More stories

  • in

    Transitional genomes and nutritional role reversals identified for dual symbionts of adelgids (Aphidoidea: Adelgidae)

    1.Szathmáry E, Smith JM. The major evolutionary transitions. Nature 1995;374:227–32.PubMed 
    Article 

    Google Scholar 
    2.West SA, Fisher RM, Gardner A, Kiers ET. Major evolutionary transitions in individuality. Proc Natl Acad Sci USA. 2015;112:10112–9.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    3.Moran NA. The coevolution of bacterial endosymbionts and phloem-feeding insects. Ann Mo Bot Gard. 2001;88:35–44.Article 

    Google Scholar 
    4.Bennett GM, Moran NA. Heritable symbiosis: the advantages and perils of an evolutionary rabbit hole. Proc Natl Acad Sci USA. 2015;112:10169–76.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    5.Gil R, Sabater-Munoz B, Latorre A, Silva FJ, Moya A. Extreme genome reduction in Buchnera spp.: toward the minimal genome needed for symbiotic life. Proc Natl Acad Sci USA. 2002;99:4454–8.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    6.Tamames J, Gil R, Latorre A, Pereto J, Silva FJ, Moya A. The frontier between cell and organelle: genome analysis of Candidatus Carsonella ruddii. BMC Evol Biol. 2007;7:181.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    7.Husnik F, Nikoh N, Koga R, Ross L, Duncan RP, Fujie M, et al. Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell 2013;153:1567–78.CAS 
    PubMed 
    Article 

    Google Scholar 
    8.Wilson ACC, Duncan RP. Signatures of host/symbiont genome coevolution in insect nutritional endosymbioses. Proc Natl Acad Sci USA. 2015;112:10255–61.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    9.von Dohlen CD, Kohler S, Alsop ST, McManus WR. Mealybug β-proteobacterial endosymbionts contain γ-proteobacterial symbionts. Nature 2001;412:433–6.Article 

    Google Scholar 
    10.McCutcheon JP, McDonald BR, Moran NA. Convergent evolution of metabolic roles in bacterial co-symbionts of insects. Proc Natl Acad Sci USA. 2009;106:15394–9.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    11.Gatehouse LN, Sutherland P, Forgie SA, Kaji R, Christeller JT. Molecular and histological characterization of primary (Betaproteobacteria) and secondary (Gammaproteobacteria) endosymbionts of three mealybug species. Appl Environ Microbiol. 2012;78:1187–97.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    12.Bennett GM, Moran NA. Small, smaller, smallest: the origins and evolution of ancient dual symbioses in a phloem-feeding insect. Genome Biol Evol. 2013;5:1675–88.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    13.Bressan A, Mulligan KL. Localization and morphological variation of three bacteriome-inhabiting symbionts within a planthopper of the genus Oliarus (Hemiptera: Cixiidae): Bacteriome-inhabiting symbionts in Oliarus filicicola. Environ Microbiol Rep. 2013;5:499–505.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    14.Bennett GM, Mao M. Comparative genomics of a quadripartite symbiosis in a planthopper host reveals the origins and rearranged nutritional responsibilities of anciently diverged bacterial lineages. Environ Microbiol. 2018;20:4461–72.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    15.von Dohlen CD, Spaulding U, Patch KB, Weglarz KM, Foottit RG, Havill NP, et al. Dynamic acquisition and loss of dual-obligate symbionts in the plant-sap-feeding Adelgidae (Hemiptera: Sternorrhyncha: Aphidoidea). Front Microbiol. 2017;8:1037.Article 

    Google Scholar 
    16.Mao M, Yang X, Poff K, Bennett G. Comparative genomics of the dual-obligate symbionts from the treehopper, Entylia carinata (Hemiptera: Membracidae), provide insight into the origins and evolution of an ancient symbiosis. Genome Biol Evol. 2017;9:1803–15.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    17.McCutcheon JP, Moran NA. Functional convergence in reduced genomes of bacterial symbionts spanning 200 my of evolution. Genome Biol Evol. 2010;2:708–18.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    18.McCutcheon JP, von Dohlen CD. An interdependent metabolic patchwork in the nested symbiosis of mealybugs. Curr Biol. 2011;21:1366–72.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    19.Sloan DB, Moran NA. Genome reduction and co-evolution between the primary and secondary bacterial symbionts of psyllids. Mol Biol Evol. 2012;29:3781–92.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    20.Hall AAG, Morrow JL, Fromont C, Steinbauer MJ, Taylor GS, Johnson SN, et al. Codivergence of the primary bacterial endosymbiont of psyllids versus host switches and replacement of their secondary bacterial endosymbionts. Environ Microbiol. 2016;18:2591–603.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    21.Tamas I, Klasson L, Canbäck B, Näslund AK, Eriksson A-S, Wernegreen JJ, et al. 50 million years of genomic stasis in endosymbiotic bacteria. Science 2002;296:2376–9.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    22.Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 2000;407:81–6.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    23.Moran NA, Tran P, Gerardo NM. Symbiosis and insect diversification: an ancient symbiont of sap-feeding insects from the bacterial phylum Bacteroidetes. Appl Environ Microbiol. 2005;71:8802–10.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    24.Gruwell ME, Hardy NB, Gullan PJ, Dittmar K. Evolutionary relationships among primary endosymbionts of the mealybug subfamily Phenacoccinae (Hemiptera: Coccoidea: Pseudococcidae). Appl Environ Microbiol. 2010;76:7521–5.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    25.Koga R, Moran NA. Swapping symbionts in spittlebugs: evolutionary replacement of a reduced genome symbiont. ISME J. 2014;8:1237–46.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    26.Mao M, Bennett GM. Symbiont replacements reset the co-evolutionary relationship between insects and their heritable bacteria. ISME J. 2020;14:1384–95.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    27.Braendle C, Miura T, Bickel R, Shingleton AW, Kambhampati S, Stern DL. Developmental origin and evolution of bacteriocytes in the aphid–Buchnera symbiosis. PLoS Biol. 2003;1:e21.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    28.Weglarz KM, Havill NP, Burke GR, von Dohlen CD. Partnering with a pest: genomes of hemlock woolly adelgid symbionts reveal atypical nutritional provisioning patterns in dual-obligate bacteria. Genome Biol Evol. 2018;10:1607–21.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    29.Toenshoff ER, Penz T, Narzt T, Collingro A, Schmitz-Esser S, Pfeiffer S, et al. Bacteriocyte-associated gammaproteobacterial symbionts of the Adelges nordmannianae/piceae complex (Hemiptera: Adelgidae). ISME J 2012;6:384–96.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    30.Toenshoff ER, Gruber D, Horn M. Co-evolution and symbiont replacement shaped the symbiosis between adelgids (Hemiptera: Adelgidae) and their bacterial symbionts. Environ Microbiol. 2012;14:1284–95.CAS 
    PubMed 
    Article 

    Google Scholar 
    31.Toenshoff ER, Szabó G, Gruber D, Horn M. The pine bark adelgid, Pineus strobi, contains two novel bacteriocyte-associated gammaproteobacterial symbionts. Appl Environ Microbiol. 2014;80:878–85.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    32.von Dohlen CD, Spaulding U, Shields K, Havill NP, Rosa C, Hoover K. Diversity of proteobacterial endosymbionts in hemlock woolly adelgid (Adelges tsugae) (Hemiptera: Adelgidae) from its native and introduced range. Environ Microbiol. 2013;15:2043–62.Article 
    CAS 

    Google Scholar 
    33.Havelka J, Danilov J, Rakauskas R. Relationships between aphid species of the family Adelgidae (Hemiptera Adelgoidea) and their endosymbiotic bacteria: a case study in Lithuania. Bull Insectology. 2021;74:1–10.
    Google Scholar 
    34.Favret C, Havill NP, Miller GL, Sano M, Victor B. Catalog of the adelgids of the world (Hemiptera, Adelgidae). Zookeys 2015;534:35–54.Article 

    Google Scholar 
    35.Blackman RL, Eastop VF Aphids on the world’s trees: an identification and information guide. 1994. CAB International.36.Havill NP, Foottit RG. Biology and evolution of Adelgidae. Ann Rev Ento. 2007;52:325–49.CAS 
    Article 

    Google Scholar 
    37.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 
    38.Zhang J, Kobert K, Flouri T, Stamatakis A. PEAR: a fast and accurate Illumina paired-end read mergeR. Bioinformatics 2014;30:614–20.CAS 
    PubMed 
    Article 

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

    Google Scholar 
    40.Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE. 2014;9:e112963.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    41.Kolmogorov M, Yuan J, Lin Y, Pevzner PA. Assembly of long, error-prone reads using repeat graphs. Nat Biotechnol. 2019;37:540–6.CAS 
    PubMed 
    Article 

    Google Scholar 
    42.Laetsch DR, Blaxter ML. BlobTools: Interrogation of genome assemblies. F1000Research. 2017;6:1287.Article 

    Google Scholar 
    43.Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 2011;27:578–9.CAS 
    PubMed 
    Article 

    Google Scholar 
    44.Chu C, Li X, Wu Y. GAPPadder: a sensitive approach for closing gaps on draft genomes with short sequence reads. BMC Genomics. 2019;20:426.PubMed 
    PubMed Central 
    Article 
    CAS 

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

    Google Scholar 
    46.Varani AM, Siguier P, Gourbeyre E, Charneau V, Chandler M. ISsaga is an ensemble of web-based methods for high throughput identification and semi-automatic annotation of insertion sequences in prokaryotic genomes. Genome Biol. 2011;12:R30.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    47.Karp PD, Billington R, Caspi R, Fulcher CA, Latendresse M, Kothari A, et al. The BioCyc collection of microbial genomes and metabolic pathways. Brief Bioinform. 2019;20:1085–93.CAS 
    PubMed 
    Article 

    Google Scholar 
    48.Karp PD, Ong WK, Paley S, Billington R, Caspi R, Fulcher C, et al. The EcoCyc database. EcoSal Plus. 2018;8:10.1128.Article 

    Google Scholar 
    49.Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res. 2007;35:W182–5.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    50.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 
    51.Tatusov RL, Galperin MY, Natale DA, Koonin EV. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res. 2000;28:33–36.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    52.Wang Y, Tang H, DeBarry JD, Tan X, Li J, Wang X, et al. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 2012;40:e49–e49.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    53.Xu L, Dong Z, Fang L, Luo Y, Wei Z, Guo H, et al. OrthoVenn2: a web server for whole-genome comparison and annotation of orthologous clusters across multiple species. Nucleic Acids Res. 2019;47:W52–W58.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    54.Xu Y, Bi C, Wu G, Wei S, Dai X, Yin T, et al. VGSC: a web-based vector graph toolkit of genome synteny and collinearity. Biomed Res Int. 2016;2016:7823429.PubMed 
    PubMed Central 

    Google Scholar 
    55.Adeolu M, Alnajar S, Naushad S, S Gupta R. Genome-based phylogeny and taxonomy of the ‘Enterobacteriales’: proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. Int J Syst Evol Microbiol. 2016;66:5575–99.CAS 
    PubMed 
    Article 

    Google Scholar 
    56.Guy L. phyloSkeleton: taxon selection, data retrieval and marker identification for phylogenomics. Bioinformatics 2017;33:1230–2.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    57.Eddy SR. Accelerated profile HMM searches. PLoS Comput Biol. 2011;7:e1002195.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    58.Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30:772–80.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    59.Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009;25:1972–3.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    60.Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014;30:1312–3.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    61.Lartillot N, Rodrigue N, Stubbs D, Richer J. PhyloBayes MPI: phylogenetic reconstruction with infinite mixtures of profiles in a parallel environment. Syst Biol. 2013;62:611–5.CAS 
    PubMed 
    Article 

    Google Scholar 
    62.Husník F, Chrudimský T, Hypša V. Multiple origins of endosymbiosis within the Enterobacteriaceae (γ-Proteobacteria): convergence of complex phylogenetic approaches. BMC Biology. 2011;9:1–17.Article 

    Google Scholar 
    63.Emms DM, Kelly S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 2019;20:238.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    64.Hesse C, Schulz F, Bull CT, Shaffer BT, Yan Q, Shapiro N, et al. Genome-based evolutionary history of Pseudomonas spp. Environ Microbiol. 2018;20:2142–59.CAS 
    PubMed 
    Article 

    Google Scholar 
    65.Burke GR, Normark BB, Favret C, Moran NA. Evolution and diversity of facultative symbionts from the aphid subfamily Lachninae. Appl Environ Microbiol. 2009;75:5328–35.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    66.Manzano‐Marín A, Szabó G, Simon J, Horn M, Latorre A. Happens in the best of subfamilies: establishment and repeated replacements of co‐obligate secondary endosymbionts within Lachninae aphids: co-obligate endosymbiont dynamics in the Lachninae. Environ Microbiol. 2017;19:393–408.PubMed 
    Article 
    CAS 

    Google Scholar 
    67.Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000;17:540–52.CAS 
    PubMed 
    Article 

    Google Scholar 
    68.ggplot2. Create elegant data visualisations using the grammar of graphics. https://ggplot2.tidyverse.org/. Accessed Apr 2021.69.Manzano-Marín A, Oceguera-Figueroa A, Latorre A, Jiménez-García LF, Moya A. Solving a bloody mess: B-vitamin independent metabolic convergence among gammaproteobacterial obligate endosymbionts from blood-feeding arthropods and the leech Haementeria officinalis. Genome Biol Evol. 2015;7:2871–84.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    70.Janda JM, Abbott SL. The genus Hafnia: from soup to nuts. Clin Microbiol Rev. 2006;19:12–18.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    71.Szabó G, Schulz F, Manzano-Marín A, Toenshoff ER, Horn M Evolutionary recent dual obligatory symbiosis among adelgids indicates a transition between fungus and insect associated lifestyles. bioRxiv. 2020; e-pub ahead of print 16 October 2020; https://doi.org/10.1101/2020.10.16.342642.72.Wilson ACC, Ashton PD, Calevro F, Charles H, Colella S, Febvay G, et al. Genomic insight into the amino acid relations of the pea aphid, Acyrthosiphon pisum, with its symbiotic bacterium Buchnera aphidicola. Insect Mol Biol. 2010;19:249–58.CAS 
    PubMed 
    Article 

