGICC/SCENGEN 5.3: User manual (version 2). (NCAR, Boulder, Colorado, 2008).
    Google Scholar 

    75.
    Wilcox, R. R. The percentage bend correlation coefficient. Psychometrika 59, 601–616, https://doi.org/10.1007/BF02294395 (1994).
    Article  MATH  Google Scholar 

    76.
    Watterson, I. G. Non-dimensional measures of climate model performance. Int. J. Climatol. 16, 379-391, https://doi.org/10.1002/(Sici)1097-0088(199604)16:43.0.Co;2-U (1996).

    77.
    Willmott, C. J. On the validation of models. Phys. Geogr. 2, 184–194, https://doi.org/10.1080/02723646.1981.10642213 (2013).
    Article  Google Scholar 

    78.
    Santer, B. D., Wigley, T. M., Schlesinge, M. E. & Mitchell, J. F. B. Developing climate scenarios from equilibrium GCM results. (Max Planck Institute for Meteorology, Hamburg, Germany, 1990). More