    Google Scholar 
    73.Sloan DB, Nakabachi A, Richards S, Qu J, Murali SC, Gibbs RA, et al. Parallel histories of horizontal gene transfer facilitated extreme reduction of endosymbiont genomes in sap-feeding insects. Mol Biol Evol. 2014;31:857–71.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    74.Hansen AK, Moran NA. The impact of microbial symbionts on host plant utilization by herbivorous insects. Mol Ecol. 2014;23:1473–96.PubMed 
    Article 

    Google Scholar 
    75.Manzano-Marı́n A, Coeur d’acier A, Clamens A-L, Orvain C, Cruaud C, Barbe V, et al. Serial horizontal transfer of vitamin-biosynthetic genes enables the establishment of new nutritional symbionts in aphids’ di-symbiotic systems. ISME J. 2020;14:259–73.Article 
    CAS 

    Google Scholar 
    76.Lo W-S, Huang Y-Y, Kuo C-H. Winding paths to simplicity: genome evolution in facultative insect symbionts. FEMS Microbiol Rev. 2016;40:855–74.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    77.Toh H, Weiss BL, Perkin SAH, Yamashita A, Oshima K, Hattori M, et al. Massive genome erosion and functional adaptations provide insights into the symbiotic lifestyle of Sodalis glossinidius in the tsetse host. Genome Res. 2006;16:149–56.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    78.Cole ST, Eiglmeier K, Parkhill J, James KD, Thomson NR, Wheeler PR, et al. Massive gene decay in the leprosy bacillus. Nature 2001;409:1007–11.CAS 
    PubMed 
    Article 

    Google Scholar 
    79.Moran NA, Bennett GM. The tiniest tiny genomes. Annu Rev Microbiol. 2014;68:195–215.CAS 
    PubMed 
    Article 

    Google Scholar 
    80.Bennett GM, McCutcheon JP, MacDonald BR, Romanovicz D, Moran NA. Differential genome evolution between companion symbionts in an insect-bacterial symbiosis. mBio 2014;5:e01697–14.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    81.Degnan PH, Ochman H, Moran NA. Sequence conservation and functional constraint on intergenic spacers in reduced genomes of the obligate symbiont Buchnera. PLoS Genet. 2011;7:e1002252.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    82.Van Leuven JT, Meister RC, Simon C, McCutcheon JP. Sympatric speciation in a bacterial endosymbiont results in two genomes with the functionality of one. Cell 2014;158:1270–80.PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    83.Gomez-Valero L. The evolutionary fate of nonfunctional DNA in the bacterial endosymbiont Buchnera aphidicola. Mol Biol Evol. 2004;21:2172–81.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    84.Manzano-Marı́n A, Coeur d’acier A, Clamens A-L, Orvain C, Cruaud C, Barbe V, et al. A freeloader? The highly eroded yet large genome of the Serratia symbiotica symbiont of Cinara strobi. Genome Biol Evol. 2018;10:2178–89.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    85.Santos-Garcia D, Silva FJ, Morin S, Dettner K, Kuechler SM. The all-rounder Sodalis: a new bacteriome-associated endosymbiont of the lygaeoid bug Henestaris halophilus (Heteroptera: Henestarinae) and a critical examination of its evolution. Genome Biol Evol. 2017;9:2893–910.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    86.Havill NP, Foottit RG, von Dohlen CD. Evolution of host specialization in the Adelgidae (Insecta: Hemiptera) inferred from molecular phylogenetics. Mol Phylogenet. 2007;44:357–70.CAS 
    Article 

    Google Scholar 
    87.Manzano-Marı́n A, Latorre A. Snapshots of a shrinking partner: genome reduction in Serratia symbiotica. Sci Rep. 2016;6:32590.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    88.Monnin D, Jackson R, Kiers ET, Bunker M, Ellers J, Henry LM. Parallel evolution in the integration of a co-obligate aphid symbiosis. Curr Biol. 2020;30:1949–57. e6CAS 
    PubMed 
    Article 

    Google Scholar 
    89.Husnik F, McCutcheon JP. Repeated replacement of an intrabacterial symbiont in the tripartite nested mealybug symbiosis. Proc Natl Acad Sci USA. 2016;113:e5416–24.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    90.Moran NA, McCutcheon JP, Nakabachi A. Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet. 2008;42:165–90.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    91.Degnan PH, Leonardo TE, Cass BN, Hurwitz B, Stern D, Gibbs RA, et al. Dynamics of genome evolution in facultative symbionts of aphids. Environ Microbiol. 2010;12:2060–9.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    92.Burke GR, Moran NA. Massive genomic decay in Serratia symbiotica, a recently evolved symbiont of aphids. Genome Biol Evol. 2011;3:195–208.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    93.Munson MA, Baumann P, Clark MA, Baumann L, Moran NA, Voegtlin DJ, et al. Evidence for the establishment of aphid-eubacterium endosymbiosis in an ancestor of four aphid families. J Bacteriol. 1991;173:6321–4.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    94.Moran NA, Munson MA, Baumann P, Ishikawa H. A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts. Proc R Soc B 1993;253:167–71.Article 

    Google Scholar 
    95.Kuechler SM, Gibbs G, Burckhardt D, Dettner K, Hartung V. Diversity of bacterial endosymbionts and bacteria-host co-evolution in Gondwanan relict moss bugs (Hemiptera: Coleorrhyncha: Peloridiidae). Environ Microbiol. 2013;15:2031–42.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    96.Thao ML, Moran NA, Abbot P, Brennan EB, Burckhardt DH, Baumann P. Cospeciation of psyllids and their primary prokaryotic endosymbionts. Appl Environ Microbiol. 2000;66:2898–905.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    97.Thao ML, Baumann P. Evolutionary relationships of primary prokaryotic endosymbionts of whiteflies and their hosts. Appl Environ Microbiol. 2004;70:3401–6.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    98.Meseguer AS, Manzano-Marín A, Coeur d’Acier A, Clamens AL, Godefroid M, Jousselin E. Buchnera has changed flatmate but the repeated replacement of co-obligate symbionts is not associated with the ecological expansions of their aphid hosts. Mol Ecol. 2017;26:2363–78.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    99.McCutcheon JP, Moran NA. Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. Proc Natl Acad Sci USA. 2007;104:19392–7.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    100.Rao Q, Rollat-Farnier PA, Zhu DT, Santos-Garcia D, Silva FJ, Moya A, et al. Genome reduction and potential metabolic complementation of the dual endosymbionts in the whitefly Bemisia tabaci. BMC Genomics. 2015;16:226.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    101.Rosenblueth M, Sayavedra L, Sámano-Sánchez H, Roth A, Martínez-Romero E. Evolutionary relationships of flavobacterial and enterobacterial endosymbionts with their scale insect hosts (Hemiptera: Coccoidea). J Evol Biol. 2012;25:2357–68.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    102.Michalik K, Szklarzewicz T, Kalandyk-Kołodziejczyk M, Jankowska W, Michalik A. Bacteria belonging to the genus Burkholderia are obligatory symbionts of the eriococcids Acanthococcus aceris Signoret, 1875 and Gossyparia spuria (Modeer, 1778) (Insecta, Hemiptera, Coccoidea). Arthropod Struct Dev. 2016;45:265–72.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    103.Van Ham RC, Kamerbeek J, Palacios C, Rausell C, Abascal F, Bastolla U, et al. Reductive genome evolution in Buchnera aphidicola. Proc Natl Acad Sci USA. 2003;100:581–6.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    104.Vogel KJ, Moran NA. Effect of host genotype on symbiont titer in the aphid-Buchnera symbiosis. Insects 2011;2:423–34.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    105.Bennett GM, McCutcheon JP, McDonald BR, Moran NA. Lineage-specific patterns of genome deterioration in obligate symbionts of sharpshooter leafhoppers. Genome Biol Evol. 2015;8:296–301.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    106.Havill NP, Griffin BP, Andersen JC, Foottit RG, Justesen MJ, Caccone A, et al. Species delimitation and invasion history of the balsam woolly adelgid, Adelges (Dreyfusia) piceae (Hemiptera: Aphidoidea: Adelgidae), species complex. Syst Entomol. 2021;46:186–204.Article 

    Google Scholar  More

  • in

    Selective feeding in Southern Ocean key grazers—diet composition of krill and salps

    1.Pakhomov, E. A., Froneman, P. W. & Perissinotto, R. Salp/krill interactions in the Southern Ocean: Spatial segregation and implications for the carbon flux. Deep Sea Res. II 49, 1881–1907 (2002).CAS 
    Article 

    Google Scholar 
    2.Steinberg, D. K. et al. Long-term (1993–2013) changes in macrozooplankton off the Western Antarctic Peninsula. Deep Sea Res. I 101, 54–70 (2015).Article 

    Google Scholar 
    3.Whitehouse, M. J. et al. Role of krill versus bottom-up factors in controlling phytoplankton biomass in the northern Antarctic waters of South Georgia. Mar. Ecol. Prog. Ser. 393, 69–82 (2009).CAS 
    Article 

    Google Scholar 
    4.Tarling, G. A. & Fielding, S. in Biology and Ecology of Antarctic krill (ed Siegel, V.) 279–319 (Springer International Publishing, 2016).5.Henschke, N., Everett, J. D., Richardson, A. J. & Suthers, I. M. Rethinking the role of salps in the ocean. Trends Ecol. Evol. 31, 720–733 (2016).PubMed 
    Article 

    Google Scholar 
    6.Cavan, E. L. et al. The importance of Antarctic krill in biogeochemical cycles. Nat. Commun. 10, 4742 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    7.Belcher, A. et al. Krill faecal pellets drive hidden pulses of particulate organic carbon in the marginal ice zone. Nat. Commun. 10, 889 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    8.Phillips, B., Kremer, P. & Madin, L. P. Defecation by Salpa thompsoni and its contribution to vertical flux in the Southern Ocean. Mar. Biol. 156, 455–467 (2009).Article 

    Google Scholar 
    9.Siegel, V. & Watkins, J. L. in Biology and Ecology of Antarctic krill (ed Siegel, V.) 21–100 (Springer International Publishing, 2016).10.Atkinson, A. et al. Krill (Euphausia superba) distribution contracts southward during rapid regional warming. Nat. Clim. Change 9, 142–147 (2019).Article 

    Google Scholar 
    11.Vaughan, D. G. et al. Recent rapid regional climate warming on the Antarctic Peninsula. Clim. Change 60, 243–274 (2003).Article 

    Google Scholar 
    12.Ducklow, H. W. et al. Marine pelagic ecosystems: the West Antarctic Peninsula. Philos. Trans. R. Soc. B. 362, 67–94 (2007).Article 

    Google Scholar 
    13.Montes-Hugo, M. et al. Recent changes in phytoplankton communities associated with rapid regional climate change along the Western Antarctic Peninsula. Science 323, 1470–1473 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    14.Clarke, A. et al. Climate change and the marine ecosystem of the western Antarctic Peninsula. Philos. T. R. Soc., B 362, 149–166 (2007).Article 

    Google Scholar 
    15.Atkinson, A., Siegel, V., Pakhomov, E. & Rothery, P. Long-term decline in krill stock and increase in salps within the Southern Ocean. Nature 432, 100–103 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    16.Loeb, V. et al. Effects of sea-ice extent and krill or salp dominance on the Antarctic food web. Nature 387, 897–900 (1997).CAS 
    Article 

    Google Scholar 
    17.Flores, H. et al. Impact of climate change on Antarctic krill. Mar. Ecol. Prog. Ser. 458, 1–19 (2012).Article 

    Google Scholar 
    18.Cox, M. J. et al. No evidence for a decline in the density of Antarctic krill Euphausia superba Dana, 1850, in the Southwest Atlantic sector between 1976 and 2016. J. Crust. Biol. 38, 656–661 (2018).19.Foxton, P. The Distribution and Life-history of Salpa thompsoni Foxton with observations on a Related Species, Salpa gerlachei Foxton (The University Press, 1966).20.Bernard, K. S., Steinberg, D. K. & Schofield, O. M. E. Summertime grazing impact of the dominant macrozooplankton off the Western Antarctic Peninsula. Deep Sea Res. I 62, 111–122 (2012).Article 

    Google Scholar 
    21.Condon, R. H. et al. Jellyfish blooms result in a major microbial respiratory sink of carbon in marine systems. Proc. Natl Acad. Sci. 108, 10225–10230 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    22.Meyer, M. A. & Elsayed, S. Z. Grazing of Euphausia superba Dana on natural phytoplankton populations. Polar Biol. 1, 193–197 (1983).Article 

    Google Scholar 
    23.Haberman, K. L., Ross, R. M. & Quetin, L. B. Diet of the Antarctic krill (Euphausia superba Dana): II. Selective grazing in mixed phytoplankton assemblages. J. Exp. Mar. Biol. Ecol. 283, 97–113 (2003).Article 

    Google Scholar 
    24.Schmidt, K. & Atkinson, A. in Biology and Ecology of Antarctic krill (ed Siegel, V.) 175–224 (Springer International Publishing, 2016).25.Andersen, V. in The Biology of Pelagic Tunicates (ed Bone, Q.) 125–137 (Oxford University Press, 1998).26.Mitra, A. et al. Bridging the gap between marine biogeochemical and fisheries sciences; configuring the zooplankton link. Prog. Oceanogr. 129, 176–199 (2014).Article 

    Google Scholar 
    27.Sailley, S. F., Polimene, L., Mitra, A., Atkinson, A. & Allen, J. I. Impact of zooplankton food selectivity on plankton dynamics and nutrient cycling. J. Plankton Res. 37, 519–529 (2015).CAS 
    Article 

    Google Scholar 
    28.Hamner, W. M., Hamner, P. P., Strand, S. W. & Gilmer, R. W. Behavior of Antarctic krill, Euphausia superba: Chemoreception, feeding, schooling, and molting. Science 220, 433–435 (1983).CAS 
    PubMed 
    Article 

    Google Scholar 
    29.DeMott, W. R. in Behavioural Mechanisms of Food Selection (ed Hughes, R. N.) 569–594 (Springer, 1990).30.Le Fèvre, J., Legendre, L. & Rivkin, R. B. Fluxes of biogenic carbon in the Southern Ocean: Roles of large microphagous zooplankton. J. Mar. Syst. 17, 325–345 (1998).Article 

    Google Scholar 
    31.Moline, M. A., Claustre, H., Frazer, T. K., Schofield, O. & Vernet, M. Alteration of the food web along the Antarctic Peninsula in response to a regional warming trend. Glob. Change Biol. 10, 1973–1980 (2004).Article 

    Google Scholar 
    32.Frischer, M. E. et al. Selective feeding and linkages to the microbial food web by the doliolid Dolioletta gegenbauri. Limnol. Oceanogr. 66, 1993–2010 (2021).Article 

    Google Scholar 
    33.Dadon-Pilosof, A., Lombard, F., Genin, A., Sutherland, K. R. & Yahel, G. Prey taxonomy rather than size determines salp diets. Limnol. Oceanogr. 64, 1996–2010 (2019).Article 

    Google Scholar 
    34.Metfies, K., Nicolaus, A., von Harbou, L., Bathmann, U. & Peeken, I. Molecular analyses of gut contents: elucidating the feeding of co-occurring salps in the Lazarev Sea from a different perspective. Antarct. Sci. 26, 5545–5553 (2014).Article 

    Google Scholar 
    35.Cleary, A. C., Durbin, E. G. & Casas, M. C. Feeding by Antarctic krill Euphausia superba in the West Antarctic Peninsula: differences between fjords and open waters. Mar. Ecol. Prog. Ser. 595, 39–54 (2018).CAS 
    Article 

    Google Scholar 
    36.Pompanon, F. et al. Who is eating what: Diet assessment using next generation sequencing. Mol. Ecol. 21, 1931–1950 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    37.Passmore, A. J. et al. DNA as a dietary biomarker in Antarctic krill, Euphausia superba. Mar. Biotechnol. 8, 686–696 (2006).CAS 
    Article 

    Google Scholar 
    38.von Harbou, L. et al. Salps in the Lazarev Sea, Southern Ocean: I. Feeding dynamics. Mar. Biol. 158, 2009–2026 (2011).Article 

    Google Scholar 
    39.Vernet, M. et al. Primary production throughout austral fall, during a time of decreasing daylength in the western Antarctic Peninsula. Mar. Ecol. Prog. Ser. 452, 45–61 (2012).CAS 
    Article 

    Google Scholar 
    40.Moreau, S. et al. Variability of the microbial community in the western Antarctic Peninsula from late fall to spring during a low ice cover year. Polar Biol. 33, 1599–1614 (2010).Article 

    Google Scholar 
    41.Selz, V. et al. Distribution of Phaeocystis antarctica-dominated sea ice algal communities and their potential to seed phytoplankton across the western Antarctic Peninsula in spring. Mar. Ecol. Prog. Ser. 586, 91–112 (2018).CAS 
    Article 

    Google Scholar 
    42.Nichols, D. S., Nichols, P. D. & Sullivan, C. W. Fatty acid, sterol and hydrocarbon composition of Antarctic sea ice diatom communities during the spring bloom in McMurdo Sound. Antarct. Sci. 5, 271–278 (1993).Article 

    Google Scholar 
    43.Fahl, K. & Kattner, G. Lipid Content and fatty acid composition of algal communities in sea-ice and water from the Weddell Sea (Antarctica). Polar Biol. 13, 405–409 (1993).Article 

    Google Scholar 
    44.Boyd, C. M., Heyraud, M. & Boyd, C. N. Feeding of the Antarctic krill Euphausia superba. J. Crust. Biol. 4, 123–141 (1984).Article 

    Google Scholar 
    45.Bone, Q., Carré, C. & Chang, P. Tunicate feeding filters. J. Mar. Biol. Assoc. U. K. 83, 907–919 (2003).Article 

    Google Scholar 
    46.Nelson, M. M., Phleger, C. F., Mooney, B. D. & Nichols, P. D. Lipids of gelatinous Antarctic zooplankton: Cnidaria and Ctenophora. Lipids 35, 551–559 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    47.Huntley, M. E., Sykes, P. F. & Marin, V. Biometry and trophodynamics of Salpa thompsoni Foxton (Tunicata: Thaliacea) near the Antarctic Peninsula in austral summer, 1983–1984. Polar Biol. 10, 59–70 (1989).Article 

    Google Scholar 
    48.Hopkins, T. L. Food web of an Antarctic midwater ecosystem. Mar. Biol. 89, 197–212 (1985).Article 

    Google Scholar 
    49.Paffenhöfer, G. A. & Köster, M. Digestion of diatoms by planktonic copepods and doliolids. Mar. Ecol. Prog. Ser. 297, 303–310 (2005).Article 

    Google Scholar 
    50.von Harbou, L. Trophodynamics of Salps in the Atlantic Southern Ocean. PhD thesis, University of Bremen (2009).51.Hargraves, P. E. The ebridian flagellates Ebria and Hermesinum. Plankton Biol. Ecol. 49, 9–16 (2002).
    Google Scholar 
    52.Cavan, E. L. et al. Attenuation of particulate organic carbon flux in the Scotia Sea, Southern Ocean, is controlled by zooplankton fecal pellets. Geophys. Res. Lett. 42, 821–830 (2015).CAS 
    Article 

    Google Scholar 
    53.Smith, K. L. Jr. et al. Large salp bloom export from the upper ocean and benthic community response in the abyssal northeast Pacific: day to week resolution. Limnol. Oceanogr. 59, 745–757 (2014).CAS 
    Article 

    Google Scholar 
    54.Cadée, G. C., González, H. & Schnack-Schiel, S. B. Krill diet affects faecal string settling. Polar Biol. 12, 75–80 (1992).
    Google Scholar 
    55.Ploug, H., Iversen, M. H., Koski, M. & Buitenhuis, E. T. Production, oxygen respiration rates, and sinking velocity of copepod fecal pellets: Direct measurements of ballasting by opal and calcite. Limnol. Oceanogr. 53, 469–476 (2008).CAS 
    Article 

    Google Scholar 
    56.Atkinson, A., Schmidt, K., Fielding, S., Kawaguchi, S. & Geissler, P. A. Variable food absorption by Antarctic krill: Relationships between diet, egestion rate and the composition and sinking rates of their fecal pellets. Deep Sea Res. II 59-60, 147–158 (2012).CAS 
    Article 

    Google Scholar 
    57.Schmidt, K., Atkinson, A., Pond, D. W. & Ireland, L. C. Feeding and overwintering of Antarctic krill across its major habitats: The role of sea ice cover, water depth, and phytoplankton abundance. Limnol. Oceanogr. 59, 17–36 (2014).Article 

    Google Scholar 
    58.Cripps, G. C., Watkins, J. L., Hill, H. J. & Atkinson, A. Fatty acid content of Antarctic krill Euphausia superba at South Georgia related to regional populations and variations in diet. Mar. Ecol. Prog. Ser. 181, 177–188 (1999).CAS 
    Article 

    Google Scholar 
    59.Schmidt, K., Atkinson, A., Petzke, K.-J., Voss, M. & Pond, D. W. Protozoans as a food source for Antarctic krill, Euphausia superba: Complementary insights from stomach content, fatty acids, and stable isotopes. Limnol. Oceanogr. 51, 2409–2427 (2006).CAS 
    Article 

    Google Scholar 
    60.Hagen, W., Van Vleet, E. S. & Kattner, G. Seasonal lipid storage as overwintering strategy of Antarctic krill. Mar. Ecol. Prog. Ser. 134, 85–89 (1996).CAS 
    Article 

    Google Scholar 
    61.Kawaguchi, S. & Takahashi, Y. Antarctic krill (Euphausia superba Dana) eat salps. Polar Biol. 16, 479–481 (1996).
    Google Scholar 
    62.Clarke, L. J., Bestley, S., Bissett, A. & Deagle, B. E. A globally distributed Syndiniales parasite dominates the Southern Ocean micro-eukaryote community near the sea-ice edge. ISME J. 13, 734–737 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    63.Coats, D. W. & Park, M. G. Parasitism of photosynthetic dinoflagellates by three strains of Amoebophrya (Dinophyta): Parasite survival, infectivity, generation time, and host specificity. J. Phycol. 38, 520–528 (2002).Article 

    Google Scholar 
    64.Sutherland, K. R., Madin, L. P. & Stocker, R. Filtration of submicrometer particles by pelagic tunicates. Proc. Natl Acad. Sci. 107, 15129–15134 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    65.Gómez-Gutiérrez, J. & Morales-Avila, J. R. in Biology and Ecology of Antarctic krill (ed Siegel, V.) 351–387 (Springer International Publishing, 2006).66.Cleary, A. C., Casas, M. C., Durbin, E. G. & Gómez-Gutiérrez, J. Parasites in Antarctic krill guts inferred from DNA sequences. Antarct. Sci. 31, 16–22 (2019).Article 

    Google Scholar 
    67.Zamora-Terol, S., Novotny, A. & Winder, M. Molecular evidence of host-parasite interactions between zooplankton and Syndiniales. Aquat. Ecol. 55, 125–134 (2021).CAS 
    Article 

    Google Scholar 
    68.Kawaguchi, S., Ichii, T. & Naganobu, M. Do krill and salps compete? Contrary evidence from the krill fisheries. CCAMLR Sci. 5, 205–216 (1998).
    Google Scholar 
    69.Fadeev, E. et al. Microbial communities in the east and west Fram Strait during sea ice melting season. Front. Mar. Sci. 5, 429 (2018).Article 

    Google Scholar 
    70.Vestheim, H. & Jarman, S. N. Blocking primers to enhance PCR amplification of rare sequences in mixed samples – a case study on prey DNA in Antarctic krill stomachs. Front. Zool. 5, 12 (2008).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    71.Ludwig, W. et al. ARB: a software environment for sequence data. Nucleic Acids Res. 32, 1363–1371 (2004).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    72.R Foundation for Statistical Computing. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2019).73.Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    74.Callahan, B. DADA2 Pipeline Tutorial (1.16), available online: https://benjjneb.github.io/dada2/tutorial.html. Accessed: 3 Feb 2020.75.Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J. 17, 3 (2011).Article 

    Google Scholar 
    76.Guillou, L. et al. The protist ribosomal reference database (PR2): A catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Res. 41, D597–D604 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    77.Gong, W. & Marchetti, A. Estimation of 18S gene copy number in marine eukaryotic plankton using a next-generation sequencing approach. Front. Mar. Sci. 6, 219 (2019).Article 

    Google Scholar 
    78.Metfies, K. et al. Uncovering the intricacies of microbial community dynamics at Helgoland Roads at the end of a spring bloom using automated sampling and 18S meta-barcoding. PLoS ONE 15, e0233921 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    79.Catlett, D. et al. Evaluation of accuracy and precision in an amplicon sequencing workflow for marine protist communities. Limnol. Oceanogr. Methods 18, 20–40 (2019).Article 

    Google Scholar 
    80.Kattner, G. & Fricke, H. S. G. Simple gas-liquid-chromatographic method for the simultaneous determination of fatty-acids and alcohols in wax esters of marine organisms. J. Chromatogr. 361, 263–268 (1986).CAS 
    Article 

    Google Scholar 
    81.Gloor, G. B., Macklaim, J. M., Pawlowsky-Glahn, V. & Egozcue, J. J. Microbiome datasets are compositional: And this is not optional. Front. Microbiol. 8, 2224 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    82.Palarea-Albaladejo, J. & Martín-Fernández, J. A. zCompositions—R package for multivariate imputation of left-censored data under a compositional approach. Chemometrics Intell. Lab. Syst. 143, 85–96 (2015).CAS 
    Article 

    Google Scholar 
    83.Fernandes, A. D., Macklaim, J. M., Linn, T. G., Reid, G. & Gloor, G. B. ANOVA-Like differential expression (ALDEx) analysis for mixed population RNA-Seq. PLoS ONE 8, e67019 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    84.Quinn, T. P., Richardson, M. F., Lovell, D. & Crowley, T. M. propr: an R-package for identifying proportionally abundant features using compositional data analysis. Sci. Rep. 7, 16252 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    85.Bian, G. et al. The gut microbiota of healthy aged chinese is similar to that of the healthy young. mSphere 2, e00327–00317 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    86.Gloor, G. B. & Reid, G. Compositional analysis: A valid approach to analyze microbiome high-throughput sequencing data. Can. J. Microbiol. 62, 692–703 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    87.Borstein, S. R. dietr: An R package for calculating fractional trophic levels from quantitative and qualitative diet data. Hydrobiologia 847, 4285–4294 (2020).Article 

    Google Scholar 
    88.Lechowicz, M. J. The sampling characteristics of electivity indices. Oecologia 52, 22–30 (1982).PubMed 
    Article 

    Google Scholar 
    89.Dalsgaard, J., St John, M., Kattner, G., Muller-Navarra, D. & Hagen, W. Fatty acid trophic markers in the pelagic marine environment. Adv. Mar. Biol. 46, 225–340 (2003).PubMed 
    Article 

    Google Scholar 
    90.Graeve, M., Kattner, G. & Hagen, W. Diet-induced changes in the fatty acid composition of Arctic herbivorous copepods: Experimental evidence of trophic markers. J. Exp. Mar. Biol. Ecol. 182, 97–110 (1994).CAS 
    Article 

    Google Scholar 
    91.Kharlamenko, V. I., Zhukova, N. V., Khotimchenko, S. V., Svetashev, V. I. & Kamenev, G. M. Fatty acids as markers of food sources in a shallow-water hydrothermal ecosystem (Kraternaya Bight, Yankich Island, Kurile Islands). Mar. Ecol. Prog. Ser. 120, 231–241 (1995).CAS 
    Article 

    Google Scholar 
    92.Greenacre, M. Compositional Data Analysis in Practice (CRC Press, Taylor & Francis Group, 2018).93.Suh, H.-L. & Nemoto, T. Comparative morphology of filtering structure of five species of Euphausia (Euphausiacea, Crustacea) from the Antarctic Ocean. Proc. NIPR Symp. Polar Biol. 1, 72–83 (1987).
    Google Scholar 
    94.Alldredge, A. L. & Madin, L. P. Pelagic tunicates: unique herbivores in the marine plankton. Bioscience 32, 655–663 (1982).Article 

    Google Scholar 
    95.Kelly, P. S. The Ecological Role of Salpa Thompsoni in the Kerguelen Plateau Region of the Southern Ocean: A First Comprehensive Evaluation. PhD thesis, University of Tasmania (2019).96.Ericson, J. A. et al. Seasonal and interannual variations in the fatty acid composition of adult Euphausia superba Dana, 1850 (Euphausiacea) samples derived from the Scotia Sea krill fishery. J. Crust. Biol. 38, 662–672 (2018).
    Google Scholar 
    97.Martin, D. L., Ross, R. M., Quetin, L. B. & Murray, A. E. Molecular approach (PCR-DGGE) to diet analysis in young Antarctic krill Euphausia superba. Mar. Ecol. Prog. Ser. 319, 155–165 (2006).CAS 
    Article 

    Google Scholar 
    98.Matsuoka, K. et al. Quantarctica, an integrated mapping environment for Antarctica, the Southern Ocean, and sub-Antarctic islands. Environ. Model. Softw. 140, 105015 (2021).Article 

    Google Scholar  More

  • in

    Historical land use has long-term effects on microbial community assembly processes in forest soils

    1.Fierer N. Embracing the unknown: disentangling the complexities of the soil microbiome. Nat Rev Microbiol. 2017;15:579–90.CAS 
    Article 

    Google Scholar 
    2.Ellis EC. Anthropogenic transformation of the terrestrial biosphere. Philos Trans R Soc A-Math Phys Eng Sci. 2011;369:1010–35.Article 

    Google Scholar 
    3.Jangid K, Williams MA, Franzluebbers AJ, Schmidt TM, Coleman DC, Whitman WB. Land-use history has a stronger impact on soil microbial community composition than aboveground vegetation and soil properties. Soil Biol Biochem. 2011;43:2184–93.CAS 
    Article 

    Google Scholar 
    4.Ramirez KS, Lauber CL, Knight R, Bradford MA, Fierer N. Consistent effects of nitrogen fertilization on soil bacterial communities in contrasting systems. Ecology. 2010;91:3463–70.Article 

    Google Scholar 
    5.Hermans SM, Taylor M, Grelet G, Curran-Cournane F, Buckley HL, Handley KM, et al. From pine to pasture: land use history has long-term impacts on soil bacterial community composition and functional potential. FEMS Microbiol Ecol. 2020;96:1–12.6.Keiser AD, Knoepp JD, Bradford MA. Disturbance decouples biogeochemical cycles across forests of the Southeastern US. Ecosystems. 2016;19:50–61.Article 

    Google Scholar 
    7.Goss-Souza D, Mendes LW, Borges CD, Baretta D, Tsai SM, Rodrigues J. Soil microbial community dynamics and assembly under long-term land use change. FEMS Microbiol Ecol. 2017;93:1–13.8.Tripathi BM, Stegen JC, Kim M, Dong K, Adams JM, Lee YK. Soil pH mediates the balance between stochastic and deterministic assembly of bacteria. The ISME Journal. 2018;12:1072–83.CAS 
    Article 

    Google Scholar 
    9.Barnett SE, Youngblut ND, Buckley DH. Soil characteristics and land-use drive bacterial community assembly patterns. FEMS Microbiol Ecol. 2020;96:1–11.10.Osburn ED, McBride SG, Aylward FO, Badgley BD, Strahm BD, Knoepp JD, et al. Soil bacterial and fungal communities exhibit distinct long-term responses to disturbance in temperate forests. Front Microbiol. 2019;10:2872.11.Pruesse E, Peplies J, Glöckner FO. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics. 2012;28:1823–9.CAS 
    Article 

    Google Scholar 
    12.Mirarab S, Nguyen N, Guo S, Wang LS, Kim J, Warnow T, et al. PASTA: ultra-large multiple sequence alignment for nucleotide and amino-acid sequences. J Comput Biol. 2014;22:377–86.Article 

    Google Scholar 
    13.Wang P, Li SP, Yang X, Zhou J, Shu W, Jiang L. Mechanisms of soil bacterial and fungal community assembly differ among and within islands. Environ Microbiol. 2020;22:1559–71.Article 

    Google Scholar 
    14.Price MN, Dehal PS, Arkin AP. FastTree 2 – approximately maximum-likelihood trees for large alignments. PLoS ONE. 2010;5:e9490.Article 

    Google Scholar 
    15.Stegen JC, Lin X, Fredrickson JK, Chen X, Kennedy DW, Murray CJ, et al. Quantifying community assembly processes and identifying features that impose them. ISME J. 2013;7:2069–79.Article 

    Google Scholar 
    16.Fillinger L, Hug K, Griebler, C. Selection imposed by local environmental conditions drives differences in microbial community composition across geographically distinct groundwater aquifers. FEMS Microbiol. Ecol. 2019;95:1–12.17.Powell JR, Karunaratne S, Campbell CD, Yao H, Robinson L, Singh BK. Deterministic processes vary during community assembly for ecologically dissimilar taxa. Nat Commun. 2015;6:8444.CAS 
    Article 

    Google Scholar 
    18.Peay KG, Schubert MG, Nguyen NH, Bruns TD. Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules. Mol Ecol. 2012;21:4122–36.Article 

    Google Scholar 
    19.Elliott KJ, Vose JM. The contribution of the Coweeta Hydrologic Laboratory to developing an understanding of long-term (1934-2008) changes in managed and unmanaged forests. For Ecol Manag. 2011;261:900–10.Article 

    Google Scholar 
    20.Zhang X, Johnston ER, Liu W, Li L, Han X. Environmental changes affect the assembly of soil bacterial community primarily by mediating stochastic processes. Global Change Biology. 2016;22:198–207.Article 

    Google Scholar 
    21.Dini-Andreote F, Stegen JC, Elsas JD, van, Salles JF. Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. Proc Natl Acad Sci USA. 2015;112:E1326–32.CAS 
    Article 

    Google Scholar  More

  • in

    Twenty-year trends in antimicrobial resistance from aquaculture and fisheries in Asia

    We reviewed and mapped antimicrobial resistance in aquatic food animals in Asia during a period of substantial industry growth. Our findings indicate that between 2000 and 2018, antimicrobial resistance in bacteria from cultured aquatic food animals was stable (33%) while the resistance from wild-caught aquatic food animals decreased sharply (52% to 22%). These trends represent currently available evidence from point prevalence surveys, which serve as a surrogate in the absence of systematic surveillance and should be interpreted cautiously. Structured, systematic surveillance will be imperative to document trends in multi-drug resistance at the sub-national level in the future.Our results are consistent with an analysis of antimicrobial resistance in aquaculture-derived bacteria from forty countries, nearly half of which in Asia, which identified a global mean multi-antibiotic resistance index of .25, and a higher index ( >.35) in low-income and middle-income countries in Asia27. Although antimicrobial use in surveys from cultured animals was most frequently unspecified, in the limited surveys that recorded whether on-farm antimicrobials were either used or not used (n = 63; 11%), use was associated with higher multi-drug resistance than the absence of use (p  More

  • in

    Future phytoplankton diversity in a changing climate

    1.Food and Agriculture Organization of the United Nations. The State of World Fisheries and Aquaculture http://www.fao.org/3/i2727e/i2727e00.htm (2012).2.Isbell, F. et al. Biodiversity increases the resistance of ecosystem productivity to climate extremes. Nature 526, 574–577 (2015).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    3.IPBES. Summary for policymakers of the global assessment report on biodiversity and ecosystem services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services https://doi.org/10.5281/zenodo.3553579 (2019).4.Tittensor, D. P. et al. A mid-term analysis of progress toward international biodiversity targets. Science 346, 241–244 (2014).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    5.Dornelas, M. et al. Assemblage time series reveal biodiversity change but not systematic loss. Science 344, 296–299 (2014).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    6.Gonzalez, A. et al. Estimating local biodiversity change: a critique of papers claiming no net loss of local diversity. Ecology 97, 1949–1960 (2016).PubMed 
    Article 

    Google Scholar 
    7.Elahi, R. et al. Recent trends in local-scale marine biodiversity reflect community structure and human impacts. Curr. Biol. 25, 1938–1943 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    8.Blowes, S. A. et al. The geography of biodiversity change in marine and terrestrial assemblages. Science 366, 339–345 (2019).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    9.McCann, K. S. The diversity–stability debate. Nature 405, 228–233 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    10.Loreau, M. Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294, 804–808 (2001).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    11.Covich, A. P. et al. The role of biodiversity in the functioning of freshwater and marine benthic ecosystems. Bioscience 54, 767–775 (2004).Article 

    Google Scholar 
    12.Hooper, D. U. et al. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol. Monogr. 75, 3–35 (2005).Article 

    Google Scholar 
    13.Widdicombe, C. E., Eloire, D., Harbour, D., Harris, R. P. & Somerfield, P. J. Long-term phytoplankton community dynamics in the Western English Channel. J. Plankton Res. 32, 643–655 (2010).Article 

    Google Scholar 
    14.Eloire, D. et al. Temporal variability and community composition of zooplankton at station L4 in the Western Channel: 20 years of sampling. J. Plankton Res. 32, 657–679 (2010).Article 

    Google Scholar 
    15.Hillebrand, H. et al. In Handbook on Marine Environment Protection (eds Salomon, M. & Markus, T.) 21 (Springer, 2018).16.Bindoff, N. L. et al. In IPCC Special Report on the Ocean and Cryosphere in a Changing Climate (eds H.-O. Pörtner, D. C. Roberts, V. Masson-Delmotte, P. Zhai, M. Tignor, E. Poloczanska, K. Mintenbeck, A. Alegría, M. Nicolai, A. Okem, J. Petzold, B. Rama, N. M. W) Cambridge University Press (2019).17.Barton, A. D., Irwin, A. J., Finkel, Z. V. & Stock, C. A. Anthropogenic climate change drives shift and shuffle in North Atlantic phytoplankton communities. Proc. Natl Acad. Sci. USA 113, 2964–2969 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    18.Pecuchet, L. et al. Spatio‐temporal dynamics of multi‐trophic communities reveal ecosystem‐wide functional reorganization. Ecography 43, 197–208 (2020).Article 

    Google Scholar 
    19.Poloczanska, E. S. et al. Responses of marine organisms to climate change across oceans. Front. Mar. Sci. 3, 62 (2016).20.Pennekamp, F. et al. Biodiversity increases and decreases ecosystem stability. Nature 563, 109–112 (2018).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    21.Duffy, J. E., Godwin, C. M. & Cardinale, B. J. Biodiversity effects in the wild are common and as strong as key drivers of productivity. Nature 549, 261–264 (2017).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    22.Worm, B. et al. Impacts of biodiversity loss on ocean ecosystem services. Science 314, 787–790 (2006).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    23.Blois, J. L., Zarnetske, P. L., Fitzpatrick, M. C. & Finnegan, S. Climate change and the past, present, and future of biotic interactions. Science 341, 499–504 (2013).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    24.Dossena, M. et al. Warming alters community size structure and ecosystem functioning. Proc. R. Soc. B Biol. Sci. 279, 3011–3019 (2012).Article 

    Google Scholar 
    25.Brander, K. & Kiørboe, T. Decreasing phytoplankton size adversely affects ocean food chains. Glob. Chang. Biol. https://doi.org/10.1111/gcb.15216 (2020).26.Mouw, C. B., Barnett, A., McKinley, G. A., Gloege, L. & Pilcher, D. Phytoplankton size impact on export flux in the global ocean. Glob. Biogeochem. Cycles 30, 1542–1562 (2016).ADS 
    CAS 
    Article 

    Google Scholar 
    27.Riahi, K. et al. RCP 8.5—a scenario of comparatively high greenhouse gas emissions. Clim. Change 109, 33–57 (2011).ADS 
    CAS 
    Article 

    Google Scholar 
    28.Magnan, A. K. et al. Implications of the Paris agreement for the ocean. Nat. Clim. Chang. 6, 732–735 (2016).ADS 
    Article 

    Google Scholar 
    29.Kuhn, A. M. et al. Temporal and spatial scales of correlation in marine phytoplankton communities. J. Geophys. Res. Ocean. 124, 9417–9438 (2019).ADS 
    Article 

    Google Scholar 
    30.Sonnewald, M., Dutkiewicz, S., Hill, C. & Forget, G. Elucidating ecological complexity: unsupervised learning determines global marine eco-provinces. Sci. Adv. 6, eaay4740 (2020).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    31.Dutkiewicz, S., Boyd, P. W. & Riebesell, U. Exploring biogeochemical and ecological redundancy in phytoplankton communities in the global ocean. Glob. Chang. Biol. 27, 1196–1213 (2021).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    32.Flombaum, P., Wang, W.-L., Primeau, F. W. & Martiny, A. C. Global picophytoplankton niche partitioning predicts overall positive response to ocean warming. Nat. Geosci. 13, 116–120 (2020).ADS 
    CAS 
    Article 

    Google Scholar 
    33.Righetti, D., Vogt, M., Gruber, N., Psomas, A. & Zimmermann, N. E. Global pattern of phytoplankton diversity driven by temperature and environmental variability. Sci. Adv. 5, eaau6253 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    34.Ibarbalz, F. M. et al. Global trends in marine plankton diversity across kingdoms of life. Cell 179, 1084–1097.e21 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    35.Bopp, L. et al. Multiple stressors of ocean ecosystems in the 21st century: projections with CMIP5 models. Biogeosciences 10, 6225–6245 (2013).ADS 
    Article 

    Google Scholar 
    36.Kwiatkowski, L. et al. Twenty-first century ocean warming, acidification, deoxygenation, and upper-ocean nutrient and primary production decline from CMIP6 model projections. Biogeosciences 17, 3439–3470 (2020).ADS 
    CAS 
    Article 

    Google Scholar 
    37.Cabré, A., Marinov, I. & Leung, S. Consistent global responses of marine ecosystems to future climate change across the IPCC AR5 earth system models. Clim. Dyn. 45, 1253–1280 (2015).Article 

    Google Scholar 
    38.Bopp, L., Aumont, O., Cadule, P., Alvain, S. & Gehlen, M. Response of diatoms distribution to global warming and potential implications: a global model study. Geophys. Res. Lett. 32, n/a−n/a (2005).Article 
    CAS 

    Google Scholar 
    39.Dutkiewicz, S. et al. Dimensions of marine phytoplankton diversity. Biogeosciences 17, 609–634 (2020).ADS 
    Article 

    Google Scholar 
    40.Dutkiewicz, S., Scott, J. R. & Follows, M. J. Winners and losers: ecological and biogeochemical changes in a warming ocean. Glob. Biogeochem. Cycles 27, 463–477 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    41.Marinov, I., Doney, S. C. & Lima, I. D. Response of ocean phytoplankton community structure to climate change over the 21st century: partitioning the effects of nutrients, temperature, and light. Biogeosciences 7, 3941–3959 (2010).ADS 
    Article 

    Google Scholar 
    42.Dutkiewicz, S., Ward, B. A., Scott, J. R. & Follows, M. J. Understanding predicted shifts in diazotroph biogeography using resource competition theory. Biogeosciences 11, 5445–5461 (2014).ADS 
    Article 

    Google Scholar 
    43.Dutkiewicz, S. et al. Impact of ocean acidification on the structure of future phytoplankton communities. Nat. Clim. Chang. 5, 1002–1006 (2015).ADS 
    CAS 
    Article 

    Google Scholar 
    44.Kooijman, S. A. L. M. & Troost, T. A. Quantitative steps in the evolution of metabolic organisation as specified by the dynamic energy budget theory. Biol. Rev. 82, 113–142 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    45.Lévy, M., Jahn, O., Dutkiewicz, S., Follows, M. J. & D’Ovidio, F. The dynamical landscape of marine phytoplankton diversity. J. R. Soc. Interface 12, 20150481 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    46.Beaugrand, G., Edwards, M., Raybaud, V., Goberville, E. & Kirby, R. R. Future vulnerability of marine biodiversity compared with contemporary and past changes. Nat. Clim. Chang. 5, 695–701 (2015).ADS 
    Article 

    Google Scholar 
    47.Thomas, M. K., Kremer, C. T., Klausmeier, C. A. & Litchman, E. A global pattern of thermal adaptation in marine phytoplankton. Science 338, 1085–1088 (2012).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    48.Hillebrand, H. et al. Biodiversity change is uncoupled from species richness trends: consequences for conservation and monitoring. J. Appl. Ecol. 55, 169–184 (2018).Article 

    Google Scholar 
    49.Litchman, E. & Klausmeier, C. A. Trait-based community ecology of phytoplankton. Annu. Rev. Ecol. Evol. Syst. 39, 615–639 (2008).Article 

    Google Scholar 
    50.Lindeman, R. L. The trophic-dynamic aspect of ecology. Ecology 23, 399–417 (1942).Article 

    Google Scholar 
    51.Stock, C. A. et al. Reconciling fisheries catch and ocean productivity. Proc. Natl Acad. Sci. USA 114, E1441–E1449 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    52.Armengol, L., Calbet, A., Franchy, G., Rodríguez-Santos, A. & Hernández-León, S. Planktonic food web structure and trophic transfer efficiency along a productivity gradient in the tropical and subtropical Atlantic Ocean. Sci. Rep. 9, 2044 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    53.Cram, J. A. et al. The role of particle size, ballast, temperature, and oxygen in the sinking flux to the deep sea. Glob. Biogeochem. Cycles 32, 858–876 (2018).ADS 
    CAS 
    Article 

    Google Scholar 
    54.Kéfi, S., Dakos, V., Scheffer, M., Van Nes, E. H. & Rietkerk, M. Early warning signals also precede non-catastrophic transitions. Oikos 122, 641–648 (2013).Article 

    Google Scholar 
    55.Doncaster, C. P. et al. Early warning of critical transitions in biodiversity from compositional disorder. Ecology 97, 3079–3090 (2016).PubMed 
    Article 

    Google Scholar 
    56.Gunderson, L. H. Ecological resilience—in theory and application. Annu. Rev. Ecol. Syst. 31, 425–439 (2000).Article 

    Google Scholar 
    57.Benedetti, F. et al. The seasonal and inter-annual fluctuations of plankton abundance and community structure in a North Atlantic Marine Protected Area. Front. Mar. Sci. 6, 214 (2019).58.Pannard, A., Bormans, M. & Lagadeuc, Y. Short-term variability in physical forcing in temperate reservoirs: effects on phytoplankton dynamics and sedimentary fluxes. Freshw. Biol. 52, 12–27 (2007).CAS 
    Article 

    Google Scholar 
    59.Vidal, T., Calado, A. J., Moita, M. T. & Cunha, M. R. Phytoplankton dynamics in relation to seasonal variability and upwelling and relaxation patterns at the mouth of Ria de Aveiro (West Iberian Margin) over a four-year period. PLoS One 12, e0177237 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    60.Cermeño, P., de Vargas, C., Abrantes, F. & Falkowski, P. G. Phytoplankton biogeography and community stability in the ocean. PLoS One 5, e10037 (2010).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    61.Allen, S. et al. Interannual stability of phytoplankton community composition in the North-East Atlantic. Mar. Ecol. Prog. Ser. 655, 43–57 (2020).ADS 
    Article 

    Google Scholar 
    62.Barton, A. D., Lozier, M. S. & Williams, R. G. Physical controls of variability in North Atlantic phytoplankton communities. Limnol. Oceanogr. 60, 181–197 (2015).ADS 
    Article 

    Google Scholar 
    63.Collins, S., Rost, B. & Rynearson, T. A. Evolutionary potential of marine phytoplankton under ocean acidification. Evol. Appl. 7, 140–155 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    64.Lohbeck, K. T., Riebesell, U. & Reusch, T. B. H. Adaptive evolution of a key phytoplankton species to ocean acidification. Nat. Geosci. 5, 346–351 (2012).ADS 
    CAS 
    Article 

    Google Scholar 
    65.Irwin, A. J., Finkel, Z. V., Müller-Karger, F. E. & Troccoli Ghinaglia, L. Phytoplankton adapt to changing ocean environments. Proc. Natl Acad. Sci. USA 112, 5762–5766 (2015).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    66.Cael, B. B. et al. Marine ecosystem changepoints spread under ocean warming in an Earth System Model. Geophys. Res. Lett.67.Cael, B. B., Dutkiewicz, S. & Henson, S. A. Abrupt shifts in 21st-century plankton communities. Sci. Adv.68.Parmesan, C. & Yohe, G. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42 (2003).ADS 
    CAS 
    Article 

    Google Scholar 
    69.Burrows, M. T. et al. The pace of shifting climate in marine and terrestrial ecosystems. Science 334, 652–655 (2011).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    70.Chivers, W. J., Walne, A. W. & Hays, G. C. Mismatch between marine plankton range movements and the velocity of climate change. Nat. Commun. 8, 14434 (2017).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    71.Poloczanska, E. S. et al. Global imprint of climate change on marine life. Nat. Clim. Chang. 3, 919–925 (2013).ADS 
    Article 

    Google Scholar 
    72.Jonkers, L., Hillebrand, H. & Kucera, M. Global change drives modern plankton communities away from the pre-industrial state. Nature 570, 372–375 (2019).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    73.Pond, D. W., Tarling, G. A. & Mayor, D. J. Hydrostatic pressure and temperature effects on the membranes of a seasonally migrating marine copepod. PLoS One 9, e111043 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    74.Mayor, D. J., Sommer, U., Cook, K. B. & Viant, M. R. The metabolic response of marine copepods to environmental warming and ocean acidification in the absence of food. Sci. Rep. 5, 13690 (2015).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    75.Richardson, D. M. & Pyšek, P. Elton, C.S. 1958: The ecology of invasions by animals and plants. London: Methuen. Prog. Phys. Geogr. Earth Environ. 31, 659–666 (2007).Article 

    Google Scholar 
    76.May, R. M. Qualitative stability in model ecosystems. Ecology 54, 638–641 (1973).Article 

    Google Scholar 
    77.Lotze, H. K. et al. Global ensemble projections reveal trophic amplification of ocean biomass declines with climate change. Proc. Natl Acad. Sci. USA 116, 12907–12912 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    78.Barange, M. et al. Impacts of climate change on marine ecosystem production in societies dependent on fisheries. Nat. Clim. Chang. 4, 211–216 (2014).ADS 
    Article 

    Google Scholar 
    79.Marañón, E. et al. Unimodal size scaling of phytoplankton growth and the size dependence of nutrient uptake and use. Ecol. Lett. 16, 371–379 (2013).PubMed 
    Article 

    Google Scholar 
    80.Sokolov, A. P. et al. The MIT Integrated Global System Model (IGSM) Version 2: Model Description and Baseline Evaluation Joint Program Report Series, pp. 40 https://globalchange.mit.edu/publication/14579 (2005).81.Dutkiewicz, S. et al. Ocean colour signature of climate change. Nat. Commun. 10, 578 (2019).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    82.Monier, E., Scott, J. R., Sokolov, A. P., Forest, C. E. & Schlosser, C. A. An integrated assessment modeling framework for uncertainty studies in global and regional climate change: the MIT IGSM-CAM (version 1.0). Geosci. Model Dev. 6, 2063–2085 (2013).ADS 
    Article 

    Google Scholar 
    83.Moss, R. H. et al. The next generation of scenarios for climate change research and assessment. Nature 463, 747–756 (2010).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    84.Buitenhuis, E. T. et al. MAREDAT: towards a world atlas of MARine Ecosystem DATa. Earth Syst. Sci. Data 5, 227–239 (2013).ADS 
    Article 

    Google Scholar 
    85.Ward, B. A. Temperature-correlated changes in phytoplankton community structure are restricted to polar waters. PLoS One 10, e0135581 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    86.Dutkiewicz, S. GUD IGSM depth integrated biomass https://doi.org/10.7910/DVN/LWHQNS (2021).87.Dutkiewicz, S. & Jahn, O. GUD IGSM numerical code and inputs https://doi.org/10.7910/DVN/UA8VNU (2021). More

  • in

    Phytoplankton communities in temporary ponds under different climate scenarios

    1.Walther, G. R. et al. Ecological responses to recent climate change. Nature 416, 389–395 (2002).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    2.Mooij, W. M. et al. The impact of climate change on lakes in the Netherlands: A review. Aquat. Ecol. 39, 381–400 (2005).CAS 
    Article 

    Google Scholar 
    3.Walter, B., Peters, J. & van Beusekom, J. E. E. The effect of constant darkness and short light periods on the survival and physiological fitness of two phytoplankton species and their growth potential after re-illumination. Aquat. Ecol. 51, 591–603 (2017).CAS 
    Article 

    Google Scholar 
    4.Woodward, G., Perkins, D. M. & Brown, L. E. Climate change and freshwater ecosystems: Impacts across multiple levels of organization. Philos. Trans. R. Soc. B Biol. Sci. 365, 2093–2106 (2010).Article 

    Google Scholar 
    5.Wagner, H., Fanesi, A. & Wilhelm, C. Title: Freshwater phytoplankton responses to global warming. J. Plant Physiol. 203, 127–134 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    6.Gilbert, J. A. Some phytoplankton like it hot. Nat. Clim. Change 3, 954–955 (2013).ADS 
    Article 

    Google Scholar 
    7.Hense, I., Meier, H. E. M. & Sonntag, S. Projected climate change impact on Baltic Sea cyanobacteria: Climate change impact on cyanobacteria. Clim. Change 119, 391–406 (2013).CAS 
    Article 

    Google Scholar 
    8.Trombetta, T. et al. Water temperature drives phytoplankton blooms in coastal waters. PLoS One 14, e0214933 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    9.Jin, P. & Agustí, S. Fast adaptation of tropical diatoms to increased warming with trade-offs. Sci. Rep. 8, 17771 (2018).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    10.Pinceel, T., Buschke, F., Weckx, M., Brendonck, L. & Vanschoenwinkel, B. Climate change jeopardizes the persistence of freshwater zooplankton by reducing both habitat suitability and demographic resilience. BMC Ecol. 18, 1–9 (2018).Article 

    Google Scholar 
    11.Shin, H. R. & Kneitel, J. M. Warming interacts with inundation timing to influence the species composition of California vernal pool communities. Hydrobiologia 843, 93–105 (2019).Article 

    Google Scholar 
    12.Montrone, A. et al. Climate change impacts on vernal pool hydrology and vegetation in northern California. J. Hydrol. 574, 1003–1013 (2019).ADS 
    Article 

    Google Scholar 
    13.Williams, D. D. The biology of temporary waters. Biol. Tempor. Waters https://doi.org/10.1093/acprof:oso/9780198528128.001.0001 (2007).Article 

    Google Scholar 
    14.Waterkeyn, A., Grillas, P., Vanschoenwinkel, B. & Brendonck, L. Invertebrate community patterns in Mediterranean temporary wetlands along hydroperiod and salinity gradients. Freshw. Biol. 53, 1808–1822 (2008).CAS 
    Article 

    Google Scholar 
    15.Lemmens, P. et al. How to maximally support local and regional biodiversity in applied conservation? Insights from pond management. PLoS One 8, e72538 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    16.Lischeid, G. et al. Natural ponds in an agricultural landscape: External drivers, internal processes, and the role of the terrestrial-aquatic interface. Limnologica 68, 5–16 (2018).CAS 
    Article 

    Google Scholar 
    17.Mancinelli, G., Mali, S. & Belmonte, G. Species richness and taxonomic distinctness of zooplankton in ponds and small lakes from Albania and North Macedonia: The role of bioclimatic factors. Water (Switzerland) 11, 2384 (2019).
    Google Scholar 
    18.Gołdyn, B., Kowalczewska-Madura, K. & Celewicz-Gołdyn, S. Drought and deluge: Influence of environmental factors on water quality of kettle holes in two subsequent years with different precipitation. Limnologica 54, 14–22 (2015).Article 
    CAS 

    Google Scholar 
    19.Salmaso, N. & Tolotti, M. Phytoplankton and anthropogenic changes in pelagic environments. Hydrobiologia https://doi.org/10.1007/s10750-020-04323-w (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    20.Celewicz, S., Czyż, M. J. & Gołdy, B. Feeding patterns in Eubranchipus grubii (Dybowski 1860) (Branchiopoda: Anostraca) and its potential influence on the phytoplankton communities of vernal pools. J. Limnol. 77, 276–284 (2018).Article 

    Google Scholar 
    21.Rasconi, S., Winter, K. & Kainz, M. J. Temperature increase and fluctuation induce phytoplankton biodiversity loss—Evidence from a multi-seasonal mesocosm experiment. Ecol. Evol. 7, 2936–2946 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    22.Celewicz-Goldyn, S. & Kuczynska-Kippen, N. Ecological value of macrophyte cover in creating habitat for microalgae (diatoms) and zooplankton (rotifers and crustaceans) in small field and forest water bodies. PLoS One 12, e0177317 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    23.Kozak, A., Celewicz-Gołdyn, S. & Kuczyńska-Kippen, N. Cyanobacteria in small water bodies: The effect of habitat and catchment area conditions. Sci. Total Environ. 646, 1578–1587 (2019).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    24.Iacarella, J. C., Barrow, J. L., Giani, A., Beisner, B. E. & Gregory-Eaves, I. Shifts in algal dominance in freshwater experimental ponds across differing levels of macrophytes and nutrients. Ecosphere 9, e02086 (2018).Article 

    Google Scholar 
    25.Toseland, A. et al. The impact of temperature on marine phytoplankton resource allocation and metabolism. Nat. Clim. Change 3, 979–984 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    26.Richardson, J. et al. Response of cyanobacteria and phytoplankton abundance to warming, extreme rainfall events and nutrient enrichment. Glob. Change Biol. 25, 3365–3380 (2019).ADS 
    Article 

    Google Scholar 
    27.De Senerpont Domis, L. N., Mooij, W. M. & Huisman, J. Climate-induced shifts in an experimental phytoplankton community: A mechanistic approach. Hydrobiologia 584, 403–413 (2007).Article 

    Google Scholar 
    28.Boyce, D. G., Lewis, M. R. & Worm, B. Global phytoplankton decline over the past century. Nature 466, 591–596 (2010).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    29.Hinder, S. L. et al. Changes in marine dinoflagellate and diatom abundance under climate change. Nat. Clim. Change 2, 271–275 (2012).ADS 
    Article 

    Google Scholar 
    30.Winder, M. & Sommer, U. Phytoplankton response to a changing climate. Hydrobiologia 698, 5–16 (2012).Article 

    Google Scholar 
    31.Machado, K. B., Vieira, L. C. G. & Nabout, J. C. Predicting the dynamics of taxonomic and functional phytoplankton compositions in different global warming scenarios. Hydrobiologia 830, 115–134 (2019).CAS 
    Article 

    Google Scholar 
    32.O’Neil, J. M., Davis, T. W., Burford, M. A. & Gobler, C. J. The rise of harmful cyanobacteria blooms: The potential roles of eutrophication and climate change. Harmful Algae 14, 313–334 (2012).Article 
    CAS 

    Google Scholar 
    33.Rasconi, S., Gall, A., Winter, K. & Kainz, M. J. Increasing water temperature triggers dominance of small freshwater plankton. PLoS One 10, e0140449 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    34.Wirth, C., Limberger, R. & Weisse, T. Temperature × light interaction and tolerance of high water temperature in the planktonic freshwater flagellates Cryptomonas (Cryptophyceae) and Dinobryon (Chrysophyceae). J. Phycol. 55, 404–414 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    35.Wang, H. et al. High antioxidant capability interacts with respiration to mediate two Alexandrium species growth exploitation of photoperiods and light intensities. Harmful Algae 82, 26–34 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    36.Fakhri, M., Arifin, N. B., Budianto, B., Yuniarti, A. & Hariati, A. M. Effect of salinity and photoperiod on growth of microalgae Nannochloropsis sp. and Tetraselmis sp. Nat. Environ. Pollut. Technol. 14, 563–566 (2015).
    Google Scholar 
    37.Torzillo, G., Sacchi, A. & Materassi, R. Temperature as an important factor affecting productivity and night biomass loss in Spirulina platensis grown outdoors in tubular photobioreactors. Bioresour. Technol. 38, 95–100 (1991).Article 

    Google Scholar 
    38.Shatwell, T., Köhler, J. & Nicklisch, A. Temperature and photoperiod interactions with phosphorus-limited growth and competition of two diatoms. PLoS One 9, e102367 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    39.Li, G., Talmy, D. & Campbell, D. A. Diatom growth responses to photoperiod and light are predictable from diel reductant generation. J. Phycol. 53, 95–107 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    40.Reynolds, C. S. Vegetation Processes in the Pelagic: A Model for Ecosystem Theory. Excellence in Ecology Vol. 77 (Ecology Institute, 1997).
    Google Scholar 
    41.Elliott, J. A., Jones, I. D. & Thackeray, S. J. Testing the sensitivity of phytoplankton communities to changes in water temperature and nutrient load, in a temperate lake. Hydrobiologia 559, 401–411 (2006).CAS 
    Article 

    Google Scholar 
    42.Jöhnk, K. D. et al. Summer heatwaves promote blooms of harmful cyanobacteria. Glob. Change Biol. 14, 495–512 (2008).ADS 
    Article 

    Google Scholar 
    43.Elliott, J. A. Is the future blue–green? A review of the current model predictions of how climate change could affect pelagic freshwater cyanobacteria. Water Res. 46, 1364–1371 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    44.Ullah, H., Nagelkerken, I., Goldenberg, S. U. & Fordham, D. A. Climate change could drive marine food web collapse through altered trophic flows and cyanobacterial proliferation. PLoS Biol. 16, e2003446 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    45.Hansson, L. A. et al. Food-chain length alters community responses to global change in aquatic systems. Nat. Clim. Change 3, 228–233 (2013).ADS 
    Article 

    Google Scholar 
    46.Burgmer, T. & Hillebrand, H. Temperature mean and variance alter phytoplankton biomass and biodiversity in a long-term microcosm experiment. Oikos 120, 922–933 (2011).Article 

    Google Scholar 
    47.Hillebrand, H., Burgmer, T. & Biermann, E. Running to stand still: Temperature effects on species richness, species turnover, and functional community dynamics. Mar. Biol. 159, 2415–2422 (2012).Article 

    Google Scholar 
    48.Lewandowska, A. M. et al. Responses of primary productivity to increased temperature and phytoplankton diversity. J. Sea Res. 72, 87–93 (2012).ADS 
    Article 

    Google Scholar 
    49.Lewandowska, A. M., Hillebrand, H., Lengfellner, K. & Sommer, U. Temperature effects on phytoplankton diversity—The zooplankton link. J. Sea Res. 85, 359–364 (2014).ADS 
    Article 

    Google Scholar 
    50.Bergkemper, V., Stadler, P. & Weisse, T. Moderate weather extremes alter phytoplankton diversity—A microcosm study. Freshw. Biol. 63, 1211–1224 (2018).CAS 
    Article 

    Google Scholar 
    51.McMinn, A. & Martin, A. Dark survival in a warming world. Proc. R. Soc. B Biol. Sci. 280, 20122909 (2013).CAS 
    Article 

    Google Scholar 
    52.Waibel, A., Peter, H. & Sommaruga, R. Importance of mixotrophic flagellates during the ice-free season in lakes located along an elevational gradient. Aquat. Sci. 81, 1–10 (2019).CAS 
    Article 

    Google Scholar 
    53.Chen, B. Patterns of thermal limits of phytoplankton. J. Plankton Res. 37, 285–292 (2015).Article 

    Google Scholar 
    54.Reeves, S., McMinn, A. & Martin, A. The effect of prolonged darkness on the growth, recovery and survival of Antarctic sea ice diatoms. Polar Biol. 34, 1019–1032 (2011).Article 

    Google Scholar 
    55.van de Poll, W. H., Abdullah, E., Visser, R. J. W., Fischer, P. & Buma, A. G. J. Taxon-specific dark survival of diatoms and flagellates affects Arctic phytoplankton composition during the polar night and early spring. Limnol. Oceanogr. 65, 903–914 (2020).ADS 
    Article 

    Google Scholar 
    56.Poniewozik, M. & Juráň, J. Extremely high diversity of euglenophytes in a small pond in eastern Poland. Plant Ecol. Evol. 151, 18–34 (2018).Article 

    Google Scholar 
    57.Shafik, H. M., Herodek, S., Présing, M. & Vörös, L. Factors effecting growth and cell composition of cyanoprokaryote Cylindrospermopsis raciborskii (Wołoszyńska) Seenayya et Subba Raju. Algol. Stud. Hydrobiol. Suppl. 103, 75–93 (2001).
    Google Scholar 
    58.Tang, E. P. Y. & Vincent, W. F. Effects of daylength and temperature on the growth and photosynthesis of an Arctic cyanobacterium, Schizothrix calcicola (Oscillatoriaceae). Eur. J. Phycol. 35, 263–272 (2000).Article 

    Google Scholar 
    59.Agasild, H., Zingel, P., Tõnno, I., Haberman, J. & Nõges, T. Contribution of different zooplankton groups in grazing on phytoplankton in shallow eutrophic Lake Võrtsjärv (Estonia). Hydrobiologia 584, 167–177 (2007).Article 

    Google Scholar 
    60.Gołdyn, R. & Kowalczewska-Madura, K. Interactions between phytoplankton and zooplankton in the hypertrophic Swarzȩdzkie Lake in western Poland. J. Plankton Res. 30, 33–42 (2008).Article 
    CAS 

    Google Scholar 
    61.Tovar-Sanchez, A., Duarte, C. M., Hernández-León, S. & Sañudo-Wilhelmy, S. A. Krill as a central node for iron cycling in the Southern Ocean. Geophys. Res. Lett. 34, L11601 (2007).ADS 
    Article 
    CAS 

    Google Scholar 
    62.Hunt, R. J. & Matveev, V. F. The effects of nutrients and zooplankton community structure on phytoplankton growth in a subtropical Australian reservoir: An enclosure study. Limnologica 35, 90–101 (2005).Article 

    Google Scholar 
    63.Yvon-Durocher, G. et al. Five years of experimental warming increases the biodiversity and productivity of phytoplankton. PLoS Biol. 13, e1002324 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    64.Gołdyn, B., Chudzińska, M., Barałkiewicz, D. & Celewicz-Gołdyn, S. Heavy metal contents in the sediments of astatic ponds: Influence of geomorphology, hydroperiod, water chemistry and vegetation. Ecotoxicol. Environ. Saf. 118, 103–111 (2015).PubMed 
    Article 
    CAS 

    Google Scholar 
    65.IPCC. Climate Change 2007: The Physical Science Basis (Cambridge University Press, 2007).
    Google Scholar 
    66.Christensen, J. H. & Christensen, O. B. A summary of the PRUDENCE model projections of changes in European climate by the end of this century. Clim. Change 81, 7–30 (2007).ADS 
    Article 

    Google Scholar 
    67.Beniston, M. et al. Future extreme events in European climate: An exploration of regional climate model projections. Clim. Change 81, 71–95 (2007).Article 

    Google Scholar 
    68.Anderson, M. J. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26, 32–46 (2001).
    Google Scholar 
    69.Arbizu, P. M. pairwiseAdonis: Pairwise Multilevel Comparison Using Adonis. R Packag. version 0.0.1. (2017).70.Rink, B. & Raak, C. J. F. Principal response curves: Analysis of time-dependent multivariate responses of biological community to stress. Environ. Toxicol. Chem. 18, 138–148 (1999).Article 

    Google Scholar 
    71.Lepš, J. & Šmilauer, P. Multivariate Analysis of Ecological Data using CANOCO. Bulletin of the Ecological Society of America Vol. 87 (Cambridge University Press, 2003).MATH 
    Book 

    Google Scholar 
    72.Jongman, R. H. G., Ter Braak, C. J. F. & van Tongeren, O. F. R. Data Analysis in Community and Landscape Ecology. Data Analysis in Community and Landscape Ecology (Cambridge University Press, 1995). https://doi.org/10.1017/cbo9780511525575.Book 

    Google Scholar 
    73.ter Braak, J. F. C. & Šmilauer, P. Canoco Reference Manual and CanoDraw for Windows User’s Guide (Microcomputer Power, 2002).
    Google Scholar 
    74.R Development Core Team. R: A Language and Environment for Statistical Computing (2020).75.Oksanen, J. et al. vegan: Community Ecology Package. R Packag. version 2.5-7 (2020). More

  • in

    Climate warming promotes pesticide resistance through expanding overwintering range of a global pest

    Insect preparationWe collected 200–300 larvae and pupae of the diamondback moth from cabbage and cauliflower fields in Wuhan, Beijing, and Shenyang in late September from 2008 to 2012. We mixed all collections into one stock colony because of no geographic differentiation in this species from these sites59. We reared all individuals on cabbage leaves spread evenly across five screen cages (35 × 35 × 15 cm) in growth chambers at constant temperature (25 ± 1 °C) with 15-h light:9-h dark photoperiod, and relative humidity set at 60 ± 10%. We moved any new pupae to new screen cages for adult emergence. Emerged adults were fed with 10% honey solution in cotton balls. To collect eggs, we dipped four small pieces of laboratory film (7 × 5 cm) in fresh cabbage juice for 3–5 s and hung the treated film pieces on the top of each screen cage. To further enlarge the population for our experiments, we reared these insects in the artificial diet in plastic boxes at 25 ± 1 °C. We transferred 200 eggs to the surface of 120 g artificial diet (Southland Products Incorporated, USA) in each plastic box (10 × 10 × 9 cm). The hatched larvae dropped to the surface of the artificial diet and fed on it. Once individuals developed into 3rd or 4th instar larvae, pupae or adults, they were exposed to 10 °C for 24 h (to simulate gradually reduced temperatures in late autumn and allow a thermal acclimation) just before they were placed to the low-temperature regimes for overwintering tests. Overall, we obtained >7000 larvae and >8000 pupae for the laboratory experiment, and >8000 larvae, >8000 pupae, >4000 adults for the field experiment. We have compared the life history traits of insects reared on the artificial diet with natural host plants (cabbage leaves), they performed similarly (Peng and Li, unpublished data).Laboratory experiment of winter survivalSite selectionTo identify what factor determines winter survival under different winter thermal conditions, we conducted a laboratory experiment that simulated temperature regimes of 10 selected sites across a latitudinal gradient in China (Fig. 1, Supplementary Table 1) at which this species is known to occur and damage cruciferous crops during the growing season.Temperature treatmentTo simulate the winter temperatures in the 10 geographically distinct sites (Fig. 1a, Supplementary Table 1), we collected daily mean temperatures during winter (November to next April of 1966–2010) at each site from China Meteorological Data Service Centre (http://data.cma.cn/en). Then, we fitted a polynomial model to the temporal changes of winter daily mean temperatures for each site (Fig. 1b). To simplify the logistics of temperature control procedures, we set all temperature regimes in combinations of linear decline, horizontal maintenance and linear increase to mimic the polynomial changes of winter temperatures in the 10 sites, and adjusted temperature every 10 days as needed (Fig. 1c). We controlled the winter temperature changes of the 10 sites with climate chambers (RXZ-280B, Jiangnan Ltd., Ningbo, China) and refrigerators (Royalstar BCD-246GER) according to curves in Fig. 1c.Experimental protocolsWe conducted a winter survival experiment with 10 low-temperature regimes (Fig. 1c). We exposed 6050 larvae and 7150 pupae to 10 low-temperature regimes according to the experiment design (Fig. 1c). Then we sampled 55 larvae and 65 pupae every 10 days from each temperature regime resulting in 11 sampling points. Sampled larvae were placed at 25 °C for 1.5 days to observe the survival based on if their body kept fresh green60 and appendage moved after touching with a brush34. The pupae were placed at 25 °C, RH 70–80% and photoperiod of 16 L:8D for emergence to determine the survival (emergence rate). These samples were not returned to the temperature treatments. Thus, no individual was measured more than once and each sample interval represents an independent observation.Field survival experiments across 12 geographic sitesTo verify the cold survivals from the laboratory simulation and identify the best predictor under natural conditions, we conducted field experiments to explore the winter survival for multiple years at various geographic sites in China (Fig. 1a, Supplementary Table 1). The diamondback moth overwinters either in remaining cabbage plants or in fallen leaves (post-harvest conditions) in regions without standing cabbage crops in the winter. We tested the winter survival of larvae, pupae and adults in the caged cabbage plants or post-harvest conditions in fallen leaves on the soil surface at each site for 3–4 months. We transferred 30 larvae, 30 pupae or 30 adults from our stock rearing to a cabbage plant in the field. Then each plant was covered with a screen cage to avoid disturbance and contain focal individuals (see Supplementary Fig. 2). We set 6–8 cages for larvae, pupae and adults, respectively, in a field in November or early December. After an exposure of 1, 2, 3 and 4 months, we collected 2 cages of larvae, 2 cages of pupae and 2 cages of adults from the field at each sampling point and kept individuals in the laboratory (25 ± 1 °C, RH 65–75%, L:D = 16:8 h) for two days. We checked the survival status of the larvae based on the change in body coloration (i.e. if the larval body kept fresh green colour)60, pupal survival based on whether adults could emerge from the pupae, and adult survival based on if their appendage moved after touching with a brush.To simulate the field microenvironment of post-harvest conditions in winter, we filled half of a glass jar (diameter = 5.5 cm, height = 14 cm) with moist soil. Then, we transferred 30 larvae or 30 pupae to the soil surface, covered the insects with leaves, and then covered the glass jar with a nylon net (see Supplementary Fig. 2). We buried 6–8 jars for larvae and pupae, respectively, and kept the top of the jar at ground surface level at each site in November and early December. Because almost all adults died in few days within the jar, we did not test the adult survival in post-harvest conditions. After an exposure of 1, 2, 3 and 4 months, we took 2 jars of larvae and 2 jars of pupae per sampling period from the field and placed them in the laboratory with 25 ± 1 °C, RH 65–75%, L:D = 16:8 h for 2 days. The survival status of the larvae and pupae was checked with the same procedures as the overwintering tests on caged cabbage plants. Note that as in the standing plant experiment, no individual was tested more than once assuming that each observation is independent at the replicate level.Modelling and predicting winter survivalModel developmentOur goal was to identify key metrics that best predict the winter survival of the diamondback moth across a climatic gradient. To achieve this goal, we took several steps. First, we fit a set of predictive models to the laboratory experiments to identify which metric and model best describes survival under controlled conditions. We focused on three alternative predictors: the lowest daily mean temperature (MinDTmean), mean temperature (DTmean) combined with exposure days, and low-temperature degree-days (LTDD). The MinDTmean model assumes that survival can simply be predicted as a function of the lowest temperature an individual experienced during its exposure time. The DTmean model assumes that survival depends on both the average temperature individuals experience below the cold threshold for survival (11 °C)32 and exposure duration (note that exposure time varied systematically in 10-day increments). Finally, the LTDD model predicts survival depending on coldness below the cold threshold. We calculated LTDD by summing up negative deviations of daily mean temperatures from the cold threshold (11.0 °C) during each exposure period for each simulated geographic site (Fig. 1c). To detect potential relationships, we fit each model using three different functions, i.e. linear, exponential and sigmoid models to describe the survival probability (Supplementary Table 2, Fig. 1). We estimated parameters of models in SigmaStat 3.5 and compared model fit using R2 and AIC values (see detailed models in Supplementary Table 2).Field validation of survival modelsTo validate winter survival models derived from the laboratory (see models in Supplementary Table 2) for complex and variable field conditions, we compared model predictions to observed survivals in field experiments across 12 different geographic sites over 5 years (Fig. 1a, Supplementary Table 1). To make the connection, we first collected daily mean temperatures recorded at the nearest weather stations to our field sites from China Meteorological Data Service Centre. We then calculated MinDTmean, DTmean and exposure days, and LTDD for each site for each treated period and input these values into these laboratory models to predict winter survival. Note, that because the coefficients were calculated from the laboratory experiment, predictions are completely independent of survival observed under field conditions. During the model validation, we excluded the field data of south China, e.g. Guangzhou, Changsha and Wuhan where the warmer temperatures allowed moths to continue their regular life cycle during the whole winter, resulting in unrealistic winter survival. We also excluded replicates in which glass jars were filled with water and destroyed the tested insects. We used linear regression to compare predicted survival with field observations. The validity of each model was evaluated based on the variance explained, slopes of linear regressions and prediction bias (i.e. deviation from unity slope). Finally, we selected the exponential model driven by LTDD as the model to predict the global distribution of winter survival due to its lowest AIC value (Supplementary Table 2) and the least bias (Supplementary Table 3, Fig. 2) among all models.Global prediction of overwintering range shiftTo extrapolate our winter survival predictions to a global scale under present and future climate conditions, we downloaded global historical daily mean temperature data for 50 years (1967–2016) from Berkeley Earth (1° × 1° grid, http://berkeleyearth.org/data/). We added 1, 2, 3, 4, 5 and 6 °C to mean temperatures of 2012–2016, respectively, to represent the different future warming scenarios37. Then, we calculated the annual LTDD in the northern hemisphere with Eq. (1) and in the southern hemisphere with Eq. (2). For xi,j  x0, we excluded the xi,j for the calculation LTDD. For Eq. (1), we started the calculation of LTDD from July 1st (Julian date 182), ended on June 30th of next year (Julian date 181) to cover the whole low-temperature season in the northern hemisphere cross the calendar year. We used LTDD for every year during past conditions to our validated survival model (LTDD-dependent exponential model) and further calculated the expected corresponding yearly winter survival and 5-year mean survival. Since the diamondback moth only feeds on Brassicaceae plants61, we incorporated host availability to refine the pest distributions. We retrieved Brassicaceae occurrence data during 1967–2016 (3,720,971 records) from the Global Biodiversity Information Facility (GBIF) database (www.gbif.org), and excluded unknown and duplicate records; 919,808 records were retained to model the global distribution of host plants. We used a dataset of eight selected bioclimatic variables as described in a previous Brassicaceae biogeographic study62, including isothermality (bio3), temperature seasonality (bio4), min temperature of coldest month (bio6), mean temperature of wettest quarter (bio8), mean temperature of driest quarter (bio9), precipitation seasonality (bio15), precipitation of warmest quarter (bio18), precipitation of coldest quarter (bio19) from Worldclim dataset63 (http://worldclim.org). We ran the species distribution model using the Maxent algorithm in R package dismo64. Model outputs were presented in grid ranks of host plant presence probability from 0 (unsuitable) to 1 (most suitable). Based on the known distribution of Brassicaceae, we only included grid cells with Brassicaceae presence probability ≥0.3 for our final survival and distribution analysis to ensure the presence of the host plant and mapped them with Arcmap 10.2 (Environmental Systems Research Institute) (see Fig. 3a, e). To show spatial-temporal changes in the geographic distribution of winter survival, we quantified the historical change (expansions or contractions) in the overwintering range based on the total numbers of grids for each year between 1967 and 2016 relative to the baseline area in 1967 (see Fig. 3f) and further calculated average changes of every 5 years (see Fig. 3b). We selected sites in the overwintering marginal belt (with winter survival between 1 and 5%) in the baseline year (1967), calculated the annual LTDD of these sites from 1967 to 2016, and built the linear trend of annual LTDD for years 1967–2016 (see Fig. 3g). We predicted distribution changes for future scenarios (added 1, 2, 3, 4, 5 and 6 °C to the current mean temperatures of 2012–2016) relative to the baseline area of 1967–1971 (see Fig. 3c, d).Meta-analysis linking pesticide resistance to overwintering typeData preparation: literature search and selection criteriaWe performed a comprehensive literature survey to collect data on pesticide resistance of the diamondback moth worldwide. We searched for publications in databases of ISI Web of Science, Scopus and China National Knowledge Infrastructure (CNKI) using keywords “pesticide resistance” in combination with “diamondback moth” or “Plutella xylostella” and expanded references in the selected papers. We reviewed titles, abstracts and in many cases the full articles for relevance and agreement with our inclusion criteria. Studies were included if they (1) monitored the pesticide resistance of field populations, (2) used the leaf dip bioassay method to test pesticide resistance which is the most commonly used method recommended by Insecticide Resistance Action Committee (IRAC, http://www.irac-online.org); (3) provided resistance ratio of field populations. Resistance ratio (abbreviated as RR) is the magnitude of pesticide resistance and is commonly calculated by dividing the median lethal concentration (LC50) of a tested field population by LC50 of the susceptible population (without exposure to pesticide). The LC50 is commonly estimated from a concentration-mortality curve of a given pesticide. The preliminary literature search resulted in 2151 studies out of which 62 matched these criteria. A PRISMA diagram describing details of our literature search is available in Supplementary Fig. 4.Data preparation: data extractionWe extracted data from each selected publication, the names of pesticides, sampling locations and years of field populations, number of tested individuals in a bioassay, resistance ratio of field populations (RR), LC50 of field populations (LC50field) and susceptible populations (LC50susceptible), and 95% confidence intervals (CIs) of LC50field and LC50susceptible. Some studies generated results from multiple types of pesticides with the same field population, each of which was considered as a different entry. Finally, we gathered 1806 entries for pesticide resistance of field populations of the diamondback moth.Data preparation: calculation of the weighted effect sizeWe conducted a meta-analysis to test if pesticide resistance levels vary across different types of overwintering sites. To account for differences in sample sizes and variances in resistance ratios across studies, we calculated the corrected (weighted) resistance ratio for each study following the method in Hedges et al.65. We calculated the logarithm of resistance ratio (logRR) to present the effect size for each entry and further calculated the weighted effect size (wlogRR) by$${{{{{rm{wlogRR}}}}}}={{{{{rm{logRR}}}}}}times w$$
    (3)
    where w is the weighting factor of each entry, with w = 1/sqrt(VlogRR)66. To consider the contribution from both field and susceptible population, the pooled variance VlogRR was calculated as follows65:$${{{{{{rm{V}}}}}}}_{{{{{{rm{logRR}}}}}}}=frac{{{{{{{{rm{SE}}}}}}}_{{{{{{rm{field}}}}}}}}^{2}}{{n}_{{{{{{rm{field}}}}}}}times {{{{{{{rm{LC50}}}}}}}_{{{{{{rm{field}}}}}}}}^{2}}+frac{{{{{{{{rm{SE}}}}}}}_{{{{{{rm{susceptible}}}}}}}}^{2}}{{n}_{{{{{{rm{susceptible}}}}}}}times {{{{{{{rm{LC50}}}}}}}_{{{{{{rm{susceptible}}}}}}}}^{2}}$$
    (4)
    where LC50field and LC50susceptible, SEfield and SEsusceptible, nfield and nsusceptible, are LC50, the standard error of LC50 and sample size for field population and susceptible population, respectively. SEfield and SEsusceptible can be calculated from their own confidence intervals (95% CI)67:$${{{{{rm{SE}}}}}}=frac{{{{{{{rm{CI}}}}}}}_{{{{{{rm{upper}}}}}}{{{{{rm{limit}}}}}}}-{{{{{{rm{CI}}}}}}}_{{{{{{rm{lower}}}}}}{{{{{rm{limit}}}}}}}}{2times 1.96}$$
    (5)
    where CIupper limit is the upper limit and CIlower limit is the lower limit of the 95% CI for LC50.We used the prognostic method68 to estimate VlogRR for entries that miss either 95% CI or LC50 based on the average VlogRR of the other complete entries.Data preparation: potential moderator variablesSeveral factors could influence pesticide resistance besides overwintering temperatures. The effective temperature degree-days (ETDD) may change the annual number of generations, the intensity of pesticide application, and thus the selection stress47, e.g. between 7.4 and 33 °C for the diamondback moth32. In addition, the variety of pesticides used in a study may also affect the resistance levels through their mode of actions (the lethal mechanism) and cross-resistance69,70. To account for these potentially confounding factors, we collected the mode of action for each variety of pesticides from IRAC, and calculated LTDD, ETDD and overwintering type for each of the 1806 original records. We collected data for daily mean temperatures for each site from Berkeley Earth. For each location, we calculated the mean annual LTDD, ETDD and winter survival average across the 5 years before the sample. We split the sampling sites into three types based on predicted winter survival of the diamondback moth: (1) the permanent (overwintering) sites: locations with the mean winter survivals ≥5%, (2) marginal sites: locations with the mean winter survivals 1–5%, (3) transient (non-overwintering) sites: locations with the mean winter survivals More

  • in

    Native soil amendments combined with commercial arbuscular mycorrhizal fungi increase biomass of Panicum amarum

    1.Elmqvist, T. et al. Benefits of restoring ecosystem services in urban areas. Curr. Opin. Environ. Sustain. 14, 101–108 (2015).Article 

    Google Scholar 
    2.Jones, H. P. et al. Restoration and repair of Earth’s damaged ecosystems. Proc. R. Soc. B Biol. Sci. https://doi.org/10.1098/rspb.2017.2577 (2018).Article 

    Google Scholar 
    3.Rey Benayas, J. M., Newton, A. C., Diaz, A. & Bullock, J. M. Enhancement of biodiversity and ecosystem services by ecological restoration: A meta-analysis. Science 325, 1121–1124. https://doi.org/10.1126/science.1172460 (2009).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    4.Brudvig, L. A. et al. Interpreting variation to advance predictive restoration science. J. Appl. Ecol. 54, 1018–1027. https://doi.org/10.1111/1365-2664.12938 (2017).Article 

    Google Scholar 
    5.Suding, K. N. Toward an era of restoration in ecology: Successes, failures, and opportunities ahead. Annu. Rev. Ecol. Evol. Syst. 42, 465–487. https://doi.org/10.1146/annurev-ecolsys-102710-145115 (2011).Article 

    Google Scholar 
    6.Reynolds, H. L., Packer, A., Bever, J. D. & Clay, K. Grassroots ecology: Plant-microbe-soil interactions as drivers of plant community structure and dynamics. Ecology 84, 2281–2291 (2003).Article 

    Google Scholar 
    7.Van Der Heijden, M. G. A., Bardgett, R. D. & Van Straalen, N. M. The unseen majority: Soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol. Lett. 11, 296–310 (2008).Article 

    Google Scholar 
    8.Hoeksema, J. D. et al. A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol. Lett. 13, 394–407. https://doi.org/10.1111/j.1461-0248.2009.01430.x (2010).Article 
    PubMed 

    Google Scholar 
    9.Schultz, P. A. et al. Evidence of a mycorrhizal mechanism for the adaptation of Andropogon gerardii (Poaceae) to high- and low-nutrient prairies. Am. J. Bot. 88, 1650–1656. https://doi.org/10.2307/3558410 (2001).CAS 
    Article 
    PubMed 

    Google Scholar 
    10.Koske, R. E., & Gemma, J. N. Mycorrhizae and succession in plantings of beachgrass in sand dunes. Am. J. Bot. 84(1), 118–130 (1997).Article 

    Google Scholar 
    11.Smith, M. E., Facelli, J. M. & Cavagnaro, T. R. Interactions between soil properties, soil microbes and plants in remnant-grassland and old-field areas: a reciprocal transplant approach. Plant Soil 433, 127–145. https://doi.org/10.1007/s11104-018-3823-2 (2018).CAS 
    Article 

    Google Scholar 
    12.Tipton, A. G., Middleton, E. L., Spollen, W. G. & Galen, C. Anthropogenic and soil environmental drivers of arbuscular mycorrhizal community composition differ between grassland ecosystems. Botany 97, 85–99. https://doi.org/10.1139/cjb-2018-0072 (2019).Article 

    Google Scholar 
    13.Hamman, S. T. & Hawkes, C. V. Biogeochemical and microbial legacies of non-native grasses can affect restoration success. Restor. Ecol. 21, 58–66. https://doi.org/10.1111/j.1526-100X.2011.00856.x (2013).Article 

    Google Scholar 
    14.Emery, S. M. & Rudgers, J. A. Beach restoration efforts influenced by plant variety, soil inoculum, and site effects. J. Coast. Res. 27, 636. https://doi.org/10.2112/jcoastres-d-10-00120.1 (2010).Article 

    Google Scholar 
    15.Sylvia, D. M., Jarstfer, A. G. & Vosátka, M. Comparisons of vesicular-arbuscular mycorrhizal species and inocula formulations in a commercial nursery and on diverse Florida beaches. Biol. Fertil. Soils 16, 139–144. https://doi.org/10.1007/BF00369416 (1993).Article 

    Google Scholar 
    16.Sylvia, D. M. & Will, M. E. Establishment of vesicular-arbuscular mycorrhizal fungi and other microorganisms on a beach replenishment site in Florida. Appl. Environ. Microbiol. 54, 348–352 (1988).ADS 
    CAS 
    Article 

    Google Scholar 
    17.Wubs, E. R. J., van der Putten, W. H., Bosch, M. & Bezemer, T. M. Soil inoculation steers restoration of terrestrial ecosystems. Nat. Plants 2, 16107. https://doi.org/10.1038/nplants.2016.107 (2016).Article 
    PubMed 

    Google Scholar 
    18.Bothe, H., Turnau, K. & Regvar, M. The potential role of arbuscular mycorrhizal fungi in protecting endangered plants and habitats. Mycorrhiza 20, 445–457. https://doi.org/10.5586/asbp.2008.019 (2010).Article 
    PubMed 

    Google Scholar 
    19.Middleton, E. L. & Bever, J. D. Inoculation with a native soil community advances succession in a grassland restoration. Restor. Ecol. 20, 218–226. https://doi.org/10.1111/j.1526-100X.2010.00752.x (2012).Article 

    Google Scholar 
    20.Crawford, K. M., Busch, M. H., Locke, H. & Luecke, N. C. Native soil microbial amendments generate trade-offs in plant productivity, diversity, and soil stability in coastal dune restorations. Restor. Ecol. https://doi.org/10.1111/rec.13073 (2019).Article 

    Google Scholar 
    21.Eom, A. H., Hartnett, D. C. & Wilson, G. W. T. Host plant species effects on arbuscular mycorrhizal fungal communities in tallgrass prairie. Oecologia 122, 435–444. https://doi.org/10.1007/s004420050050 (2000).ADS 
    Article 
    PubMed 

    Google Scholar 
    22.Brundrett, M. C. & Tedersoo, L. Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol. 220, 1108–1115 (2018).Article 

    Google Scholar 
    23.Bever, J. D., Mangan, S. A. & Alexander, H. M. Maintenance of plant species diversity by pathogens. Annu. Rev. Ecol. Evol. Syst. 46, 305–325. https://doi.org/10.1146/annurev-ecolsys-112414-054306 (2015).Article 

    Google Scholar 
    24.Crawford, K. M. et al. When and where plant-soil feedback may promote plant coexistence: a meta-analysis. Ecol. Lett. 22, 13278. https://doi.org/10.1111/ele.13278 (2019).Article 

    Google Scholar 
    25.Mills, K. E. & Bever, J. D. Maintenance of diversity within plant communities: Soil pathogens as agents of negative feedback. Ecology 79, 1595–1601. https://doi.org/10.1890/0012-9658(1998)079[1595:MODWPC]2.0.CO;2 (1998).Article 

    Google Scholar 
    26.Koziol, L. et al. The plant microbiome and native plant restoration: The example of native mycorrhizal fungi. Bioscience 68, 996–1006 (2018).Article 

    Google Scholar 
    27.Maltz, M. R. & Treseder, K. K. Sources of inocula influence mycorrhizal colonization of plants in restoration projects: A meta-analysis. Restor. Ecol. 23, 625–634. https://doi.org/10.1111/rec.12231 (2015).Article 

    Google Scholar 
    28.Koziol, L. & Bever, J. D. AMF, phylogeny, and succession: Specificity of response to mycorrhizal fungi increases for late-successional plants. Ecosphere https://doi.org/10.1002/ecs2.1555 (2016).Article 

    Google Scholar 
    29.Middleton, E. L. et al. Locally adapted arbuscular mycorrhizal fungi improve vigor and resistance to herbivory of native prairie plant species. Ecosphere 6, 276. https://doi.org/10.1890/ES15-00152.1 (2015).Article 

    Google Scholar 
    30.Solís-Domínguez, F. A., Valentín-Vargas, A., Chorover, J. & Maier, R. M. Effect of arbuscular mycorrhizal fungi on plant biomass and the rhizosphere microbial community structure of mesquite grown in acidic lead/zinc mine tailings. Sci. Total Environ. 409, 1009–1016. https://doi.org/10.1016/j.scitotenv.2010.11.020 (2011).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    31.Vogelsang, K. M., Reynolds, H. L. & Bever, J. D. Mycorrhizal fungal identity and richness determine the diversity and productivity of a tallgrass prairie system. New Phytol. 172, 554–562. https://doi.org/10.1111/j.1469-8137.2006.01854.x (2006).Article 
    PubMed 

    Google Scholar 
    32.Larimer, A. L., Bever, J. D. & Clay, K. Consequences of simultaneous interactions of fungal endophytes and arbuscular mycorrhizal fungi with a shared host grass. Oikos 121, 2090–2096. https://doi.org/10.1111/j.1600-0706.2012.20153.x (2012).Article 

    Google Scholar 
    33.Sikes, B. A., Cottenie, K. & Klironomos, J. N. Plant and fungal identity determines pathogen protection of plant roots by arbuscular mycorrhizas. J. Ecol. 97, 1274–1280. https://doi.org/10.1111/j.1365-2745.2009.01557.x (2009).Article 

    Google Scholar 
    34.Defeo, O. et al. Threats to sandy beach ecosystems: A review. Estuar. Coast. Shelf Sci. 81, 1–12 (2009).ADS 
    Article 

    Google Scholar 
    35.Feagin, R. A. et al. Going with the flow or against the grain? The promise of vegetation for protecting beaches, dunes, and barrier islands from erosion. Front. Ecol. Environ. 13, 203–210 (2015).Article 

    Google Scholar 
    36.Feagin, R. A. et al. The role of beach and sand dune vegetation in mediating wave run up erosion. Estuar Coast Shelf Sci. 219, 97–106. https://doi.org/10.1016/j.ecss.2019.01.018 (2019).ADS 
    Article 

    Google Scholar 
    37.Sigren, J. M., Figlus, J. & Armitage, A. R. Coastal sand dunes and dune vegetation: Restoration, erosion, and storm protection. Shore Beach 82, 5–12 (2014).
    Google Scholar 
    38.Sigren, J. M. et al. The effects of coastal dune volume and vegetation on storm-induced property damage: Analysis from Hurricane Ike. J. Coast Res. 341, 164–173. https://doi.org/10.2112/jcoastres-d-16-00169.1 (2018).Article 

    Google Scholar 
    39.Silva, R. et al. Response of vegetated dune-beach systems to storm conditions. Coast. Eng. 109, 53–62. https://doi.org/10.1016/j.coastaleng.2015.12.007 (2016).Article 

    Google Scholar 
    40.Lane, C., Wright, S. J., Roncal, J. & Maschinski, J. Characterizing environmental gradients and their influence on vegetation zonation in a subtropical coastal sand dune system. J. Coast. Res. 4, 213–224. https://doi.org/10.2112/07-0853.1 (2008).CAS 
    Article 

    Google Scholar 
    41.Miller, T. E., Gornish, E. S. & Buckley, H. L. Climate and coastal dune vegetation: Disturbance, recovery, and succession. Plant Ecol. 206, 97–104. https://doi.org/10.1007/s11258-009-9626-z (2010).Article 

    Google Scholar 
    42.Hewitt, E. J. & Eden, A. Sand and water culture methods used in the study of plant nutrition. Analyst 78, 329–330 (1953).
    Google Scholar 
    43.R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, Austria). https://www.R-project.org/ (2020).
    Google Scholar 
    44.Farrer, E. C. & Goldberg, D. E. Litter drives ecosystem and plant community changes in cattail invasion. Ecol. Appl. 19, 398–412. https://doi.org/10.1890/08-0485.1 (2009).Article 
    PubMed 

    Google Scholar 
    45.Bauer, J. T., Koziol, L. & Bever, J. D. Local adaptation of mycorrhizae communities changes plant community composition and increases aboveground productivity. Oecologia https://doi.org/10.1007/s00442-020-04598-9 (2020).Article 
    PubMed 

    Google Scholar 
    46.Ohsowski, B. M., Klironomos, J. N., Dunfield, K. E. & Hart, M. M. The potential of soil amendments for restoring severely disturbed grasslands. Appl. Soil. Ecol. 60, 77–83. https://doi.org/10.1016/j.apsoil.2012.02.006 (2012).Article 

    Google Scholar 
    47.Koziol, L. & Bever, J. D. The missing link in grassland restoration: arbuscular mycorrhizal fungi inoculation increases plant diversity and accelerates succession. J. Appl. Ecol. 54, 1301–1309. https://doi.org/10.1111/1365-2664.12843 (2017).Article 

    Google Scholar 
    48.Bertness, M. D. & Callaway, R. Positive interactions in communities. Trends Ecol. Evol. 9, 191–193. https://doi.org/10.1016/0169-5347(94)90088-4 (1994).CAS 
    Article 
    PubMed 

    Google Scholar 
    49.Heneghan, L. et al. Integrating soil ecological knowledge into restoration management. Restor. Ecol. 16, 608–617. https://doi.org/10.1111/j.1526-100X.2008.00477.x (2008).Article 

    Google Scholar 
    50.Wubs, E. R. J. et al. Single introductions of soil biota and plants generate long-term legacies in soil and plant community assembly. Ecol. Lett. 22, 1145–1151 (2019).Article 

    Google Scholar 
    51.Hestrin, R., Hammer, E. C., Mueller, C. W. & Lehmann, J. Synergies between mycorrhizal fungi and soil microbial communities increase plant nitrogen acquisition. Commun. Biol. 2, 233–242. https://doi.org/10.1038/s42003-019-0481-8 (2019).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar  More